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Genomics, Molecular, Genetics, and Diversity of Plant Disease Resistance

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A special issue of Pathogens (ISSN 2076-0817).

Deadline for manuscript submissions: closed (30 April 2021) | Viewed by 51307

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Dr. Valentyna Klymiuk

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Guest Editor

University of Saskatchewan, Saskatoon, SK, Canada
Interests: plant genetics and genomics; plant pathology; molecular biology; host-parasite interactions; population genetics

Prof. Dr. Tzion Fahima

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Guest Editor

Department of Evolutionary and Environmental Biology and The Institute of Evolution, University of Haifa, Haifa, Israel
Interests: plant disease resistance; host-parasite co-evolution; plant genomics; gene cloning; wild cereals; domestication evolution

Special Issue Information

Dear Colleagues,

Plants are faced with thousands of pathogens and developed surveillance system that can detect the presence of the pathogen and activate powerful defense responses. Known plant resistance mechanisms have been classified to: (i) PAMP-triggered immunity activated by surface-localized receptors that recognize microbial-associated (MAMPs) or pathogen-associated molecular patterns (PAMPs); (ii) effector-triggered immunity (ETI), race-specific resistance, activated by intracellular immune receptors (mostly by nucleotide-binding leucine-rich-repeat receptors (NLRs)) that recognize pathogen effector proteins; (iii) various molecular pathways that led to broad-spectrum quantitative (partial) disease resistance.

Nowadays, many new technologies and resources for elucidation of nature and mechanisms underlying disease resistance in plants became to be available, including reference genomes, omics technics and modern phenotyping.

Crop wild relatives serve as promising sources for novel exotic disease resistance genes/alleles and provide excellent opportunities for evolutionary studies in relation to domestication and host-parasite co-evolution.

In this special issue, we welcome research papers dealing with topics related to the genomics, molecular genetics and diversity of plant disease resistance. This themed article collection aims to cover whole-genome analyses in single or different plant species for disease resistance gene/protein structures, including but not limited to evolutionary studies. QRL mapping, fine mapping and QRL/resistance gene (R-gene) cloning research papers, as well as R-gene/R-protein allelic diversity studies and population genetic studies are welcome for submission. Manuscripts that describe the investigation of molecular interactions between R-proteins with other host or pathogen proteins are also in scope of this special issue. Furthermore, contributions highlighting the usefulness of new genotyping, phenotyping and modelling techniques to improve the understanding and prediction of disease resistance traits (e.g. fungal, bacterial, viral, etc.), will also be considered.

Dr. Valentyna Klymiuk
Prof. Dr. Tzion Fahima
Guest Editors

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Keywords

disease resistance gene
NLR
QRL mapping
host-parasite interactions
plant genomics
resistance alleles
plant-pathogen co-evolution
crop wild relatives

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Published Papers (10 papers)

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Research

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19 pages, 1747 KiB

Open AccessArticle

Structural and Functional Genomics of the Resistance of Cacao to Phytophthora palmivora

by Jonathan Javier Mucherino Muñoz, Cláusio Antônio Ferreira de Melo, Raner José Santana Silva, Edna Dora Martins Newman Luz and Ronan Xavier Corrêa

Pathogens 2021, 10(8), 961; https://doi.org/10.3390/pathogens10080961 - 30 Jul 2021

Cited by 8 | Viewed by 3861

Abstract

Black pod disease, caused by Phytophthora spp., is one of the main diseases that attack cocoa plantations. This study validated, by association mapping, 29 SSR molecular markers flanking to QTL (Quantitative Trait Loci) associated with Phytophthora palmivora Butler (Butler) (PP) resistance, in three local ancient varieties of the Bahia (Comum, Pará, and Maranhão), varieties that have a high potential in the production of gourmet chocolate. Four SSR loci associated with resistance to PP were detected, two on chromosome 8, explaining 7.43% and 3.72% of the Phenotypic Variation (%PV), one on chromosome 2 explaining 2.71%PV and one on chromosome 3 explaining 1.93%PV. A functional domains-based annotation was carried out, in two Theobroma cacao (CRIOLLO and MATINA) reference genomes, of 20 QTL regions associated with cocoa resistance to the pathogen. It was identified 164 (genome CRIOLLO) and 160 (genome MATINA) candidate genes, hypothetically involved in the recognition and activation of responses in the interaction with the pathogen. Genomic regions rich in genes with Coiled-coils (CC), nucleotide binding sites (NBS) and Leucine-rich repeat (LRR) domains were identified on chromosomes 1, 3, 6, 8, and 10, likewise, regions rich in Receptor-like Kinase domain (RLK) and Ginkbilobin2 (GNK2) domains were identified in chromosomes 4 and 6. Full article

(This article belongs to the Special Issue Genomics, Molecular, Genetics, and Diversity of Plant Disease Resistance)

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16 pages, 3948 KiB

Open AccessArticle

Selection for Plastic, Pathogen-Inducible Recombination in a Red Queen Model with Diploid Antagonists

by Sviatoslav Rybnikov, Zeev Frenkel, Abraham B. Korol and Tzion Fahima

Pathogens 2021, 10(7), 898; https://doi.org/10.3390/pathogens10070898 - 16 Jul 2021

Cited by 3 | Viewed by 2311

Abstract

Antagonistic interactions and co-evolution between a host and its parasite are known to cause oscillations in the population genetic structure of both species (Red Queen dynamics). Potentially, such oscillations may select for increased sex and recombination in the host, although theoretical models suggest that this happens under rather restricted values of selection intensity, epistasis, and other parameters. Here, we explore a model in which the diploid parasite succeeds to infect the diploid host only if their phenotypes at the interaction-mediating loci match. Whenever regular oscillations emerge in this system, we test whether plastic, pathogen-inducible recombination in the host can be favored over the optimal constant recombination. Two forms of the host recombination dependence on the parasite pressure were considered: either proportionally to the risk of infection (prevention strategy) or upon the fact of infection (remediation strategy). We show that both forms of plastic recombination can be favored, although relatively infrequently (up to 11% of all regimes with regular oscillations, and up to 20% of regimes with obligate parasitism). This happens under either strong overall selection and high recombination rate in the host, or weak overall selection and low recombination rate in the host. In the latter case, the system’s dynamics are considerably more complex. The prevention strategy is favored more often than the remediation one. It is noteworthy that plastic recombination can be favored even when any constant recombination is rejected, making plasticity an evolutionary mechanism for the rescue of host recombination. Full article

(This article belongs to the Special Issue Genomics, Molecular, Genetics, and Diversity of Plant Disease Resistance)

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12 pages, 1858 KiB

Open AccessArticle

Genome Sequencing of Paecilomyces Penicillatus Provides Insights into Its Phylogenetic Placement and Mycoparasitism Mechanisms on Morel Mushrooms

by Xinxin Wang, Jingyu Peng, Lei Sun, Gregory Bonito, Yuxiu Guo, Yu Li and Yongping Fu

Pathogens 2020, 9(10), 834; https://doi.org/10.3390/pathogens9100834 - 13 Oct 2020

Cited by 26 | Viewed by 3990

Abstract

Morels (Morchella spp.) are popular edible fungi with significant economic and scientific value. However, white mold disease, caused by Paecilomyces penicillatus, can reduce morel yield by up to 80% in the main cultivation area in China. Paecilomyces is a polyphyletic genus and the exact phylogenetic placement of P. penicillatus is currently still unclear. Here, we obtained the first high-quality genome sequence of P. penicillatus generated through the single-molecule real-time (SMRT) sequencing platform. The assembled draft genome of P. penicillatus was 40.2 Mb, had an N50 value of 2.6 Mb and encoded 9454 genes. Phylogenetic analysis of single-copy orthologous genes revealed that P. penicillatus is in Hypocreales and closely related to Hypocreaceae, which includes several genera exhibiting a mycoparasitic lifestyle. CAZymes analysis demonstrated that P. penicillatus encodes a large number of fungal cell wall degradation enzymes. We identified many gene clusters involved in the production of secondary metabolites known to exhibit antifungal, antibacterial, or insecticidal activities. We further demonstrated through dual culture assays that P. penicillatus secretes certain soluble compounds that are inhibitory to the mycelial growth of Morchella sextelata. This study provides insights into the correct phylogenetic placement of P. penicillatus and the molecular mechanisms that underlie P. penicillatus pathogenesis. Full article

(This article belongs to the Special Issue Genomics, Molecular, Genetics, and Diversity of Plant Disease Resistance)

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19 pages, 6631 KiB

Open AccessArticle

A Post-Haustorial Defense Mechanism is Mediated by the Powdery Mildew Resistance Gene, PmG3M, Derived from Wild Emmer Wheat

by Zhen-Zhen Wei, Valentyna Klymiuk, Valeria Bocharova, Curtis Pozniak and Tzion Fahima

Pathogens 2020, 9(6), 418; https://doi.org/10.3390/pathogens9060418 - 28 May 2020

Cited by 8 | Viewed by 3295

Abstract

The destructive wheat powdery mildew disease is caused by the fungal pathogen Blumeria graminis f. sp. tritici (Bgt). PmG3M, derived from wild emmer wheat Triticum dicoccoides accession G305-3M, is a major gene providing a wide-spectrum resistance against Bgt. PmG3M was previously mapped to wheat chromosome 6B using an F₆ recombinant inbred line (RIL) mapping population generated by crossing G305-3M with the susceptible T. durum wheat cultivar Langdon (LDN). In the current study, we aimed to explore the defense mechanisms conferred by PmG3M against Bgt. Histopathology of fungal development was characterized in artificially inoculated leaves of G305-3M, LDN, and homozygous RILs using fluorescence and light microscopy. G305-3M exhibited H₂O₂ accumulation typical of a hypersensitive response, which resulted in programmed cell death (PCD) in Bgt-penetrated epidermal cells, while LDN showed well-developed colonies without PCD. In addition, we observed a post-haustorial resistance mechanism that arrested the development of fungal feeding structures and pathogen growth in both G305-3M and resistant RIL, while LDN and a susceptible RIL displayed fully developed digitated haustoria and massive accumulation of fungal biomass. In contrast, both G305-3M and LDN exhibited callose deposition in attempt to prevent fungal invasion, supporting this as a mechanism of a basal defense response not associated with PmG3M resistance mechanism per se. The presented results shed light on the resistance mechanisms conferred by PmG3M against wheat powdery mildew. Full article

(This article belongs to the Special Issue Genomics, Molecular, Genetics, and Diversity of Plant Disease Resistance)

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16 pages, 2748 KiB

Open AccessArticle

Genomic Features of Cladobotryum dendroides, Which Causes Cobweb Disease in Edible Mushrooms, and Identification of Genes Related to Pathogenicity and Mycoparasitism

by Rong Xu, Xiaochen Liu, Bing Peng, Peibin Liu, Zhuang Li, Yueting Dai and Shijun Xiao

Pathogens 2020, 9(3), 232; https://doi.org/10.3390/pathogens9030232 - 20 Mar 2020

Cited by 18 | Viewed by 4552

Abstract

Cladobotryum dendroides, which causes cobweb disease in edible mushrooms, is one of the major fungal pathogens. Our previous studies focused on the genetic and morphological characterization of this fungus, as well as its pathogenicity and the identification of appropriate fungicides. However, little is known about the genome characters, pathogenic genes, and molecular pathogenic mechanisms of C. dendroides. Herein, we reported a high-quality de novo genomic sequence of C. dendroides and compared it with closely-related fungi. The assembled C. dendroides genome was 36.69 Mb, consisting of eight contigs, with an N50 of 4.76 Mb. This genome was similar in size to that of C. protrusum, and shared highly conserved syntenic blocks and a few inversions with C. protrusum. Phylogenetic analysis revealed that, within the Hypocreaceae, Cladobotryum was closer to Mycogone than to Trichoderma, which is consistent with phenotypic evidence. A significant number of the predicted expanded gene families were strongly associated with pathogenicity, virulence, and adaptation. Our findings will be instrumental for the understanding of fungi–fungi interactions, and for exploring efficient management strategies to control cobweb disease. Full article

(This article belongs to the Special Issue Genomics, Molecular, Genetics, and Diversity of Plant Disease Resistance)

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11 pages, 1650 KiB

Open AccessArticle

Distribution and Nucleotide Diversity of Yr15 in Wild Emmer Populations and Chinese Wheat Germplasm

by Yu He, Lihua Feng, Yun Jiang, Lianquan Zhang, Jun Yan, Gang Zhao, Jirui Wang, Guoyue Chen, Bihua Wu, Dengcai Liu, Lin Huang and Tzion Fahima

Pathogens 2020, 9(3), 212; https://doi.org/10.3390/pathogens9030212 - 13 Mar 2020

Cited by 19 | Viewed by 3696

Abstract

Stripe rust, caused by Puccinia striiformis f. sp. tritici (Pst), is a devastating fungal disease of wheat. The wild emmer gene, Yr15 (Wtk1), which confers a strong broad-spectrum resistance to Pst isolates, is composed of kinase and pseudokinase domains. The analysis of 361 wild emmer accessions from a wide range of natural habitats confirms that functional Wtk1 is distributed mainly along a narrow axis from Mt. Carmel to Mt. Hermon regions, in the northern part of Israel, where environmental conditions are favorable to the onset of stripe rust. An analysis of full-length Wtk1 DNA sequences from 49 wild emmer accessions identified three haplotypes and extremely low nucleotide diversity (π = 0.00002). The sequence diversity of Wtk1 is 9.5 times lower than that of broad-spectrum partial resistance gene Yr36 (π = 0.00019), and both are in sharp contrast to the high level of nucleotide diversity previously reported for race-specific resistance genes (e.g., Lr10 and Pm3). However, the nonfunctional wtk1 sequences possess high level of nucleotide diversity (π = 0.07). These results may reflect the different resistance mechanisms and the different evolutionary processes that shaped these resistance genes. Yr15 was absent in 189 Chinese wheat landraces and was present in only 1.02% of the 583 tested modern Chinese wheat cultivars. These results corroborate our previous results showing that Yr15 was absent in 94% of a worldwide collection of 513 wheat cultivars, therefore indicating the importance of Yr15 in wheat stripe rust resistance breeding programs in China and elsewhere around the globe. Full article

(This article belongs to the Special Issue Genomics, Molecular, Genetics, and Diversity of Plant Disease Resistance)

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18 pages, 1014 KiB

Open AccessArticle

Comparative Transcriptome Analysis of Two Cucumber Cultivars with Different Sensitivity to Cucumber Mosaic Virus Infection

by Zdeno Šubr, Lukáš Predajňa, Katarína Šoltys, Boris Bokor, Jaroslav Budiš and Miroslav Glasa

Pathogens 2020, 9(2), 145; https://doi.org/10.3390/pathogens9020145 - 21 Feb 2020

Cited by 10 | Viewed by 4058

Abstract

Cucumber mosaic virus (CMV), with extremely broad host range including both monocots and dicots around the world, belongs to most important viral crop threats. Either natural or genetically constructed sources of resistance are being intensively investigated; for this purpose, exhaustive knowledge of molecular virus-host interaction during compatible and incompatible infection is required. New technologies and computer-based “omics” on various levels contribute markedly to this topic. In this work, two cucumber cultivars with different response to CMV challenge were tested, i.e., sensitive cv. Vanda and resistant cv. Heliana. The transcriptomes were prepared from both cultivars at 18 days after CMV or mock inoculation. Subsequently, four independent comparative analyses of obtained data were performed, viz. mock- and CMV-inoculated samples within each cultivar, samples from mock-inoculated cultivars to each other and samples from virus-inoculated cultivars to each other. A detailed picture of CMV-influenced genes, as well as constitutive differences in cultivar-specific gene expression was obtained. The compatible CMV infection of cv. Vanda caused downregulation of genes involved in photosynthesis, and induction of genes connected with protein production and modification, as well as components of signaling pathways. CMV challenge caused practically no change in the transcription profile of the cv. Heliana. The main differences between constitutive transcription activity of the two cultivars relied in the expression of genes responsible for methylation, phosphorylation, cell wall organization and carbohydrate metabolism (prevailing in cv. Heliana), or chromosome condensation and glucan biosynthesis (prevailing in cv. Vanda). Involvement of several genes in the resistant cucumber phenotype was predicted; this can be after biological confirmation potentially applied in breeding programs for virus-resistant crops. Full article

(This article belongs to the Special Issue Genomics, Molecular, Genetics, and Diversity of Plant Disease Resistance)

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16 pages, 1669 KiB

Open AccessArticle

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

by Moshe Ronen, Hanan Sela, Eyal Fridman, Rafael Perl-Treves, Doris Kopahnke, Alexandre Moreau, Roi Ben-David and Arye Harel

Pathogens 2019, 8(4), 275; https://doi.org/10.3390/pathogens8040275 - 29 Nov 2019

Cited by 9 | Viewed by 4305

Abstract

Net blotch (NB) is a major disease of barley caused by the fungus Pyrenophora teres f. teres (Ptt), and P. teres f. maculata (Ptm). Ptt and Ptm infect the cultivated crop (Hordeum vulgare) and its wild relatives (H. vulgare ssp. spontaneum and H. murinum ssp. glaucum). 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 Ptt (n = 15) and Ptm (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 (Ptt vs. Ptm). 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. Ptm has significantly higher necrotrophic and saprotrophic growth rates than Ptt, and for both a significant negative correlation was found between light intensity exposure and growth rates. Full article

(This article belongs to the Special Issue Genomics, Molecular, Genetics, and Diversity of Plant Disease Resistance)

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21 pages, 4755 KiB

Open AccessArticle

Non-Specific Lipid Transfer Proteins in Triticum kiharae Dorof. et Migush.: Identification, Characterization and Expression Profiling in Response to Pathogens and Resistance Inducers

by Tatyana I. Odintsova, Marina P. Slezina, Ekaterina A. Istomina, Tatyana V. Korostyleva, Alexey S. Kovtun, Artem S. Kasianov, Larisa A. Shcherbakova and Alexander M. Kudryavtsev

Pathogens 2019, 8(4), 221; https://doi.org/10.3390/pathogens8040221 - 5 Nov 2019

Cited by 18 | Viewed by 3412

Abstract

Non-specific lipid-transfer proteins (nsLTPs) represent a family of plant antimicrobial peptides (AMPs) implicated in diverse physiological processes. However, their role in induced resistance (IR) triggered by non-pathogenic fungal strains and their metabolites is poorly understood. In this work, using RNA-seq data and our AMP search pipeline, we analyzed the repertoire of nsLTP genes in the wheat Triticum kiharae and studied their expression in response to Fusarium oxysporum infection and treatment with the intracellular metabolites of Fusarium sambucinum FS-94. A total of 243 putative nsLTPs were identified, which were classified into five structural types and characterized. Expression analysis showed that 121 TkLTPs including sets of paralogs with identical mature peptides displayed specific expression patters in response to different treatments pointing to their diverse roles in resistance development. We speculate that upregulated nsLTP genes are involved in protection due to their antimicrobial activity or signaling functions. Furthermore, we discovered that in IR-displaying plants, a vast majority of nsLTP genes were downregulated, suggesting their role as negative regulators of immune mechanisms activated by the FS-94 elicitors. The results obtained add to our knowledge of the role of nsLTPs in IR and provide candidate molecules for genetic engineering of crops to enhance disease resistance. Full article

(This article belongs to the Special Issue Genomics, Molecular, Genetics, and Diversity of Plant Disease Resistance)

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25 pages, 2278 KiB

Open AccessEditor’s ChoiceReview

Phenylpropanoid Pathway Engineering: An Emerging Approach towards Plant Defense

by Vivek Yadav, Zhongyuan Wang, Chunhua Wei, Aduragbemi Amo, Bilal Ahmed, Xiaozhen Yang and Xian Zhang

Pathogens 2020, 9(4), 312; https://doi.org/10.3390/pathogens9040312 - 23 Apr 2020

Cited by 270 | Viewed by 16357

Abstract

Pathogens hitting the plant cell wall is the first impetus that triggers the phenylpropanoid pathway for plant defense. The phenylpropanoid pathway bifurcates into the production of an enormous array of compounds based on the few intermediates of the shikimate pathway in response to cell wall breaches by pathogens. The whole metabolomic pathway is a complex network regulated by multiple gene families and it exhibits refined regulatory mechanisms at the transcriptional, post-transcriptional, and post-translational levels. The pathway genes are involved in the production of anti-microbial compounds as well as signaling molecules. The engineering in the metabolic pathway has led to a new plant defense system of which various mechanisms have been proposed including salicylic acid and antimicrobial mediated compounds. In recent years, some key players like phenylalanine ammonia lyases (PALs) from the phenylpropanoid pathway are proposed to have broad spectrum disease resistance (BSR) without yield penalties. Now we have more evidence than ever, yet little understanding about the pathway-based genes that orchestrate rapid, coordinated induction of phenylpropanoid defenses in response to microbial attack. It is not astonishing that mutants of pathway regulator genes can show conflicting results. Therefore, precise engineering of the pathway is an interesting strategy to aim at profitably tailored plants. Here, this review portrays the current progress and challenges for phenylpropanoid pathway-based resistance from the current prospective to provide a deeper understanding. Full article

(This article belongs to the Special Issue Genomics, Molecular, Genetics, and Diversity of Plant Disease Resistance)

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