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Powdery Mildew Resistance Genetics
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Powdery Mildew Resistance Genetics

A special issue of Genes (ISSN 2073-4425). This special issue belongs to the section "Plant Genetics and Genomics".

Deadline for manuscript submissions: closed (15 March 2021) | Viewed by 34071

Special Issue Editor

Prof. Dr. José M. Leitão

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Guest Editor
MED-Mediterranean Institute for Agriculture, Environment and Development, Faculdade de Ciências e Tecnologia, Universidade do Algarve, Campus de Gambelas, 8005‐139 Faro, Portugal
Interests: molecular biology; plant genetics; plant genomics; plant biotechnology; plant breeding; genotyping; epigenetics; plant tissue culture; genetic diversity; molecular markers development; plant disease resistance; marker assisted selection; legumes; linkage analysis; experimental mutagenesis; DNA repair; plant cytogenetics
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Special Issue Information

Dear Colleagues,

Powdery mildew caused by obligate biotrophic fungi of the order Erysiphales is a widespread disease that infects a wide variety of angiospermic plant species. In crops, the effect of powdery mildew is often devastating, resulting in a high percentage of unmarketable products and heavy yield reduction. The use of crops that are genetically resistant to pathogens not only decreases the cultivation costs but also reduces the environmental pollution caused by chemical control of plant diseases. Novel sources of genetic resistance to powdery mildew are continuously being identified.

In some species, resistance is conferred by dominantly inherited pre-invasive and post-invasive defense mechanisms that directly target the pathogen. In other cases, powdery mildew resistance was found to be determined by QTLs or by a dominantly inherited single locus. The most impressive resistance is conferred by the recessive mildew resistance locus o (mlo). Naturally occurring or experimentally induced mutations in this locus can lead the loss of function of the coded transmembrane protein MLO, resulting in strong broad-spectrum immunity to the fungus.

Common to monocotyledonous and dicotyledonous plants, the MLO family is encoded by a variable number of loci from which only one locus—or, in some cases, multiple loci—needs to be mutated to achieve complete immunity. The simplicity of the Mlo-associated recessive resistance has attracted multiple experimental mutagenic and gene editing projects that are currently being implemented.

This Special Issue welcomes high-quality research and review articles on any aspect of the genetics of powdery mildew resistance, including studies on the modulation of the resistance and cross-effects with other biotic or with abiotic stress factors.

Prof. Dr. José M. Leitão
Guest Editor

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Keywords

  • powdery mildew
  • powdery mildew resistance
  • pre-invasive defense
  • post-invasive defense
  • mlo locus
  • Mlo proteins
  • modulation of disease resistance
  • molecular mechanism of powdery mildew resistance

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Published Papers (8 papers)

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Research

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13 pages, 4337 KiB  
Article
Genome-Wide Association Study Reveals a Genomic Region Associated with Mite-Recruitment Phenotypes in the Domesticated Grapevine (Vitis vinifera)
by Erika R. LaPlante, Margaret B. Fleming, Zoë Migicovsky and Marjorie Gail Weber
Genes 2021, 12(7), 1013; https://doi.org/10.3390/genes12071013 - 30 Jun 2021
Cited by 9 | Viewed by 2773
Abstract
Indirect defenses are plant phenotypes that reduce damage by attracting natural enemies of plant pests and pathogens to leaves. Despite their economic and ecological importance, few studies have investigated the genetic underpinnings of indirect defense phenotypes. Here, we present a genome-wide association study [...] Read more.
Indirect defenses are plant phenotypes that reduce damage by attracting natural enemies of plant pests and pathogens to leaves. Despite their economic and ecological importance, few studies have investigated the genetic underpinnings of indirect defense phenotypes. Here, we present a genome-wide association study of five phenotypes previously determined to increase populations of beneficial (fungivorous and predacious) mites on grape leaves (genus Vitis): leaf bristles, leaf hairs, and the size, density, and depth of leaf domatia. Using a common garden genetic panel of 399 V. vinifera cultivars, we tested for genetic associations of these phenotypes using previously obtained genotyping data from the Vitis9kSNP array. We found one single nucleotide polymorphism (SNP) significantly associated with domatia density. This SNP (Chr5:1160194) is near two genes of interest: Importin Alpha Isoform 1 (VIT_205s0077g01440), involved in downy mildew resistance, and GATA Transcription Factor 8 (VIT_205s0077g01450), involved in leaf shape development. Our findings are among the first to examine the genomic regions associated with ecologically important plant traits that facilitate interactions with beneficial mites, and suggest promising candidate genes for breeding and genetic editing to increase naturally occurring predator-based defenses in grapevines. Full article
(This article belongs to the Special Issue Powdery Mildew Resistance Genetics)
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16 pages, 5611 KiB  
Article
Heat Stress Pre-Exposure May Differentially Modulate Plant Defense to Powdery Mildew in a Resistant and Susceptible Barley Genotype
by Ildikó Schwarczinger, Judit Kolozsváriné Nagy, Lóránt Király, Klára Mészáros, Judit Bányai, Viola Kunos, József Fodor and András Künstler
Genes 2021, 12(5), 776; https://doi.org/10.3390/genes12050776 - 19 May 2021
Cited by 11 | Viewed by 3067
Abstract
Heat stress negatively affects barley production and under elevated temperatures defense responses to powdery mildew (Blumeria graminis f. sp. hordei, Bgh) are altered. Previous research has analyzed the effects of short-term (30 s to 2 h) heat stress, however, few data are [...] Read more.
Heat stress negatively affects barley production and under elevated temperatures defense responses to powdery mildew (Blumeria graminis f. sp. hordei, Bgh) are altered. Previous research has analyzed the effects of short-term (30 s to 2 h) heat stress, however, few data are available on the influence of long-term exposure to heat on powdery mildew infections. We simultaneously assessed the effects of short and long term heat pre-exposure on resistance/susceptibility of barley to Bgh, evaluating powdery mildew infection by analyzing symptoms and Bgh biomass with RT-qPCR in barley plants pre-exposed to high temperatures (28 and 35 °C from 30 s to 5 days). Plant defense gene expression after heat stress pre-exposure and inoculation was also monitored. Our results show that prolonged heat stress (24, 48 and 120 h) further enhanced Bgh susceptibility in a susceptible barley line (MvHV118-17), while a resistant line (MvHV07-17) retained its pathogen resistance. Furthermore, prolonged heat stress significantly repressed the expression of several defense-related genes (BAX inhibitor-1, Pathogenesis related-1b and Respiratory burst oxidase homologue F2) in both resistant and susceptible barley lines. Remarkably, heat-suppressed defense gene expression returned to normal levels only in MvHV07-17, a possible reason why this barley line retains Bgh resistance even at high temperatures. Full article
(This article belongs to the Special Issue Powdery Mildew Resistance Genetics)
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18 pages, 2372 KiB  
Article
Discovery and Characterization of a Novel Tomato mlo Mutant from an EMS Mutagenized Micro-Tom Population
by Zhe Yan, Michela Appiano, Ageeth van Tuinen, Fien Meijer-Dekens, Danny Schipper, Dongli Gao, Robin Huibers, Richard G. F. Visser, Yuling Bai and Anne-Marie A. Wolters
Genes 2021, 12(5), 719; https://doi.org/10.3390/genes12050719 - 11 May 2021
Cited by 11 | Viewed by 4360
Abstract
In tomato (Solanum lycopersicum), there are at least three SlMLO (Mildew resistance Locus O) genes acting as susceptibility genes for the powdery mildew disease caused by Oidium neolycopersici, namely SlMLO1, SlMLO5 and SlMLO8. Of the three [...] Read more.
In tomato (Solanum lycopersicum), there are at least three SlMLO (Mildew resistance Locus O) genes acting as susceptibility genes for the powdery mildew disease caused by Oidium neolycopersici, namely SlMLO1, SlMLO5 and SlMLO8. Of the three homologs, the SlMLO1 gene plays a major role since a natural mutant allele called ol-2 can almost completely prevent fungal penetration by formation of papillae. The ol-2 allele contains a 19-bp deletion in the coding sequence of the SlMLO1 gene, resulting in a premature stop codon within the second cytoplasmic loop of the predicted protein. In this study, we have developed a new genetic resource (M200) in the tomato cv. Micro-Tom genetic background by means of ethyl methane sulfonate (EMS) mutagenesis. The mutant M200 containing a novel allele (the m200 allele) of the tomato SlMLO1 gene showed profound resistance against powdery mildew with no fungal sporulation. Compared to the coding sequence of the SlMLO1 gene, the m200 allele carries a point mutation at T65A. The SNP results in a premature stop codon L22* located in the first transmembrane domain of the complete SlMLO1 protein. The length of the predicted protein is 21 amino acids, while the SlMLO1 full-length protein is 513 amino acids. A high-resolution melting (HRM) marker was developed to distinguish the mutated m200 allele from the SlMLO1 allele in backcross populations. The mutant allele conferred recessive resistance that was associated with papillae formation at fungal penetration sites of plant epidermal cells. A comprehensive list of known mlo mutations found in natural and artificial mutants is presented, which serves as a particularly valuable resource for powdery mildew resistance breeding. Full article
(This article belongs to the Special Issue Powdery Mildew Resistance Genetics)
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18 pages, 8248 KiB  
Article
Identification of Novel Loci and Candidate Genes for Resistance to Powdery Mildew in a Resequenced Cucumber Germplasm
by Xiaoping Liu, Xingfang Gu, Hongwei Lu, Panna Liu, Han Miao, Yuling Bai and Shengping Zhang
Genes 2021, 12(4), 584; https://doi.org/10.3390/genes12040584 - 16 Apr 2021
Cited by 19 | Viewed by 3894
Abstract
Powdery mildew (PM) is one of the most serious diseases in cucumber and causes huge yield loss. Multiple quantitative trait loci (QTLs) for PM resistance have been reported in previous studies using a limited number of cucumber accessions. In this study, a cucumber [...] Read more.
Powdery mildew (PM) is one of the most serious diseases in cucumber and causes huge yield loss. Multiple quantitative trait loci (QTLs) for PM resistance have been reported in previous studies using a limited number of cucumber accessions. In this study, a cucumber core germplasm (CG) consisting of 94 resequenced lines was evaluated for PM resistance in four trials across three years (2013, 2014, and 2016). These trials were performed on adult plants in the field with natural infection. Using genome-wide association study (GWAS), 13 loci (pmG1.1, pmG1.2, pmG2.1, pmG2.2, pmG3.1, pmG4.1, pmG4.2, pmG5.1, pmG5.2, pmG5.3, pmG5.4, pmG6.1, and pmG6.2) associated with PM resistance were detected on all chromosomes except for Chr.7. Among these loci, ten were mapped to chromosomal intervals where QTLs had been reported in previous studies, while, three (pmG2.1, pmG3.1, and pmG4.1) were novel. The loci of pmG2.1, pmG5.2, pmG5.3 showed stronger signal in four trials. Based on the annotation of homologous genes in Arabidopsis and pairwise LD correlation analysis, candidate genes located in the QTL intervals were predicted. SNPs in these candidate genes were analyzed between haplotypes of highly resistant (HR) and susceptible (HS) CG lines, which were defined based on combing disease index data of all trials. Furthermore, candidate genes (Csa5G622830 and CsGy5G015660) reported in previous studies for PM resistance and cucumber orthologues of several PM susceptibility (S) genes (PMR5, PMR-6, and MLO) that are colocalized with certain QTLs, were analyzed for their potential contribution to the QTL effect on both PM and DM in the CG population. This study shows that the CG germplasm is a very valuable resource carrying known and novel QTLs for both PM and DM resistance, which can be exploited in cucumber breeding. Full article
(This article belongs to the Special Issue Powdery Mildew Resistance Genetics)
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25 pages, 9434 KiB  
Article
Comparative Analysis, Characterization and Evolutionary Study of Dirigent Gene Family in Cucurbitaceae and Expression of Novel Dirigent Peptide against Powdery Mildew Stress
by Vivek Yadav, Zhongyuan Wang, Xiaozhen Yang, Chunhua Wei, Xuan Changqing and Xian Zhang
Genes 2021, 12(3), 326; https://doi.org/10.3390/genes12030326 - 24 Feb 2021
Cited by 20 | Viewed by 3287
Abstract
Dirigent (DIR) proteins are induced under various stress conditions and involved in sterio- and regio-selective coupling of monolignol. A striking lack of information about dirigent genes in cucurbitaceae plants underscores the importance of functional characterization. In this study, 112 DIR genes were identified [...] Read more.
Dirigent (DIR) proteins are induced under various stress conditions and involved in sterio- and regio-selective coupling of monolignol. A striking lack of information about dirigent genes in cucurbitaceae plants underscores the importance of functional characterization. In this study, 112 DIR genes were identified in six species, and 61 genes from major cultivated species were analyzed. DIRs were analyzed using various bioinformatics tools and complemented by expression profiling. Phylogenetic analysis segregated the putative DIRs into six distinctively known subgroups. Chromosomal mapping revealed uneven distribution of genes, whereas synteny analysis exhibited that duplication events occurred during gene evolution. Gene structure analysis suggested the gain of introns during gene diversification. Gene ontology (GO) enrichment analysis indicates the participation of proteins in lignification and pathogen resistance activities. We also determined their organ-specific expression levels in three species revealing preferential expression in root and leaves. Furthermore, the number of CmDIR (CmDIR1, 6, 7 and 12) and ClDIR (ClDIR2, 5, 8, 9 and 17) genes exhibited higher expression in resistant cultivars after powdery mildew (PM) inoculation. In summary, based on the expression and in-silico analysis, we propose a role of DIRs in disease resistance mechanisms. Full article
(This article belongs to the Special Issue Powdery Mildew Resistance Genetics)
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21 pages, 1704 KiB  
Article
You Had Me at “MAGIC”!: Four Barley MAGIC Populations Reveal Novel Resistance QTL for Powdery Mildew
by Fluturë Novakazi, Lene Krusell, Jens Due Jensen, Jihad Orabi, Ahmed Jahoor, Therése Bengtsson and on behalf of the PPP Barley Consortium
Genes 2020, 11(12), 1512; https://doi.org/10.3390/genes11121512 - 18 Dec 2020
Cited by 13 | Viewed by 4685
Abstract
Blumeria graminis f. sp. hordei (Bgh), the causal agent of barley powdery mildew (PM), is one of the most important barley leaf diseases and is prevalent in most barley growing regions. Infection decreases grain quality and yields on average by 30%. [...] Read more.
Blumeria graminis f. sp. hordei (Bgh), the causal agent of barley powdery mildew (PM), is one of the most important barley leaf diseases and is prevalent in most barley growing regions. Infection decreases grain quality and yields on average by 30%. Multi-parent advanced generation inter-cross (MAGIC) populations combine the advantages of bi-parental and association panels and offer the opportunity to incorporate exotic alleles into adapted material. Here, four barley MAGIC populations consisting of six to eight founders were tested for PM resistance in field trials in Denmark. Principle component and STRUCTURE analysis showed the populations were unstructured and genome-wide linkage disequilibrium (LD) decay varied between 14 and 38 Mbp. Genome-wide association studies (GWAS) identified 11 regions associated with PM resistance located on chromosomes 1H, 2H, 3H, 4H, 5H and 7H, of which three regions are putatively novel resistance quantitative trait locus/loci (QTL). For all regions high-confidence candidate genes were identified that are predicted to be involved in pathogen defense. Haplotype analysis of the significant SNPs revealed new allele combinations not present in the founders and associated with high resistance levels. Full article
(This article belongs to the Special Issue Powdery Mildew Resistance Genetics)
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19 pages, 2715 KiB  
Article
Evidence for Allele-Specific Levels of Enhanced Susceptibility of Wheat mlo Mutants to the Hemibiotrophic Fungal Pathogen Magnaporthe oryzae pv. Triticum
by Katrin Gruner, Tobias Esser, Johanna Acevedo-Garcia, Matthias Freh, Michael Habig, Roxana Strugala, Eva Stukenbrock, Ulrich Schaffrath and Ralph Panstruga
Genes 2020, 11(5), 517; https://doi.org/10.3390/genes11050517 - 7 May 2020
Cited by 22 | Viewed by 4548
Abstract
Barley mlo mutants are well known for their profound resistance against powdery mildew disease. Recently, mlo mutant plants were generated in hexaploid bread wheat (Triticum aestivum) with the help of transgenic (transcription-activator-like nuclease, TALEN) and non-transgenic (targeted induced local lesions in [...] Read more.
Barley mlo mutants are well known for their profound resistance against powdery mildew disease. Recently, mlo mutant plants were generated in hexaploid bread wheat (Triticum aestivum) with the help of transgenic (transcription-activator-like nuclease, TALEN) and non-transgenic (targeted induced local lesions in genomes, TILLING) biotechnological approaches. While full-gene knockouts in the three wheat Mlo (TaMlo) homoeologs, created via TALEN, confer full resistance to the wheat powdery mildew pathogen (Blumeria graminis f.sp. tritici), the currently available TILLING-derived Tamlo missense mutants provide only partial protection against powdery mildew attack. Here, we studied the infection phenotypes of TALEN- and TILLING-derived Tamlo plants to the two hemibiotrophic pathogens Zymoseptoria tritici, causing Septoria leaf blotch in wheat, and Magnaporthe oryzae pv. Triticum (MoT), the causal agent of wheat blast disease. While Tamlo plants showed unaltered outcomes upon challenge with Z. tritici, we found evidence for allele-specific levels of enhanced susceptibility to MoT, with stronger powdery mildew resistance correlated with more invasive growth by the blast pathogen. Surprisingly, unlike barley mlo mutants, young wheat mlo mutant plants do not show undesired pleiotropic phenotypes such as spontaneous callose deposits in leaf mesophyll cells or signs of early leaf senescence. In conclusion, our study provides evidence for allele-specific levels of enhanced susceptibility of Tamlo plants to the hemibiotrophic wheat pathogen MoT. Full article
(This article belongs to the Special Issue Powdery Mildew Resistance Genetics)
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Review

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15 pages, 341 KiB  
Review
Specific Resistance of Barley to Powdery Mildew, Its Use and Beyond: A Concise Critical Review
by Antonín Dreiseitl
Genes 2020, 11(9), 971; https://doi.org/10.3390/genes11090971 - 21 Aug 2020
Cited by 31 | Viewed by 5258
Abstract
Powdery mildew caused by the airborne ascomycete fungus Blumeria graminis f. sp. hordei (Bgh) is one of most common diseases of barley (Hordeum vulgare). This, as with many other plant pathogens, can be efficiently controlled by inexpensive and environmentally-friendly [...] Read more.
Powdery mildew caused by the airborne ascomycete fungus Blumeria graminis f. sp. hordei (Bgh) is one of most common diseases of barley (Hordeum vulgare). This, as with many other plant pathogens, can be efficiently controlled by inexpensive and environmentally-friendly genetic resistance. General requirements for resistance to the pathogens are effectiveness and durability. Resistance of barley to Bgh has been studied intensively, and this review describes recent research and summarizes the specific resistance genes found in barley varieties since the last conspectus. Bgh is extraordinarily adaptable, and some commonly recommended strategies for using genetic resistance, including pyramiding of specific genes, may not be effective because they can only contribute to a limited extent to obtain sufficient resistance durability of widely-grown cultivars. In spring barley, breeding the nonspecific mlo gene is a valuable source of durable resistance. Pyramiding of nonspecific quantitative resistance genes or using introgressions derived from bulbous barley (Hordeum bulbosum) are promising ways for breeding future winter barley cultivars. The utilization of a wide spectrum of nonhost resistances can also be adopted once practical methods have been developed. Full article
(This article belongs to the Special Issue Powdery Mildew Resistance Genetics)
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