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Microscopic and Molecular Characterization of the Prehaustorial Resistance against Wheat Leaf Rust (Puccinia triticina) in Einkorn (Triticum monococcum).

ABSTRACT: Puccinia triticina f. sp. tritici (Eriks.), the causal agent of leaf rust, causes substantial yield losses in wheat production. In wheat many major leaf rust resistance genes have been overcome by virulent races. In contrast, the prehaustorial resistance (phr) against wheat leaf rust detected in the diploid wheat Einkorn (Triticum monoccocum var. monococcum) accession PI272560 confers race-independent resistance against isolates virulent on accessions harboring resistance genes located on the A-genome of Triticum aestivum. Phr in PI272560 leads to abortion of fungal development during the formation of haustorial mother cells and to increased hydrogen peroxide concentration in comparison to the susceptible accession 36554 (Triticum boeoticum ssp. thaoudar var. reuteri). Increased peroxidase and endochitinase activity was detected in PI272560 within 6 h after inoculation (hai). Comparative transcriptome profiling using Massive Analysis of cDNA Ends (MACE) in infected and non-infected leaves detected 14220 differentially expressed tags in PI272560 and 15472 in accession 36554. Of these 2908 and 3004, respectively, could be assigned to Gene Ontology (GO) categories of which 463 were detected in both accessions and 311 were differentially expressed between the accessions. In accordance with the concept of non-host resistance in PI272560, genes with similarity to peroxidases, chitinases, ?-1,3-glucanases and other pathogenesis-related genes were up-regulated within the first 8 hai, whereas up-regulation of such genes was delayed in 36554. Moreover, a Phosphoribulokinase gene contributing to non-host resistance in rice against stripe rust was exclusively expressed in the resistant accession PI272560. Gene expression underpinned physiological and phenotypic observations at the site of infection and are in accordance with the concept of non-host resistance.

SUBMITTER: Serfling A

PROVIDER: S-EPMC5101855 | biostudies-literature | 2016

REPOSITORIES: biostudies-literature

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Microscopic and Molecular Characterization of the Prehaustorial Resistance against Wheat Leaf Rust (Puccinia triticina) in Einkorn (Triticum monococcum).

Serfling Albrecht A Templer Sven E SE Winter Peter P Ordon Frank F

Frontiers in plant science 20161109

Puccinia triticina f. sp. tritici (Eriks.), the causal agent of leaf rust, causes substantial yield losses in wheat production. In wheat many major leaf rust resistance genes have been overcome by virulent races. In contrast, the prehaustorial resistance (phr) against wheat leaf rust detected in the diploid wheat Einkorn (Triticum monoccocum var. monococcum) accession PI272560 confers race-independent resistance against isolates virulent on accessions harboring resist ...[more]

PMID: 27881987

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Project description:Wheat leaf rust (Puccinia triticina) is one of the most significant fungal diseases of wheat, causing substantial yield losses worldwide. Infestation is currently being reduced by fungicide treatments and mostly vertical resistance. However, these measures often break down when the fungal virulence pattern changes, resulting in a breakdown of vertical resistances. In contrast, the prehaustorial resistance (phr) that occurs in the einkorn-wheat leaf rust interaction is race-independent, characterized by an early defense response of plants during the prehaustorial phase of infestation. Einkorn (Triticum monococcum) is closely related to Triticum urartu as a progenitor of wheat and generally shows a high level of resistance against leaf rust of wheat. Hence, einkorn can serve as a valuable source to improve the level of resistance to the pathogen in future wheat lines. In particular, einkorn accession PI272560 is known to exhibit a hypersensitive prehaustorial effector triggered immune reaction, preventing the infection of P. triticina. Remarkably, this effector-triggered immune reaction turned out to be atypical as it is non-race-specific (horizontal). To genetically dissect the prehaustorial resistance (phr) in PI272560, a biparental F2 population of 182 plants was established after crossing PI272560 with the susceptible T. boeoticum accession 36554. Three genetic maps comprising 2,465 DArT-seq markers were constructed, and a major QTL was detected on chromosome 5A. To locate underlying candidate genes, marker sequences flanking the respective QTL were aligned to the T. urartu reference genome and transcriptome data available from the parental accessions were used. Within the QTL interval of approximately 16.13 million base pairs, the expression of genes under inoculated and non-inoculated conditions was analyzed via a massive analysis of cDNA (MACE). Remarkably, a single gene located 3.4 Mbp from the peak marker within the major QTL was upregulated (20- to 95-fold) after the inoculation in the resistant accession in comparison to the susceptible T. boeoticum accession. This gene belongs to a berberine bridge enzyme-like protein that is suspected to interact on the plant surface with glycoside hydrolases (GH) secreted by the fungus and to induce a hypersensitive defense reaction in the plant after fungal infections.

Project description:The resistance to leaf rust (Lr) caused by Puccinia triticina in wheat (Triticum aestivum L.) has been well studied over the past decades with over 70 Lr genes being mapped on different chromosomes and numerous QTLs (quantitative trait loci) being detected or mapped using DNA markers. Such resistance is often divided into race-specific and race-nonspecific resistance. The race-nonspecific resistance can be further divided into resistance to most or all races of the same pathogen and resistance to multiple pathogens. At the molecular level, these three types of resistance may cover across the whole spectrum of pathogen specificities that are controlled by genes encoding different protein families in wheat. The objective of this study is to predict and analyze genes in three such families: NBS-LRR (nucleotide-binding sites and leucine-rich repeats or NLR), START (Steroidogenic Acute Regulatory protein [STaR] related lipid-transfer) and ABC (ATP-Binding Cassette) transporter. The focus of the analysis is on the patterns of relationships between these protein-coding genes within the gene families and QTLs detected for leaf rust resistance.We predicted 526 ABC, 1117 NLR and 144 START genes in the hexaploid wheat genome through a domain analysis of wheat proteome. Of the 1809 SNPs from leaf rust resistance QTLs in seedling and adult stages of wheat, 126 SNPs were found within coding regions of these genes or their neighborhood (5 Kb upstream from transcription start site [TSS] or downstream from transcription termination site [TTS] of the genes). Forty-three of these SNPs for adult resistance and 18 SNPs for seedling resistance reside within coding or neighboring regions of the ABC genes whereas 14 SNPs for adult resistance and 29 SNPs for seedling resistance reside within coding or neighboring regions of the NLR gene. Moreover, we found 17 nonsynonymous SNPs for adult resistance and five SNPs for seedling resistance in the ABC genes, and five nonsynonymous SNPs for adult resistance and six SNPs for seedling resistance in the NLR genes. Most of these coding SNPs were predicted to alter encoded amino acids and such information may serve as a starting point towards more thorough molecular and functional characterization of the designated Lr genes. Using the primer sequences of 99 known non-SNP markers from leaf rust resistance QTLs, we found candidate genes closely linked to these markers, including Lr34 with distances to its two gene-specific markers being 1212 bases (to cssfr1) and 2189 bases (to cssfr2).This study represents a comprehensive analysis of ABC, NLR and START genes in the hexaploid wheat genome and their physical relationships with QTLs for leaf rust resistance at seedling and adult stages. Our analysis suggests that the ABC (and START) genes are more likely to be co-located with QTLs for race-nonspecific, adult resistance whereas the NLR genes are more likely to be co-located with QTLs for race-specific resistance that would be often expressed at the seedling stage. Though our analysis was hampered by inaccurate or unknown physical positions of numerous QTLs due to the incomplete assembly of the complex hexaploid wheat genome that is currently available, the observed associations between (i) QTLs for race-specific resistance and NLR genes and (ii) QTLs for nonspecific resistance and ABC genes will help discover SNP variants for leaf rust resistance at seedling and adult stages. The genes containing nonsynonymous SNPs are promising candidates that can be investigated in future studies as potential new sources of leaf rust resistance in wheat breeding.

Project description:BackgroundDomesticated einkorn (Triticum monococcum L.) is one of the oldest cultivated cereal crops in the world. Its small genome size (~ 5.7 GB), low ploidy (2n = 2x = 14, AmAm) and high genetic polymorphism make this species very attractive for use as a diploid model for understanding the genomics and proteomics of Triticeae. Einkorn, however, is still a recalcitrant monocotyledonous species for the application of modern biotechnologies, including transgenesis. This paper reports the factors that may influence transgene delivery, integration, expression and inheritance in einkorn.ResultsIn this study, we report the successful genetic transformation of einkorn using biolistic-mediated DNA delivery. Immature embryo-derived tissues of spring einkorn were bombarded with a plasmid containing the reporter gene GFP (green fluorescent protein) driven by the rice actin promoter (act1) and the selectable bar gene (bialaphos resistance gene) driven by the maize ubiquitin promoter (ubi1). Adjustments to various parameters such as gas pressure, microcarrier size and developmental stage of target tissue were essential for successful transient and stable transformation. Bombarded einkorn tissues are recalcitrant to regenerating plants, but certain modifications of the culture medium have been shown to increase the production of transgenic events. In various experiments, independent transgenic plants were produced at frequencies ranging from 0.0 to 0.6%. Molecular analysis, marker gene expression and herbicide treatment demonstrated that gfp/bar genes were stably integrated into the einkorn genome and successfully inherited over several generations. The transgenes, as dominant loci, segregated in both Mendelian and non-Mendelian fashion due to multiple insertions. Fertile homozygous T1-T2 populations of transgenic einkorn that are resistant to herbicides were selected.ConclusionTo the best of our knowledge, this is the first report of the production of genetically modified einkorn plants. We believe that the results of our research could be a starting point for the application of the current biotechnological-based technologies, such as transgenesis and genome editing, to accelerate comparative functional genomics in einkorn and other cereals.

Project description:Wheat leaf rust caused by the pathogenic fungus, Puccinia triticina, is a serious threat to bread wheat and durum production in many areas of the world. This plant-pathogen interaction has been studied extensively at the molecular genetics level however, proteomics data are still relatively scarce. The present study investigated temporal changes in the abundance of the apoplastic fluid proteome of resistant and susceptible wheat leaves infected with P. triticina race-1, using a label-free LC-MS-based approach. In general, there was very little difference between inoculated and control apoplastic proteomes in either host, until haustoria had become well established in the susceptible host, although the resistant host responds to pathogen challenge sooner. In the earlier samplings (up to 72 h after inoculation) there were just 46 host proteins with significantly changing abundance, and pathogen proteins were detected only rarely and not reproducibly. This is consistent with the biotrophic lifestyle of P. triticina, where the invading pathogen initially causes little tissue damage or host cell death, which occur only later during the infection cycle. The majority of the host proteins with altered abundance up to 72 h post-inoculation were pathogen-response-related, including peroxidases, chitinases, ?-1-3-endo-glucanases, and other PR proteins. Five days after inoculation with the susceptible apoplasm it was possible to detect 150 P. triticina proteins and 117 host proteins which had significantly increased in abundance as well as 33 host proteins which had significantly decreased in abundance. The latter represents potential targets of pathogen effectors and included enzymes which could damage the invader. The pathogen-expressed proteins-seen most abundantly in the incompatible interaction-were mostly uncharacterized proteins however, many of their functions could be inferred through homology-matching with pBLAST. Pathogen proteins also included several candidate effector proteins, some novel, and some which have been reported previously. All MS data have been deposited in the PRIDE archive (www.ebi.ac.uk/pride/archive/) under Project PXD012586.

Project description:The Canada Western Red Spring wheat (Triticum aestivum L.) cultivars AAC Concord, AAC Prevail, CDC Hughes, Lillian, Glenlea, and elite line BW961 express a spectrum of resistance to leaf rust caused by Puccinia triticina Eriks. This study aimed to identify and map the leaf rust resistance of the cultivars using three doubled haploid populations, AAC Prevail/BW961 (PB), CDC Hughes/AAC Concord (HC), and Lillian/Glenlea (LG). The populations were evaluated for seedling resistance in the greenhouse and adult plant disease response in the field at Morden, MB for 3 years and genotyped with the 90K wheat Infinium iSelect SNP array. Genetic maps were constructed to perform QTL analysis on the seedling and field leaf rust data. A total of three field leaf rust resistance QTL segregated in the PB population, five in the HC, and six in the LG population. In the PB population, BW961 contributed two QTL on chromosomes 2DS and 7DS, and AAC Prevail contributed a QTL on 4AL consistent across trials. Of the five QTL in HC, AAC Concord contributed two QTL on 4AL and 7AL consistent across trials and a QTL on 3DL.1 that provided seedling resistance only. CDC Hughes contributed two QTL on 1DS and 3DL.2. Lillian contributed four QTL significant in at least two of the three trials on 2BS, 4AL, 5AL, and 7AL, and Glenlea two QTL on 4BL and 7BL. The 1DS QTL from CDC Hughes, the 2DS from BW961, the 4AL from the AAC Prevail, AAC Concord, and Lillian, and the 7AL from AAC Concord and Lillian conferred seedling leaf rust resistance. The QTL on 4AL corresponded with Lr30 and was the same across cultivars AAC Prevail, AAC Concord, and Lillian, whereas the 7AL corresponding with LrCen was coincident between AAC Concord and Lillian. The 7DS and 2DS QTL in BW961 corresponded with Lr34 and Lr2a, respectively, and the 1DS QTL in CDC Hughes with Lr21. The QTL identified on 5AL could represent a novel gene. The results of this study will widen our knowledge of leaf rust resistance genes in Canadian wheat and their utilization in resistance breeding.

Dataset Information

Microscopic and Molecular Characterization of the Prehaustorial Resistance against Wheat Leaf Rust (Puccinia triticina) in Einkorn (Triticum monococcum).

Publications

Microscopic and Molecular Characterization of the Prehaustorial Resistance against Wheat Leaf Rust (<i>Puccinia triticina</i>) in Einkorn (<i>Triticum monococcum</i>).

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