Dissecting the first phased dikaryotic genomes of the wheat rust pathogen Puccinia triticina reveals the mechanisms of somatic exchange in nature

AbstractAlthough somatic hybridization (SH) has been proposed as a means of accelerating rust pathogen virulence evolution in the absence of sexual recombination, previous studies are limited to the laboratory and none have revealed how this process happens. Using long-read sequencing, we generated dikaryotic phased genomes and annotations for three Australian field-collected isolates of the wheat leaf rust pathogen (Puccinia triticina; Pt), including a putative asexual hybrid (Pt64) and two putative parental isolates (Pt104 and Pt53; 132-141 Mb,155-176 contigs, N50 of 1.9-2.1 Mb). The genetic dissection based on the high-quality phased genomes including whole-genome alignments, phylogenetic and syntenic analyses along with short-read sequencing of 27 additional Pt isolates convergently demonstrated that Pt64, which rendered several commercial hybrid wheat cultivars susceptible to leaf rust, arose from SH between isolates within the Pt53 and Pt104 lineages. Parentage analysis demonstrated the role of mitotic crossover in the derivation of both nuclei of Pt64. Within HD mating type genes, the distinct specificity regions in Pt64 and the distinct phylogenetic pattern of the remaining admixed isolates suggested high genetic variation in specificity-related regions on the b locus intrinsically associated with the SH. This study not only provided a fundamental platform for investigating genomic variation underlying virulence evolution in one of the most devastating wheat pathogens, but also offered an in-depth understanding of the mechanisms of naturally occurring SH. This asexual mechanism can be broadly exploited by any dikaryotic pathogen to accelerate virulence evolution, and understanding this process is both urgent and crucial for sustainable pathogen control.ImportanceStrategies to manage plant rust pathogens are challenged by the constant emergence of new virulence. Although somatic hybridization has been proposed as a means by which rusts could overcome host resistance rapidly and cause crop loss, there is very little evidence of this process in nature and the mechanisms underlying it are not known. This study generated and analysed the first dikaryotic phased genomes of the wheat leaf rust pathogen, identifying an isolate as a hybrid and for the first time unveiling parasexuality via mitotic crossover in a rust pathogen. The erosion of the resistance of several hybrid wheat cultivars in agriculture by the hybrid rust has important implications for breeding efforts targeting durable resistance and sustained rust control.

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Physiologic specialization of wheat leaf rust (Puccinia triticina Eriks.) in the Slovak Republic in 2005, 2006 and 2008

Czech Journal of Genetics and Plant Breeding ◽

10.17221/38/2010-cjgpb ◽

2010 ◽

Vol 46 (No. 3) ◽

pp. 114-121 ◽

Cited By ~ 1

Author(s):

A. Hanzalová ◽

J. Huszár ◽

E. Herzová ◽

P. Bartoš

Keyword(s):

Leaf Rust ◽

Slovak Republic ◽

Puccinia Triticina ◽

Near Isogenic Lines ◽

Wheat Cultivars ◽

Wheat Leaf Rust ◽

Wheat Leaf ◽

Winter Wheat Cultivars ◽

Low Incidence ◽

Different Parts

In 2005, 2006 and 2008 the virulence of wheat leaf rust population was studied on Thatcher near-isogenic lines with Lr1, Lr2a, Lr2b, Lr2c, Lr3a, Lr9, Lr10, Lr13, Lr15, Lr17, Lr19, Lr21, Lr23, Lr24, Lr26 and Lr28. Samples of leaf rust (141 in total) were obtained from different parts of Slovakia. Resistance gene Lr9 was effective to all tested isolates except three isolates from 2008. No virulence was found to Lr19 and genes Lr24 and Lr28 were also highly effective. Low incidence of virulence to Lr2a was observed. Sixty-five winter wheat cultivars registered in Slovakia were tested with seven leaf rust isolates in the greenhouse. Cultivar Bona Dea was the most resistant of all.

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Virulence of wheat leaf rust (Puccinia triticina Eriks.) in the years 2013–2015 and resistance of wheat cultivars in Slovakia

Cereal Research Communications ◽

10.1556/0806.44.2016.030 ◽

2016 ◽

Vol 44 (4) ◽

pp. 585-593 ◽

Cited By ~ 4

Author(s):

A. Hanzalová ◽

P. Bartoš ◽

T. Sumíková

Keyword(s):

Leaf Rust ◽

Puccinia Triticina ◽

Wheat Cultivars ◽

Wheat Leaf Rust ◽

Wheat Leaf

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Geographical Distribution of Physiologic Races of Puccinia triticina and Postulation of Resistance Genes in New Wheat Cultivars in Egypt

International Journal of Phytopathology ◽

10.33687/phytopath.001.01.0018 ◽

2012 ◽

Vol 1 (1) ◽

pp. 73-80 ◽

Cited By ~ 1

Author(s):

Nour E. K. Soliman ◽

Ashraf M. M. Abdelbacki ◽

Mohammad A.A. Najeeb ◽

Reda I. Omara

Keyword(s):

Leaf Rust ◽

Geographical Distribution ◽

Resistance Genes ◽

Puccinia Triticina ◽

Wheat Cultivars ◽

Wheat Leaf Rust ◽

Rust Disease ◽

Lr Genes ◽

Wheat Leaf ◽

Physiologic Races

Knowledge of the geographical distribution for physiologic races of Puccinia triticina and identification of leaf rust resistance genes (Lr ,s) in the recent Egyptian wheat cultivars are essential for maximizing resistance in future-bred cultivars. The aim of this study was to know the status of resistance in Egyptian wheat cultivars against wheat leaf rust and the most frequent race distributed. Infected samples were collected from five Governorates, i.e., Dakahlia, Kafr el-Sheikh, Beheira, Sharqia and Sohag comprised the wheat growing area in Egypt. These samples were isolated, purified and identified on the differential stes. Gene postulation was done using fifteen identified races on Egyptian wheat cultivars correlated with Lr genes. Thirty three races identified during three seasons 2009/2010, 2010/2011 and 2011/2012. The most frequent race was TK (10%) followed by race BB (7.58%), PK (6.55%), TT (4.82%), PT (3.79%) and MT (3.44%). Moreover, races; BB, TT and PT were present during three seasons while these races appeared in some Governorates and disappeared in other Governorates. On the other hand, the most frequently occurring gene in ten Egyptian wheat cultivars was Lr35 (70%), followed by Lr22 (60%), Lr27 (40%), Lr34 (30%), Lr19 (30%),Lr18 (10%),Lr36 (10%) and Lr46 (10%), eight out of sixteen Lr genes were not present in the tested cultivars. It is concluded that there was a good variation in Lr genes carried by wheat cultivars commercially grown in Egypt. Therefore, strategies for deploying resistance genes to prolong effective disease resistance are suggested to control wheat leaf rust disease.

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Characterization of wheat leaf rust pathogen (Puccinia triticina) in some parts of Ethiopia and seedling evaluation of durum wheat (Triticum turgidum) cultivars to the pathogen

African Journal of Agricultural Research ◽

10.5897/ajar2019.14026 ◽

2020 ◽

Vol 15 (2) ◽

pp. 291-296

Author(s):

Tesfaye Habtamu ◽

Badebo Ayele ◽

Dejene Mashilla

Keyword(s):

Durum Wheat ◽

Leaf Rust ◽

Triticum Turgidum ◽

Puccinia Triticina ◽

Wheat Leaf Rust ◽

Rust Pathogen ◽

Wheat Leaf

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Leaf Rust on Aegilops speltoides Caused by a New Forma Specialis of Puccinia triticina

Phytopathology ◽

10.1094/phyto.2004.94.1.94 ◽

2004 ◽

Vol 94 (1) ◽

pp. 94-101 ◽

Cited By ~ 17

Author(s):

Pnina Ben Yehuda ◽

Tamar Eilam ◽

Jacob Manisterski ◽

Ayelet Shimoni ◽

Yehoshua Anikster

Keyword(s):

Leaf Rust ◽

Host Preference ◽

Natural Habitat ◽

Puccinia Triticina ◽

Aegilops Speltoides ◽

Wheat Cultivars ◽

Wheat Leaf Rust ◽

Forma Specialis ◽

Wheat Leaf ◽

First Time

A leaf rust attacking Aegilops speltoides in its natural habitat is reported for the first time. It was found in two locations in northern and central Israel. The two collections from A. speltoides resemble wheat leaf rust, Puccinia triticina, in most spore dimensions, in the morphology of the substomatal vesicle of the urediniospore, and in DNA content in pycniospore nuclei. Similarly to P. triticina isolates from wheat, isolates taken from A. speltoides are compatible with Thalictrum speciosissimum as an aecial host and they are crossed easily with wheat leaf rust isolates. However, isolates from A. speltoides differ from wheat leaf rust in their telial host range. They are avirulent to cultivated wheat cultivars, but attack hundreds of A. speltoides accessions that were immune to wheat leaf rust. This distinct host preference justifies delineation of the newly found leaf rust as a forma specialis (f. sp. speltoides) within P. triticina.

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Wheat leaf rust (Puccinia triticina Eriks.) virulence frequency and detection of resistance genes in wheat cultivars registered in the Czech Republic in 2016–2018

Czech Journal of Genetics and Plant Breeding ◽

10.17221/86/2019-cjgpb ◽

2020 ◽

Vol 56 (No. 3) ◽

pp. 87-92 ◽

Cited By ~ 1

Author(s):

Alena Hanzalová ◽

Veronika Dumalasová ◽

Ondřej Zelba

Keyword(s):

Molecular Markers ◽

Leaf Rust ◽

Puccinia Triticina ◽

Near Isogenic Lines ◽

Wheat Cultivars ◽

Wheat Leaf Rust ◽

The Czech Republic ◽

Lr Genes ◽

Wheat Leaf ◽

Virulence Frequency

In 2016–2018 virulence of the Czech wheat leaf rust population was studied on Thatcher near-isogenic lines, carrying different Lr genes, and 130 leaf rust isolates. Virulence to Lr9 was found only sporadically. Virulence frequency to Lr2a, Lr2b, Lr2c and Lr28 was lower than in previous years. All tested isolates were avirulent to Lr19. Lr24 conditioned resistance to majority of isolates. Nineteen recently registered Czech cultivars were tested with six isolates of the pathogen and Lr genes were postulated. Presence of genes Lr1, Lr10, Lr19, Lr24, Lr26, Lr28, Lr34 and Lr37 was tested by molecular markers. Lr37 prevailed, followed by Lr genes 10, 24, 28, 1 and 26; genes Lr19 and Lr34 were not determined.

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A Chromosome-Scale Assembly of the Wheat Leaf Rust Pathogen Puccinia triticina Provides Insights Into Structural Variations and Genetic Relationships With Haplotype Resolution

Frontiers in Microbiology ◽

10.3389/fmicb.2021.704253 ◽

2021 ◽

Vol 12 ◽

Author(s):

Jing Qin Wu ◽

Long Song ◽

Yi Ding ◽

Chongmei Dong ◽

Mafruha Hasan ◽

...

Keyword(s):

Leaf Rust ◽

Molecular Mechanisms ◽

Genetic Relationships ◽

Durable Resistance ◽

Puccinia Triticina ◽

Wheat Leaf Rust ◽

Structural Variations ◽

Rust Disease ◽

Rust Pathogen ◽

Wheat Leaf

Despite the global economic importance of the wheat leaf rust pathogen Puccinia triticina (Pt), genomic resources for Pt are limited and chromosome-level assemblies of Pt are lacking. Here, we present a complete haplotype-resolved genome assembly at a chromosome-scale for Pt using the Australian pathotype 64-(6),(7),(10),11 (Pt64; North American race LBBQB) built upon the newly developed technologies of PacBio and Hi-C sequencing. PacBio reads with ∼200-fold coverage (29.8 Gb data) were assembled by Falcon and Falcon-unzip and subsequently scaffolded with Hi-C data using Falcon-phase and Proximo. This approach allowed us to construct 18 chromosome pseudomolecules ranging from 3.5 to 12.3 Mb in size for each haplotype of the dikaryotic genome of Pt64. Each haplotype had a total length of ∼147 Mb, scaffold N50 of ∼9.4 Mb, and was ∼93% complete for BUSCOs. Each haplotype had ∼29,800 predicted genes, of which ∼2,000 were predicted as secreted proteins (SPs). The investigation of structural variants (SVs) between haplotypes A and B revealed that 10% of the total genome was spanned by SVs, highlighting variations previously undetected by short-read based assemblies. For the first time, the mating type (MAT) genes on each haplotype of Pt64 were identified, which showed that MAT loci a and b are located on two chromosomes (chromosomes 7 and 14), representing a tetrapolar type. Furthermore, the Pt64 assembly enabled haplotype-based evolutionary analyses for 21 Australian Pt isolates, which highlighted the importance of a haplotype resolved reference when inferring genetic relationships using whole genome SNPs. This Pt64 assembly at chromosome-scale with full phase information provides an invaluable resource for genomic and evolutionary research, which will accelerate the understanding of molecular mechanisms underlying Pt-wheat interactions and facilitate the development of durable resistance to leaf rust in wheat and sustainable control of rust disease.

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First Detection in North America of Virulence in Wheat Leaf Rust (Puccinia triticina) to Seedling Plants of Wheat with Lr21

Plant Disease ◽

10.1094/pdis-04-11-0275 ◽

2011 ◽

Vol 95 (8) ◽

pp. 1032-1032 ◽

Cited By ~ 14

Author(s):

J. A. Kolmer ◽

J. A. Anderson

Keyword(s):

North Dakota ◽

Leaf Rust ◽

Spring Wheat ◽

Puccinia Triticina ◽

The United States ◽

Wheat Cultivars ◽

Wheat Leaf Rust ◽

Hard Red Spring Wheat ◽

Wheat Leaf ◽

Red Winter Wheat

Leaf rust resistance gene Lr21 is present in hard red spring wheat (Triticum aestivum) cultivars grown in Minnesota, North Dakota, South Dakota, Manitoba, and Saskatchewan. Isolates of Puccinia triticina, the causal organism of wheat leaf rust, with virulence to this gene have not been previously detected in annual virulence surveys in the United States. (2). In 2010, hard red spring wheat cvs. Faller, RB07 (1), and Glenn, all with Lr21, had 0 to 5% levels of leaf rust severity, which was higher than in previous years in research plots in North Dakota and Minnesota. Leaf rust collections from wheat cultivars and germplasm lines with Lr21 at three locations in Minnesota and North Dakota were increased on plants of the leaf rust susceptible wheat Thatcher and the Thatcher line with Lr21. Single uredinia from the collections were isolated and increased on seedlings of Thatcher. The single uredinial isolates were inoculated to 7- to 8-day-old seedling plants of the set of 19 differential lines that are currently used in the leaf rust virulence surveys (2). Thatcher lines with Lr3bg, Lr14b, Lr20, and Lr23 were also tested. The isolates were also inoculated to seedling plants of hard red spring wheat cultivars with Lr21: Glenn, Steele-ND, Faller, RB07, Amidon, AC Cora, and McKenzie (3). Previous standardized methods for growing seedling plants, increase of rust isolates, inoculation, incubation, and evaluation of infection types (IT) were used (2). All tests with the Thatcher differential lines and the cultivars with Lr21 were repeated at least twice. Virulence phenotypes were described based on virulence to the 19 differentials in the P. triticina virulence nomenclature system used in the United States. (2). Two virulence phenotypes, TFBJQ and TFBGQ, with virulence to Lr21 were found at the three locations. TFBJQ is virulent (IT 3 to 4) to genes Lr1, 2a, 2c, 3, 10, 14a, 14b, 20, 21, 24, 26, 28, and avirulent (IT 0 to 2+) to genes Lr3ka, Lr3bg, Lr9, Lr11, Lr17, Lr18, Lr30, LrB, and Lr39/41. TFBGQ was avirulent to Lr14a and Lr20, but identical to TFBJQ for virulence and avirulence to the other resistance genes. Isolates of both phenotypes were virulent on seedlings of Faller, Glenn, RB07 (1), Steele-ND, AC Cora, and Amidon. McKenzie had IT of 2+ due to the additional presence of Lr16 (3). Both TFBJQ and TFBGQ have intermediate IT of 2+ to Lr16; IT 2+3 to Lr23, and are completely virulent to Lr1, Lr2a, and Lr10 that are present in hard red spring wheat cultivars. Both phenotypes have high IT to Lr24 and Lr26 that are present in soft red winter wheat and hard red winter wheat cultivars. The Lr21 virulent phenotypes likely arose by mutation from the group of P. triticina genotypes in the simple sequence repeat group NA-5 (4) that have intermediate IT of ;2- to ;2+ to the Thatcher line with Lr21. P. triticina isolates with virulence to Lr21 are a new threat to wheat production since in 2010 more than 50% of the hard red spring wheat acreage in Minnesota and North Dakota relied on Lr21 for effective resistance to leaf rust. References: (1) J. A. Anderson et al. J. Plant Regist. 3:175, 2009. (2) J. A. Kolmer et al. Plant Dis. 94:775, 2010. (3) B. McCallum and P. Seto-Goh. Can. J. Plant Pathol. 32:387, 2010. (4) M. E. Ordoñez and J. A. Kolmer. Phytopathology 99:750, 2009.

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