Identification and mapping of Sr46 from Aegilops tauschii accession CIae 25 conferring resistance to race TTKSK (Ug99) of wheat stem rust pathogen

Abstract Parasexuality contributes to diversity and adaptive evolution of haploid (monokaryotic) fungi. However, non-sexual genetic exchange mechanisms are not defined in dikaryotic fungi (containing two distinct haploid nuclei). Newly emerged strains of the wheat stem rust pathogen, Puccinia graminis f. sp. tritici (Pgt), such as Ug99, are a major threat to global food security. Here, we provide genomics-based evidence supporting that Ug99 arose by somatic hybridisation and nuclear exchange between dikaryons. Fully haplotype-resolved genome assembly and DNA proximity analysis reveal that Ug99 shares one haploid nucleus genotype with a much older African lineage of Pgt, with no recombination or chromosome reassortment. These findings indicate that nuclear exchange between dikaryotes can generate genetic diversity and facilitate the emergence of new lineages in asexual fungal populations.

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Emergence of the Ug99 lineage of the wheat stem rust pathogen through somatic hybridisation

10.1101/692640 ◽

2019 ◽

Cited By ~ 1

Author(s):

Feng Li ◽

Narayana M. Upadhyaya ◽

Jana Sperschneider ◽

Oadi Matny ◽

Hoa Nguyen-Phuc ◽

...

Keyword(s):

Stem Rust ◽

Puccinia Graminis ◽

Wheat Stem Rust ◽

Haploid Nucleus ◽

Somatic Hybridisation ◽

Global Food Security ◽

Proximity Analysis ◽

Rust Pathogen ◽

Nuclear Exchange ◽

Global Food

AbstractParasexuality contributes to diversity and adaptive evolution of haploid (monokaryotic) fungi. However non-sexual genetic exchange mechanisms are not defined in dikaryotic fungi (containing two distinct haploid nuclei). Newly emerged strains of the wheat stem rust pathogen, Puccinia graminis f. sp. tritici (Pgt), such as Ug99, are a major threat to global food security. Here we show that Ug99 arose by somatic hybridisation and nuclear exchange between dikaryons. Fully haplotype-resolved genome assembly and DNA proximity analysis revealed that Ug99 shares one haploid nucleus genotype with a much older African lineage of Pgt, with no recombination or reassortment. Generation of genetic variation by nuclear exchange may favour the evolution of dikaryotism by providing an advantage over diploidy.

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

Plant Disease ◽

10.1094/pdis-01-14-0062-re ◽

2014 ◽

Vol 98 (10) ◽

pp. 1309-1320 ◽

Cited By ~ 4

Author(s):

Jeness C. Scott ◽

Jacob Manisterski ◽

Hanan Sela ◽

Pnina Ben-Yehuda ◽

Brian J. Steffenson

Keyword(s):

Stem Rust ◽

High Frequency ◽

Infection Type ◽

Low Frequency ◽

Puccinia Graminis ◽

Aegilops Species ◽

Wheat Stem Rust ◽

Transfer Resistance ◽

Desert Region ◽

Rust Pathogen

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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Comparative genomics of Australian isolates of the wheat stem rust pathogen Puccinia graminis f. sp. tritici reveals extensive polymorphism in candidate effector genes

Frontiers in Plant Science ◽

10.3389/fpls.2014.00759 ◽

2015 ◽

Vol 5 ◽

Cited By ~ 42

Author(s):

Narayana M. Upadhyaya ◽

Diana P. Garnica ◽

Haydar Karaoglu ◽

Jana Sperschneider ◽

Adnane Nemri ◽

...

Keyword(s):

Comparative Genomics ◽

Stem Rust ◽

Puccinia Graminis ◽

Wheat Stem Rust ◽

Effector Genes ◽

Rust Pathogen

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The Gene Sr33, an Ortholog of Barley Mla Genes, Encodes Resistance to Wheat Stem Rust Race Ug99

Science ◽

10.1126/science.1239028 ◽

2013 ◽

Vol 341 (6147) ◽

pp. 786-788 ◽

Cited By ~ 205

Author(s):

Sambasivam Periyannan ◽

John Moore ◽

Michael Ayliffe ◽

Urmil Bansal ◽

Xiaojing Wang ◽

...

Keyword(s):

Bread Wheat ◽

Stem Rust ◽

Haplotype Analysis ◽

Aegilops Tauschii ◽

Coiled Coil ◽

Puccinia Graminis ◽

The Caspian Sea ◽

Wheat Stem Rust ◽

Wheat Gene ◽

Leucine Rich Repeat Protein

Wheat stem rust, caused by the fungus Puccinia graminis f. sp. tritici, afflicts bread wheat (Triticum aestivum). New virulent races collectively referred to as “Ug99” have emerged, which threaten global wheat production. The wheat gene Sr33, introgressed from the wild relative Aegilops tauschii into bread wheat, confers resistance to diverse stem rust races, including the Ug99 race group. We cloned Sr33, which encodes a coiled-coil, nucleotide-binding, leucine-rich repeat protein. Sr33 is orthologous to the barley (Hordeum vulgare) Mla mildew resistance genes that confer resistance to Blumeria graminis f. sp. hordei. The wheat Sr33 gene functions independently of RAR1, SGT1, and HSP90 chaperones. Haplotype analysis from diverse collections of Ae. tauschii placed the origin of Sr33 resistance near the southern coast of the Caspian Sea.

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Isozyme Studies on the Origin and Evolution of Puccinia Graminis F. SP. Tritici in Australia

Australian Journal of Biological Sciences ◽

10.1071/bi9820231 ◽

1982 ◽

Vol 35 (2) ◽

pp. 231 ◽

Cited By ~ 50

Author(s):

JJ Burdon ◽

DR Marshall ◽

NH Luig ◽

DJS Gow

Keyword(s):

Stem Rust ◽

Major Change ◽

Puccinia Graminis ◽

Flora Of Australia ◽

Wheat Stem Rust ◽

Origin And Evolution ◽

Enzyme Systems ◽

Rust Pathogen

Isozyme phenotypes for eight enzyme systems were used to assess the origins and evolution of P. graminis f. sp. tritici (the wheat stem rust pathogen) in Australia. The results obtained by this approach agreed with pathways postulated on the basis of virulence studies, confirming the suggestion that most of the major changes in the wheat stem rust pathogen flora of Australia have resulted from overseas introductions. Moreover, they suggest that, although the more recent of these were from Africa, the first major change detected occurred as a result of an introduction from elsewhere.

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Allele Characterization of Genes Required for rpg4-Mediated Wheat Stem Rust Resistance Identifies Rpg5 as the R Gene

Phytopathology ◽

10.1094/phyto-01-13-0030-r ◽

2013 ◽

Vol 103 (11) ◽

pp. 1153-1161 ◽

Cited By ~ 22

Author(s):

D. Arora ◽

T. Gross ◽

R. Brueggeman

Keyword(s):

Amino Acid ◽

Stem Rust ◽

Rust Resistance ◽

Nucleotide Substitution ◽

Wild Barley ◽

Stop Codon ◽

Stem Rust Resistance ◽

R Gene ◽

Wheat Stem Rust ◽

Rust Pathogen

A highly virulent form of the wheat stem rust pathogen Puccinia graminis f. sp. tritici race TTKSK is virulent on both wheat and barley, presenting a major threat to world food security. The recessive and temperature-sensitive rpg4 gene is the only effective source of resistance identified in barley (Hordeum vulgare) against P. graminis f. sp. tritici race TTKSK. Efforts to position clone rpg4 localized resistance to a small interval on barley chromosome 5HL, tightly linked to the rye stem rust (P. graminis f. sp. secalis) resistance (R) gene Rpg5. High-resolution genetic analysis and post-transcriptional gene silencing of the genes at the rpg4/Rpg5 locus determined that three tightly linked genes (Rpg5, HvRga1, and HvAdf3) are required together for rpg4-mediated wheat stem rust resistance. Alleles of the three genes were analyzed from a diverse set of 14 domesticated barley lines (H. vulgare) and 8 wild barley accessions (H. vulgare subsp. spontaneum) to characterize diversity that may determine incompatibility (resistance). The analysis determined that HvAdf3 and HvRga1 code for predicted functional proteins that do not appear to contain polymorphisms determining the compatible (susceptible) interactions with the wheat stem rust pathogen and were expressed at the transcriptional level from both resistant and susceptible barley lines. The HvAdf3 alleles shared 100% amino acid identity among all 22 genotypes examined. The P. graminis f. sp. tritici race QCCJ-susceptible barley lines with HvRga1 alleles containing the limited amino acid substitutions unique to the susceptible varieties also contained predicted nonfunctional rpg5 alleles. Thus, susceptibility in these lines is likely due to the nonfunctional RPG5 proteins. The Rpg5 allele analysis determined that 9 of the 13 P. graminis f. sp. tritici race QCCJ-susceptible barley lines contain alleles that either code for predicted truncated proteins as the result of a single nucleotide substitution, resulting in a stop codon at amino acid 161, a single cytosine indel causing a frame shift, and a stop codon at amino acid 217, or an indel that deleted the entire STPK domain. The three P. graminis f. sp. tritici race QCCJ-susceptible lines (Swiss landraces Hv489, Hv492, and Hv611) and the wild barley accession WBDC160 contain rpg5 alleles predicted to encode full-length proteins containing a nonsynonomous nucleotide substitution that results in the amino acid substitution E1287A. This amino acid substitution present in the uncharacterized C-terminal domain is not found in any resistant line and may be important to elicit the resistance reaction. These data suggest that rpg4-mediated resistance against many wheat stem rust pathogen races, including P. graminis f. sp. tritici race TTKSK, rely on the Rpg5 R gene; thus, rpg4- and Rpg5-mediated resistance rely on a common R gene and should not be considered completely distinct. The data also determined that Rpg5 gene-specific molecular markers could be used to detect rpg4-mediated wheat stem rust resistance for marker-assisted selection.

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Constructing Physical and Genomic Maps forPuccinia striiformisf. sp.tritici, the Wheat Stripe Rust Pathogen, by Comparing Its EST Sequences to the Genomic Sequence ofP. graminisf. sp.tritici, the Wheat Stem Rust Pathogen

Comparative and Functional Genomics ◽

10.1155/2009/302620 ◽

2009 ◽

Vol 2009 ◽

pp. 1-13 ◽

Cited By ~ 2

Author(s):

Jinbiao Ma ◽

Xianming Chen ◽

Meinan Wang ◽

Zhensheng Kang

Keyword(s):

Stripe Rust ◽

Stem Rust ◽

Genomic Sequence ◽

Molecular Mapping ◽

Puccinia Striiformis ◽

Rust Fungus ◽

Wheat Stem Rust ◽

Wheat Stripe Rust ◽

Physical Relationship ◽

Rust Pathogen

The wheat stripe rust fungus,Puccinia striiformisf. sp.tritici(Pst), does not have a known alternate host for sexual reproduction, which makes it impossible to study gene linkages through classic genetic and molecular mapping approaches. In this study, we compared 4,219Pstexpression sequence tags (ESTs) to the genomic sequence ofP. graminisf. sp.tritici(Pgt), the wheat stem rust fungus, using BLAST searches. The percentages of homologous genes varied greatly among differentPstlibraries with 54.51%, 51.21%, and 13.61% for the urediniospore, germinated urediniospore, and haustorial libraries, respectively, with an average of 33.92%. The 1,432Pstgenes with significant homology withPgtsequences were grouped into physical groups corresponding to 237Pgtsupercontigs. The physical relationship was demonstrated by 12 pairs (57%), out of 21 selectedPstgene pairs, through PCR screening of aPstBAC library. The results indicate that thePgtgenome sequence is useful in constructingPstphysical maps.

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