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Molecular Genetics and Genomics of Plant-Pathogen Interactions

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A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Plant Sciences".

Deadline for manuscript submissions: closed (31 October 2023) | Viewed by 22488

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Special Issue Editors

Prof. Dr. Vijai Bhadauria

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Guest Editor

Department of Plant Pathology, College of Plant Protection, China Agricultural University, Beijing 100193, China
Interests: plant pathology; pathogenomics; effector biology; fungal virulence/pathogenicity; plant-pathogen interactions; quantitative genetics; plant disease resistance; minichromosomes in fungal pathogens

Prof. Dr. Wensheng Zhao

E-Mail Website
Guest Editor

College of Plant Protection, China Agricultural University, 100193 Beijing, China
Interests: plant immunity; plant pathology; plant-microbe interaction; plant biotechnology

Special Issue Information

Dear Colleagues,

Plants lack an adaptive immune system; therefore, they rely solely on their innate immunity, mainly composed of cell surface and intracellular receptors, to fend off potential pathogens. Cell surface receptors are plasma membrane-resident pattern recognition receptors (PRRs) that detect conserved molecular signatures of potential pathogens called pathogen-associated molecular patterns (PAMPs) through direct binding. The detection of PAMPs by PRRs triggers PAMP-triggered immunity (PTI), which is very effective against the vast majority of potential pathogens roaming in the environment. Diseases are, therefore, exceptions, and only in rare cases can pathogens successfully infect plants. The pathogens do it by subduing PTI using their effectors, which are small proteins secreted by the pathogens into the host cell cytoplasm. Plants have evolved intracellular receptors called nucleotide-binding leucine-rich repeat (NLR) receptors to detect these cytoplasmic effectors, activating effector-triggered immunity. So, this dynamic interaction between effectors and plant immune network determines the outcome of plant-pathogen interactions, i.e., susceptibility or resistance. The special issue aims to provide selected contributions to this complex interplay between plants and their pathogens with genomics and genetics perspectives. In addition, the special issue also welcomes articles pertaining to pathogenomics, fungal virulence/pathogenicity and genomes of emerging fungal pathogens of plants.

Potential topics include, but are not limited to:

Pathogenomics
Genomics of emerging pathogens of crops
Effector biology
Virulence/pathogenicity
Plant disease resistance and genetic sources of disease resistance
Molecular mechanisms underlying plant-pathogen interactions
Enabling technologies to dissect plant disease resistance and pathogen virulence/pathogenicity
OMICS (genomics, transcriptomics and proteomics) of plant-pathogen interactions
Genetic dissection of crop resistance

Prof. Dr. Vijai Bhadauria
Prof. Dr. Wensheng Zhao
Guest Editors

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Keywords

plant-pathogen interactions
effectors
plant disease resistance genes
molecular genetics
pathogen genomes
pathogenomics
CRISPR-Cas9
genetic sources of disease resistance
OMICS

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Published Papers (10 papers)

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31 pages, 6530 KiB

Open AccessArticle

Transcriptome Analysis Reveals a Comprehensive Virus Resistance Response Mechanism in Pecan Infected by a Novel Badnavirus Pecan Virus

by Jiyu Zhang, Tao Wang, Zhanhui Jia, Xiaodong Jia, Yongzhi Liu, Jiping Xuan, Gang Wang and Fan Zhang

Int. J. Mol. Sci. 2022, 23(21), 13576; https://doi.org/10.3390/ijms232113576 - 5 Nov 2022

Cited by 5 | Viewed by 2323

Abstract

Pecan leaf-variegated plant, which was infected with a novel badnavirus named pecan mosaic virus (PMV) detected by small RNA deep sequencing, is a vital model plant for studying the molecular mechanism of retaining green or chlorosis of virus-infected leaves. In this report, PMV infection in pecan leaves induced PAMP-triggered immunity (PTI) and effector-triggered immunity (ETI). PMV infection suppressed the expressions of key genes of fatty acid, oleic acid (C18:1), and very-long-chain fatty acids (VLCFA) biosynthesis, indicating that fatty acids-derived signaling was one of the important defense pathways in response to PMV infection in pecan. PMV infection in pecans enhanced the expressions of pathogenesis-related protein 1 (PR1). However, the transcripts of phenylalanine ammonia-lyase (PAL) and isochorismate synthase (ICS) were downregulated, indicating that salicylic acid (SA) biosynthesis was blocked in pecan infected with PMV. Meanwhile, disruption of auxin signaling affected the activation of the jasmonic acid (JA) pathway. Thus, C18:1 and JA signals are involved in response to PMV infection in pecan. In PMV-infected yellow leaves, damaged chloroplast structure and activation of mitogen-activated protein kinase 3 (MPK3) inhibited photosynthesis. Cytokinin and SA biosynthesis was blocked, leading to plants losing immune responses and systemic acquired resistance (SAR). The repression of photosynthesis and the induction of sink metabolism in the infected tissue led to dramatic changes in carbohydrate partitioning. On the contrary, the green leaves of PMV infection in pecan plants had whole cell tissue structure and chloroplast clustering, establishing a strong antiviral immunity system. Cytokinin biosynthesis and signaling transductions were remarkably strengthened, activating plant immune responses. Meanwhile, cytokinin accumulation in green leaves induced partial SA biosynthesis and gained comparatively higher SAR compared to that of yellow leaves. Disturbance of the ribosome biogenesis might enhance the resistance to PMV infection in pecan and lead to leaves staying green. Full article

(This article belongs to the Special Issue Molecular Genetics and Genomics of Plant-Pathogen Interactions)

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18 pages, 3439 KiB

Open AccessArticle

A R2R3 MYB Transcription Factor, TaMYB391, Is Positively Involved in Wheat Resistance to Puccinia striiformis f. sp. tritici

by Mehari Desta Hawku, Fuxin He, Xingxuan Bai, Md Ashraful Islam, Xueling Huang, Zhensheng Kang and Jun Guo

Int. J. Mol. Sci. 2022, 23(22), 14070; https://doi.org/10.3390/ijms232214070 - 15 Nov 2022

Cited by 12 | Viewed by 2178

Abstract

A biotrophic fungus, Puccinia striiformis f.sp. tritici (Pst), which causes stripe rust disease in wheat is the most yield-limiting factor in wheat production. Plants have complex defense mechanisms against invading pathogens. Hypersensitive response (HR), a kind of programmed cell death (PCD) at the infection site, is among these defense mechanisms. Transcription factors (TFs) play a crucial role in plant defense response against invading pathogens. Myeloblastosis (MYB) TFs are among the largest TFs families that are involved in response to both biotic and abiotic stresses. However, little is known about the mechanisms of MYB TFs during the interaction between wheat and the stripe rust fungus. Here, we identified an R2R3 MYB TF from wheat, designated as TaMYB391, and characterized its functional role during wheat–Pst interaction. Our data indicated that TaMYB391 is induced by Pst infection and exogenous application of salicylic acid (SA) and abscisic acid (ABA). TaMYB391 is localized in the nucleus of both wheat and Nicotiana benthamiana. Transient overexpression of TaMYB391 in N. benthamiana triggered HR-related PCD accompanied by increased electrolyte leakage, high accumulation of reactive oxygen species (ROS), and transcriptional accumulation of SA defense-related genes and HR-specific marker genes. Overexpression of TaMYB391 in wheat significantly enhanced wheat resistance to stripe rust fungus through the induction of pathogenesis-related (PR) genes, ROS accumulation and hypersensitive cell death. On the other hand, RNAi-mediated silencing of TaMYB391 decreased the resistance of wheat to Pst accompanied by enhanced growth of the pathogen. Together our findings demonstrate that TaMYB391 acts as a positive regulator of HR-associated cell death and positively contributes to the resistance of wheat to the stripe rust fungus by regulating certain PR genes, possibly through SA signaling pathways. Full article

(This article belongs to the Special Issue Molecular Genetics and Genomics of Plant-Pathogen Interactions)

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20 pages, 2893 KiB

Open AccessArticle

Novel Virulence Factors Deciphering Klebsiella pneumoniae KpC4 Infect Maize as a Crossing-Kingdom Pathogen: An Emerging Environmental Threat

by Min Huang, Pengfei He, Pengbo He, Yixin Wu, Shahzad Munir and Yueqiu He

Int. J. Mol. Sci. 2022, 23(24), 16005; https://doi.org/10.3390/ijms232416005 - 15 Dec 2022

Cited by 2 | Viewed by 2107

Abstract

Klebsiella pneumoniae is not only a human and animal opportunistic pathogen, but a food-borne pathogen. Cross-kingdom infection has been focused on since K. pneumoniae was identified as the pathogen of maize, banana, and pomegranate. Although the pathogenicity of K. pneumoniae strains (from ditch water, maize, and human) on plant and mice has been confirmed, there are no reports to explain the molecular mechanisms of the pathogen. This study uncovered the K. pneumoniae KpC4 isolated from maize top rot for the determination of various virulence genes and resistance genes. At least thirteen plant disease-causing genes are found to be involved in the disruption of plant defense. Among them, rcsB is responsible for causing disease in both plants and animals. The novel sequence types provide solid evidence that the pathogen invades plant and has robust ecological adaptability. It is imperative to perform further studies on the verification of these KpC4 genes’ functions to understand the molecular mechanisms involved in plant–pathogen interactions. Full article

(This article belongs to the Special Issue Molecular Genetics and Genomics of Plant-Pathogen Interactions)

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20 pages, 2694 KiB

Open AccessArticle

Transcriptomic Analysis of Resistant and Wild-Type Botrytis cinerea Isolates Revealed Fludioxonil-Resistance Mechanisms

by Mei Liu, Junbo Peng, Xuncheng Wang, Wei Zhang, Ying Zhou, Hui Wang, Xinghong Li, Jiye Yan and Liusheng Duan

Int. J. Mol. Sci. 2023, 24(2), 988; https://doi.org/10.3390/ijms24020988 - 4 Jan 2023

Cited by 6 | Viewed by 3018

Abstract

Botrytis cinerea, the causal agent of gray mold, is one of the most destructive pathogens of cherry tomatoes, causing fruit decay and economic loss. Fludioxonil is an effective fungicide widely used for crop protection and is effective against tomato gray mold. The emergence of fungicide-resistant strains has made the control of B. cinerea more difficult. While the genome of B. cinerea is available, there are few reports regarding the large-scale functional annotation of the genome using expressed genes derived from transcriptomes, and the mechanism(s) underlying such fludioxonil resistance remain unclear. The present study prepared RNA-sequencing (RNA-seq) libraries for three B. cinerea strains (two highly resistant (LR and FR) versus one highly sensitive (S) to fludioxonil), with and without fludioxonil treatment, to identify fludioxonil responsive genes that associated to fungicide resistance. Functional enrichment analysis identified nine resistance related DEGs in the fludioxonil-induced LR and FR transcriptome that were simultaneously up-regulated, and seven resistance related DEGs down-regulated. These included adenosine triphosphate (ATP)-binding cassette (ABC) transporter-encoding genes, major facilitator superfamily (MFS) transporter-encoding genes, and the high-osmolarity glycerol (HOG) pathway homologues or related genes. The expression patterns of twelve out of the sixteen fludioxonil-responsive genes, obtained from the RNA-sequence data sets, were validated using quantitative real-time PCR (qRT-PCR). Based on RNA-sequence analysis, it was found that hybrid histidine kinase, fungal HHKs, such as BOS1, BcHHK2, and BcHHK17, probably involved in the fludioxonil resistance of B. cinerea, in addition, a number of ABC and MFS transporter genes that were not reported before, such as BcATRO, BMR1, BMR3, BcNMT1, BcAMF1, BcTOP1, BcVBA2, and BcYHK8, were differentially expressed in the fludioxonil-resistant strains, indicating that overexpression of these efflux transporters located in the plasma membranes may associate with the fludioxonil resistance mechanism of B. cinerea. All together, these lines of evidence allowed us to draw a general portrait of the anti-fludioxonil mechanisms for B. cinerea, and the assembled and annotated transcriptome data provide valuable genomic resources for further study of the molecular mechanisms of B. cinerea resistance to fludioxonil. Full article

(This article belongs to the Special Issue Molecular Genetics and Genomics of Plant-Pathogen Interactions)

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16 pages, 2737 KiB

Open AccessArticle

Transcriptional Analysis of the Differences between ToLCNDV-India and ToLCNDV-ES Leading to Contrary Symptom Development in Cucumber

by Thuy T. B. Vo, Won Kyong Cho, Yeonhwa Jo, Aamir Lal, Bupi Nattanong, Muhammad Amir Qureshi, Marjia Tabssum, Elisa Troiano, Giuseppe Parrella, Eui-Joon Kil, Taek-Kyun Lee and Sukchan Lee

Int. J. Mol. Sci. 2023, 24(3), 2181; https://doi.org/10.3390/ijms24032181 - 22 Jan 2023

Viewed by 2615

Abstract

Tomato leaf curl New Delhi virus-ES (ToLCNDV-ES), a high threat to cucurbits in the Mediterranean Basin, is listed as a different strain from the Asian ToLCNDV isolates. In this study, the infectivity of two clones previously isolated from Italy and Pakistan were compared in cucumbers, which resulted in the opposite symptom appearance. The swapping subgenome was processed; however, the mechanisms related to the disease phenotype remain unclear. To identify the disease-associated genes that could contribute to symptom development under the two ToLCNDV infections, the transcriptomes of ToLCNDV-infected and mock-inoculated cucumber plants were compared 21 days postinoculation. The number of differentially expressed genes in ToLCNDV-India-infected plants was 10 times higher than in ToLCNDV-ES-infected samples. The gene ontology (GO) and pathway enrichment were analyzed using the Cucurbits Genomics Database. The flavonoid pathway-related genes were upregulated in ToLCNDV-ES, but some were downregulated in ToLCNDV-India infection, suggesting their role in resistance to the two ToLCNDV infections. The relative expression levels of the selected candidate genes were validated by qRT-PCR under two ToLCNDV-infected conditions. Our results reveal the different infectivity of the two ToLCNDVs in cucumber and also provide primary information based on RNA-seq for further analysis related to different ToLCNDV infections. Full article

(This article belongs to the Special Issue Molecular Genetics and Genomics of Plant-Pathogen Interactions)

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17 pages, 2629 KiB

Open AccessArticle

An Agrobacterium-Mediated Transient Expression Method for Functional Assay of Genes Promoting Disease in Monocots

by Haijiao Xu, Qingle Chang, Luli Huang, Peiyao Wei, Yulu Song, Zejian Guo, You-Liang Peng and Jun Fan

Int. J. Mol. Sci. 2023, 24(8), 7636; https://doi.org/10.3390/ijms24087636 - 21 Apr 2023

Cited by 1 | Viewed by 3301

Abstract

Agrobacterium-mediated transient expression (AMTE) has been widely used for high-throughput assays of gene function in diverse plant species. However, its application in monocots is still limited due to low expression efficiency. Here, by using histochemical staining and a quantitative fluorescence assay of β-glucuronidase (GUS) gene expression, we investigated factors affecting the efficiency of AMTE on intact barley plants. We found prominent variation in GUS expression levels across diverse vectors commonly used for stable transformation and that the vector pCBEP produced the highest expression. Additionally, concurrent treatments of plants with one day of high humidity and two days of darkness following agro-infiltration also significantly increased GUS expression efficiency. We thus established an optimized method for efficient AMTE on barley and further demonstrated its efficiency on wheat and rice plants. We showed that this approach could produce enough proteins suitable for split-luciferase assays of protein-protein interactions on barley leaves. Moreover, we incorporated the AMTE protocol into the functional dissection of a complex biological process such as plant disease. Based on our previous research, we used the pCBEP vector to construct a full-length cDNA library of genes upregulated during the early stage of rice blast disease. A subsequent screen of the library by AMTE identified 15 candidate genes (out of ~2000 clones) promoting blast disease on barley plants. Four identified genes encode chloroplast-related proteins: OsNYC3, OsNUDX21, OsMRS2-9, and OsAk2. These genes were induced during rice blast disease; however, constitutive overexpression of these genes conferred enhanced disease susceptibility to Colletotrichum higginsianum in Arabidopsis. These observations highlight the power of the optimized AMTE approach on monocots as an effective tool for facilitating functional assays of genes mediating complex processes such as plant-microbe interactions. Full article

(This article belongs to the Special Issue Molecular Genetics and Genomics of Plant-Pathogen Interactions)

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14 pages, 3244 KiB

Open AccessArticle

Unleashing the Potential of EIL Transcription Factors in Enhancing Sweet Orange Resistance to Bacterial Pathologies: Genome-Wide Identification and Expression Profiling

by Yajun Su, Suming Dai, Na Li, Alessandra Gentile, Cong He, Jing Xu, Kangle Duan, Xue Wang, Bing Wang and Dazhi Li

Int. J. Mol. Sci. 2023, 24(16), 12644; https://doi.org/10.3390/ijms241612644 - 10 Aug 2023

Cited by 2 | Viewed by 1387

Abstract

The ETHYLENE INSENSITIVE3-LIKE (EIL) family is one of the most important transcription factor (TF) families in plants and is involved in diverse plant physiological and biochemical processes. In this study, ten EIL transcription factors (CsEILs) in sweet orange were systematically characterized via whole-genome analysis. The CsEIL genes were unevenly distributed across the four sweet orange chromosomes. Putative cis-acting regulatory elements (CREs) associated with CsEIL were found to be involved in plant development, as well as responses to biotic and abiotic stress. Notably, quantitative reverse transcription polymerase chain reaction (qRT-PCR) revealed that CsEIL genes were widely expressed in different organs of sweet orange and responded to both high and low temperature, NaCl treatment, and to ethylene-dependent induction of transcription, while eight additionally responded to Xanthomonas citri pv. Citri (Xcc) infection, which causes citrus canker. Among these, CsEIL2, CsEIL5 and CsEIL10 showed pronounced upregulation. Moreover, nine genes exhibited differential expression in response to Candidatus Liberibacter asiaticus (CLas) infection, which causes Citrus Huanglongbing (HLB). The genome-wide characterization and expression profile analysis of CsEIL genes provide insights into the potential functions of the CsEIL family in disease resistance. Full article

(This article belongs to the Special Issue Molecular Genetics and Genomics of Plant-Pathogen Interactions)

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19 pages, 7458 KiB

Open AccessArticle

Structure-Function Characterisation of Eop1 Effectors from the Erwinia-Pantoea Clade Reveals They May Acetylate Their Defence Target through a Catalytic Dyad

by Vishant Tomar, Erik H. A. Rikkerink, Janghoon Song, Svetla Sofkova-Bobcheva and Vincent G. M. Bus

Int. J. Mol. Sci. 2023, 24(19), 14664; https://doi.org/10.3390/ijms241914664 - 28 Sep 2023

Viewed by 1516

Abstract

The YopJ group of acetylating effectors from phytopathogens of the genera Pseudomonas and Ralstonia have been widely studied to understand how they modify and suppress their host defence targets. In contrast, studies on a related group of effectors, the Eop1 group, lag far behind. Members of the Eop1 group are widely present in the Erwinia-Pantoea clade of Gram-negative bacteria, which contains phytopathogens, non-pathogens and potential biocontrol agents, implying that they may play an important role in agroecological or pathological adaptations. The lack of research in this group of YopJ effectors has left a significant knowledge gap in their functioning and role. For the first time, we perform a comparative analysis combining AlphaFold modelling, in planta transient expressions and targeted mutational analyses of the Eop1 group effectors from the Erwinia-Pantoea clade, to help elucidate their likely activity and mechanism(s). This integrated study revealed several new findings, including putative binding sites for inositol hexakisphosphate and acetyl coenzyme A and newly postulated target-binding domains, and raises questions about whether these effectors function through a catalytic triad mechanism. The results imply that some Eop1s may use a catalytic dyad acetylation mechanism that we found could be promoted by the electronegative environment around the active site. Full article

(This article belongs to the Special Issue Molecular Genetics and Genomics of Plant-Pathogen Interactions)

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11 pages, 5536 KiB

Open AccessReview

The Hidden Truths of Fungal Virulence and Adaptation on Hosts: Unraveling the Conditional Dispensability of Minichromosomes in the Hemibiotrophic Colletotrichum Pathogens

by Vijai Bhadauria, Manyu Zhang, Wendi Ma, Jun Yang, Wensheng Zhao and You-Liang Peng

Int. J. Mol. Sci. 2024, 25(1), 198; https://doi.org/10.3390/ijms25010198 - 22 Dec 2023

Cited by 2 | Viewed by 1263

Abstract

Colletotrichum spp. are ascomycete fungi and cause anthracnose disease in numerous crops of economic significance. The genomes of these fungi are distributed among ten core chromosomes and two to three minichromosomes. While the core chromosomes regulate fungal growth, development and virulence, the extent to which the minichromosomes are involved in these processes is still uncertain. Here, we discuss the minichromosomes of three hemibiotrophic Colletotrichum pathogens, i.e., C. graminicola, C. higginsianum and C. lentis. These minichromosomes are typically less than one megabase in length, characterized by containing higher repetitive DNA elements, lower GC content, higher frequency of repeat-induced point mutations (RIPMs) and sparse gene distribution. Molecular genetics and functional analyses have revealed that these pathogens harbor one conditionally dispensable minichromosome, which is dispensable for fungal growth and development but indispensable for fungal virulence on hosts. They appear to be strain-specific innovations and are highly compartmentalized into AT-rich and GC-rich blocks, resulting from RIPMs, which may help protect the conditionally dispensable minichromosomes from erosion of already scarce genes, thereby helping the Colletotrichum pathogens maintain adaptability on hosts. Overall, understanding the mechanisms underlying the conditional dispensability of these minichromosomes could lead to new strategies for controlling anthracnose disease in crops. Full article

(This article belongs to the Special Issue Molecular Genetics and Genomics of Plant-Pathogen Interactions)

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