Publications
Selected Publications
Li Y., Wei Z.Z., Fatiukha A., Jaiwar S., Wang H., Hasan S., Liu Z., Sela H., Krugman T., Fahima T.
Theoretical and Applied Genetics: 1-17, 2021
Abstract
We identified TdPm60 alleles from wild emmer wheat (WEW), an ortholog of Pm60 from T. urartu, which constitutes a strong candidate for PmG16 mildew resistance. Deployment of PmG16 in Israeli modern bread wheat cultivar Ruta improved the resistance to several local Bgt isolates. Wild emmer wheat (WEW), the tetraploid progenitor of durum and bread wheat, is a valuable genetic resource for resistance to powdery mildew fungal disease caused by Blumeria graminis f. sp. tritici (Bgt). PmG16 gene, derived from WEW, confers high resistance to most tested Bgt isolates. We mapped PmG16 to a 1.4-cM interval between the flanking markers uhw386 and uhw390 on Chromosome 7AL. Based on gene annotation of WEW reference genome Zavitan_V1, 34 predicted genes were identified within the ~ 3.48-Mb target region. Six genes were annotated as associated with disease resistance, of which TRIDC7AG077150.1 was found to be highly similar to Pm60, previously cloned from Triticum urartu, and resides in the same syntenic region. The functional molecular marker (FMM) for Pm60 (M-Pm60-S1) co-segregated with PmG16, suggesting the Pm60 ortholog from WEW (designated here as TdPm60) as a strong candidate for PmG16. Sequence alignment identified only eight SNPs that differentiate between TdPm60 and TuPm60. Furthermore, TdPm60 was found to be present also in the WEW donor lines of the powdery mildew resistance genes MlIW172 and MlIW72, mapped to the same region of Chromosome 7AL as PmG16, suggesting that TdPm60 constitutes a candidate also for these genes. Furthermore, screening of additional 230 WEW accessions with Pm60 specific markers revealed 58 resistant accessions from the Southern Levant that harbored TdPm60, while none of the susceptible accessions showed the presence of this gene. Deployment of PmG16 in Israeli modern bread wheat cultivar Ruta conferred resistance against several local Bgt isolates.
Tandem protein kinases emerge as new regulators of plant immunity
Klymiuk V., Coaker G., Fahima, T., Pozniak C.
Molecular Plant-Microbe Interactions: 1094-1102, 2021
Abstract
Plant-pathogen interactions result in disease development in a susceptible host. Plants actively resist pathogens via a complex immune system comprising both surface-localized receptors that sense the extracellular space as well as intracellular receptors recognizing pathogen effectors. To date, the majority of cloned resistance genes encode intracellular nucleotide-binding leucine-rich repeat receptor proteins. Recent discoveries have revealed tandem kinase proteins (TKPs) as another important family of intracellular proteins involved in plant immune responses. Five TKP genes-barley Rpg1 and wheat WTK1 (Yr15), WTK2 (Sr60), WTK3 (Pm24), and WTK4-protect against devastating fungal diseases. Moreover, a large diversity and numerous putative TKPs exist across the plant kingdom. This review explores our current knowledge of TKPs and serves as a basis for future studies that aim to develop and exploit a deeper understanding of innate plant immunity receptor proteins.[Formula: see text] Copyright © 2021 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.
Three previously characterized resistances to yellow rust are encoded by a single locus Wtk1
Klymiuk V., Fatiukha A., Raats D., Bocharova V., Huang L., Feng L., Jaiwar S., Pozniak C., Coaker G., Dubcovsky J., Fahima, T.
Journal of Experimental Botany, 71(9): 2561-2572, 2020
Abstract
Wheat (Triticum aestivum L.) is a global commodity, and its production is a key component underpinning worldwide food security. Yellow rust, also known as stripe rust, is a wheat disease caused by the fungus Puccinia striiformis Westend f. sp. tritici (Pst), and results in yield losses in most wheat growing areas. Recently, the rapid global spread of genetically diverse sexually derived Pst races, which have now largely replaced the previous clonally propagated slowly evolving endemic populations, has resulted in further challenges for the protection of global wheat yields. However, advances in the application of genomics approaches, in both the host and pathogen, combined with classical genetic approaches, pathogen and disease monitoring, provide resources to help increase the rate of genetic gain for yellow rust resistance via wheat breeding while reducing the carbon footprint of the crop. Here we review key elements in the evolving battle between the pathogen and host, with a focus on solutions to help protect future wheat production from this globally important disease.
Wheat tandem kinases provide insights on disease‐resistance gene flow and host–parasite co‐evolution
Klymiuk V., Fatiukha A., Fahima T.
The Plant Journal, 98(4): 667-679, 2019
Abstract
Stripe (yellow) rust, caused by the fungus Puccinia striiformis f. sp. tritici (Pst), is a destructive disease of wheat spread globally. Wild emmer wheat (Triticum turgidum ssp. dicoccoides; WEW) is known as a source for novel Pst resistance genes (R-gene), but our knowledge on wheat-Pst co-evolution in natural populations is limited. Yr15 is a WEW (accession G25) gene, which confers a broad-spectrum resistance to Pst, and encodes a tandem kinase-pseudokinase protein designated as WTK1. Exon-intron comparisons of multiple WTK1 homoeologous and paralogous copies scattered in allopolyploid wheat genomes enabled us to develop functional molecular markers (FMMs), which were used for population genetic study. The functional allele (Wtk1) was absent in a worldwide collection of 513 wheat cultivars, except for 32 introgression lines with Yr15 from G25, as well as in 84% of the 382 tested WEW accessions collected across the Fertile Crescent. Yr15 was found to be distributed along a narrow axis from Mt Carmel to the Anti-Lebanon Mountains ridge, mostly at elevations above c. 500 m, where the climatic conditions are favorable for disease development, therefore providing insights on gene flow and host-parasite co-evolution in WEW natural habitats. Moreover, the worldwide absence of Wtk1 in cultivated wheat and in WEW natural populations from southeast Turkey, where wheat is believed to have been domesticated, proposes that Yr15 was rather left behind, than lost during domestication. Our results highlight the importance of conservation of WEW populations in their natural habitats for discovery of novel R-genes and studies of host-parasite co-evolution.
Cloning of the wheat Yr15 resistance gene sheds light on the plant tandem kinase-pseudokinase family
Klymiuk V., Yaniv E., Huang L., Raats D., Fatiukha A., Chen S., Feng L., Frenkel Z., Krugman T., Lidzbarsky G., Chang W., Jaaskelainen M.J., Schudoma C., Paulin L., Laine P., Bariana H., Sela H., Saleem K., Sorensen C.K., Hovmoller M.S., Distelfeld A., Chalhoub B., Dubcovsky J., Korol A.B., Schulman A.H., Fahima T.
Nature Communications, 9: 3735, 2018
Abstract
Yellow rust, caused by Puccinia striiformis f. sp. tritici (Pst), is a devastating fungal disease threatening much of global wheat production. Race-specific resistance (R)-genes are used to control rust diseases, but the rapid emergence of virulent Pst races has prompted the search for a more durable resistance. Here, we report the cloning of Yr15, a broad-spectrum R-gene derived from wild emmer wheat, which encodes a putative kinase-pseudokinase protein, designated as wheat tandem kinase 1, comprising a unique R-gene structure in wheat. The existence of a similar gene architecture in 92 putative proteins across the plant kingdom, including the barley RPG1 and a candidate for Ug8, suggests that they are members of a distinct family of plant proteins, termed here tandem kinase-pseudokinases (TKPs). The presence of kinase-pseudokinase structure in both plant TKPs and the animal Janus kinases sheds light on the molecular evolution of immune responses across these two kingdoms.
Shifting the limits in wheat research and breeding using a fully annotated reference genome
International Wheat Genome Sequencing Consortium (IWGSC), R Appels, ...
Science 361 (6403), eaar7191, 2018
Abstract
An annotated reference sequence representing the hexaploid bread wheat genome in 21 pseudomolecules has been analyzed to identify the distribution and genomic context of coding and noncoding elements across the A, B, and D subgenomes. With an estimated coverage of 94% of the genome and containing 107,891 high-confidence gene models, this assembly enabled the discovery of tissue- and developmental stage–related coexpression networks by providing a transcriptome atlas representing major stages of wheat development. Dynamics of complex gene families involved in environmental adaptation and end-use quality were revealed at subgenome resolution and contextualized to known agronomic single-gene or quantitative trait loci. This community resource establishes the foundation for accelerating wheat research and application through improved understanding of wheat biology and genomics-assisted breeding.
Wild emmer genome architecture and diversity elucidate wheat evolution and domestication
R Avni, M Nave, O Barad, K Baruch, SO Twardziok, H Gundlach, I Hale, ...
Science, 357 (6346): 93-97, 2017
Abstract
Modern wheat, which underlies the diet of many across the globe, has a long history of selection and crosses among different species. Avni et al. used the Hi-C method of genome confirmation capture to assemble and annotate the wild allotetraploid wheat (Triticum turgidum). They then identified the putative causal mutations in genes controlling shattering (a key domestication trait among cereal crops). They also performed an exome capture–based analysis of domestication among wild and domesticated genotypes of emmer wheat. The findings present a compelling overview of the emmer wheat genome and its usefulness in an agricultural context for understanding traits in modern bread wheat.
Evolution and adaptation of wild emmer wheat populations to biotic and abiotic stresses
Huang L., Raats D., Sela H., Klymiuk V., Lidzbarsky G., Feng L., Krugman T., Fahima T.
Annual Review of Phytopathology, 54: 279-301, 2016
Abstract
The genetic bottlenecks associated with plant domestication and subsequent selection in man-made agroecosystems have limited the genetic diversity of modern crops and increased their vulnerability to environmental stresses. Wild emmer wheat, the tetraploid progenitor of domesticated wheat, distributed along a wide range of ecogeographical conditions in the Fertile Crescent, has valuable "left behind" adaptive diversity to multiple diseases and environmental stresses. The biotic and abiotic stress responses are conferred by series of genes and quantitative trait loci (QTLs) that control complex resistance pathways. The study of genetic diversity, genomic organization, expression profiles, protein structure and function of biotic and abiotic stress-resistance genes, and QTLs could shed light on the evolutionary history and adaptation mechanisms of wild emmer populations for their natural habitats. The continuous evolution and adaptation of wild emmer to the changing environment provide novel solutions that can contribute to safeguarding food for the rapidly growing human population.
Genomic analysis of 6,000-year-old cultivated grain illuminates the domestication history of barley
Mascher M., Schuenemann V.J., Davidovich U., Marom N., Himmelbach A., Hübner S., Korol A., David M., Riehl S., Schreiber M., Green R.E., Dawson I.K., Russell J., Kilian B., Muehlbauer G.J., Waugh R., Fahima T.
Nature Genetics, 48: 1089-1093, 2016
Abstract
The cereal grass barley was domesticated about 10,000 years before the present in the Fertile Crescent and became a founder crop of Neolithic agriculture1. Here we report the genome sequences of five 6,000-year-old barley grains excavated at a cave in the Judean Desert close to the Dead Sea. Comparison to whole-exome sequence data from a diversity panel of present-day barley accessions showed the close affinity of ancient samples to extant landraces from the Southern Levant and Egypt, consistent with a proposed origin of domesticated barley in the Upper Jordan Valley. Our findings suggest that barley landraces grown in present-day Israel have not experienced major lineage turnover over the past six millennia, although there is evidence for gene flow between cultivated and sympatric wild populations. We demonstrate the usefulness of ancient genomes from desiccated archaeobotanical remains in informing research into the origin, early domestication and subsequent migration of crop species.
Raats D., Frenkel Z., Krugman T., Dodek I., Sela H., Šimková H., Magni F., Cattonaro F., Vautrin S., Bergès H., Wicker T., Keller B., Leroy P., Philippe R., Paux E., Doležel J., Feuillet C., Korol A.B., Fahima T.
Genome Biology, 14: R138, 2013
Abstract
Background
The wheat genome sequence is an essential tool for advanced genomic research and improvements. The generation of a high-quality wheat genome sequence is challenging due to its complex 17 Gb polyploid genome. To overcome these difficulties, sequencing through the construction of BAC-based physical maps of individual chromosomes is employed by the wheat genomics community. Here, we present the construction of the first comprehensive physical map of chromosome 1BS, and illustrate its unique gene space organization and evolution.
Results
Fingerprinted BAC clones were assembled into 57 long scaffolds, anchored and ordered with 2,438 markers, covering 83% of chromosome 1BS. The BAC-based chromosome 1BS physical map and gene order of the orthologous regions of model grass species were consistent, providing strong support for the reliability of the chromosome 1BS assembly. The gene space for chromosome 1BS spans the entire length of the chromosome arm, with 76% of the genes organized in small gene islands, accompanied by a two-fold increase in gene density from the centromere to the telomere.
Conclusions
This study provides new evidence on common and chromosome-specific features in the organization and evolution of the wheat genome, including a non-uniform distribution of gene density along the centromere-telomere axis, abundance of non-syntenic genes, the degree of colinearity with other grass genomes and a non-uniform size expansion along the centromere-telomere axis compared with other model cereal genomes. The high-quality physical map constructed in this study provides a solid basis for the assembly of a reference sequence of chromosome 1BS and for breeding applications.
Sela H., Spiridon L.N., Petrescu A.J., Akerman M., Mandel-Gutfreund Y., Nevo E., Loutre C., Keller B., Schulman A.H., Fahima T.
Molecular Plant Pathology 13(3): 276-287, 2012
Abstract
In this study, we explore the diversity and its distribution along the wheat leaf rust resistance protein LR10 three-dimensional structure. Lr10 is a leaf rust resistance gene encoding a coiled coil-nucleotide-binding site-leucine-rich repeat (CC-NBS-LRR) class of protein. Lr10 was cloned and sequenced from 58 accessions representing diverse habitats of wild emmer wheat in Israel. Nucleotide diversity was very high relative to other wild emmer wheat genes (π= 0.029). The CC domain was found to be the most diverse domain and subject to positive selection. Superimposition of the diversity on the CC three-dimensional structure showed that some of the variable and positively selected residues were solvent exposed and may interact with other proteins. The LRR domain was relatively conserved, but showed a hotspot of amino acid variation between two haplotypes in the ninth repeat. This repeat was longer than the other LRRs, and three-dimensional modelling suggested that an extensive α helix structure was formed in this region. The two haplotypes also differed in splicing regulation motifs. In genotypes with one haplotype, an intron was alternatively spliced in this region, whereas, in genotypes with the other haplotype, this intron did not splice at all. The two haplotypes are proposed to be ancient and maintained by balancing selection.
A kinase-START gene confers temperature-dependent resistance to wheat stripe rust
Fu D., Uauy C., Distelfeld A., Blechl A., Epstein L., Chen X., Sela H., Fahima T., Dubcovsky J.
Science, 323(5919): 1357-1360, 2009
Abstract
Stripe rust is a devastating fungal disease that afflicts wheat in many regions of the world. New races of Puccinia striiformis, the pathogen responsible for this disease, have overcome most of the known race-specific resistance genes. We report the map-based cloning of the gene Yr36 (WKS1), which confers resistance to a broad spectrum of stripe rust races at relatively high temperatures (25° to 35°C). This gene includes a kinase and a putative START lipid-binding domain. Five independent mutations and transgenic complementation confirmed that both domains are necessary to confer resistance. Yr36 is present in wild wheat but is absent in modern pasta and bread wheat varieties, and therefore it can now be used to improve resistance to stripe rust in a broad set of varieties.
A NAC gene regulating senescence improves grain protein, zinc, and iron content in wheat
Fu D., Uauy C., Distelfeld A., Blechl A., Epstein L., Chen X., Sela H., Fahima T., Dubcovsky J.
Science, 314 (5803), 1298-1301, 2006
Abstract
Enhancing the nutritional value of food crops is a means of improving human nutrition and health. We report here the positional cloning of Gpc-B1, a wheat quantitative trait locus associated with increased grain protein, zinc, and iron content. The ancestral wild wheat allele encodes a NAC transcription factor (NAM-B1) that accelerates senescence and increases nutrient remobilization from leaves to developing grains, whereas modern wheat varieties carry a nonfunctional NAM-B1 allele. Reduction in RNA levels of the multiple NAM homologs by RNA interference delayed senescence by more than 3 weeks and reduced wheat grain protein, zinc, and iron content by more than 30%.
Domestication quantitative trait loci in Triticum dicoccoides, the progenitor of wheat
Peng J., Ronin Y., Fahima T., Röder M.S., Li Y., Nevo E., Korol A.
Proceedings of the National Academy of Sciences ,100 (5): 2489-2494, 2003
Abstract
Wild emmer wheat, Triticum dicoccoides, is the progenitor of modern tetraploid and hexaploid cultivated wheats. Our objective was to map domestication-related quantitative trait loci (QTL) in T. dicoccoides. The studied traits include brittle rachis, heading date, plant height, grain size, yield, and yield components. Our mapping population was derived from a cross between T. dicoccoides and Triticum durum. Approximately 70 domestication QTL effects were detected, nonrandomly distributed among and along chromosomes. Seven domestication syndrome factors were proposed, each affecting 5–11 traits. We showed: (i) clustering and strong effects of some QTLs; (ii) remarkable genomic association of strong domestication-related QTLs with gene-rich regions; and (iii) unexpected predominance of QTL effects in the A genome. The A genome of wheat may have played a more important role than the B genome during domestication evolution. The cryptic beneficial alleles at specific QTLs derived from T. dicoccoides may contribute to wheat and cereal improvement.
Positional cloning of the wheat vernalization gene VRN1
Yan L., Loukoianov A., Tranquilli G., Helguera M., Fahima T., Dubcovsky J.
Proceedings of the National Academy of Sciences, 100 (10), 6263-6268, 2003
Abstract
Winter wheats require several weeks at low temperature to flower. This process, vernalization, is controlled mainly by the VRN1 gene. Using 6,190 gametes, we found VRN1 to be completely linked to MADS-box genes AP1 and AGLG1 in a 0.03-centimorgan interval flanked by genes Cysteine and Cytochrome B5. No additional genes were found between the last two genes in the 324-kb Triticum monococcum sequence or in the colinear regions in rice and sorghum. Wheat AP1 and AGLG1 genes were similar to Arabidopsis meristem identity genes AP1 and AGL2, respectively. AP1 transcription was regulated by vernalization in both apices and leaves, and the progressive increase of AP1 transcription was consistent with the progressive effect of vernalization on flowering time. Vernalization was required for AP1 transcription in apices and leaves in winter wheat but not in spring wheat. AGLG1 transcripts were detected during spike differentiation but not in vernalized apices or leaves, suggesting that AP1 acts upstream of AGLG1. No differences were detected between genotypes with different VRN1 alleles in the AP1 and AGLG1 coding regions, but three independent deletions were found in the promoter region of AP1. These results suggest that AP1 is a better candidate for VRN1 than AGLG1. The epistatic interactions between vernalization genes VRN1 and VRN2 suggested a model in which VRN2 would repress directly or indirectly the expression of AP1. A mutation in the promoter region of AP1 would result in the lack of recognition of the repressor and in a dominant spring growth habit.
Full list of Publications
Govta, N., Govta, L., Sela, H., Peleg, G., Distelfeld, A., Fahima, T., Beckles, D.M. and Krugman, T.
Authorea Preprints, 2024
Abstract
Nitrogen (N) deficiency critically affects wheat development and productivity. Our study aimed to decipher tolerance mechanisms to N deficiency regulated by a QTL transferred into bread wheat from wild emmer wheat (WEW). Root system architecture (RSA) and transcriptome modifications in response to severe N deficiency were compared between the introgression (IL99) and its cultivated parent. Higher plasticity was demonstrated in IL99 by modifying the growth strategy of RSA coordinated with shoot development. These included a shift in root orientation from shallow to steep, more and longer roots, and higher root networks, enabling nutrient acquisition from a larger volume and deeper soil layers. Transcriptome analyses revealed gene-expression reprogramming, highlighted by unique GO and KEGG-enriched pathways in leaves and toots. Based on transcriptome results and protein-protein interaction, we identified promising candidate genes associated with uptake of NO 3 - (high-affinity transporter NRT2.4), increased root lignification ( trans-cinnamate 4-monooxygenase (CYP73A), and 4-coumarate-CoA ligase (4CL)). Jasmonic acid, known as associated with plasticity of RSA, was predominant among other plant hormones identified in this study, by activating allene oxide synthase ( AOS1), TIFY proteins, transcription factors MTB2 and MYC2. Transcriptomic and developmental changes in IL99 demonstrated fundamental mechanisms underlying its enhanced N-use efficiency and stress tolerance attributed to WEW.
Govta, N., Fatiukha, A., Govta, L., Pozniak, C., Distelfeld, A., Fahima, T., Beckles, D.M. and Krugman, T.
Theoretical and Applied Genetics, 137(8), pp.1-18, 2024
Abstract
Nitrogen (N) is an important macronutrient critical to wheat growth and development; its deficiency is one of the main factors causing reductions in grain yield and quality. N availability is significantly affected by drought or flooding, that are dependent on additional factors including soil type or duration and severity of stress. In a previous study, we identified a high grain protein content QTL (QGpc.huj.uh-5B.2) derived from the 5B chromosome of wild emmer wheat, that showed a higher proportion of explained variation under water-stress conditions. We hypothesized that this QTL is associated with tolerance to N deficiency as a possible mechanism underlying the higher effect under stress. To validate this hypothesis, we introgressed the QTL into the elite bread wheat var. Ruta, and showed that under N-deficient field conditions the introgression IL99 had a 33% increase in GPC (p < 0.05) compared to the recipient parent. Furthermore, evaluation of IL99 response to severe N deficiency (10% N) for 14 days, applied using a semi-hydroponic system under controlled conditions, confirmed its tolerance to N deficiency. Fine-mapping of the QTL resulted in 26 homozygous near-isogenic lines (BC4F5) segregating to N-deficiency tolerance. The QTL was delimited from − 28.28 to − 1.29 Mb and included 13 candidate genes, most associated with N-stress response, N transport, and abiotic stress responses. These genes may improve N-use efficiency under severely N-deficient environments. Our study demonstrates the importance of WEW as a source of novel candidate genes for sustainable improvement in tolerance to N deficiency in wheat.
Atlas of tandem kinase proteins across the plant kingdom
Fahima, T., Reveguk, T., Fatiukha, A., Potapenko, E., Reveguk, I., Sela, H., Klymiuk, V., Li, Y., Pozniak, C., Wicker, T. and Coaker, G.
PREPRINT (Version 1) available at Research Square [https://doi.org/10.21203/rs.3.rs-4468450/v1], 2024
Abstract
Plant pathogens pose a continuous threat to global food production. Recent discoveries in plant immunity research unveiled a unique protein family characterized by an unusual resistance protein structure that combines two kinase domains (KD). This study demonstrates the widespread occurrence of tandem-kinase proteins (TKPs) across the plant kingdom. An examination of 104 plant species' genomes uncovered 2,682 TKPs. The majority (95.6%) of these KDs are part of the RLK-Pelle receptor-like kinase family, which is crucial for cell surface responses in plant immunity. Notably, 90% of TKPs comprise dual KDs, with over 50% being pseudokinases. Over 56% of these proteins harbor 127 different integrated domains, and over 47% include a transmembrane domain. TKP pseudokinases and/or integrated domains probably serve as decoys, engaging with pathogen effectors to trigger plant immunity. The TKP Atlas we created sheds light on the mechanisms of TKP convergent molecular evolution and potential function.
Direct binding of a fungal effector by the wheat RWT4 tandem kinase activates defense
Sung, Y.C., Li, Y., Bernasconi, Z., Baik, S., Asuke, S., Keller, B., Fahima, T. and Coaker, G.
bioRxiv, pp.2024-04, 2024
Abstract
Plants have intricate innate immune receptors that detect pathogens. Research has intensely focused on two receptor classes recognizing external and internal threats. Recent research has identified a class of disease resistance proteins called tandem kinase proteins (TKPs). We investigated RWT4, a wheat TKP that confers resistance to the devastating fungal pathogen Magnaporthe oryzae. We established a rice protoplast system, revealing RWT4 specifically recognizes the AvrPWT4 effector, leading to the transcription of defense genes and inducing cell death. RWT4 possesses both kinase and pseudokinase domains, with its kinase activity essential for defense. RWT4 directly interacts with and transphosphorylates AvrPWT4. Biolayer interferometry revealed both RWT4 kinase and pseudokinase regions bind the effector. Sequence similarity and structural modeling revealed an integrated partial kinase duplication in RWT4’s kinase region as critical for effector interaction and defense activation. Collectively, these findings demonstrate that TKPs can directly bind a recognized effector, leading to downstream defense activation.
Li, M., Zhang, H., Xiao, H., Zhu, K., Shi, W., Zhang, D., Wang, Y., Yang, L., Wu, Q., Xie, J. and Chen, Y.
Nature Communications, 15(1), p.3124, 2024
Abstract
Crop wild relatives offer natural variations of disease resistance for crop improvement. Here, we report the isolation of broad-spectrum powdery mildew resistance gene Pm36, originated from wild emmer wheat, that encodes a tandem kinase with a transmembrane domain (WTK7-TM) through the combination of map-based cloning, PacBio SMRT long-read genome sequencing, mutagenesis, and transformation. Mutagenesis assay reveals that the two kinase domains and the transmembrane domain of WTK7-TM are critical for the powdery mildew resistance function. Consistently, in vitro phosphorylation assay shows that two kinase domains are indispensable for the kinase activity of WTK7-TM. Haplotype analysis uncovers that Pm36 is an orphan gene only present in a few wild emmer wheat, indicating its single ancient origin and potential contribution to the current wheat gene pool. Overall, our findings not only provide a powdery mildew resistance gene with great potential in wheat breeding but also sheds light into the mechanism underlying broad-spectrum resistance.
Govta, N., Fatiukha, A., Govta, L., Pozniak, C., Distelfeld, A., Fahima, T., Beckles, D. and Krugman, T.
PREPRINT (Version 1) available at Research Square [https://doi.org/10.21203/rs.3.rs-3979153/v1], 2023
Abstract
Nitrogen (N) is an essential macronutrient for wheat growth and development, its deficiency negatively affects grain yield and grain protein content (GPC). We describe here the dissection of the high grain protein content (GPC) QTL (QGpc.huj.uh-5B.2) derived from chromosome 5B of tetraploid wild emmer wheat, after its introgression into bread wheat (Ruta) by marker assisted selection. The introgression line (IL99) grown for trait validation under three environments, had 33% higher GPC (p<0.05) compared to Ruta, only under low (LN) at the seedling stage. The pleiotropic effect of the QTL on tolerance to N deficiency was confirmed using a semi-hydroponic system under severe LN (10% N) at the seedlings stage. We further dissected the QTL by fine mapping which enabled to delimit the QTL region from ~ 28.55 Mb to a chromosomal segment of only ~ 1.29 Mb that was shared among 12 LN tolerant near-isogenic lines, and which all had the WEW haplotype. This region included 13 potential candidate genes for LN tolerance, annotated as associated with N-stress response (15-cis-ZETA-CAROTENE ISOMERASE), N transport (UREIDE PERMEASE1 and IMPORTIN SUBUNIT BETA-1), and six involved in stress responses (e.g., ATXR6, HISTONE-LYSINE N-METHYLTRANSFERASE), while two genes were uncharacterized. These candidate genes may improve tolerance to nitrogen deficiency and by extension, high nitrogen use efficiency and GPC in N deficient environments. Our study demonstrates the importance of WEW as a source of novel variation for genes and QTLs useful for a sustainable improvement tolerance to N deficiency in wheat.
Li Y., Wei Z.Z., Sela H., Govta L., Klymiuk V., Roychowdhury R., Chawla H.S., Ens J., Wiebe K., Bocharova V., Ben-David R., Pawar P.B., Zhang Y., Jaiwar S., Molnár I., Doležel J., Coaker G., Pozniak C.J., Fahima T.
Plant Communications, 100660, 2023
Abstract
Gene cloning in repeat-rich polyploid genomes remains challenging. Here, we describe a strategy for overcoming major bottlenecks in cloning of the powdery mildew resistance gene (R-gene) Pm69 derived from tetraploid wild emmer wheat. A conventional positional cloning approach was not effective owing to suppressed recombination. Chromosome sorting was compromised by insufficient purity. A Pm69 physical map, constructed by assembling Oxford Nanopore Technology (ONT) long-read genome sequences, revealed a rapidly evolving nucleotide-binding leucine-rich repeat (NLR) R-gene cluster with structural variations. A single candidate NLR was identified by anchoring RNA sequencing reads from susceptible mutants to ONT contigs and was validated by virus-induced gene silencing. Pm69 is likely a newly evolved NLR and was discovered in only one location across the wild emmer wheat distribution range in Israel. Pm69 was successfully introgressed into cultivated wheat, and a diagnostic molecular marker was used to accelerate its deployment and pyramiding with other R-genes.
Li Y., Roychowdhury R., Govta L., Jaiwar S., Wei Z.-Z., Shams I., Fahima T.
Phytopathology, 113:5, 884-892, 2023
Abstract
Reactive oxygen species (ROS)- and hypersensitive response (HR)-mediated cell death have long been known to play critical roles in plant immunity to pathogens. Wheat powdery mildew caused by Blumeria graminis f. sp. tritici (Bgt) is a destructive wheat pathogen. Here, we report a quantitative analysis of the proportion of infected cells with local apoplastic ROS (apoROS) versus intracellular ROS (intraROS) accumulation in various wheat accessions that carry different disease resistance genes (R genes) at a series of time points postinfection. The proportion of apoROS accumulation was 70 to 80% of the infected wheat cells detected in both compatible and incompatible host−pathogen interactions. However, intensive intraROS accumulation followed by localized cell death responses was detected in 11 to 15% of the infected wheat cells, mainly in wheat lines that carried nucleotide-binding leucine-rich repeat R genes (e.g., Pm3F, Pm41, TdPm60, MIIW72, and Pm69). The lines that carry unconventional R genes, Pm24 (Wheat Tandem Kinase 3) and pm42 (a recessive R gene), showed fewer intraROS responses, whereas 11% of Pm24 line-infected epidermis cells still showed HR cell death, suggesting that different resistance pathways are activated there. Here, we also demonstrated that ROS could not act as a strong systemic signal for inducing high resistance to Bgt in wheat, although it induced the expression of pathogenesis-related genes. These results provide new insights into the contribution of intraROS and localized cell death to immune responses against wheat powdery mildew.
Pathogen perception and deception in plant immunity by kinase fusion proteins
Fahima T., Coaker G.
Nature Genetics volume: 55, 908–909, 2023
Abstract
Two studies describe kinase fusion proteins (KFPs) that regulate the perception and deception of wheat pathogens. These highlight the emergence of KFPs as plant immune regulators and emphasize the importance of crop wild relatives as a reservoir for resistance breeding and global food security.
Advances in crop resistance breeding using modern genomic tools
Huang L., Li Y., Chen S., Periyannan S., Fahima T.
Frontiers in Plant Science: Vol. 14: 1143689, 2023
Abstract
Plant diseases constitute a major threat to global crop production and food security. Plants respond to pathogens using a two-tier innate immune system triggered by both cell-surface-localized pattern-recognition receptors (PRRs) and intracellular nucleotide-binding leucine-rich repeat receptors (NLRs)(reviewed by Zhou and Zhang, 2020; Ngou et al., 2022). The deployment of immune receptors to breed disease-resistant cultivars is an effective and sustainable approach to controlling crop diseases. However, it largely relies on the ability to identify and transfer novel and useful resistance (R) genes rapidly from the source to commercial crop varieties. Over the last two decades, with advances in DNA sequencing, molecular marker, and genotyping techniques, remarkable progress has been made in the identification of R-genes both from crop species and their wild relatives. Subsequently, novel strategies have been implemented through the in-depth understanding of the R-gene-mediated resistance mechanisms and the ability to transfer R-genes rapidly into commercial cultivars.
Dosage differences in 12-OXOPHYTODIENOATE REDUCTASE genes modulate wheat primary root growth
Gabay G., Wang H., Zhang J., Moriconi J., Burguener G.F., Howell T.R., Lukaszewski A., Staskawicz B., Cho M.-J., Tanaka J., Fahima T., Ke H., Dehesh K., Zhang G.-L., Gou J.-Y., Hamberg M., Santa Maria G.E., Dubcovsky J.
Nature Communications: Vol. 14, 539, 2023
Abstract
Wheat, an essential crop for global food security, is well adapted to a wide variety of soils. However, the gene networks shaping different root architectures remain poorly understood. We report here that dosage differences in a cluster of monocot-specific 12-OXOPHYTODIENOATE REDUCTASE genes from subfamily III (OPRIII) modulate key differences in wheat root architecture, which are associated with grain yield under water-limited conditions. Wheat plants with loss-of-function mutations in OPRIII show longer seminal roots, whereas increased OPRIII dosage or transgenic over-expression result in reduced seminal root growth, precocious development of lateral roots and increased jasmonic acid (JA and JA-Ile). Pharmacological inhibition of JA-biosynthesis abolishes root length differences, consistent with a JA-mediated mechanism. Transcriptome analyses of transgenic and wild-type lines show significant enriched JA-biosynthetic and reactive oxygen species (ROS) pathways, which parallel changes in ROS distribution. OPRIII genes provide a useful entry point to engineer root architecture in wheat and other cereals.
Sung Y.C., Zhu J., Li Y., Fahima T., Coaker G.L.
Phytopathology: 112(11), 169-170, 2023
Long-read genome sequencing accelerated the cloning of Pm69 by resolving the complexity of a rapidly evolving resistance gene cluster in wheat
Li Y., Wei Z., Sela H., Govta L., Klymiuk V., Roychowdhury R., Chawla H.S., Ens J., Wiebe K., Bocharova V., Ben-David R., Pawar P.B., Jaiwar S., Molnar I., Dolezel J., Pozniak C.J., Fahima T.
bioRxiv; DOI: 10.1101/2022.10.14.512294. 2022
Abstract
Gene cloning in repeat-rich polyploid genomes remains challenging. Here we describe a strategy for overcoming major bottlenecks in the cloning of the powdery mildew (Pm) resistance gene (R-gene) Pm69 derived from tetraploid wild emmer wheat (WEW). A conventional positional cloning approach encountered suppressed recombination due to structural variations, while chromosome sorting yielded an insufficient purity level. A Pm69 physical map, constructed by assembling ONT long-read genome sequences, revealed a rapidly evolving nucleotide-binding leucine-rich repeat (NLR) R-gene cluster. A single candidate NLR was identified within this cluster by anchoring RNASeq reads of susceptible mutants to ONT contigs and was validated by the virus-induced gene silencing (VIGS) approach. Pm69, comprising Rx_N with RanGAP interaction sites, NB-ARC, and LRR domains, is probably a newly evolved NLR discovered only in one location across the WEW distribution range in the Fertile Crescent. Pm69 was successfully introgressed into durum and bread wheat, and a diagnostic molecular marker could be used to accelerate its deployment and pyramiding with other resistance genes.
Wu Q., Chen Y., Li B., Li J., Zhang P., Xie J., Zhang H., Guo G., Lu P., Li M., Zhu K., Li W., Fahima T., Nevo E., Li H., Dong L., Liu Z.
Journal of Genetics and Genomics, 49(8): pp. 787-795, 2022
Abstract
Wild emmer wheat (Triticum dicoccoides, WEW) is an immediate progenitor of both the cultivated tetraploid and hexaploid wheats and it harbors rich genetic diversity against powdery mildew caused by Blumeria graminis f. sp. tritici (Bgt). A powdery mildew resistance gene MlIW172 originated from WEW accession IW172 (G-797-M) was fine mapped in a 0.048 centimorgan (cM) genetic interval on 7AL, corresponding to a genomic region spanning 233 kb, 1 Mb and 800 kb in Chinese Spring, WEW Zavitan, and T. urartu G1812, respectively. MlIW172 was found to encode a typical NLR protein NLRIW172 and physically located in an NBS-LRR gene cluster. NLRIW172 was subsequently identified as a new allele of Pm60, and its function was validated by EMS mutagenesis and transgenic complementation. Haplotype analysis of the Pm60 alleles revealed diversifications in sequence variation in the locus and PAV (presence and absence variations) in WEW populations. Four common single nucleotide variations (SNV) were detected between the Pm60 alleles from WEW and T. urartu, indicative of speciation divergence between the two different wheat progenitors. The newly identified Pm60 alleles and haplotypes in WEW are anticipated to be valuable for breeding powdery mildew resistance wheat cultivars via marker-assisted selection.
Detection of crop diseases using enhanced variability imagery data and convolutional neural networks
Kendler Sh., Aharoni R., Young S., Sela H.,Kis-Papo T., Fahima T., Fishbain B.
Computers and Electronics in Agriculture, Vol. 193:106732, 2022
Abstract
The timely detection of crop diseases is critical for securing crop productivity, lowering production costs, and minimizing agrochemical use. This study presents a crop disease identification method that is based on Convolutional Neural Networks (CNN) trained on images taken with consumer-grade cameras. Specifically, this study addresses the early detection of wheat yellow rust, stem rust, powdery mildew, potato late blight, and wild barley net blotch. To facilitate this, pictures were taken in situ without modifying the scene, the background, or controlling the illumination. Each image was then split into several patches, thus retaining the original spatial resolution of the image while allowing for data variability. The resulting dataset was highly diverse since the disease manifestation, imaging geometry, and illumination varied from patch to patch. This diverse dataset was used to train various CNN architectures to find the best match. The resulting classification accuracy was 95.4 ± 0.4%. These promising results lay the groundwork for autonomous early detection of plant diseases. Guidelines for implementing this approach in realistic conditions are also discussed.
Li Y., Wei Z.Z., Fatiukha A., Jaiwar S., Wang H., Hasan S., Liu Z., Sela H., Krugman T., Fahima T.
Theoretical and applied Genetics, 134(10): 3489-3489, 2021
Abstract
Wild emmer wheat (WEW), the tetraploid progenitor of durum and bread wheat, is a valuable genetic resource for resistance to powdery mildew fungal disease caused by Blumeria graminis f. sp. tritici (Bgt). PmG16 gene, derived from WEW, confers high resistance to most tested Bgt isolates. We mapped PmG16 to a 1.4-cM interval between the flanking markers uhw386 and uhw390 on Chromosome 7AL. Based on gene annotation of WEW reference genome Zavitan_V1, 34 predicted genes were identified within the ~ 3.48-Mb target region. Six genes were annotated as associated with disease resistance, of which TRIDC7AG077150.1 was found to be highly similar to Pm60, previously cloned from Triticum urartu, and resides in the same syntenic region. The functional molecular marker (FMM) for Pm60 (M-Pm60-S1) co-segregated with PmG16, suggesting the Pm60 ortholog from WEW (designated here as TdPm60) as a strong candidate for PmG16. Sequence alignment identified only eight SNPs that differentiate between TdPm60 and TuPm60. Furthermore, TdPm60 was found to be present also in the WEW donor lines of the powdery mildew resistance genes MlIW172 and MlIW72, mapped to the same region of Chromosome 7AL as PmG16, suggesting that TdPm60 constitutes a candidate also for these genes. Furthermore, screening of additional 230 WEW accessions with Pm60 specific markers revealed 58 resistant accessions from the Southern Levant that harbored TdPm60, while none of the susceptible accessions showed the presence of this gene. Deployment of PmG16 in Israeli modern bread wheat cultivar Ruta conferred resistance against several local Bgt isolates.
Tandem protein kinases emerge as new regulators of plant immunity
Klymiuk V., Coaker G., Fahima T., Pozniak C.J.
Molecular Plant-Microbe Interactions, 34(10): 1094-1102, 2021
Abstract
Plant–pathogen interactions result in disease development in a susceptible host. Plants actively resist pathogens via a complex immune system comprising both surface-localized receptors that sense the extracellular space as well as intracellular receptors recognizing pathogen effectors. To date, the majority of cloned resistance genes encode intracellular nucleotide-binding leucine-rich repeat receptor proteins. Recent discoveries have revealed tandem kinase proteins (TKPs) as another important family of intracellular proteins involved in plant immune responses. Five TKP genes—barley Rpg1 and wheat WTK1 (Yr15), WTK2 (Sr60), WTK3 (Pm24), and WTK4—protect against devastating fungal diseases. Moreover, a large diversity and numerous putative TKPs exist across the plant kingdom. This review explores our current knowledge of TKPs and serves as a basis for future studies that aim to develop and exploit a deeper understanding of innate plant immunity receptor proteins.
Zhang Q., Li Y., Li Y., Fahima T., Shen Q., Xie C.
Pathogens, 11(1):25, 2021
Abstract
Powdery mildew, caused by the fungus Blumeria graminis f. sp. tritici (Bgt), has limited wheat yields in many major wheat-production areas across the world. Introducing resistance genes from wild relatives into cultivated wheat can enrich the genetic resources for disease resistance breeding. The powdery mildew resistance gene Pm60 was first identified in diploid wild wheat Triticum urartu (T. urartu). In this study, we used durum as a ‘bridge’ approach to transfer Pm60 and Pm60b into hexaploid common wheat. Synthetic hexaploid wheat (SHW, AABBAuAu), developed by crossing T. urartu (AuAu) with durum (AABB), was used for crossing and backcrossing with common wheat. The Pm60 alleles were tracked by molecular markers and the resistance to powdery mildew. From BC1F1 backcross populations, eight recombinant types were identified based on five Pm60-flanking markers, which indicated different sizes of the introgressed chromosome segments from T. urartu. Moreover, we have selected two resistance-harboring introgression lines with high self-fertility, which could be easily used in wheat breeding system. Our results showed that the durum was an excellent ‘bridge’ for introducing the target gene from diploid T. urartu into the hexaploid cultivated wheat. Moreover, these introgression lines could be deployed in wheat resistance breeding programs, together with the assistance of the molecular markers for Pm60 alleles.
Rybnikov S., Frenkel Z., Korol A.B., Fahima T.
Pathogens, 10(7): 898, 2021
Abstract
Antagonistic interactions and co-evolution between a host and its parasite are known to cause oscillations in the population genetic structure of both species (Red Queen dynamics). Potentially, such oscillations may select for increased sex and recombination in the host, although theoretical models suggest that this happens under rather restricted values of selection intensity, epistasis, and other parameters. Here, we explore a model in which the diploid parasite succeeds to infect the diploid host only if their phenotypes at the interaction-mediating loci match. Whenever regular oscillations emerge in this system, we test whether plastic, pathogen-inducible recombination in the host can be favored over the optimal constant recombination. Two forms of the host recombination dependence on the parasite pressure were considered: either proportionally to the risk of infection (prevention strategy) or upon the fact of infection (remediation strategy). We show that both forms of plastic recombination can be favored, although relatively infrequently (up to 11% of all regimes with regular oscillations, and up to 20% of regimes with obligate parasitism). This happens under either strong overall selection and high recombination rate in the host, or weak overall selection and low recombination rate in the host. In the latter case, the system’s dynamics are considerably more complex. The prevention strategy is favored more often than the remediation one. It is noteworthy that plastic recombination can be favored even when any constant recombination is rejected, making plasticity an evolutionary mechanism for the rescue of host recombination.
Wu Q., Zhao F., Chen Y., Zhang P., Zhang H., Guo G., Xie J., Dong L., Lu P., Li M., Ma S., Fahima T., Nevo E., Li H., Zhang Y., Liu Z.
Plant Biotechnology Journal: 1288-1290, 2021
Gabay G., Zhang J., Burguener G.F., Howell T., Wang H., Fahima T., Lukaszewski A., Moriconi J.I., Santa Maria G.E., Dubcovsky, J.
The Plant Genome, e20079, 2021
Abstract
Good understanding of the genes controlling root development is required to engineer root systems better adapted to different soil types. In wheat (Triticum aestivum L.), the 1RS.1BL wheat-rye (Secale cereale L.) translocation has been associated with improved drought tolerance and a large root system. However, an isogenic line carrying an interstitial segment from wheat chromosome arm 1BS in the distal region of the 1RS arm (1RSRW ) showed reduced grain yield and shorter roots both in the field and in hydroponic cultures relative to isogenic lines with the complete 1RS arm. In this study, we used exome capture to characterize 1RSRW and its parental lines T-9 and 1B+40. We show that 1RSRW has a 7.0 Mb duplicated 1RS region and a 4.8 Mb 1BS insertion colinear with the 1RS duplication, resulting in triplicated genes. Lines homozygous for 1RSRW have short seminal roots, while lines heterozygous for this chromosome have roots of intermediate length. By contrast, near-isogenic lines carrying only the 1BS distal region or the 1RS-1BS duplication have long seminal roots similar to 1RS, suggesting a limited effect of the 1BS genes. These results suggest that the dosage of duplicated 1RS genes is critical for seminal root length. An induced deletion encompassing 38 orthologous wheat and rye duplicated genes restored root length and confirmed the importance of gene dosage in the short-root phenotype. We explored the expression profiles and functional annotation of these genes and discuss their potential as candidate genes for the regulation of seminal root length in wheat.
Genomic Architecture of Phenotypic Plasticity in Response to Water Stress in Tetraploid Wheat
Fatiukha A., Deblieck M., Klymiuk V., Merchuk-Ovnat L., Peleg Z., Ordon F., Fahima T., Korol A., Saranga Y., Krugman T.
International Journal of Molecular Sciences, 22(4): 1723, 2021
Abstract
Phenotypic plasticity is one of the main mechanisms of adaptation to abiotic stresses via changes in critical developmental stages. Altering flowering phenology is a key evolutionary strategy of plant adaptation to abiotic stresses, to achieve the maximum possible reproduction. The current study is the first to apply the linear regression residuals as drought plasticity scores while considering the variation in flowering phenology and traits under non-stress conditions. We characterized the genomic architecture of 17 complex traits and their drought plasticity scores for quantitative trait loci (QTL) mapping, using a mapping population derived from a cross between durum wheat (Triticum turgidum ssp. durum) and wild emmer wheat (T. turgidum ssp. dicoccoides). We identified 79 QTLs affected observed traits and their plasticity scores, of which 33 reflected plasticity in response to water stress and exhibited epistatic interactions and/or pleiotropy between the observed and plasticity traits. Vrn-B3 (TaTF1) residing within an interval of a major drought-escape QTL was proposed as a candidate gene. The favorable alleles for most of the plasticity QTLs were contributed by wild emmer wheat, demonstrating its high potential for wheat improvement. Our study presents a new approach for the quantification of plant adaptation to various stresses and provides new insights into the genetic basis of wheat complex traits under water-deficit stress.
The Wild Emmer Wheat Gene PmG16, Conferring Resistance to Powdery Mildew, is an Orthologue of Pm60 from Triticum Urartu
Li Y., Wei Z., Fatiukha A., Jaiwar S., Wang H., Hasan S., Liu Z., Sela H., Krugman T., Fahima T.
Preprint, DOI:10.21203/rs.3.rs-166805/v1, 2021
Abstract
Wild emmer wheat (WEW), the tetraploid progenitor of durum and bread wheat, is a valuable genetic resource for resistance to powdery mildew fungal disease caused by Blumeria graminis f. sp. tritici (Bgt). PmG16 gene, derived from WEW, confers high resistance to most tested Bgt isolates. We mapped PmG16 to a 1.4 cM interval between the anking markers uhw386 and uhw390 on Chromosome 7AL. Based on gene annotation of WEW reference genome Zavitan_V1, 34 predicted genes were identi ed within the~ 3.48 Mb target region. Six genes were annotated as associated with disease resistance, of which TRIDC7AG077150. 1 was found to be highly similar to Pm60, previously cloned from Triticum urartu and residing in the same syntenic region. A functional molecular marker (FMM) for Pm60 (M-Pm60-S1) cosegregated with PmG16, suggesting that WEW PmG16 is probably an orthologue of Pm60 from Triticum urartu (designated here as TdPm60). Sequence alignment identi ed only eight SNPs that differentiate between TdPm60 and TuPm60. Furthermore, our results suggest that other WEW powdery mildew resistance genes MlIW172 and MlIW72, that also mapped to the same region of Chromosome 7AL, might be identical or allelic to TdPm60. Screening of 230 WEW accessions with Pm60 speci c markers, 58 resistant accessions were identi ed from Southern Levant harboring the TdPm60 allele, while all the susceptible accessions showed no PCR ampli cations. Deployment of TdPm60 is clearly more advantageous over TuPm60 since it can be rapidly introgressed by classical breeding approaches into bread wheat genetic background.
Liang Y., Chen Y.X., Li D.Q., Cheng J.P., Zhao G., Fahima T., Yan J.
JAPS, Journal of Animal and Plant Sciences, 31(1): 188-202, 2021
Abstract
Mineral nutrient malnutrition, especially deficiency of selenium (Se) affects the health of approximately one billion people worldwide. Wild emmer wheat (Triticum turgidum ssp. dicoccoides), the progenitor of common wheat, harbors a rich genetic diversity for mineral nutrients. The study was conducted on two wild emmer wheat genotypes differing in Se tolerance (R113, Se-sensitive; R171, Se-tolerant) with 2 Se application methods and 3 Se levels (foliar rates of 0, 11.5 and 23 mg.L-1; fertigation rates of 0, 5 and 10 mg.kg-1) in 2017 having 5 replications, at an experimental farm, Sichuan Province, China. It evaluated the effects of Se application on wild emmer wheat growth, grain yield and quality, and 14 other trace elements absorption and translocation in sink-source organs (flag leaves, husks and grains). The results showed that both foliar Se and fertigated Se application methods increased Se contents in sink-source organs, wheat health benefits and yield, while the foliar application was more effective than fertigation. Moreover, two Se application methods decreased toxic trace elements (Pb, Al, As, Li and Cd) contents in wheat, indicating a possible antagonistic effect. Accordingly, this study provided useful information concerning agronomic biofortification of wheat, indicating that it is feasible to apply Se in fertilization programmes to inhibit the heavy metal elements contents and improve yield and quality in agricultural crops. The higher Se, Fe, Zn and Mo contents found in R171 suggested that its germplasm conferred higher abilities for mineral uptake and accumulation, which can be used for genetic studies of wheat nutritional value and for further improvement of domesticated cereals.
Spectral light-reflection data dimensionality reduction for timely detection of yellow rust
Aharoni, R., Klymiuk, V., Sarusi, B., Young, S., Fahima, T., Fishbain, B., Kendler, S.
Precision Agriculture, 22(1), 267-286, 2021
Abstract
Yellow rust (YR) wheat disease is one of the major threats to worldwide wheat production, and it often spreads rapidly to new and unexpected geographic locations. To cope with this threat, integrated pathogen management strategies combine disease-resistant plants, sensors monitoring technologies, and fungicides either preventively or curatively, which come with their associated monetary and environmental costs. This work presents a methodology for timely detection of YR that cuts down on hardware and computational requirements. It enables frequent detailed monitoring of the spread of YR, hence providing the opportunity to better target mitigation efforts which is critical for successful integrated disease management. The method is trained to detect YR symptoms using reflectance spectrum (VIS–NIR) and a classification algorithm at different stages of YR development to distinguish them from typical defense responses occurring in resistant wheat. The classification method was trained and tested on four different spectral datasets. The results showed that using a full spectral range, a selection of the top 5% significant spectral features, or five typical multispectral bands for early detection of YR in infected plants yielded a true positive rate of ~ 86%, for infected plants. The same data analysis with digital camera bands provided a true positive rate of 77%. These findings lay the groundwork for the development of high-throughput YR screening in the field implementing multispectral digital camera sensors that can be mounted on autonomous vehicles or a drone as part of an integrated disease management scheme
Wheat genomics and breeding: bridging the gap
Hussain B., Akpınar B.A., Alaux M., Algharib A.M., Sehgal D., Ali Z., Appels R., Aradottir G.I., Batley J., Bellec A., Bentley A.R., Cagirici H.B., Cattivelli L., Choulet F., Cockram J., Desiderio F., Devaux P., Dogramaci M., Dorado G., Dreisigacker S., Edwards D., El-Hassouni K., Eversole K., Fahima T., Figueroa M., Gálvez S., Gill K.S., Govta L., Gul A., Hensel G., Hernandez P., Herrera L.C., Ibrahim A., Kilian B., Korzun V., Krugman T., Li YingHui, Liu ShuYu, Mahmoud A.F., Morgounov A., Muslu T., Naseer, F., Ordon, F., Paux, E., Perovic, D., Reddy, G.V.P., Reif, J.C., Reynolds, M., Roychowdhury, R., Rudd, J., Sen, T.Z., Sukumaran S., Tiwari V.K., Ullah N., Unver T., Yazar S., Buda, H.
AgriRxiv, 2021
Abstract
Recent technological advances in next-generation sequencing (NGS) technologies have dramatically reduced the cost of DNA sequencing, allowing species with large and complex genomes to be sequenced. Although bread wheat (Triticum aestivum L.) is one of the world's most important food crops, until very recently efficient exploitation of molecular marker-assisted breeding approaches has lagged behind that achieved in other crop species due to its large polyploid genome. However, an international public-private effort spanning nine years reported over 65% draft genome of bread wheat in 2014, and finally, after more than a decade culminated in the release of a gold-standard, fully annotated reference wheat genome assembly in 2017. Shortly thereafter, in 2020, the genome of assemblies of additional fifteen global wheat accessions were released. Wheat has now entered into the pan-genomic era where basic resources can be efficiently exploited. Wheat genotyping with a few hundred markers has been replaced by genotyping arrays capable of genotyping hundreds of wheat lines using thousands of markers, providing fast, relatively inexpensive, and reliable data for exploitation in wheat breeding. These advances have opened up a new horizon for marker-assisted selection (MAS) and genomic selection (GS) in wheat. Herein, we review the advances and perspectives in wheat genetics and genomics, with a focus on key traits including grain yield, yield-related traits, end-use quality and resistance to biotic and abiotic stresses. We also enlisted several reported candidate and cloned candidate genes responsible for the aforesaid traits of interest. Furthermore, we report on the improvement in the aforementioned quantitative traits through the use of (i) clustered regularly interspaced short palindromic repeats/CRISPR-associated protein 9 (CRISPR/Cas9) mediated gene-editing, (ii) positional cloning methods, and of genomic selection. Finally, we make recommendations on the utilization of genomics for the next-generation wheat breeding and provide a practical example of using the latest, in silico bioinformatics tools that were based on the wheat reference genome sequence.
A CNL protein in wild emmer wheat confers powdery mildew resistance
Li M., Dong L., Li B., Wang Z., Xie J., Qiu D., Li Y., Shi W., Yang L., Wu Q., Chen Y., Lu P., Guo G., Zhang H., Zhang P., Zhu K, Li Y., Zhang Y., Wang R., Yuan C., Liu W., Yu D., Luo M.C., Fahima T., Nevo E., Li H., Liu, Z.
New Phytologist, 228(3): 1027-1037, 2020
Abstract
Powdery mildew, a fungal disease caused by Blumeria graminis f. sp. tritici (Bgt), has a serious impact on wheat production. Loss of resistance in cultivars prompts a continuing search for new sources of resistance. Wild emmer wheat (Triticum turgidum ssp. dicoccoides, WEW), the progenitor of both modern tetraploid and hexaploid wheats, harbors many powdery mildew resistance genes. We report here the positional cloning and functional characterization of Pm41, a powdery mildew resistance gene derived from WEW, which encodes a coiled-coil, nucleotide-binding site and leucine-rich repeat protein (CNL). Mutagenesis and stable genetic transformation confirmed the function of Pm41 against Bgt infection in wheat. We demonstrated that Pm41 was present at a very low frequency (1.81%) only in southern WEW populations. It was absent in other WEW populations, domesticated emmer, durum, and common wheat, suggesting that the ancestral Pm41 was restricted to its place of origin and was not incorporated into domesticated wheat. Our findings emphasize the importance of conservation and exploitation of the primary WEW gene pool, as a valuable resource for discovery of resistance genes for improvement of modern wheat cultivars.
Liang Y., Li D., Chen Y., Cheng J., Zhao G., Fahima T., Yan J.
3 Biotech 10 (8): 1-14, 2020
Abstract
Hydroponic experiments were conducted to investigate the effects of different concentrations of sodium selenate (Na2SeO4) and sodium selenite (Na2SeO3) on durum wheat seed germination and seedling growth under salt stress. The treatments used were 0 and 50 mM NaCl solutions, each supplemented with Na2SeO4 or Na2SeO3 at 0, 0.1, 1, 2, 4, 8, or 10 μM. Salt alone significantly inhibited seed germination and reduced seedling growth. Addition of low concentrations (0.1-4 μM) of Na2SeO4 or Na2SeO3 mitigated the adverse effects of salt stress on seed germination, biomass accumulation, and other physiological attributes. Among them, 1 μM Na2SeO4 was most effective at restoring seed germination rate, germination energy, and germination index, significantly increasing these parameters by about 12.35, 24.17, and 11.42%, respectively, compared to salt-stress conditions. Adding low concentrations of Na2SeO4 or Na2SeO3 to the salt solution also had positive effects on chlorophyll fluorescence indices, decreased the concentrations of free proline and malondialdehyde, as well as electrolyte leakage, and increased catalase, superoxide dismutase, and peroxidase activities in roots and shoots. However, high concentrations (8-10 μM) of Na2SeO4 or Na2SeO3 disrupted seed germination and seedling growth, with damage caused by Na2SeO3 being more severe than that by Na2SeO4. It is thus clear that exogenous selenium can improve the adaptability of processing wheat to salt stress and maintain higher photosynthetic rate by decreasing the accumulation of reactive oxygen species and alleviating the degree of membrane lipid peroxidation. Na2SeO4 was more effective than Na2SeO3 at all given concentrations.
Wei Z.Z., Klymiuk V., Bocharova V., Pozniak C., Fahima T.
Pathogens, 9(6): 418, 2020
Abstract
The destructive wheat powdery mildew disease is caused by the fungal pathogen Blumeria graminis f. sp. tritici (Bgt). PmG3M, derived from wild emmer wheat Triticum dicoccoides accession G305-3M, is a major gene providing a wide-spectrum resistance against Bgt. PmG3M was previously mapped to wheat chromosome 6B using an F6 recombinant inbred line (RIL) mapping population generated by crossing G305-3M with the susceptible T. durum wheat cultivar Langdon (LDN). In the current study, we aimed to explore the defense mechanisms conferred by PmG3M against Bgt. Histopathology of fungal development was characterized in artificially inoculated leaves of G305-3M, LDN, and homozygous RILs using fluorescence and light microscopy. G305-3M exhibited H2O2 accumulation typical of a hypersensitive response, which resulted in programmed cell death (PCD) in Bgt-penetrated epidermal cells, while LDN showed well-developed colonies without PCD. In addition, we observed a post-haustorial resistance mechanism that arrested the development of fungal feeding structures and pathogen growth in both G305-3M and resistant RIL, while LDN and a susceptible RIL displayed fully developed digitated haustoria and massive accumulation of fungal biomass. In contrast, both G305-3M and LDN exhibited callose deposition in attempt to prevent fungal invasion, supporting this as a mechanism of a basal defense response not associated with PmG3M resistance mechanism per se. The presented results shed light on the resistance mechanisms conferred by PmG3M against wheat powdery mildew.
Li Y., Qiu L., Liu X., Zhang Q., Zhuansun X., Fahima T., Krugman T., Sun Q., Xie C.
International Journal of Molecular Sciences, 21(2): 673, 2020
Abstract
Our previous study indicated that glycerol application induced resistance to powdery mildew (Bgt) in wheat by regulating two important signal molecules, glycerol-3-phosphate (G3P) and oleic acid (OA18:1). Transcriptome analysis of wheat leaves treated by glycerol and inoculated with Bgt was performed to identify the activated immune response pathways. We identified a set of differentially expressed transcripts (e.g., TaGLI1, TaACT1, and TaSSI2) involved in glycerol and fatty acid metabolism that were upregulated in response to Bgt infection and might contribute to G3P and OA18:1 accumulation. Gene Ontology (GO) enrichment analysis revealed GO terms induced by glycerol, such as response to jasmonic acid (JA), defense response to bacterium, lipid oxidation, and growth. In addition, glycerol application induced genes (e.g., LOX, AOS, and OPRs) involved in the metabolism pathway of linolenic and alpha-linolenic acid, which are precursor molecules of JA biosynthesis. Glycerol induced JA and salicylic acid (SA) levels, while glycerol reduced the auxin (IAA) level in wheat. Glycerol treatment also induced pathogenesis related (PR) genes, including PR-1, PR-3, PR-10, callose synthase, PRMS, RPM1, peroxidase, HSP70, HSP90, etc. These results indicate that glycerol treatment regulates fatty acid metabolism and hormones cross-talk and induces the expression of PR genes that together contribute to Bgt resistance in wheat.
Three previously characterized resistances to yellow rust are encoded by a single locus Wtk1
Klymiuk V., Fatiukha A., Raats D., Bocharova V., Huang L., Feng L., Jaiwar S., Pozniak C., Coaker G., Dubcovsky J., Fahima T.
Journal of experimental botany, 71(9): 2561-2572, 2020
Abstract
The wild emmer wheat (Triticum turgidum ssp. dicoccoides; WEW) yellow (stripe) rust resistance genes Yr15, YrG303, and YrH52 were discovered in natural populations from different geographic locations. They all localize to chromosome 1B but were thought to be non-allelic based on differences in resistance response. We recently cloned Yr15 as a Wheat Tandem Kinase 1 (WTK1) and show here that these three resistance loci co-segregate in fine-mapping populations and share an identical full-length genomic sequence of functional Wtk1. Independent ethyl methanesulfonate (EMS)- mutagenized susceptible yrG303 and yrH52 lines carried single nucleotide mutations in Wtk1 that disrupted function. A comparison of the mutations for yr15, yrG303, and yrH52 mutants showed that while key conserved residues were intact, other conserved regions in critical kinase subdomains were frequently affected. Thus, we concluded that Yr15-, YrG303-, and YrH52-mediated resistances to yellow rust are encoded by a single locus, Wtk1. Introgression of Wtk1 into multiple genetic backgrounds resulted in variable phenotypic responses, confirming that Wtk1-mediated resistance is part of a complex immune response network. WEW natural populations subjected to natural selection and adaptation have potential to serve as a good source for evolutionary studies of different traits and multifaceted gene networks.
Durum wheat as a bridge between wild emmer wheat genetic resources and bread wheat
Klymiuk V., Fatiukha A., Huang L., Wei Z.Z., Kis-Papo T., Saranga Y., Krugman T., Fahima T.
Application of Genetic and Genomic Research in Cereals. Woodhead Publishing (An imprint of Elsevier): 201–230, 2019
Abstract
The primary stages of domestication and consequent polyploidization processes of bread wheat (Triticum aestivum, BBAADD) have diminished the genetic diversity within cultivated wheat germplasm. Wild emmer wheat (Triticum dicoccoides, BBAA), the progenitor of wheat, is a promising source for beneficial agronomical traits; however, introgression of such alleles into bread wheat was hampered by various factors, such as necrosis in F1 pentaploid hybrids, failed seedling establishment, and frequent sterility. Therefore, we suggest to utilize durum wheat (Triticum durum, BBAA) as a bridge for transferring favorable alleles into bread wheat. We propose to screen wild emmer germplasm for valuable traits, cross promising accessions with durum varieties, confirm the phenotype in segregating populations, map the target gene(s)/quantitative trait loci (QTLs), and use marker-assisted selection for introgression into bread wheat. Here, we discuss the proposed concept and provide examples of successful transfer of traits such as drought resistance, high grain protein, resistance to stripe rust, powdery mildew, and fusarium head blight.
A wheat/rye polymorphism affects seminal root length and yield across different irrigation regimes
Howell T., Moriconi J. I., Zhao X., Hegarty J., Fahima T., Santa-Maria G. E., Dubcovsky J.
Journal of Experimental Botany, 70: 4027-4037, 2019
Abstract
The introgression of a small segment of wheat (Triticum aestivum L.) chromosome arm 1BS in the distal region of the rye (Secale cereale L.) 1RS.1BL arm translocation in wheat (henceforth 1RSRW) was previously associated with reduced grain yield, carbon isotope discrimination, and stomatal conductance, suggesting reduced access to soil moisture. Here we show that lines with the normal 1RS arm have longer roots than lines with the 1RSRW arm in both field and hydroponic experiments. In the 1RSRW lines, differences in seminal root length were associated with a developmentally regulated arrest of the root apical meristem (RAM). Approximately 10 d after germination, the seminal roots of the 1RSRW plants showed a gradual reduction in elongation rate, and stopped growing a week later. Seventeen days after germination, the roots of the 1RSRW plants showed altered gradients of reactive oxygen species and emergence of lateral roots close to the RAM, suggesting changes in the root meristem. The 1RSRW lines also showed reduced biomass (estimated by the normalized difference vegetation index) and grain yield relative to the 1RS lines, with larger differences under reduced or excessive irrigation than under normal irrigation. These results suggest that this genetic variation could be useful to modulate root architecture.
Variation in stripe rust resistance and morphological traits in wild emmer wheat populations
Huang L., Feng L., He Y., Tang Z., He J., Sela H., Krugman T., Fahima, T., Liu D., Wu B.
Agronomy, 9(2): 44, 2019
Abstract
Wild emmer wheat (Triticum dicoccoides), the tetraploid progenitor of cultivated wheats, is indigenous to the Near East Fertile Crescent. An important center of distribution is found today in and around the catchment area of the upper Jordan Valley in Israel and surrounding regions. In the current study, the field stripe rust resistance and morphological traits were analyzed using 98 sample accessions that represented the geographical distribution of wild emmer populations in Israel and its vicinity. The resistance tests at two field locations revealed that the majority of the wild emmer accessions possess quantitative resistance against stripe rust. This could be due to the high frequency of Yr36 in the wild emmer populations. The identification of potentially novel stripe rust resistance in this set of germplasm is highly significant. In total, 11 morphological traits were examined in this study. Wide range of natural variation was revealed in the tested morphological traits. Most of the morphological traits had significant correlations with climate variables, indicating that the local environmental conditions have a profound effect on shaping the genetic structure of wild emmer wheat. Our results suggest that wild emmer wheat has the enormous potential to improve stripe rust resistance and various important agronomical traits in wheat.
Fatiukha A., Filler N., Lupo I., Lidzbarsky G., Klymiuk V., Korol A.B., Pozniak C., Fahima, T., Krugman, T
Theoretical and Applied Genetics, 133(1): 119-131, 2019
Abstract
Genetic dissection of GPC and TKW in tetraploid durum × WEW RIL population, based on high-density SNP genetic map, revealed 12 GPC QTLs and 11 TKW QTLs, with favorable alleles for 11 and 5 QTLs, respectively, derived from WEW. Wild emmer wheat (Triticum turgidum ssp. dicoccoides, WEW) was shown to exhibit high grain protein content (GPC) and therefore possess a great potential for improvement of cultivated wheat nutritional value. Genetic dissection of thousand kernel weight (TKW) and grain protein content (GPC) was performed using a high-density genetic map constructed based on a recombinant inbred line (RIL) population derived from a cross between T. durum var. Svevo and WEW acc. Y12-3. Genotyping of 208 F6 RILs with a 15 K wheat single nucleotide polymorphism (SNP) array yielded 4166 polymorphic SNP markers, of which 1510 were designated as skeleton markers. A total map length of 2169 cM was obtained with an average distance of 1.5 cM between SNPs. A total of 12 GPC QTLs and 11 TKW QTLs were found under five different environments. No significant correlations were found between GPC and TKW across all environments. Four major GPC QTLs with favorable alleles from WEW were found on chromosomes 4BS, 5AS, 6BS and 7BL. The 6BS GPC QTL coincided with the physical position of the NAC transcription factor TtNAM-B1, underlying the cloned QTL, Gpc-B1. Comparisons of the physical intervals of the GPC QTLs described here with the results previously reported in other durum × WEW RIL population led to the discovery of seven novel GPC QTLs. Therefore, our research emphasizes the importance of GPC QTL dissection in diverse WEW accessions as a source of novel alleles for improvement of GPC in cultivated wheat.
Fatiukha A., Klymiuk V., Peleg Z., Saranga Y., Cakmak I., Krugman T., Korol A.B., Fahima T.
The Plant Journal, 101(3): 555-572, 2019
Abstract
Dissection of the genetic basis of wheat ionome is crucial for understanding the physiological and biochemical processes underlying mineral accumulation in seeds, as well as for efficient crop breeding. Most of the elements essential for plants are metals stored in seeds as chelate complexes with phytic acid or sulfur-containing compounds. We assume that the involvement of phosphorus and sulfur in metal chelation is the reason for strong phenotypic correlations within ionome. Adjustment of element concentrations for the effect of variation in phosphorus and sulfur seed content resulted in drastic change of phenotypic correlations between the elements. The genetic architecture of wheat grain ionome was characterized by quantitative trait loci (QTL) analysis using a cross between durum and wild emmer wheat. QTL analysis of the adjusted traits and two-trait analysis of the initial traits paired with either P or S considerably improved QTL detection power and accuracy, resulting in the identification of 105 QTLs and 617 QTL effects for 11 elements. Candidate gene search revealed some potential functional associations between QTLs and corresponding genes within their intervals. Thus, we have shown that accounting for variation in P and S is crucial for understanding of the physiological and genetic regulation of mineral composition of wheat grain ionome and can be implemented for other plants.
Distribution and Nucleotide Diversity of Yr15 in Wild Emmer Populations and Chinese Wheat Germplasm
Y He, L Feng, Y Jiang, L Zhang, J Yan, G Zhao, J Wang, G Chen, B Wu, ...
Pathogens 9 (3), 212
2020
A Fatiukha, V Klymiuk, Z Peleg, Y Saranga, I Cakmak, T Krugman, ...
The Plant Journal 101 (3), 555-572
2020
Y Li, L Qiu, X Liu, Q Zhang, X Zhuansun, T Fahima, T Krugman, Q Sun, ...
International journal of molecular sciences 21 (2), 673
2020
G Gabay, TR Howell, J Zhang, T Fahima, A Lukaszewski, J Dubcovsky
Plant and Animal Genome XXVIII Conference (January 11-15, 2020)
2020
Y Liang, Y Chen, D Liu, J Cheng, G Zhao, T Fahima, J Yan
Phyton 89 (2), 423
2020
A Fatiukha, N Filler, I Lupo, G Lidzbarsky, V Klymiuk, AB Korol, C Pozniak, ...
Theoretical and Applied Genetics 133 (1), 119-131
2020
A wheat/rye polymorphism affects seminal root length and yield across different irrigation regimes
T Howell, JI Moriconi, X Zhao, J Hegarty, T Fahima, GE Santa-Maria, ...
Journal of experimental botany 70 (15), 4027-4037
2019
Wheat tandem kinases provide insights on disease‐resistance gene flow and host–parasite co‐evolution
V Klymiuk, A Fatiukha, T Fahima
The Plant Journal 98 (4), 667-679
2019
Variation in stripe rust resistance and morphological traits in wild emmer wheat populations
L Huang, L Feng, Y He, Z Tang, J He, H Sela, T Krugman, T Fahima, D Liu, ...
Agronomy 9 (2), 44
2019
V Klymiuk, A Fatiukha, T Fahima
Plant and Animal Genome XXVII Conference (January 12-16, 2019)
2019
V Klymiuk, A Fatiukha, T Fahima
Plant and Animal Genome XXVII Conference (January 12-16, 2019)
2019
T Fahima, T Krugman
2019
POSITIONAL CLONING OF THE RUST RESISTANCE GENE, YR15, DERIVED FROM WILD EMMER WHEAT
T Fahima, V Klymiuk, E Yaniv, L Huang, RD Dina, FA Andrii
VII Съезд Вавиловского общества генетиков и селекционеров, посвященный 100 …
2019
Ecological diversity of algae in the Alakol lake natural reserve, Kazakhstan
A Jiyenbekov, S Barinova, A Bigaliev, S Nurashov, E Sametova, T Fahima
Botanica Pacifica 8 (2), 1-12
2019
A Fatiukha, M Deblieck, V Klymiuk, L Merchuk-Ovnat, Z Peleg, F Ordon, ...
bioRxiv, 565820
2019
Durum wheat as a bridge between wild emmer wheat genetic resources and bread wheat
V Klymiuk, A Fatiukha, L Huang, Z Wei, T Kis-Papo, Y Saranga, ...
Applications of Genetic and Genomic Research in Cereals, 201-230
2019
The Institute of Evolution wild cereal gene bank at the University of Haifa
T Krugman, E Nevo, A Beharav, H Sela, T Fahima
Israel Journal of Plant Sciences 65 (3-4), 129-146
2018
Cloning of the wheat Yr15 resistance gene sheds light on the plant tandem kinase-pseudokinase family
V Klymiuk, E Yaniv, L Huang, D Raats, A Fatiukha, S Chen, L Feng, ...
Nature communications 9 (1), 1-12
2018
Shifting the limits in wheat research and breeding using a fully annotated reference genome
International Wheat Genome Sequencing Consortium (IWGSC), R Appels, ...
Science 361 (6403), eaar7191
2018
AL Vuorinen, R Kalendar, T Fahima, H Korpelainen, E Nevo, ...
Agronomy 8 (7), 107
2018
Z WANG, J XIE, G Li, D ZHANG, G LI, T FANG, Y CHEN, L Jun, Q WU, ...
Journal of Integrative Agriculture 17 (6), 1267-1275
2018
J Yan, WT Xue, RZ Yang, HB Qin, G Zhao, F Tzion, JP Cheng
Czech Journal of Genetics and Plant Breeding 54 (2), 52-58
2018
R Ben-David, A Dinoor, Z Peleg, T Fahima
Frontiers in plant science 9, 75
2018
Algal comparative floristic of the Alakol Lake Natural State Reserve and other lakes in Kazakhstan
A Jiyenbekov, S Barinova, A Bigaliev, S Nurashov, E Sametova, T Fahima
MOJ Ecology & Environmental Sciences 3 (4), 252-258
2018
Bioindication using diversity and ecology of algae of the Alakol Lake, Kazakhstan
A Jienbekov, S Barinova, A Bigaliev, S Nurashov, E Sametova, T Fahima
Applied Ecology and Environmental Research 16 (6), 7799-7831
2018
SR Rybnikov, ZM Frenkel, T Fahima, AB Korol
bioRxiv, 478966
2018
T Howell, JI Moriconi, X Zhao, J Hegarty, T Fahima, GE Santa-Maria, ...
bioRxiv, 463281
2018
Wild emmer genome architecture and diversity elucidate wheat evolution and domestication
R Avni, M Nave, O Barad, K Baruch, SO Twardziok, H Gundlach, I Hale, ...
Science 357 (6346), 93-97
2017
Ancestral QTL alleles from wild emmer wheat enhance root development under drought in modern wheat
L Merchuk-Ovnat, T Fahima, JE Ephrath, T Krugman, Y Saranga
Frontiers in Plant Science 8, 703
2017
The development of the a world database of freshwater algae-indicators
S Barinova, T Fahima
Journal of Environment and Ecology 8 (1), 1-7
2017
Characterizing barley seed macro-and micro-nutrients under multiple environmental conditions
WT Xue, A Gianinetti, R Wang, ZJ Zhan, J Yan, Y Jiang, T Fahima, G Zhao, ...
Cereal Research Communications 44 (4), 639-649
2016
The hijacking of a receptor kinase–driven pathway by a wheat fungal pathogen leads to disease
G Shi, Z Zhang, TL Friesen, D Raats, T Fahima, RS Brueggeman, S Lu, ...
Science advances 2 (10), e1600822
2016
L Merchuk-Ovnat, T Fahima, T Krugman, Y Saranga
Plant Science 251, 23-34
2016
Genomic analysis of 6,000-year-old cultivated grain illuminates the domestication history of barley
M Mascher, VJ Schuenemann, U Davidovich, N Marom, A Himmelbach, ...
Nature Genetics 48 (9), 1089-1093
2016
Evolution and adaptation of wild emmer wheat populations to biotic and abiotic stresses
L Huang, D Raats, H Sela, V Klymiuk, G Lidzbarsky, L Feng, T Krugman, ...
Annual review of phytopathology 54 (1), 279-301
2016
Distribution and haplotype diversity of WKS resistance genes in wild emmer wheat natural populations
L Huang, H Sela, L Feng, Q Chen, T Krugman, J Yan, J Dubcovsky, ...
Theoretical and Applied Genetics 129 (5), 921-934
2016
L Merchuk-Ovnat, V Barak, T Fahima, F Ordon, GA Lidzbarsky, T Krugman, ...
Frontiers in plant science 7, 452
2016
Sequencing and Analysis of Wheat Chromosome 1B
F Choulet, H Rimbert, AA Josselin, B Darrier, P Sourdille, F Balfourier, ...
Plant and Animal Genome XXIV Conference; IWGSC Standards and Protocoles …
2016
D Jorge, F Tzion, K Tamar, H Tyson
United States Department of Agriculture
2016
Transcriptome profiling of wheat glumes in wild emmer, hulled landraces and modern cultivars
H Zou, R Tzarfati, S Hübner, T Krugman, T Fahima, S Abbo, Y Saranga, ...
BMC genomics 16 (1), 1-14
2015
JY Gou, K Li, K Wu, X Wang, H Lin, D Cantu, C Uauy, A Dobon-Alonso, ...
The Plant Cell 27 (6), 1755-1770
2015
M Maccaferri, A Ricci, S Salvi, SG Milner, E Noli, PL Martelli, R Casadio, ...
Plant biotechnology journal 13 (5), 648-663
2015
E FİLİZ, A Distelfeld, T Fahima, ÖK METİN, E Nevo, S Weining, ...
Turkish Journal of Agriculture and Forestry 39 (5), 786-796
2015
E Yaniv, D Raats, Y Ronin, AB Korol, A Grama, H Bariana, J Dubcovsky, ...
Molecular Breeding 35 (1), 1-12
2015
Genetic dissection of quantitative powdery mildew resistance loci in tetraploid wheat
R Ben-David, Z Peleg, A Dinoor, Y Saranga, AB Korol, T Fahima
Molecular breeding 34 (4), 1647-1658
2014
Novel quantitative trait loci underlying major domestication traits in tetraploid wheat
R Tzarfati, V Barak, T Krugman, T Fahima, S Abbo, Y Saranga, AB Korol
Molecular Breeding 34 (4), 1613-1628
2014
M Maccaferri, MA Cane, MC Sanguineti, S Salvi, MC Colalongo, A Massi, ...
BMC genomics 15 (1), 1-21
2014
H Sela, LN Spiridon, H Ashkenazi, NK Bhullar, S Brunner, AJ Petrescu, ...
Molecular Plant-Microbe Interactions 27 (8), 835-845
2014
Functional characterization of GPC-1 genes in hexaploid wheat
R Avni, R Zhao, S Pearce, Y Jun, C Uauy, F Tabbita, T Fahima, A Slade, ...
Planta 239 (2), 313-324
2014
Cleaved amplified polymorphic sequences (CAPS) markers in plant biology/Ed
D Raats, E Yaniv, A Distelfeld, R Ben-David, J Shanir, V Bocharova, ...
Shavrukov YNY: NOVA Publ 2014
2014
Application of CAPS markers for genomic studies in wild emmer wheat
D Raats, E Yaniv, A Distelfeld, R Ben-David, J Shanir, V Bocharova, ...
Cleaved amplified polymorphic sequences (CAPS) markers in plant biology. New …
2014
D Raats, Z Frenkel, T Krugman, I Dodek, H Sela, H Šimková, F Magni, ...
Genome biology 14 (12), 1-19
2013
C Pont, F Murat, S Guizard, R Flores, S Foucrier, Y Bidet, UM Quraishi, ...
The Plant Journal 76 (6), 1030-1044
2013
A physical map of the short arm of wheat chromosome 1A
J Breen, T Wicker, M Shatalina, Z Frenkel, I Bertin, R Philippe, ...
PLoS One 8 (11), e80272
2013
D Jorge, F Tzion, B Ann
United States Department of Agriculture
2013
F Tzion, D Jorge
United States Department of Agriculture
2013
QTL location and analysis of selenium content in tetraploid wheat grain.
RZ Yang, R Wang, WT Xue, J Yan, G Zhao, T Fahima, JP Cheng
Guizhou Agricultural Sciences, 1-10
2013
Studies on rock conditioning for hard rock tunnelling by a mobile laboratory
KY Levent, F Aksu, S Tokcan, U Gumus, A Yazici, S Akdemir
2013
J Yan, F Wang, R Yang, T Xiao, T Fahima, Y Saranga, A Korol, E Nevo, ...
Advance in Barley Sciences, 169-183
2013
Genomic asymmetry in allopolyploid plants: wheat as a model
M Feldman, AA Levy, T Fahima, A Korol
Journal of experimental botany 63 (14), 5045-5059
2012
H Sela, LN Spiridon, AJ PETRESCU, M Akerman, ...
Molecular plant pathology 13 (3), 276-287
2012
W Xie, R Ben-David, B Zeng, A Distelfeld, MS Röder, A Dinoor, T Fahima
Theoretical and Applied Genetics 124 (5), 911-922
2012
W Xie, R Ben-David, B Zeng, A Dinoor, C Xie, Q Sun, MS Röder, ...
Molecular breeding 29 (2), 399-412
2012
T Krugman, Z Peleg, L Quansah, V Chagué, AB Korol, E Nevo, Y Saranga, ...
Functional & Integrative Genomics 11 (4), 565-583
2011
D Cantu, SP Pearce, A Distelfeld, MW Christiansen, C Uauy, E Akhunov, ...
BMC genomics 12 (1), 1-17
2011
Genetic analysis of wheat domestication and evolution under domestication
Z Peleg, T Fahima, AB Korol, S Abbo, Y Saranga
Journal of experimental botany 62 (14), 5051-5061
2011
Expression and cellular localization of ZIP1 transporter under zinc deficiency in wild emmer wheat
E Durmaz, C Coruh, G Dinler, MA Grusak, Z Peleg, Y Saranga, T Fahima, ...
Plant Molecular Biology Reporter 29 (3), 582-596
2011
Y Jun, W Fang, Q Haibo, C Guoxiong, N Eviatar, T Fahima, C Jianping
Biological trace element research 142 (3), 773-786
2011
T Wicker, KFX Mayer, H Gundlach, M Martis, B Steuernagel, U Scholz, ...
The Plant Cell 23 (5), 1706-1718
2011
QTL analysis of 1000-grain weight under different ecological environment in tetraploid wheat.
J Yan, RZ Yang, WT Xue, LL Zhang, J Li, T Fahima, JP Cheng
Guizhou Agricultural Sciences, 6-10
2011
J Yan, LL Zhang, B Wan, JB Gou, YC Wang, CM Xu, T Fahmina, ...
J Sichuan Agric Univ 29 (2), 147-153
2011
H Sela, C Loutre, B Keller, A Schulman, E Nevo, A Korol, T Fahima
Theoretical and applied genetics 122 (1), 175-187
2011
NAC from wheat for increasing grain protein content
J Dubcovsky, T Fahima, C Uauy, A Distelfeld
US Patent 7,820,882
2010
Genetic control over silica deposition in wheat awns
Z Peleg, Y Saranga, T Fahima, A Aharoni, R Elbaum
Physiologia plantarum 140 (1), 10-20
2010
Identification and mapping of PmG16, a powdery mildew resistance gene derived from wild emmer wheat
R Ben-David, W Xie, Z Peleg, Y Saranga, A Dinoor, T Fahima
Theoretical and applied genetics 121 (3), 499-510
2010
J Cheng, J Yan, H Sela, J Manisterski, D Lewinsohn, E Nevo, T Fahima
Physiologia plantarum 139 (3), 269-279
2010
Genetic diversity for grain nutrients in wild emmer wheat: potential for wheat improvement
M Chatzav, Z Peleg, L Ozturk, A Yazici, T Fahima, I Cakmak, Y Saranga
Annals of botany 105 (7), 1211-1220
2010
T Krugman, V Chagué, Z Peleg, S Balzergue, J Just, AB Korol, E Nevo, ...
Functional & integrative genomics 10 (2), 167-186
2010
D Cantu, K Wu, F Daolin, C Uauy, A Distelfeld, L Epstein, P Ronald, ...
IN VITRO CELLULAR & DEVELOPMENTAL BIOLOGY-ANIMAL 46, S13-S13
2010
G Chen, T Krugman, T Fahima, K Chen, Y Hu, M Röder, E Nevo, A Korol
Genetic Resources and Crop Evolution 57 (1), 85-99
2010
HF Gomez-Becerra, A Yazici, L Ozturk, H Budak, Z Peleg, A Morgounov, ...
Euphytica 171 (1), 39-52
2010
C Loutre, T Wicker, S Travella, P Galli, S Scofield, T Fahima, C Feuillet, ...
The Plant Journal 60 (6), 1043-1054
2009
程剑平, 梁强, 严俊, 黄丽丽
麦类作物学报 29 (6), 111521118
2009
G Li, T Fang, H Zhang, C Xie, H Li, T Yang, E Nevo, T Fahima, Q Sun, ...
Theoretical and applied genetics 119 (3), 531-539
2009
ZVI Peleg, T Fahima, T Krugman, S Abbo, DAN Yakir, AB Korol, ...
Plant, cell & environment 32 (7), 758-779
2009
Z Peleg, I Cakmak, L Ozturk, A Yazici, Y Jun, H Budak, AB Korol, ...
Theoretical and applied genetics 119 (2), 353-369
2009
H Sela, J Cheng, Y Jun, E Nevo, T Fahima
Genome 52 (6), 557-565
2009
A kinase-START gene confers temperature-dependent resistance to wheat stripe rust
D Fu, C Uauy, A Distelfeld, A Blechl, L Epstein, X Chen, H Sela, T Fahima, ...
science 323 (5919), 1357-1360
2009
G Chen, T Komatsuda, M Pourkheirandish, M SAMERI, K SATO, ...
Breeding science 59 (1), 21-26
2009
Variance analysis of grain selenium contents in wild Emmer wheat, Triticum dicoccoide.
CX Zhang, J Yan, JP Cheng, HB Qin, GX Chen, T Fahima
Journal of Tropical and Subtropical Botany 17 (3), 229-236
2009
P Zvi, C Ismail, O Levent, Y Atilla, J Yan, B Hikmet, B Abraham, F Tzion, ...
Theor Appl Climatol 119 (3), 353-369
2009
Evolution of the Yr15 region in the Poideae
J Tanskanen, C Moisy, E Yaniv, L Paulin, R Kalendar, H Belcram, ...
19th international Triticeae Mapping Initiative-3rd COST Tritigen, Clermont …
2009
QA Liang, J Yan, LL Huang, T Fahima, JP Cheng
Guizhou Agricultural Sciences, 10-12
2009
G Chen, T Komatsuda, M Pourkheirandish, M Sameri, K Sato, T Krugman, ...
Breeding Science 59 (1), 21-26
2009
A Distelfeld, A Korol, J Dubcovsky, C Uauy, T Blake, T Fahima
Molecular Breeding 22 (1), 25-38
2008
High-density genetic map of durum wheat× wild emmer wheat based on SSR and DArT markers
Z Peleg, Y Saranga, T Suprunova, Y Ronin, MS Röder, A Kilian, AB Korol, ...
Theoretical and Applied Genetics 117 (1), 103-115
2008
Z Peleg, Y Saranga, A Yazici, T Fahima, L Ozturk, I Cakmak
Plant and Soil 306 (1), 57-67
2008
Z Peleg, T Fahima, S Abbo, T Krugman, Y Saranga
Genome 51 (3), 187-195
2008
X Ji, C Xie, Z Ni, T Yang, E Nevo, T Fahima, Z Liu, Q Sun
Euphytica 159 (3), 385-390
2008
DR Ben, Z Peleg, W Xie, Y Saranga, A Dinoor, AB Korol, T Fahima
Sydney University Press
2008
Towards positional cloning of the stripe rust resistance gene YR15, derived from wild emmer wheat
E Yaniv, JA Tanskanen, R Kalendar, AH Schulman, T Fahima
Triticeae genomics for the advancement of essential European crops …
2008
R Kalendar, AL Vuorinen, T Fahima, H Korpelainen, N Eviatar, ...
Triticeae genomics for the advancement of essential European crops …
2008
Z Peleg, Y Saranga, T Krugman, S Abbo, MS Röder, A Kilian, D Yakir, ...
Sydney University Press
2008
Differential gene expression in wild emmer wheat genotypes contrasting in drought resistance
T Krugman, V Chagué, Z Peleg, L Brodsky, S Balzergue, N Boudet, ...
Sydney University Press
2008
Physiological-genetic dissection of drought resistance in wild emmer wheat
Y Saranga, Z Peleg, T Fahima
Sydney University Press
2008
Allelic diversity associated with aridity gradient in wild emmer wheat populations
ZVI Peleg, Y Saranga, T Krugman, S Abbo, E Nevo, T Fahima
Plant, Cell & Environment 31 (1), 39-49
2008
Identification of a novel gene (Hsdr4) involved in water-stress tolerance in wild barley
T Suprunova, T Krugman, A Distelfeld, T Fahima, E Nevo, A Korol
Plant Molecular Biology 64 (1), 17-34
2007
Multiple QTL‐effects of wheat Gpc‐B1 locus on grain protein and micronutrient concentrations
A Distelfeld, I Cakmak, Z Peleg, L Ozturk, AM Yazici, H Budak, Y Saranga, ...
Physiologia plantarum 129 (3), 635-643
2007
Validation of a candidate gene for increased grain protein content in wheat
D Jorge, F Tzion, B Ann
United States Department of Agriculture
2007
Wild emmer wheat as a source for high-grain-protein genes: Map-based cloning of Gpc-B1
A Distelfeld, T Fahima
Israel Journal of Plant Sciences 55 (3-4), 297-306
2007
N Gasmanova, A LEBEDA, I DOLEžALOVÁ, T Cohen, T PAVLÍČEK, ...
Acta Biologica Cracoviensia series Botanica 49 (1), 39-46
2007
Drought resistance in wild emmer wheat: physiology, ecology, and genetics
Z Peleg, T Fahima, Y Saranga
Israel journal of plant sciences 55 (3-4), 289-296
2007
A Korol, T Fahima, E Nevo
US Patent App. 11/464,370
2006
A NAC gene regulating senescence improves grain protein, zinc, and iron content in wheat
C Uauy, A Distelfeld, T Fahima, A Blechl, J Dubcovsky
Science 314 (5803), 1298-1301
2006
The ripples of" The Big (agricultural) Bang": the spread of early wheat cultivation
S Abbo, A Gopher, Z Peleg, Y Saranga, T Fahima, F Salamini, ...
Genome 49 (8), 861-863
2006
A Distelfeld, C Uauy, T Fahima, J Dubcovsky
New Phytologist 169 (4), 753-763
2006
C Uauy, JC Brevis, X Chen, I Khan, L Jackson, O Chicaiza, A Distelfeld, ...
Theoretical and Applied Genetics 112 (1), 97-105
2005
A Korol, T Fahima, E Nevo
US Patent App. 10/965,735
2005
F Zhang, G Chen, Q Huang, O Orion, T Krugman, T Fahima, AB Korol, ...
Theoretical and Applied Genetics 110 (3), 445-453
2005
Genetic diversity for drought resistance in wild emmer wheat and its ecogeographical associations
Z Peleg, T Fahima, S Abbo, T Krugman, E Nevo, D Yakir, Y Saranga
Plant, Cell & Environment 28 (2), 176-191
2005
U Cristobal, JC BREVIS, XX CHEN, K Imtiaz, L JACKSON, O CHICAIZA, ...
Theoretical and applied genetics 112 (1), 97-105
2005
Status of barley germplasm collections in Israel.
T Fahima
Cereal genetic resources in Europe., 116-117
2005
J Cheng, J Yan, T Krugman, T Fahima
Biotechnology letters 27 (2), 83-89
2005
I Cakmak, A Torun, E Millet, M FELDMAN, T FAHIMA, A KOROL, E NEVO, ...
Soil science and plant nutrition 50 (7), 1047-1054
2004
Pollen-mediated method for transformation of maize, tomato or melon
A Korol, T Fahima, E Nevo
US Patent 6,806,399
2004
T Suprunova, T Krugman, T Fahima, G Chen, I Shams, A Korol, E Nevo
Plant, cell & environment 27 (10), 1297-1308
2004
Wild barley eibi1 mutation identifies a gene essential for leaf water conservation
G Chen, M Sagi, S Weining, T Krugman, T Fahima, AB Korol, E Nevo
Planta 219 (4), 684-693
2004
Microsatellites within genes: structure, function, and evolution
YC Li, AB Korol, T Fahima, E Nevo
Molecular biology and evolution 21 (6), 991-1007
2004
G Chen, T Suprunova, T Krugman, T Fahima, E Nevo
Seed Science Research 14 (2), 137-146
2004
C Xie, Q Sun, Z Ni, T Yang, E Nevo, T Fahima
Plant Breeding 123 (2), 198-200
2004
A Distelfeld, C Uauy, S Olmos, AR Schlatter, J Dubcovsky, T Fahima
Functional & Integrative Genomics 4 (1), 59-66
2004
İ Çakmak, A Torun, E Millet, M Feldman, T Fahima, A Korol, E Nevo, ...
Soil science and plant nutrition 50 (7), 1047-1054
2004
Positional cloning of a gene responsible for high grain protein content in tetraploid wheat
J Dubcovsky, T Fahima
BARD
2004
A Distelfeld, C Uauy, S Olmos, A Schlatter, J Dubcovsky, T Fahima
Funct Integr Genomics 4, 59-66
2004
G Chen, K Tamar, T Fahima, F Zhang, AB Korol, E Nevo
Journal of arid environments 56 (1), 95-105
2004
Precise mapping of a locus affecting grain protein content in durum wheat
S Olmos, A Distelfeld, O Chicaiza, AR Schlatter, T Fahima, V Echenique, ...
Theoretical and Applied Genetics 107 (7), 1243-1251
2003
A Cenci, N Chantret, X Kong, Y Gu, OD Anderson, T Fahima, A Distelfeld, ...
Theoretical and Applied Genetics 107 (5), 931-939
2003
Positional cloning of the wheat vernalization gene VRN1
L Yan, A Loukoianov, G Tranquilli, M Helguera, T Fahima, J Dubcovsky
Proceedings of the National Academy of Sciences 100 (10), 6263-6268
2003
Domestication quantitative trait loci in Triticum dicoccoides, the progenitor of wheat
J Peng, Y Ronin, T Fahima, MS Röder, Y Li, E Nevo, A Korol
Proceedings of the National Academy of Sciences 100 (5), 2489-2494
2003
ED Owuor, A Beharav, T Fahima, VM Kirzhner, AB Korol, E Nevo
Genetic Resources and Crop Evolution 50 (2), 213-224
2003
H Buerstmayr, M Stierschneider, B Steiner, M Lemmens, M Griesser, ...
Euphytica 130 (1), 17-23
2003
YC Li, T Fahima, MS Röder, VM Kirzhner, A Beiles, AB Korol, E Nevo
Heredity 90 (2), 150-156
2003
Positional cloning of a gene responsible for high grain protein content in tetraploid wheat
D Jorge, F Tzion, B Ann
United States Department of Agriculture
2003
C Xie, Q Sun, Z Ni, T Yang, E Nevo, T Fahima
Theoretical and Applied Genetics 106 (2), 341-345
2003
VARIATION FOR RESISTANCE TO FUSARIUM HEAD BLIGHT IN TRITICUM DICOCCOIDES
H Buerstmayr, M Stierschneider, B Steiner, M Lemmens, M Griesser, ...
National Fusarium Head Blight Forum Proceedings, 199
2002
Microsatellites: genomic distribution, putative functions and mutational mechanisms: a review
YC Li, AB Korol, T Fahima, A Beiles, E Nevo
Molecular ecology 11 (12), 2453-2465
2002
YC Li, MS Röder, T Fahima, VM Kirzhner, A Beiles, AB Korol, E Nevo
Heredity 89 (2), 127-132
2002
F Zhang, Y Gutterman, T Krugman, T Fahima, E Nevo
Israel Journal of Plant Sciences 50 (4), 271-276
2002
E Nevo, AB Korol, A Beiles, T Fahima
Springer Science & Business Media
2002
T Fahima, MS Röder, K Wendehake, VM Kirzhner, E Nevo
Theoretical and Applied Genetics 104 (1), 17-29
2002
Very high mutation rate in offspring of Chernobyl accident liquidators
HS Weinberg, AB Korol, VM Kirzhner, A Avivi, T Fahima, E Nevo, ...
Proceedings of the Royal Society of London. Series B: Biological Sciences …
2001
YC Li, T Krugman, T Fahima, A Beiles, AB Korol, E Nevo
Theoretical and Applied Genetics 102 (6), 853-864
2001
QTLs for agronomic traits in tetraploid wild emmer wheat (Triticum dicoccoides)
P Junhua, B Koro, T Fahima
Sichuan Nongye Daxue Xuebao (China)
2001
JP Cheng, JH Peng, T Fahima, AB Korol, LR Kong, MS Roder, YI Ronin, ...
Israel Journal of Plant Sciences
2001
QTL analysis of drought resistance in wild barley, Hordeum spontaneum.
Q Huang, Z Lu, T Krugman, T Fahima, C Guoxiong, M Roder, E Nevo, ...
TIsrael Journal of Plant Sciences
2001
T Fahima, JH Peng, JP Cheng, MS Roder, YI Ronin, YC Li, AB Korol, ...
Israel Journal of Plant Sciences
2001
YC Li, T Fahima, JH Peng, MS Röder, VM Kirzhner, A Beiles, AB Korol, ...
Theoretical and Applied Genetics 101 (7), 1029-1038
2000
J Peng, AB Korol, T Fahima, MS Röder, YI Ronin, YC Li, E Nevo
Genome Research 10 (10), 1509-1531
2000
YC Li, T Fahima, T Krugman, A Beiles, MS Röder, AB Korol, E Nevo
Conservation Genetics 1 (3), 191-207
2000
JH Peng, T Fahima, MS Röder, QY Huang, A Dahan, YC Li, A Grama, ...
Genetica 109 (3), 199-210
2000
Y Li, T Fahima, AB Korol, J Peng, V Kirzhner, A Beiles, E Nevo
Molecular Biology and Evolution 17 (6), 851-862
2000
YC Li, MS Röder, T Fahima, VM Kirzhner, A Beiles, AB Korol, E Nevo
Theoretical and Applied Genetics 100 (7), 985-999
2000
JH Peng, T Fahima, MS Röder, YC Li, A Grama, E Nevo
The New Phytologist 146 (1), 141-154
2000
Genetic Diversity at Resistance Gene Clusters in Wild Populations of Lactuca
M Richard, N Eviatar, K Abraham, F Tzion
United States Department of Agriculture
2000
Moreira-Filho, O., 63 Moreteau, B., 165 Munjal, A., 165 Murphy, RW, 227 Nevo, E., 177
J Albornoz, CE Argarana, J Arnold, PW Atkinson, JC Avise, FJ Ayala, ...
Genetica 105 (308), 308
2000
V Chague, T Fahima, A Dahan, GL Sun, AB Korol, YI Ronin, A Grama, ...
Genome 42 (6), 1050-1056
1999
RAPD divergence caused by microsite edaphic selection in wild barley
ED Owuor, T Fahima, A Beharav, A Korol, E Nevo
Genetica 105 (2), 177-192
1999
Microclimatic stress and adaptive DNA differentiation in wild emmer wheat, Triticum dicoccoides
YC Li, T Fahima, A Beiles, AB Korol, E Nevo
Theoretical and Applied Genetics 98 (6), 873-883
1999
JH Peng, T Fahima, MS Röder, YC Li, A Dahan, A Grama, YI Ronin, ...
Theoretical and applied genetics 98 (6), 862-872
1999
RAPD polymorphism of wild emmer wheat populations, Triticum dicoccoides, in Israel
T Fahima, GL Sun, A Beharav, T Krugman, A Beiles, E Nevo
Theoretical and Applied Genetics 98 (3), 434-447
1999
EI Andreyuk, AF Antipchuk, GA Iutinskaja, T Fahima, E Nevo
Mikrobiologichnyi Zhurnal 61 (2), 3-9
1999
T Fahima, MS Röder, A Grama, E Nevo
Theoretical and Applied Genetics 96 (2), 187-195
1998
HS Weinberg, E Nevo, A Korol
Occupational Health and Industrial Medicine 4 (38), 173
1998
HS Weinberg, E Nevo, A Korol, T Fahima, G Rennert, S Shapiro
Environmental Health Perspectives 105 (suppl 6), 1479-1481
1997
Population genetic response to microsite ecological stress in wild barley, Hordeum spontaneum
ED Owuor, T Fahima, A Beiles, A Korol, E Nevo
Molecular Ecology 6 (12), 1177-1187
1997
GL Sun, T Fahima, AB Korol, T Turpeinen, A Grama, YI Ronin, E Nevo
Theoretical and Applied Genetics 95 (4), 622-628
1997
Increasing of Trichoderma hamatum and Talaromyces flavus on root of healthy and useful hosts
T Fahima, Y Henis
Biological control of soil-borne plant pathogens, 296-322
1997
YI Ronin, AB Korol, T Fahima, VM Kirzhner, E Nevo
Biometrics, 1428-1439
1996
HS Weinberg, T Nevo, A Korol, T Fahima, G Rennert, S Shapiro
1996
Parathion degradation by Xanthomonas sp. and its crude enzyme extract in clay suspensions
S Masaphy, T Fahima, D Levanon, Y Henis, U Mingelgrin
Journal of environmental quality 25 (6), 1248-1255
1996
Random amplified polymorphic DNA of the Spalax ehrenbergi superspecies in Israel
BENS RACHEL, T Fahima, E Nevo
Israel Journal of Ecology and Evolution 42 (4), 317-326
1996
T Fahima, Y Henis
Plant and Soil 176 (1), 129-137
1995
T Fahima, A Grama, A Korol, T Turpeinen, E Nevo
1995
of Liquidators Who Emigrated to Israel from
HS Weinberg, E Nevo, A Korol, T Fahima, G Rennert, S Shapiro
Environmental Health Perspectives: Supplements, 1477
1993
T Fahima, L Madi, Y Henis
Biocontrol Science and Technology 2 (1), 69-78
1992
Efficient Splicing of the Tetrahymena Group l Intron
G Dinter-Gottlieb, T Fahima, N Pobjecky
Molecular plant-microbe interactions 4 (5), 500-506
1991
T Fahima, Y Henis
Biological control of soil-borne plant pathogens., 165-180
1990
L Madi, T Fahima, Y Henis
Journal of Cellular Biochemistry 13 (Supplement), 178
1989
Biological-control of verticillium wilt of eggplant by talaromyces-flavus
T Fahima, J Katan, Y Henis
Phytoparasitica 16 (1), 67-68
1988
Capturing wheat phenotypes at the genome level
H Budak, B Hussain, BA Akpınar, M Alaux, AM Algharib, D Sehgal, Z Ali, ...
Frontiers in Plant Science, 1925
Positional cloning of a gene responsible for high grain protein content in tetraploid wheat.
JD PI, T Fahima
HF