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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 January 2023) | Viewed by 22575

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Prof. Dr. Sixue Chen

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Guest Editor

Department of Biology, University of Mississippi, Oxford, MS 38677, USA
Interests: disease triangle; guard cells; glucosinolates; proteomics; metabolomics; mass spectrometry
Special Issues, Collections and Topics in MDPI journals

Dr. Jessie Fernandez

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Guest Editor

Department of Microbiology and Cell Science, University of Florida, Gainesville, FL 32610, USA
Interests: fungal biology; plant pathogens; plant–microbe interactions; effector biology; rice blast disease
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Plant pathogens represent a significant threat to agricultural systems, causing major damage to the food industry worldwide. Pathogens are constantly adapting to evade or suppress plant defense responses to cause disease. Despite this, plants have evolved sophisticated approaches to recognize and restrict the pathogen to the infection site. A unique and intimate association between plant and pathogens is created as they are in a constant arms race to coexist or compete for survival in nature. Deciphering how plant–pathogen interactions are established is not only an essential aspect in plant pathology but also extremely important for crop improvement, sustainability, and global food security. This Special Issue on “Plant–Pathogen Interactions” welcomes original research and review articles that present recent advances in the field, with a focus on but not limited to the molecular mechanisms underlining disease progression, effector biology, plant immunity, and virulence factors. New molecular approaches or tools (including omics or multi-omics) to study plant–pathogens interactions are also welcome.

Prof. Dr. Sixue Chen
Dr. Jessie Fernandez
Guest Editors

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Keywords

pathogenicity
plant immunity
pattern-triggered immunity (PTI)
effector-triggered immunity (ETI)
effectors
avirulent
virulent
biotroph
necrotroph
interactions

Published Papers (11 papers)

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Research

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25 pages, 17947 KiB

Open AccessArticle

Integrated Transcriptome and Metabolome Dissecting Interaction between Vitis vinifera L. and Grapevine Fabavirus

by Baodong Zhang, Mengyan Zhang, Xiaojun Jia, Guojun Hu, Fang Ren, Xudong Fan and Yafeng Dong

Int. J. Mol. Sci. 2023, 24(4), 3247; https://doi.org/10.3390/ijms24043247 - 07 Feb 2023

Cited by 1 | Viewed by 1827

Abstract

Grapevine fabavirus (GFabV) is a novel member of the Fabavirus genus associated with chlorotic mottling and deformation symptoms in grapevines. To gain insights into the interaction between GFabV and grapevines, V. vinifera cv. ‘Summer Black’ infected with GFabV was investigated under field conditions through physiological, agronomic, and multi-omics approaches. GFabV induced significant symptoms on ‘Summer Black’, and caused a moderate decrease in physiological efficiency. In GFabV-infected plants, alterations in carbohydrate- and photosynthesis-related genes might trigger some defense responses. In addition, secondary metabolism involved in plant defense was progressively induced by GFabV. Jasmonic acid and ethylene signaling were down-regulated in GFabV-infected leaves and berries along with the expression of proteins related to LRR and protein kinases, suggesting that GFabV can block the defense in healthy leaves and berries. Furthermore, this study provided biomarkers for early monitoring of GFabV infection in grapevines, and contributed to a better understanding of the complex grapevine-virus interaction. Full article

(This article belongs to the Special Issue Plant Pathogen Interactions)

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16 pages, 3734 KiB

Open AccessArticle

Tomato Yellow Leaf Curl Sardinia Virus Increases Drought Tolerance of Tomato

by Camilla Sacco Botto, Slavica Matić, Amedeo Moine, Walter Chitarra, Luca Nerva, Chiara D’Errico, Chiara Pagliarani and Emanuela Noris

Int. J. Mol. Sci. 2023, 24(3), 2893; https://doi.org/10.3390/ijms24032893 - 02 Feb 2023

Cited by 2 | Viewed by 1827

Abstract

Drought stress is one of the major physiological stress factors that adversely affect agricultural production, altering critical features of plant growth and metabolism. Plants can be subjected simultaneously to abiotic and biotic stresses, such as drought and viral infections. Rewarding effects provided by viruses on the ability of host plants to endure abiotic stresses have been reported. Recently, begomoviruses causing the tomato yellow leaf curl disease in tomatoes were shown to increase heat and drought tolerance. However, biological bases underlying the induced drought tolerance need further elucidation, particularly in the case of tomato plants. In this work, tomato plants infected by the tomato yellow leaf curl Sardinia virus (TYLCSV) were subjected to severe drought stress, followed by recovery. Morphological traits, water potential, and hormone contents were measured in leaves together with molecular analysis of stress-responsive and hormone metabolism-related genes. Wilting symptoms appeared three days later in TYLCSV-infected plants compared to healthy controls and post-rehydration recovery was faster (2 vs. 4 days, respectively). Our study contributes new insights into the impact of viruses on the plant’s adaptability to environmental stresses. On a broader perspective, such information could have important practical implications for managing the effects of climate change on agroecosystems. Full article

(This article belongs to the Special Issue Plant Pathogen Interactions)

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17 pages, 12601 KiB

Open AccessArticle

Comprehensive Analysis of Major Latex-Like Protein Family Genes in Cucumber (Cucumis sativus L.) and Their Potential Roles in Phytophthora Blight Resistance

by Yunyan Kang, Jiale Tong, Wei Liu, Zhongli Jiang, Gengzheng Pan, Xianpeng Ning, Xian Yang and Min Zhong

Int. J. Mol. Sci. 2023, 24(1), 784; https://doi.org/10.3390/ijms24010784 - 02 Jan 2023

Cited by 6 | Viewed by 2105

Abstract

Major latex-like proteins (MLPs) play crucial roles in abiotic and biotic stresses. However, little was known about this gene family in cucumbers. In this study, a total of 37 putative cucumber MLP genes were identified on a genome-wide level and classified into three groups by sequence homologous comparison with Arabidopsis thaliana. Chromosome mapping suggested that only tandem duplication occurred in evolution. The multiple regulatory cis-elements related to stress, hormone, light and growth response were found in the promoter region of these CsMLP genes, indicating that CsMLPs might be widely involved in the process of plant growth, development and various stress conditions. Transcriptome analysis indicated a strong reprogramming of MLPs expression in response to Phytophthora melonis infection in cucumber. Knockdown of CsMLP1 reduced the P. melonis tolerance, while transient overexpression of CsMLP1 improved disease tolerance in cucumber. Conversely, the silence of CsMLP5 decreased the lesion area caused by P. melonis in the cotyledons, and overexpression of CsMLP5 promoted lesion expansion. Taken together, our results provide a comprehensive basis for further mining the function of CsMLP members and will also be significant for elucidating the evolutionary relationship in cucumber. Full article

(This article belongs to the Special Issue Plant Pathogen Interactions)

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26 pages, 6431 KiB

Open AccessArticle

The NF-Y Transcription Factor Family in Watermelon: Re-Characterization, Assembly of ClNF-Y Complexes, Hormone- and Pathogen-Inducible Expression and Putative Functions in Disease Resistance

by Siyu Jiang, Hui Wang, Ya Wen, Jiayu Liang, Dayong Li and Fengming Song

Int. J. Mol. Sci. 2022, 23(24), 15778; https://doi.org/10.3390/ijms232415778 - 12 Dec 2022

Viewed by 1423

Abstract

Nuclear factor Y (NF-Y) is a heterotrimeric transcription factor that binds to the CCAAT cis-element in the promoters of target genes and plays critical roles in plant growth, development, and stress responses. In the present study, we aimed to re-characterize the ClNF-Y family in watermelon, examine the assembly of ClNF-Y complexes, and explore their possible involvement in disease resistance. A total of 25 ClNF-Y genes (7 ClNF-YAs, 10 ClNF-YBs, and 8 ClNF-YCs) were identified in the watermelon genome. The ClNF-Y family was comprehensively characterized in terms of gene and protein structures, phylogenetic relationships, and evolution events. Different types of cis-elements responsible for plant growth and development, phytohormones, and/or stress responses were identified in the promoters of the ClNF-Y genes. ClNF-YAs and ClNF-YCs were mainly localized in the nucleus, while most of the ClNF-YBs were localized in the cytoplasm of cells. ClNF-YB5, -YB6, -YB7, -YB8, -YB9, and -YB10 interacted with ClNF-YC2, -YC3, -YC4, -YC5, -YC6, -YC7, and -YC8, while ClNF-YB1 and -YB3 interacted with ClNF-YC1. A total of 37 putative ClNF-Y complexes were identified, e.g., ClNF-YA1, -YA2, -YA3, and -YA7 assembled into 13, 8, 8, and 8 ClNF-Y complexes with different ClNF-YB/-YC heterodimers. Most of the ClNF-Y genes responded with distinct expression patterns to defense hormones such as salicylic acid, methyl jasmonate, abscisic acid, and ethylene precursor 1-aminocyclopropane-1-carboxylate, and to infection by the vascular infecting fungus Fusarium oxysporum f. sp. niveum. Overexpression of ClNF-YB1, -YB8, -YB9, ClNF-YC2, and -YC7 in transgenic Arabidopsis resulted in an earlier flowering phenotype. Overexpression of ClNF-YB8 in Arabidopsis led to enhanced resistance while overexpression of ClNF-YA2 and -YC2 resulted in decreased resistance against Botrytis cinerea. Similarly, overexpression of ClNF-YA3, -YB1, and -YC4 strengthened resistance while overexpression of ClNF-YA2 and -YB8 attenuated resistance against Pseudomonas syringae pv. tomato DC3000. The re-characterization of the ClNF-Y family provides a basis from which to investigate the biological functions of ClNF-Y genes in respect of growth, development, and stress response in watermelon, and the identification of the functions of some ClNF-Y genes in disease resistance enables further exploration of the molecular mechanism of ClNF-Ys in the regulation of watermelon immunity against diverse pathogens. Full article

(This article belongs to the Special Issue Plant Pathogen Interactions)

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20 pages, 2907 KiB

Open AccessArticle

Investigating Grapevine Red Blotch Virus Infection in Vitis vinifera L. cv. Cabernet Sauvignon Grapes: A Multi-Omics Approach

by Arran C. Rumbaugh, Blythe Durbin-Johnson, Emily Padhi, Larry Lerno, Raul Cauduro Girardello, Monica Britton, Carolyn Slupsky, Mysore R. Sudarshana and Anita Oberholster

Int. J. Mol. Sci. 2022, 23(21), 13248; https://doi.org/10.3390/ijms232113248 - 31 Oct 2022

Cited by 2 | Viewed by 2109

Abstract

Grapevine red blotch virus (GRBV) is a recently identified virus. Previous research indicates primarily a substantial impact on berry ripening in all varieties studied. The current study analyzed grapes’ primary and secondary metabolism across grapevine genotypes and seasons to reveal both conserved and variable impacts to GRBV infection. Vitis vinifera cv. Cabernet Sauvignon (CS) grapevines grafted on two different rootstocks (110R and 420A) were analyzed in 2016 and 2017. Metabolite profiling revealed a considerable impact on amino acid and malate acid levels, volatile aroma compounds derived from the lipoxygenase pathway, and anthocyanins synthesized in the phenylpropanoid pathway. Conserved transcriptional responses to GRBV showed induction of auxin-mediated pathways and photosynthesis with inhibition of transcription and translation processes mainly at harvest. There was an induction of plant-pathogen interactions at pre-veraison, for all genotypes and seasons, except for CS 110R in 2017. Lastly, differential co-expression analysis revealed a transcriptional shift from metabolic synthesis and energy metabolism to transcription and translation processes associated with a virus-induced gene silencing transcript. This plant-derived defense response transcript was only significantly upregulated at veraison for all genotypes and seasons, suggesting a phenological association with disease expression and plant immune responses. Full article

(This article belongs to the Special Issue Plant Pathogen Interactions)

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11 pages, 2849 KiB

Open AccessArticle

CLIBASIA_00460 Disrupts Hypersensitive Response and Interacts with Citrus Rad23 Proteins

by Junepyo Oh, Julien G. Levy, Chia-Cheng Kan, Freddy Ibanez-Carrasco and Cecilia Tamborindeguy

Int. J. Mol. Sci. 2022, 23(14), 7846; https://doi.org/10.3390/ijms23147846 - 16 Jul 2022

Cited by 4 | Viewed by 1721

Abstract

‘Candidatus Liberibacter asiaticus’ (CLas) is a bacterium that causes Huanglongbing, also known as citrus greening, in citrus plants. ‘Candidatus Liberibacter solanacearum’ (Lso) is a close relative of CLas and in the US it infects solanaceous crops, causing zebra chip disease in potato. Previously, we have identified the Lso hypothetical protein effector 1 (Lso-HPE1). This protein uses a signal peptide for secretion; disrupts programmed cell death; and interacts with tomato RAD23c, d, and e proteins, but not with RAD23a. In this study, we evaluated whether CLIBASIA_00460, the CLas homolog of Lso-HPE1 interacted with citrus RAD23 proteins and disrupted their programmed cell death. Based on the yeast two-hybrid assay results, CLIBASIA_00460 interacted with citrus RAD23c and RAD23d, but not with citrus RAD23b. These results were confirmed using bimolecular fluorescence complementation assays, which showed that these interactions occurred in cell puncta, but not in the nucleus or cytoplasm. Additionally, CLIBASIA_00460 was able to disrupt the Prf^D1416V-induced hypersensitive response. Therefore, based on the similar interactions between Lso-HPE1 and CLIBASIA_00460 with the host RAD23 proteins and their ability to inhibit cell death in plants, we propose that these effectors may have similar functions during plant infection. Full article

(This article belongs to the Special Issue Plant Pathogen Interactions)

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19 pages, 17097 KiB

Open AccessArticle

DspA/E-Triggered Non-Host Resistance against E. amylovora Depends on the Arabidopsis GLYCOLATE OXIDASE 2 Gene

by Alban Launay, Sylvie Jolivet, Gilles Clément, Marco Zarattini, Younes Dellero, Rozenn Le Hir, Mathieu Jossier, Michael Hodges, Dominique Expert and Mathilde Fagard

Int. J. Mol. Sci. 2022, 23(8), 4224; https://doi.org/10.3390/ijms23084224 - 11 Apr 2022

Cited by 5 | Viewed by 2033

Abstract

DspA/E is a type three effector injected by the pathogenic bacterium Erwinia amylovora inside plant cells. In non-host Arabidopsis thaliana, DspA/E inhibits seed germination, root growth, de novo protein synthesis and triggers localized cell death. To better understand the mechanisms involved, we performed EMS mutagenesis on a transgenic line, 13-1-2, containing an inducible dspA/E gene. We identified three suppressor mutants, two of which belonged to the same complementation group. Both were resistant to the toxic effects of DspA/E. Metabolome analysis showed that the 13-1-2 line was depleted in metabolites of the TCA cycle and accumulated metabolites associated with cell death and defense. TCA cycle and cell-death associated metabolite levels were respectively increased and reduced in both suppressor mutants compared to the 13-1-2 line. Whole genome sequencing indicated that both suppressor mutants displayed missense mutations in conserved residues of Glycolate oxidase 2 (GOX2), a photorespiratory enzyme that we confirmed to be localized in the peroxisome. Leaf GOX activity increased in leaves infected with E. amylovora in a DspA/E-dependent manner. Moreover, the gox2-2 KO mutant was more sensitive to E. amylovora infection and displayed reduced JA-signaling. Our results point to a role for glycolate oxidase in type II non-host resistance and to the importance of central metabolic functions in controlling growth/defense balance. Full article

(This article belongs to the Special Issue Plant Pathogen Interactions)

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Review

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14 pages, 1525 KiB

Open AccessReview

Regulating Death and Disease: Exploring the Roles of Metacaspases in Plants and Fungi

by Nalleli Garcia, Rachel E. Kalicharan, Lisa Kinch and Jessie Fernandez

Int. J. Mol. Sci. 2023, 24(1), 312; https://doi.org/10.3390/ijms24010312 - 24 Dec 2022

Cited by 6 | Viewed by 1830

Abstract

Identified over twenty years ago and distantly related to animal caspases are a group of cysteine proteases known as metacaspases. Throughout the years, much like caspase roles in metazoans, metacaspases have been shown to be involved in regulating cellular death in non-metazoan organisms. Yet, continued research on metacaspases describes these proteins as intricate and multifunctional, displaying striking diversity on distinct biological functions. In this review, we intend to describe the recent advances in our understanding of the divergence of metacaspase functionality in plants and fungi. We will dissect the duality of metacaspase activity in the context of plant-pathogen interactions, providing a unique lens from which to characterize metacaspases in the development, immunity, and stress responses of plants, and the development and virulence of fungi. Furthermore, we explore the evolutionary trajectory of fungal metacaspases to delineate their structure and function. Bridging the gap between metacaspase roles in immunity and pathogenicity of plant-pathogen interactions can enable more effective and targeted phytopathogen control efforts to increase production of globally important food crops. Therefore, the exploitation and manipulation of metacaspases in plants or fungi represent new potential avenues for developing mitigation strategies against plant pathogens. Full article

(This article belongs to the Special Issue Plant Pathogen Interactions)

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9 pages, 810 KiB

Open AccessReview

Does Potassium (K⁺) Contribute to High-Nitrate (NO₃⁻) Weakening of a Plant’s Defense System against Necrotrophic Fungi?

by Anis Limami, Bertrand Hirel and Jérémy Lothier

Int. J. Mol. Sci. 2022, 23(24), 15631; https://doi.org/10.3390/ijms232415631 - 09 Dec 2022

Cited by 1 | Viewed by 1398

Abstract

In this opinion article, we have analyzed the relevancy of a hypothesis which is based on the idea that in Arabidopsis thaliana jasmonic acid, a (JA)-mediated defense system against necrotrophic fungi is weakened when NO₃⁻ supply is high. Such a hypothesis is based on the fact that when NO₃⁻ supply is high, it induces an increase in the amount of bioactive ABA which induces the sequestration of the phosphatase ABI2 (PP2C) into the PYR/PYL/RCAR receptor. Consequently, the Ca sensors CBL1/9-CIPK23 are not dephosphorylated by ABI2, thus remaining able to phosphorylate targets such as AtNPF6.3 and AtKAT1, which are NO₃⁻ and K⁺ transporters, respectively. Therefore, the impact of phosphorylation on the regulation of these two transporters, could (1) reduce NO₃⁻ influx as in its phosphorylated state AtNPF6.3 shifts to low capacity state and (2) increase K⁺ influx, as in its phosphorylated state KAT1 becomes more active. It is also well known that in roots, K⁺ loading in the xylem and its transport to the shoot is activated in the presence of NO₃⁻. As such, the enrichment of plant tissues in K⁺ can impair a jasmonic acid (JA) regulatory pathway and the induction of the corresponding biomarkers. The latter are known to be up-regulated under K⁺ deficiency and inhibited when K⁺ is resupplied. We therefore suggest that increased K⁺ uptake and tissue content induced by high NO₃⁻ supply modifies the JA regulatory pathway, resulting in a weakened JA-mediated plant’s defense system against necrotrophic fungi. Full article

(This article belongs to the Special Issue Plant Pathogen Interactions)

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26 pages, 2563 KiB

Open AccessReview

Xylanase Inhibitors: Defense Players in Plant Immunity with Implications in Agro-Industrial Processing

by Silvio Tundo, Giulia Mandalà, Luca Sella, Francesco Favaron, Renesh Bedre and Raviraj M. Kalunke

Int. J. Mol. Sci. 2022, 23(23), 14994; https://doi.org/10.3390/ijms232314994 - 30 Nov 2022

Cited by 8 | Viewed by 2866

Abstract

Xylanase inhibitors (XIs) are plant cell wall proteins largely distributed in monocots that inhibit the hemicellulose degrading activity of microbial xylanases. XIs have been classified into three classes with different structures and inhibition specificities, namely Triticum aestivum xylanase inhibitors (TAXI), xylanase inhibitor proteins (XIP), and thaumatin-like xylanase inhibitors (TLXI). Their involvement in plant defense has been established by several reports. Additionally, these inhibitors have considerable economic relevance because they interfere with the activity of xylanases applied in several agro-industrial processes. Previous reviews highlighted the structural and biochemical properties of XIs and hypothesized their role in plant defense. Here, we aimed to update the information on the genomic organization of XI encoding genes, the inhibition properties of XIs against microbial xylanases, and the structural properties of xylanase-XI interaction. We also deepened the knowledge of XI regulation mechanisms in planta and their involvement in plant defense. Finally, we reported the recently studied strategies to reduce the negative impact of XIs in agro-industrial processes and mentioned their allergenicity potential. Full article

(This article belongs to the Special Issue Plant Pathogen Interactions)

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21 pages, 955 KiB

Open AccessReview

Transcriptomics Advancement in the Complex Response of Plants to Viroid Infection

by Melissa Joubert, Noëlani van den Berg, Jacques Theron and Velushka Swart

Int. J. Mol. Sci. 2022, 23(14), 7677; https://doi.org/10.3390/ijms23147677 - 12 Jul 2022

Cited by 3 | Viewed by 2088

Abstract

Viroids are the smallest plant pathogens, consisting of a single-stranded circular RNA of less than 500 ribonucleotides in length. Despite their noncoding nature, viroids elicit disease symptoms in many economically important plant hosts, and are, thus, a class of pathogens of great interest. How these viroids establish disease within host plants, however, is not yet fully understood. Recent transcriptomic studies have revealed that viroid infection influences the expression of genes in several pathways and processes in plants, including defence responses, phytohormone signalling, cell wall modification, photosynthesis, secondary metabolism, transport, gene expression and protein modification. There is much debate about whether affected pathways signify a plant response to viroid infection, or are associated with the appearance of disease symptoms in these interactions. In this review, we consolidate the findings of viroid–host transcriptome studies to provide an overview of trends observed in the data. When considered together, changes in the gene expression of different hosts upon viroid infection reveal commonalities and differences in diverse interactions. Here, we discuss whether trends in host gene expression can be correlated to plant defence or disease development during viroid infection, and highlight avenues for future research in this field. Full article

(This article belongs to the Special Issue Plant Pathogen Interactions)

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