Publications by authors named "Hanan Sela"

28 Publications

  • Page 1 of 1

TdPm60 identified in wild emmer wheat is an ortholog of Pm60 and constitutes a strong candidate for PmG16 powdery mildew resistance.

Theor Appl Genet 2021 Jun 8. Epub 2021 Jun 8.

Institute of Evolution, University of Haifa, Mt. Carmel, 3498838, Haifa, Israel.

Key Message: 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.
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http://dx.doi.org/10.1007/s00122-021-03858-3DOI Listing
June 2021

Genome-Wide Mapping of Loci for Adult-Plant Resistance to Stripe Rust in Durum Wheat Svevo Using the 90K SNP Array.

Plant Dis 2021 Apr 22;105(4):879-888. Epub 2021 Mar 22.

State Key Laboratory of Crop Stress Biology in Arid Areas and College of Plant Protection, Northwest A&F University, Yangling, Shaanxi 712100, People's Republic of China.

Stripe rust is a foliar disease in wheat caused by f. . The best way to protect wheat from this disease is by growing resistant cultivars. Tetraploid wheat can serve as a good source of valuable genetic diversity for various traits. Here, we report the mapping of nine stripe rust resistance quantitative trait loci (QTL) effective against f. in China and Israel. We used recombinant inbred lines (RILs) developed from a cross between the durum wheat cultivar Svevo and accession Zavitan. By genotyping the RIL population of 137 lines using the wheat 90K single-nucleotide polymorphism array, we mapped an adult-plant resistance locus , the most effective QTL, within a 0.75-centimorgan region in subsp. 'Svevo' on chromosome arm 1BL, corresponding to the region of 670.7 to 671.5 Mb on the Chinese Spring chromosome arm 1BL. Of the other eight minor-effect stripe rust QTL, seven were from Svevo and mapped on chromosomes 1A, 1B, 2B, 3A, 4A, and 5A, and one was from Zavitan and mapped on chromosome 2A. Several QTL with epistatic effects were identified as well. The markers linked to the resistance QTL can be useful in marker-assisted selection for incorporation of these resistance QTL into both durum and common wheat cultivars.
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http://dx.doi.org/10.1094/PDIS-09-20-1933-REDOI Listing
April 2021

Reducing the size of an alien segment carrying leaf rust and stripe rust resistance in wheat.

BMC Plant Biol 2020 Apr 9;20(1):153. Epub 2020 Apr 9.

Institute for Cereal Crops Improvement, Tel Aviv University, 69978, Tel Aviv, Israel.

Background: Leaf and stripe rusts are two major wheat diseases, causing significant yield losses. The preferred way for protecting wheat from rust pathogens is by introgression of rust resistance traits from wheat-related wild species. To avoid genetic drag due to replacement of large wheat chromosomal segments by the alien chromatin, it is necessary to shorten the alien chromosome segment in primary recombinants.

Results: Here we report on shortening of an alien chromosome segment in wheat that carries leaf and stripe rust resistance from Sharon goatgrass (Aegilops sharonensis). Rust resistant wheat introgression lines were selected and the alien region was mapped using genotyping by sequencing. Single polymorphic nucleotides (SNP) were identified and used to generate diagnostic PCR markers. Shortening of the alien fragment was achieved by induced homoeologous pairing and lines with shortened alien chromosome were identified using the PCR markers. Further reduction of the segment was achieved in tertiary recombinants without losing the rust resistance.

Conclusions: Alien chromatin in wheat with novel rust resistance genes was characterized by SNP markers and shortened by homoeologous recombination to avoid deleterious traits. The resulting wheat lines are resistant to highly virulent races of leaf and stripe rust pathogens and can be used as both resistant wheat in the field and source for gene transfer to other wheat lines/species.
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http://dx.doi.org/10.1186/s12870-020-2306-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7147030PMC
April 2020

Characterization of the Barley Net Blotch Pathosystem at the Center of Origin of Host and Pathogen.

Pathogens 2019 Nov 29;8(4). Epub 2019 Nov 29.

Department of vegetables and field crops, Institute of Plant Science, Agricultural Research Organization, The Volcani Center, Rishon LeZion 7505101, Israel.

Net blotch (NB) is a major disease of barley caused by the fungus f. (), and f. (). and infect the cultivated crop () and its wild relatives ( ssp. and ssp. ). The main goal of this research was to study the NB-causing pathogen in the crop center of origin. To address this, we have constructed a (n = 15) and (n = 12) collection isolated from three barley species across Israel. Isolates were characterized genetically and phenotypically. Aggressiveness of the isolates was determined based on necrotrophic growth rate on detached leaves of barley. In addition, isolates were genetically characterized by the mating type, followed by phylogenetic analysis, clustering them into seven groups. The analysis showed no significant differentiation of isolates based on either geographic origin, host of origin or form ( vs. ). Nevertheless, there was a significant difference in aggressiveness among the isolates regardless of host species, geographic location or sampling site. Moreover, it was apparent that the isolates derived from wild hosts were more variable in their necrotrophic growth rate, compared to isolates sampled from cultivated hosts, thereby suggesting that NB plays a major role in epidemiology at the center of barley origin where most of the diversity lies. has significantly higher necrotrophic and saprotrophic growth rates than , and for both a significant negative correlation was found between light intensity exposure and growth rates.
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http://dx.doi.org/10.3390/pathogens8040275DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6963742PMC
November 2019

Wheat domestication in light of haplotype analyses of the Brittle rachis 1 genes (BTR1-A and BTR1-B).

Plant Sci 2019 Aug 19;285:193-199. Epub 2019 May 19.

School of Plant Sciences and Food Security, Tel Aviv University, Tel Aviv, Israel. Electronic address:

Wheat domestication was a milestone in the rise of agrarian societies in the Fertile Crescent. As opposed to the freely dispersing seeds of its tetraploid progenitor wild emmer, the hallmark trait of domesticated wheat is intact, harvestable spikes. During domestication, wheat acquired recessive loss-of-function mutations in the Brittle Rachis 1 genes, both in the A genome (BTR1-A) and B genome (BTR1-B). In this study, we probe the geographical provenances of these mutations via haplotype analyses of a collection of wild and domesticated accessions. Our results show that the precursor of the domesticated haplotype of BTR1-A was detected in 32% of the wild accessions gathered throughout the Levant, from central Israel to central Turkey. In contrast, the precursor of the domesticated haplotype of BTR1-B, which carries a distinct 11 bp deletion in the promoter region, was found in only 10% of the tested wild accessions, all from the Southern Levant. Moreover, we identified of a single wild emmer accession in Southern Levant that carries the progenitor haplotypes for both BTR1-A and BTR1-B genes. These observations suggest that at least part of the emmer domestication process occurred in Southern Levant, contrary to the widely held view that the northern part of the Fertile Crescent was the center of wheat domestication.
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http://dx.doi.org/10.1016/j.plantsci.2019.05.012DOI Listing
August 2019

The Israeli-Palestinian wheat landraces collection: restoration and characterization of lost genetic diversity.

J Sci Food Agric 2020 Aug 18;100(11):4083-4092. Epub 2019 Jul 18.

Department of Vegetables and Field Crop, Institute of Plant Sciences, Agricultural Research Organization, Volcani Center, Rishon LeZion, Israel.

Background: For over a century, genetic diversity of wheat worldwide was eroded by continual selection for high yields and industrial demands. Wheat landraces cultivated in Israel and Palestine demonstrate high genetic diversity and a potentially wide repertoire of adaptive alleles. While most Israeli-Palestinian wheat landraces were lost in the transition to 'Green Revolution' semi-dwarf varieties, some germplasm collections made at the beginning of the 20th century survived in gene banks and private collections worldwide. However, fragmentation and poor conservation place this unique genetic resource at a high risk of genetic erosion. Herein, we describe a long-term initiative to restore, conserve, and characterize a collection of Israeli and Palestinian wheat landraces (IPLR).

Results: We report on (i) the IPLR construction (n = 932), (ii) the historical and agronomic context to this collection, (iii) the characterization and assessment of the IPLR's genetic diversity, and (iv) a data comparison from two distinct subcollections within IPLR: a collection made by N. Vavilov in 1926 (IPLR-VIR) and a later one (1979-1981) made by Y. Mattatia (IPLR-M). Though conducted in the same eco-geographic space, these two collections were subjected to considerably different conservation pathways. IPLR-M, which underwent only one propagation cycle, demonstrated marked genetic and phenotypic variability (within and between accessions) in comparison with IPLR-VIR, which had been regularly regenerated over ∼90 years.

Conclusion: We postulate that long-term ex situ conservation involving human and genotype × environment selection may significantly reduce accession heterogeneity and allelic diversity. Results are further discussed in a broader context of pre-breeding and conservation. © 2019 Society of Chemical Industry.
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http://dx.doi.org/10.1002/jsfa.9822DOI Listing
August 2020

Resistance of Aegilops longissima to the Rusts of Wheat.

Plant Dis 2018 Jun 2;102(6):1124-1135. Epub 2018 Apr 2.

School of Public Health, University of Minnesota, Minneapolis, 55455.

Stem rust (caused by Puccinia graminis f. sp. tritici), leaf rust (P. triticina), and stripe rust (P. striiformis f. sp. tritici) rank among the most important diseases of wheat worldwide. The development of resistant cultivars is the preferred method of controlling rust diseases because it is environmentally benign and also cost effective. However, new virulence types often arise in pathogen populations, rendering such cultivars vulnerable to losses. The identification of new sources of resistance is key to providing long-lasting disease control against the rapidly evolving rust pathogens. Thus, the objective of this research was to evaluate the wild wheat relative Aegilops longissima for resistance to stem rust, leaf rust, and stripe rust at the seedling stage in the greenhouse. A diverse collection of 394 accessions of the species, mostly from Israel, was assembled for the study, but the total number included in any one rust evaluation ranged from 308 to 379. With respect to stem rust resistance, 18.2 and 80.8% of accessions were resistant to the widely virulent U.S. and Kenyan P. graminis f. sp. tritici races of TTTTF and TTKSK, respectively. The percentage of accessions exhibiting resistance to the U.S. P. triticina races of THBJ and BBBD was 65.9 and 52.2%, respectively. Over half (50.1%) of the Ae. longissima accessions were resistant to the U.S. P. striiformis f. sp. tritici race PSTv-37. Ten accessions (AEG-683-23, AEG-725-15, AEG-803-49, AEG-1274-20, AEG-1276-22, AEG-1471-15, AEG-1475-19, AEG-2974-0, AEG-4005-20, and AEG-8705-10) were resistant to all races of the three rust pathogens used in this study. Distinct differences in the geographic distribution of resistance and susceptibility were found in Ae. longissima accessions from Israel in response to some rust races. To P. graminis f. sp. tritici race TTKSK, populations with a very high frequency of resistance were concentrated in the central and northern part of Israel, whereas populations with a comparatively higher frequency of susceptibility were concentrated in the southern part of the country. The reverse trend was observed with respect to P. striiformis f. sp. tritici race PSTv-37. The results from this study demonstrate that Ae. longissima is a rich source of rust resistance genes for wheat improvement.
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http://dx.doi.org/10.1094/PDIS-06-17-0880-REDOI Listing
June 2018

Cloning of the wheat Yr15 resistance gene sheds light on the plant tandem kinase-pseudokinase family.

Nat Commun 2018 10 3;9(1):3735. Epub 2018 Oct 3.

Institute of Evolution, University of Haifa, 199 Abba-Hushi Avenue, Mt. Carmel, 3498838, Haifa, Israel.

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.
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http://dx.doi.org/10.1038/s41467-018-06138-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6170490PMC
October 2018

Potential for re-emergence of wheat stem rust in the United Kingdom.

Commun Biol 2018 8;1:13. Epub 2018 Feb 8.

Limagrain UK Ltd, Woolpit, IP30 9UP, UK.

Wheat stem rust, a devastating disease of wheat and barley caused by the fungal pathogen f. sp. , was largely eradicated in Western Europe during the mid-to-late twentieth century. However, isolated outbreaks have occurred in recent years. Here we investigate whether a lack of resistance in modern European varieties, increased presence of its alternate host barberry and changes in climatic conditions could be facilitating its resurgence. We report the first wheat stem rust occurrence in the United Kingdom in nearly 60 years, with only 20% of UK wheat varieties resistant to this strain. Climate changes over the past 25 years also suggest increasingly conducive conditions for infection. Furthermore, we document the first occurrence in decades of on barberry in the UK . Our data illustrate that wheat stem rust does occur in the UK and, when climatic conditions are conducive, could severely harm wheat and barley production.
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http://dx.doi.org/10.1038/s42003-018-0013-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6053080PMC
February 2018

Correction to: Landraces of snake melon, an ancient Middle Eastern crop, reveal extensive morphological and DNA diversity for potential genetic improvement.

BMC Genet 2018 07 12;19(1):44. Epub 2018 Jul 12.

Mina and Everard Goodman Faculty of Life Sciences, Bar Ilan University, 5290002, Ramat Gan, Israel.

Following publication of the original article [1], the authors reported the need for a more detailed acknowledgement of the source of the samples that were analyzed and their coordinates, which are discussed in the 'Methods' section of the article. This Correction provides an addition to the 'Methods' section, and a subsequently revised 'Acknowledgements' and 'Availability of data and materials' section.
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http://dx.doi.org/10.1186/s12863-018-0632-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6042412PMC
July 2018

Landraces of snake melon, an ancient Middle Eastern crop, reveal extensive morphological and DNA diversity for potential genetic improvement.

BMC Genet 2018 05 23;19(1):34. Epub 2018 May 23.

Mina and Everard Goodman Faculty of Life Sciences, Bar Ilan University, 5290002, Ramat Gan, Israel.

Background: Snake melon (Cucumis melo var. flexuosus, "Faqqous") is a traditional and ancient vegetable in the Mediterranean area. A collection of landraces from 42 grower fields in Israel and Palestinian territories was grown and characterized in a "Common Garden" rain-fed experiment, at the morphological-horticultural and molecular level using seq-DArT markers.

Results: The different landraces ("populations") showed extensive variation in morphology and quantitative traits such as yield and femaleness, and clustered into four horticultural varieties. Yield was assessed by five harvests along the season, with middle harvests producing the highest yields. Yield correlated with early vigor, and with femaleness, but not with late vigor. At the molecular level, 2784 SNP were produced and > 90% were mapped to the melon genome. Populations were very polymorphic (46-72% of the markers biallelic in a 4 individuals sample), and observed heterozygosity was higher than the expected, suggesting gene flow among populations and extensive cross pollination among individuals in the field. Genetic distances between landraces were significantly correlated with the geographical distance between collecting sites, and with long term March precipitation average; variation in yield correlated with April temperature maxima.

Conclusions: The extensive variation suggests that selection of local snake melon could result in yield improvement. Correlations between traits and climatic variables could suggest local adaptation of landraces to the diverse environment in which they evolved. This study stresses the importance of preserving this germplasm, and its potential for breeding better snake melons as an heirloom crop in our region.
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http://dx.doi.org/10.1186/s12863-018-0619-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5966880PMC
May 2018

SNP-based pool genotyping and haplotype analysis accelerate fine-mapping of the wheat genomic region containing stripe rust resistance gene Yr26.

Theor Appl Genet 2018 Jul 17;131(7):1481-1496. Epub 2018 Apr 17.

State Key Laboratory of Crop Stress Biology for Arid Areas, Northwest A&F University, Yangling, Xianyang, 712100, Shaanxi, People's Republic of China.

Key Message: NGS-assisted super pooling emerging as powerful tool to accelerate gene mapping and haplotype association analysis within target region uncovering specific linkage SNPs or alleles for marker-assisted gene pyramiding. Conventional gene mapping methods to identify genes associated with important agronomic traits require significant amounts of financial support and time. Here, a single nucleotide polymorphism (SNP)-based mapping approach, RNA-Seq and SNP array assisted super pooling analysis, was used for rapid mining of a candidate genomic region for stripe rust resistance gene Yr26 that has been widely used in wheat breeding programs in China. Large DNA and RNA super-pools were genotyped by Wheat SNP Array and sequenced by Illumina HiSeq, respectively. Hundreds of thousands of SNPs were identified and then filtered by multiple filtering criteria. Among selected SNPs, over 900 were found within an overlapping interval of less than 30 Mb as the Yr26 candidate genomic region in the centromeric region of chromosome arm 1BL. The 235 chromosome-specific SNPs were converted into KASP assays to validate the Yr26 interval in different genetic populations. Using a high-resolution mapping population (> 30,000 gametes), we confined Yr26 to a 0.003-cM interval. The Yr26 target region was anchored to the common wheat IWGSC RefSeq v1.0 and wild emmer WEWSeq v.1.0 sequences, from which 488 and 454 kb fragments were obtained. Several candidate genes were identified in the target genomic region, but there was no typical resistance gene in either genome region. Haplotype analysis identified specific SNPs linked to Yr26 and developed robust and breeder-friendly KASP markers. This integration strategy can be applied to accelerate generating many markers closely linked to target genes/QTL for a trait of interest in wheat and other polyploid species.
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http://dx.doi.org/10.1007/s00122-018-3092-8DOI Listing
July 2018

Genome Targeted Introgression of Resistance to African Stem Rust from into Bread Wheat.

Plant Genome 2017 11;10(3)

Many accessions of the wheat wild relative Sharon goatgrass ( Eig., ) are resistant to African races of the stem rust pathogen (i.e., Ug99 group races), which currently threaten wheat production worldwide. A procedure was designed to introgress the respective resistances to specific bread wheat genomes by producing plants homozygous for the A and B genomes and hemizygous for the D and S genomes or homozygous for the A and D genomes and hemizygous for the B and S genomes. In these genotypes, which lack the allele, homeologous pairing was expected mainly between chromosomes of the D and S genomes or B and S genomes, respectively. An antigametocidal (AG) wheat mutant () was used to overcome gametocidal effects. Wheat lines initially found resistant at the seedling stage were also highly resistant at the adult plant stage in rust nurseries established in the field. DNA of 41 selected homozygous resistant lines, analyzed by the Axiom wheat 820K SNP array, showed alien chromatin mainly in wheat chromosomes 1B, 1D, and 5B. This work suggests that, in most cases, it is possible to target introgressions into the homeologous chromosome of a selected genome of bread wheat.
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http://dx.doi.org/10.3835/plantgenome2017.07.0061DOI Listing
November 2017

Wild emmer genome architecture and diversity elucidate wheat evolution and domestication.

Science 2017 07;357(6346):93-97

University of Bologna, Bologna, Italy.

Wheat ( spp.) is one of the founder crops that likely drove the Neolithic transition to sedentary agrarian societies in the Fertile Crescent more than 10,000 years ago. Identifying genetic modifications underlying wheat's domestication requires knowledge about the genome of its allo-tetraploid progenitor, wild emmer ( ssp. ). We report a 10.1-gigabase assembly of the 14 chromosomes of wild tetraploid wheat, as well as analyses of gene content, genome architecture, and genetic diversity. With this fully assembled polyploid wheat genome, we identified the causal mutations in () genes controlling shattering, a key domestication trait. A study of genomic diversity among wild and domesticated accessions revealed genomic regions bearing the signature of selection under domestication. This reference assembly will serve as a resource for accelerating the genome-assisted improvement of modern wheat varieties.
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http://dx.doi.org/10.1126/science.aan0032DOI Listing
July 2017

Discovery and characterization of two new stem rust resistance genes in Aegilops sharonensis.

Theor Appl Genet 2017 Jun 8;130(6):1207-1222. Epub 2017 Mar 8.

John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, UK.

Key Message: We identified two novel wheat stem rust resistance genes, Sr-1644-1Sh and Sr-1644-5Sh in Aegilops sharonensis that are effective against widely virulent African races of the wheat stem rust pathogen. Stem rust is one of the most important diseases of wheat in the world. When single stem rust resistance (Sr) genes are deployed in wheat, they are often rapidly overcome by the pathogen. To this end, we initiated a search for novel sources of resistance in diverse wheat relatives and identified the wild goatgrass species Aegilops sharonesis (Sharon goatgrass) as a rich reservoir of resistance to wheat stem rust. The objectives of this study were to discover and map novel Sr genes in Ae. sharonensis and to explore the possibility of identifying new Sr genes by genome-wide association study (GWAS). We developed two biparental populations between resistant and susceptible accessions of Ae. sharonensis and performed QTL and linkage analysis. In an F recombinant inbred line and an F population, two genes were identified that mapped to the short arm of chromosome 1S, designated as Sr-1644-1Sh, and the long arm of chromosome 5S, designated as Sr-1644-5Sh. The gene Sr-1644-1Sh confers a high level of resistance to race TTKSK (a member of the Ug99 race group), while the gene Sr-1644-5Sh conditions strong resistance to TRTTF, another widely virulent race found in Yemen. Additionally, GWAS was conducted on 125 diverse Ae. sharonensis accessions for stem rust resistance. The gene Sr-1644-1Sh was detected by GWAS, while Sr-1644-5Sh was not detected, indicating that the effectiveness of GWAS might be affected by marker density, population structure, low allele frequency and other factors.
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http://dx.doi.org/10.1007/s00122-017-2882-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5440502PMC
June 2017

Evolution and Adaptation of Wild Emmer Wheat Populations to Biotic and Abiotic Stresses.

Annu Rev Phytopathol 2016 08 1;54:279-301. Epub 2016 Jan 1.

Department of Evolutionary and Environmental Biology and The Institute of Evolution, University of Haifa, Haifa 3498838, Israel; email:

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.
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http://dx.doi.org/10.1146/annurev-phyto-080614-120254DOI Listing
August 2016

Distribution and haplotype diversity of WKS resistance genes in wild emmer wheat natural populations.

Theor Appl Genet 2016 May 5;129(5):921-34. Epub 2016 Feb 5.

Institute of Evolution and the Department of Evolutionary and Environmental Biology, University of Haifa, 3498838, Haifa, Israel.

Key Message: The wheat stripe rust resistance gene Yr36 ( WKS1 ) with a unique kinase-START domain architecture is highly conserved in wild emmer wheat natural populations. Wild emmer wheat (Triticum dicoccoides) populations have developed various resistance strategies against the stripe rust pathogen Puccinia striiformis f. sp. tritici (Pst). The wild emmer gene, Yr36 (WKS1), which confers partial resistance to a broad spectrum of Pst races, is composed of a kinase and a START lipid-binding domain, a unique gene architecture found only in the Triticeae tribe. The analysis of 435 wild emmer accessions from a broad range of natural habitats revealed that WKS1 and its paralogue WKS2 are present only in the southern distribution range of wild emmer in the Fertile Crescent, supporting the idea that wheat domestication occurred in the northern populations. An analysis of full-length WKS1 sequence from 54 accessions identified 15 different haplotypes and very low-nucleotide diversity (π = 0.00019). The high level of WKS1 sequence conservation among wild emmer populations is in contrast to the high level of diversity previously observed in NB-LRR genes (e.g., Lr10 and Pm3). This phenomenon may reflect the different resistance mechanisms and different evolutionary pathways that shaped these genes, and may shed light on the evolution of genes that confer partial resistance to stripe rust. Only five WKS1 coding sequence haplotypes were revealed among all tested accessions, encoding four different putative WKS1 proteins (designated P0, P1, P2, and P3). Infection tests showed that P0, P1, and P3 haplotypes display a resistance response, while P2 displayed a susceptible response. These results show that the WKS1 proteins (P0, P1, and P3) can be useful to improve wheat resistance to stripe rust.
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http://dx.doi.org/10.1007/s00122-016-2672-8DOI Listing
May 2016

Resistance of Aegilops Species from Israel to Widely Virulent African and Israeli Races of the Wheat Stem Rust Pathogen.

Plant Dis 2014 Oct;98(10):1309-1320

Department of Plant Pathology, University of Minnesota.

Widely virulent races of the stem rust pathogen (Puccinia graminis f. sp. tritici) such as those isolated from Africa (e.g., TTKSK, isolate synonym Ug99) threaten wheat production worldwide. To identify Aegilops accessions with effective resistance to such virulent stem rust races, up to 10 different species from Israel were evaluated against African races TTKSK, TTKST, and TTTSK and the Israeli race TTTTC as seedlings in the greenhouse. A wide diversity of stem rust reactions was observed across the Aegilops spp. and ranged from highly resistant (i.e., infection type 0) to highly susceptible (infection type 4). The frequency of resistance within a species to races TTTTC and TTKSK ranged from 7 and 14%, respectively, in Aegilops searsii to 98 and 100% in AE. speltoides. In all, 346 accessions were found resistant to the three African races and 138 accessions were resistant (or heterogeneous with a resistant component) to all four races. The species with broadly resistant accessions included Ae. longissima (59 accessions), Ae. peregrina (47 accessions), Ae. sharonensis (15 accessions), Ae. geniculata (9 accessions), Ae. kotschyi (5 accessions), and Ae. bicornis (3 accessions). Few geographical trends or correlations with climatic variables were observed with respect to stem rust resistance in the Aegilops spp. The exception was Ae. longissima infected with race TTTTC, where a high frequency of resistance was found in central and northern Israel and a very low frequency in southern Israel (Negev desert region). This geographical trend followed a pattern of annual precipitation in Israel, and a significant correlation was found between this variable and resistance in Ae. longissima. Although difficult, it is feasible to transfer resistance genes from Aegilops spp. into wheat through conventional wide-crossing schemes or, alternatively, a cloning and transformation approach. The broadly resistant accessions identified in this study will be valuable in these research programs.
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http://dx.doi.org/10.1094/PDIS-01-14-0062-REDOI Listing
October 2014

Linkage disequilibrium and association analysis of stripe rust resistance in wild emmer wheat (Triticum turgidum ssp. dicoccoides) population in Israel.

Theor Appl Genet 2014 Nov 16;127(11):2453-63. Epub 2014 Sep 16.

The Institute for Cereal Crops Improvement, Tel-Aviv University, P.O. Box 39040, 69978, Tel Aviv, Israel,

Key Message: Rapid LD decay in wild emmer population from Israel allows high-resolution association mapping. Known and putative new stripe rust resistance genes were found. Genome-wide association mapping (GWAM) is becoming an important tool for the discovery and mapping of loci underlying trait variation in crops, but in the wild relatives of crops the use of GWAM has been limited. Critical factors for the use of GWAM are the levels of linkage disequilibrium (LD) and genetic diversity in mapped populations, particularly in those of self-pollinating species. Here, we report LD estimation in a population of 128 accessions of self-pollinating wild emmer, Triticum turgidum ssp. dicoccoides, the progenitor of cultivated wheat, collected in Israel. LD decayed fast along wild emmer chromosomes and reached the background level within 1 cM. We employed GWAM for the discovery and mapping of genes for resistance to three isolates of Puccinia striiformis, the causative agent of wheat stripe rust. The wild emmer population was genotyped with the wheat iSelect assay including 8643 gene-associated SNP markers (wheat 9K Infinium) of which 2,278 were polymorphic. The significance of association between stripe rust resistance and each of the polymorphic SNP was tested using mixed linear model implemented in EMMA software. The model produced satisfactory results and uncovered four significant associations on chromosome arms 1BS, 1BL and 3AL. The locus on 1BS was located in a region known to contain stripe rust resistance genes. These results show that GWAM is an effective strategy for gene discovery and mapping in wild emmer that will accelerate the utilization of this genetic resource in wheat breeding.
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http://dx.doi.org/10.1007/s00122-014-2389-5DOI Listing
November 2014

Three-dimensional modeling and diversity analysis reveals distinct AVR recognition sites and evolutionary pathways in wild and domesticated wheat Pm3 R genes.

Mol Plant Microbe Interact 2014 Aug;27(8):835-45

The Pm3 gene confers resistance against wheat powdery mildew. Studies of Pm3 diversity have shown that Pm3 alleles isolated from southern populations of wild emmer wheat located in Lebanon, Jordan, Israel, and Syria are more diverse and more distant from bread wheat alleles than alleles from the northern wild wheat populations located in Turkey, Iran, and Iraq. Therefore, southern populations from Israel were studied extensively to reveal novel Pm3 alleles that are absent from the cultivated gene pool. Candidate Pm3 genes were isolated via a polymerase chain reaction cloning approach. Known and newly identified Pm3 genes were subjected to variation analysis and polymorphic amino acid residues were superimposed on a three-dimensional (3D) model of PM3. The region of highest interspecies diversity between Triticum aestivum and T. dicoccoides lies in leucine-rich repeats (LRR) 19 to 24, whereas most intraspecies diversity in T. aestivum is located in LRR 25 to 28. Interestingly, these two regions are separated by one large LRR whose propensity for flexibility facilitates the conformation of the PM3 LRR domain into two differently structured models. The combination of evolutionary and protein 3D structure analysis revealed that Pm3 genes in wild and domesticated wheat show different evolutionary histories which might have been triggered through different interactions with the powdery mildew pathogen.
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http://dx.doi.org/10.1094/MPMI-01-14-0009-RDOI Listing
August 2014

The physical map of wheat chromosome 1BS provides insights into its gene space organization and evolution.

Genome Biol 2013 Dec 20;14(12):R138. Epub 2013 Dec 20.

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.
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http://dx.doi.org/10.1186/gb-2013-14-12-r138DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4053865PMC
December 2013

Population-genetic analysis of HvABCG31 promoter sequence in wild barley (Hordeum vulgare ssp. spontaneum).

BMC Evol Biol 2012 Sep 24;12:188. Epub 2012 Sep 24.

Extreme Stress Resistance and Biotechnology Laboratory, Cold and Arid Regions Environmental and Engineering Institute, Chinese Academy of Sciences, Lanzhou 730000, China.

Background: The cuticle is an important adaptive structure whose origin played a crucial role in the transition of plants from aqueous to terrestrial conditions. HvABCG31/Eibi1 is an ABCG transporter gene, involved in cuticle formation that was recently identified in wild barley (Hordeum vulgare ssp. spontaneum). To study the genetic variation of HvABCG31 in different habitats, its 2 kb promoter region was sequenced from 112 wild barley accessions collected from five natural populations from southern and northern Israel. The sites included three mesic and two xeric habitats, and differed in annual rainfall, soil type, and soil water capacity.

Results: Phylogenetic analysis of the aligned HvABCG31 promoter sequences clustered the majority of accessions (69 out of 71) from the three northern mesic populations into one cluster, while all 21 accessions from the Dead Sea area, a xeric southern population, and two isolated accessions (one from a xeric population at Mitzpe Ramon and one from the xeric 'African Slope' of "Evolution Canyon") formed the second cluster. The southern arid populations included six haplotypes, but they differed from the consensus sequence at a large number of positions, while the northern mesic populations included 15 haplotypes that were, on average, more similar to the consensus sequence. Most of the haplotypes (20 of 22) were unique to a population. Interestingly, higher genetic variation occurred within populations (54.2%) than among populations (45.8%). Analysis of the promoter region detected a large number of transcription factor binding sites: 121-128 and 121-134 sites in the two southern arid populations, and 123-128,125-128, and 123-125 sites in the three northern mesic populations. Three types of TFBSs were significantly enriched: those related to GA (gibberellin), Dof (DNA binding with one finger), and light.

Conclusions: Drought stress and adaptive natural selection may have been important determinants in the observed sequence variation of HvABCG31 promoter. Abiotic stresses may be involved in the HvABCG31 gene transcription regulations, generating more protective cuticles in plants under stresses.
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http://dx.doi.org/10.1186/1471-2148-12-188DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3544613PMC
September 2012

Ancient diversity of splicing motifs and protein surfaces in the wild emmer wheat (Triticum dicoccoides) LR10 coiled coil (CC) and leucine-rich repeat (LRR) domains.

Mol Plant Pathol 2012 Apr 23;13(3):276-87. Epub 2011 Sep 23.

Department of Evolutionary and Environmental Biology, Institute of Evolution, University of Haifa, Mt. Carmel, Haifa 31905, Israel.

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.
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http://dx.doi.org/10.1111/j.1364-3703.2011.00744.xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6638671PMC
April 2012

Rapid linkage disequilibrium decay in the Lr10 gene in wild emmer wheat (Triticum dicoccoides) populations.

Theor Appl Genet 2011 Jan 22;122(1):175-87. Epub 2010 Sep 22.

Department of Evolutionary and Environmental Biology, Institute of Evolution, Faculty of Natural Sciences, University of Haifa, Mt. Carmel, Haifa, 31905, Israel.

Introduction: Recombination is a key evolutionary factor enhancing diversity. However, the effect of recombination on diversity in inbreeding species is expected to be low. To estimate this effect, recombination and diversity patterns of Lr10 gene were studied in natural populations of the inbreeder species, wild emmer wheat (Triticum dicoccoides). Wild emmer wheat is the progenitor of most cultivated wheats and it harbors rich genetic resources for disease resistance. Lr10 is a leaf rust resistance gene encoding three domains: a coiled-coil, nucleotide-binding site, and leucine-rich repeat (CC-NBS-LRR).

Results: Lr10 was sequenced from 58 accessions representing 12 diverse habitats in Israel. Diversity analysis revealed a high rate of synonymous and non-synonymous substitutions (d (S) = 0.029, d (N) = 0.018, respectively) in the NBS-LRR domains. Moreover, in contrast to other resistance genes, in Lr10 the CC domain was more diverse than the NBS-LRR domains (d (S) = 0.069 vs. 0.029, d (N) = 0.094 vs. 0.018) and was subjected to positive selection in some of the populations. Seventeen recombination events were detected between haplotypes, especially in the CC domain. Linkage disequilibrium (LD) analysis has shown a rapid decay from r (2) = 0.5 to r (2) = 0.1 within a 2-kb span.

Conclusion: These results suggest that recombination is a diversifying force for the R-gene, Lr10, in the selfing species T. dicoccoides. This is the first report of a short-range LD decay in wild emmer wheat.
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http://dx.doi.org/10.1007/s00122-010-1434-2DOI Listing
January 2011

Pathogen race determines the type of resistance response in the stripe rust-Triticum dicoccoides pathosystem.

Physiol Plant 2010 Jul 16;139(3):269-79. Epub 2010 Feb 16.

Department of Evolutionary and Environmental Biology, Institute of Evolution, Faculty of Science and Science Education, University of Haifa, Mt Carmel, Haifa 31905, Israel.

Wild relatives of crop plants may serve as a promising source for screening for new disease resistance genes that can be utilized in breeding programs. Triticum dicoccoides, the wild progenitor of most cultivated wheats, was shown to harbor many resistance genes against the major diseases attacking cultivated wheat. Stripe rust is a devastating fungal disease that attacks wheat in many regions of the world. New races of Puccinia striiformis Westend. f. sp. tritici, the causative agent of stripe rust, have overcome most of the known Yr resistance genes in wheat. Therefore, there is a need to search for new resistance genes in the T. dicoccoides gene pool. A set of 120 T. dicoccoides accessions, collected from 13 populations representing different habitats in Israel and vicinity, was tested for resistance to three prevalent stripe rust races (38E134, 6E16 and 6E0). Of these 120 accessions, 14, 8 and 12% were resistant to races 38E134, 6E16 and 6E0, respectively, while 57, 2 and 4% were moderately resistant to these races, respectively. A unique resistance was found in the population of Mt Hermon where >80% of the accessions showed resistance to all races. Distribution of infection types (ITs) of race 38E134 showed a normal distribution that can fit a quantitative pattern of response, while the distributions of ITs of races 6E16 and 6E0 had excess of extreme values and therefore showing a qualitative pattern of response. anova testing the main factor effects and interaction showed significant effects of population, race and their interaction on IT. Significant positive correlations were obtained between the resistance to races 6E16 and 6E0 and humidity variables of the collections sites, while resistance to race 38E134 was positively correlated with temperature variables. These results show that the pathogen race can determine the type of resistance response, qualitative or quantitative, in the stripe rust-T. dicoccoides pathosystem. The obtained results also reveal that the distribution of resistance to different pathogen races can be affected by different climatic factors.
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http://dx.doi.org/10.1111/j.1399-3054.2010.01364.xDOI Listing
July 2010

Divergent diversity patterns of NBS and LRR domains of resistance gene analogs in wild emmer wheat populations.

Genome 2009 Jun;52(6):557-65

Department of Evolutionary and Environmental Biology, Institute of Evolution, Faculty of Science and Science Education, University of Haifa, Mt. Carmel, Haifa, 31905 Israel.

Disease resistance (R) genes are intriguing in their evolution and diversity patterns because of their constant interactions with evolving pathogens. In this study, we demonstrate the use of resistance gene analog (RGA) markers to estimate genetic diversity among 13 populations (118 genotypes) of Triticum dicoccoides collected along a natural aridity gradient in Israel. The diversity patterns of 204 markers derived from two R-gene domains, nucleotide binding site (NBS) and leucine-rich repeat (LRR), were compared and contrasted. Diversity patterns of NBS domain markers differed significantly from those of the LRR domain. NBS markers showed higher between-population diversity (Fst=0.58), while LRR markers showed higher within-population diversity (Fst=0.35). Gene diversity (He) values were twofold higher in the LRR domain than in the NBS domain (0.144 vs. 0.067). LRR He values were correlated with precipitation in the spring (r=0.8, p=0.01), while NBS He values showed no correlation with any ecogeographical variable. The evolutionary and applicative inferences of these findings are discussed. The current study demonstrates that RGA profiling is an excellent tool for studying diversity of R genes in natural plant populations.
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http://dx.doi.org/10.1139/g09-030DOI Listing
June 2009

A kinase-START gene confers temperature-dependent resistance to wheat stripe rust.

Science 2009 Mar 19;323(5919):1357-60. Epub 2009 Feb 19.

Department of Plant Sciences, University of California, Davis, CA 95616, USA.

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 degrees to 35 degrees 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.
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http://dx.doi.org/10.1126/science.1166289DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4737487PMC
March 2009

Cassandra retrotransposons carry independently transcribed 5S RNA.

Proc Natl Acad Sci U S A 2008 Apr 11;105(15):5833-8. Epub 2008 Apr 11.

MTT/BI Plant Genomics Laboratory, Institute of Biotechnology, Viikki Biocenter, University of Helsinki, FIN-00014, Helsinki, Finland.

We report a group of TRIMs (terminal-repeat retrotransposons in miniature), which are small nonautonomous retrotransposons. These elements, named Cassandra, universally carry conserved 5S RNA sequences and associated RNA polymerase (pol) III promoters and terminators in their long terminal repeats (LTRs). They were found in all vascular plants investigated. Uniquely for LTR retrotransposons, Cassandra produces noncapped, polyadenylated transcripts from the 5S pol III promoter. Capped, read-through transcripts containing Cassandra sequences can also be detected in RNA and in EST databases. The predicted Cassandra RNA 5S secondary structures resemble those for cellular 5S rRNA, with high information content specifically in the pol III promoter region. Genic integration sites are common for Cassandra, an unusual feature for abundant retrotransposons. The 5S in each LTR produces a tandem 5S arrangement with an inter-5S spacing resembling that of cellular 5S. The distribution of 5S genes is very variable in flowering plants and may be partially explained by Cassandra activity. Cassandra thus appears both to have adapted a ubiquitous cellular gene for ribosomal RNA for use as a promoter and to parasitize an as-yet-unidentified group of retrotransposons for the proteins needed in its lifecycle.
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http://dx.doi.org/10.1073/pnas.0709698105DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2311327PMC
April 2008