Functional Variation of Plant–Pathogen Interactions: New Concept and Methods for Virulence Data Analyses

Classical virulence analysis is based on discovering virulence phenotypes of isolates with regard to a composition of resistance genes in a differential set of host genotypes. With such a vision, virulence phenotypes are usually treated in a genetic manner as one of two possible alleles, either virulence or avirulence in a binary locus. Therefore, population genetics metrics and methods have become prevailing tools for analyzing virulence data at multiple loci. However, a basis for resolving binary virulence phenotypes is infection type (IT) data of host–pathogen interaction that express functional traits of each specific isolate in a given situation (particular host, environmental conditions, cultivation practice, and so on). IT is determined by symptoms and signs observed (e.g., lesion type, lesion size, coverage of leaf or leaf segments by mycelium, spore production and so on), and assessed by IT scores at a generally accepted scale for each plant–pathogen system. Thus, multiple IT profiles of isolates are obtained and can be subjected to analysis of functional variation within and among operational units of a pathogen. Such an approach may allow better utilization of the information available in the raw data, and reveal a functional (e.g., environmental) component of pathogen variation in addition to the genetic one. New methods for measuring functional variation of plant–pathogen interaction with IT data were developed. The methods need an appropriate assessment scale and expert estimations of dissimilarity between IT scores for each plant–pathogen system (an example is presented). Analyses of a few data sets at different hierarchical levels demonstrated discrepancies in results obtained with IT phenotypes versus binary virulence phenotypes. The ability to measure functional IT-based variation offers promise as an effective tool in the study of epidemics caused by plant pathogens.

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Plant SWEETs: from sugar transport to plant–pathogen interaction and more unexpected physiological roles

Plant Physiology ◽

10.1093/plphys/kiab127 ◽

2021 ◽

Author(s):

Richard Breia ◽

Artur Conde ◽

Hélder Badim ◽

Ana Margarida Fortes ◽

Hernâni Gerós ◽

...

Keyword(s):

Plant Pathogen ◽

Sugar Transport ◽

High Capacity ◽

Phloem Loading ◽

Transcription Activator ◽

Pythium Irregulare ◽

Clear Cut ◽

Opposite Behavior ◽

Plant Pathogen Interaction ◽

Plant Pathogen Interactions

Abstract Sugars Will Eventually be Exported Transporters (SWEETs) have important roles in numerous physiological mechanisms where sugar efflux is critical, including phloem loading, nectar secretion, seed nutrient filling, among other less expected functions. They mediate low affinity and high capacity transport, and in angiosperms this family is composed by 20 paralogs on average. As SWEETs facilitate the efflux of sugars, they are highly susceptible to hijacking by pathogens, making them central players in plant–pathogen interaction. For instance, several species from the Xanthomonas genus are able to upregulate the transcription of SWEET transporters in rice (Oryza sativa), upon the secretion of transcription-activator-like effectors. Other pathogens, such as Botrytis cinerea or Erysiphe necator, are also capable of increasing SWEET expression. However, the opposite behavior has been observed in some cases, as overexpression of the tonoplast AtSWEET2 during Pythium irregulare infection restricted sugar availability to the pathogen, rendering plants more resistant. Therefore, a clear-cut role for SWEET transporters during plant–pathogen interactions has so far been difficult to define, as the metabolic signatures and their regulatory nodes, which decide the susceptibility or resistance responses, remain poorly understood. This fuels the still ongoing scientific question: what roles can SWEETs play during plant–pathogen interaction? Likewise, the roles of SWEET transporters in response to abiotic stresses are little understood. Here, in addition to their relevance in biotic stress, we also provide a small glimpse of SWEETs importance during plant abiotic stress, and briefly debate their importance in the particular case of grapevine (Vitis vinifera) due to its socioeconomic impact.

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Co-Occurrence of Viruses, Plant Pathogens, and Symbionts in an Underexplored Hemipteran Clade

Frontiers in Cellular and Infection Microbiology ◽

10.3389/fcimb.2021.715998 ◽

2021 ◽

Vol 11 ◽

Author(s):

McKinlee M. Salazar ◽

Mônica T. Pupo ◽

Amanda M. V. Brown

Keyword(s):

Plant Pathogen ◽

Plant Pathogens ◽

Plant Viruses ◽

Metagenomic Sequencing ◽

Base Pairs ◽

Shotgun Metagenomic Sequencing ◽

Data Clusters ◽

Blast Database ◽

Insect Symbionts ◽

Plant Pathogen Interactions

Interactions between insect symbionts and plant pathogens are dynamic and complex, sometimes involving direct antagonism or synergy and sometimes involving ecological and evolutionary leaps, as insect symbionts transmit through plant tissues or plant pathogens transition to become insect symbionts. Hemipterans such as aphids, whiteflies, psyllids, leafhoppers, and planthoppers are well-studied plant pests that host diverse symbionts and vector plant pathogens. The related hemipteran treehoppers (family Membracidae) are less well-studied but offer a potentially new and diverse array of symbionts and plant pathogenic interactions through their distinct woody plant hosts and ecological interactions with diverse tending hymenopteran taxa. To explore membracid symbiont–pathogen diversity and co-occurrence, this study performed shotgun metagenomic sequencing on 20 samples (16 species) of treehopper, and characterized putative symbionts and pathogens using a combination of rapid blast database searches and phylogenetic analysis of assembled scaffolds and correlation analysis. Among the 8.7 billion base pairs of scaffolds assembled were matches to 9 potential plant pathogens, 12 potential primary and secondary insect endosymbionts, numerous bacteriophages, and other viruses, entomopathogens, and fungi. Notable discoveries include a divergent Brenneria plant pathogen-like organism, several bee-like Bombella and Asaia strains, novel strains of Arsenophonus-like and Sodalis-like symbionts, Ralstonia sp. and Ralstonia-type phages, Serratia sp., and APSE-type phages and bracoviruses. There were several short Phytoplasma and Spiroplasma matches, but there was no indication of plant viruses in these data. Clusters of positively correlated microbes such as yeast-like symbionts and Ralstonia, viruses and Serratia, and APSE phage with parasitoid-type bracoviruses suggest directions for future analyses. Together, results indicate membracids offer a rich palette for future study of symbiont–plant pathogen interactions.

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Apoplastic Cell Death-Inducing Proteins of Filamentous Plant Pathogens: Roles in Plant-Pathogen Interactions

Frontiers in Genetics ◽

10.3389/fgene.2020.00661 ◽

2020 ◽

Vol 11 ◽

Author(s):

Ya Li ◽

Yijuan Han ◽

Mengyu Qu ◽

Jia Chen ◽

Xiaofeng Chen ◽

...

Keyword(s):

Cell Death ◽

Plant Pathogen ◽

Plant Pathogens ◽

Plant Pathogen Interactions

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CRISPR-Cas systems in the plant pathogen Xanthomonas spp. and their impact on genome plasticity

10.1101/731166 ◽

2019 ◽

Author(s):

Paula Maria Moreira Martins ◽

Andre da Silva Xavier ◽

Marco Aurelio Takita ◽

Poliane Alfemas-Zerbini ◽

Alessandra Alves de Souza

Keyword(s):

Phylogenetic Analysis ◽

Plant Pathogen ◽

Significant Variation ◽

Crop Production ◽

Plant Pathogens ◽

Economic Losses ◽

Genome Plasticity ◽

Plant Pathogen Interactions ◽

Cas Proteins

AbstractXanthomonas is one of the most important bacterial genera of plant pathogens causing economic losses in crop production worldwide. Despite its importance, many aspects of basic Xanthomonas biology remain unknown or understudied. Here, we present the first genus-wide analysis of CRISPR-Cas in Xanthomonas and describe specific aspects of its occurrence. Our results show that Xanthomonas genomes harbour subtype I-C and I-F CRISPR-Cas systems and that species belonging to distantly Xanthomonas-related genera in Xanthomonadaceae exhibit the same configuration of coexistence of the I-C and I-F CRISPR subtypes. Additionally, phylogenetic analysis using Cas proteins indicated that the CRISPR systems present in Xanthomonas spp. are the result of an ancient acquisition. Despite the close phylogeny of these systems, they present significant variation in both the number and targets of spacers. An interesting characteristic observed in this study was that the identified plasmid-targeting spacers were always driven toward plasmids found in other Xanthomonas strains, indicating that CRISPR-Cas systems could be very effective in coping with plasmidial infections. Since many effectors are plasmid encoded, CRISPR-Cas might be driving specific characteristics of plant-pathogen interactions.

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Trick or Treat: Microbial Pathogens Evolved Apoplastic Effectors Modulating Plant Susceptibility to Infection

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-07-17-0177-fi ◽

2018 ◽

Vol 31 (1) ◽

pp. 6-12 ◽

Cited By ~ 29

Author(s):

Yan Wang ◽

Yuanchao Wang

Keyword(s):

Immune Responses ◽

Plant Pathogen ◽

Plant Pathogens ◽

Plant Cell Wall ◽

Effector Proteins ◽

Microbial Pathogens ◽

Susceptibility To Infection ◽

Plant Pathogen Interactions ◽

Harsh Conditions ◽

Plant Susceptibility

The apoplastic space between the plant cell wall and the plasma membrane constitutes a major battleground for plant-pathogen interactions. To survive in harsh conditions in the plant apoplast, pathogens must cope with various immune responses. During infection, plant pathogens secrete an arsenal of effector proteins into the apoplast milieu, some of which are detected by the plant surveillance system and, thus, activate plant innate immunity. Effectors that evade plant perception act in modulating plant apoplast immunity to favor successful pathogen infection. The concerted actions of apoplastic effectors often determine the outcomes of plant-pathogen interactions. In this review, we summarize current advances on the understanding of apoplastic effectors and highlight the strategies employed by pathogens to counter host apoplastic defense.

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Photoperiod Following Inoculation of Arabidopsis with Pyricularia oryzae (syn. Magnaporthe oryzae) Influences on the Plant–Pathogen Interaction

International Journal of Molecular Sciences ◽

10.3390/ijms22095004 ◽

2021 ◽

Vol 22 (9) ◽

pp. 5004

Author(s):

Sayaka Shimizu ◽

Yuri Yamauchi ◽

Atsushi Ishikawa

Keyword(s):

Plant Pathogen ◽

Dark Period ◽

Continuous Light ◽

Defense Responses ◽

Time Of Day ◽

Pyricularia Oryzae ◽

Oxygen Species ◽

Plant Pathogen Interaction ◽

Plant Pathogen Interactions ◽

Resistance To Penetration

In plant–pathogen interactions, a proper light environment affects the establishment of defense responses in plants. In our previous experiments, we found that nonhost resistance (NHR) to Pyricularia oryzae Cav. in Arabidopsis thaliana (L.) Heynh. (Arabidopsis), in diurnal conditions, varies with the inoculation time. Moreover, we indicated that the circadian clock plays an important role in regulating time-of-day differences in NHR to P. oryzae in Arabidopsis. However, the involvement of photoperiod in regulating NHR was still not understood. To determine the photoperiod role, we performed the experiments in continuous light and darkness during the early Arabidopsis–P. oryzae interaction. We found that the light period after the inoculation in the evening enhanced the resistance to penetration. However, the dark period after the inoculation in the morning suppressed the penetration resistance. Furthermore, the genetic analysis indicated that jasmonic acid, reactive oxygen species, and tryptophan-derived metabolite(s) contribute to the photoperiod regulation of NHR in Arabidopsis. The present results denote that photoperiod plays an important role in regulating time-of-day differences in NHR to P. oryzae in Arabidopsis.

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Combining Digital Imaging and Genome Wide Association Mapping to Dissect Uncharacterized Traits in Plant/Pathogen Interactions

10.1101/296939 ◽

2018 ◽

Cited By ~ 1

Author(s):

Rachel F. Fordyce ◽

Nicole E. Soltis ◽

Celine Caseys ◽

Raoni Gwinner ◽

Jason A. Corwin ◽

...

Keyword(s):

Disease Resistance ◽

Botrytis Cinerea ◽

Plant Pathogen ◽

Digital Imaging ◽

Plant Disease Resistance ◽

Plant Disease ◽

Lesion Size ◽

Genome Wide Association ◽

Genome Wide ◽

Plant Pathogen Interactions

AbstractPlant resistance to generalist pathogens with broad host ranges, such as Botrytis cinerea, is typically quantitative and highly polygenic. Recent studies have begun to elucidate the molecular genetic basis underpinning plant-pathogen interactions using commonly measured traits including lesion size and/or pathogen biomass. Yet with the advent of digital imaging and phenomics, there are a large number of additional resistance traits available to study quantitative resistance. In this study, we used high-throughput digital imaging analysis to investigate previously uncharacterized visual traits of plant-pathogen interactions related disease resistance using the Arabidopsis thaliana/Botrytis cinerea pathosystem. Using a large collection of 75 visual traits collected from every lesion, we focused on lesion color, lesion shape, and lesion size, to test how these aspects of the interaction are genetically related. Using genome wide association (GWA) mapping in A. thaliana, we show that lesion color and shape are genetically separable traits associated with plant-disease resistance. Using defined mutants in 23 candidate genes from the GWA mapping, we could identify and show that novel loci associated with each different plant-pathogen interaction trait, which expands our understanding of the functional mechanisms driving plant disease resistance.SummaryDigital imaging allows the identification of genes controlling novel lesion traits.

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Comparative secretomics identifies conserved WAxR motif-containing effectors in rust fungi that suppress cell death in plants

10.1101/2021.08.18.456800 ◽

2021 ◽

Author(s):

Rajdeep Jaswal ◽

Himanshu Dubey ◽

Kanti Kiran ◽

Hukam Rawal ◽

Sivasubramanian Rajarammohan ◽

...

Keyword(s):

Cell Death ◽

Plant Pathogen ◽

Fungal Pathogens ◽

Plant Pathogens ◽

Rust Fungi ◽

Cell Wall Degrading Enzymes ◽

Conserved Motifs ◽

Large Numbers ◽

Biotrophic Pathogens ◽

Plant Pathogen Interaction

Identification of novel effectors with conserved features has always remained a challenge in plant-pathogen interaction studies. The introduction of the genomics era in plant-pathogen studies has led to the identification of significant candidate effectors with novel motifs such as RxLR and dEER motifs. However, in the case of fungal pathogens, limited conserved motifs associated with effectors have been discovered yet. In the present study, we have performed comparative secretome analysis for major plant pathogens of diverse nutrition mechanisms with the aim of dissecting the features underlying their corresponding secretome and conserved motifs. We showed that rust fungi possess the lowest Cell wall degrading enzymes (CWDEs) consortium lower than other biotrophic pathogens. We also showed rust fungi possess the highest secretory superoxide dismutase (SOD) than other studied plant pathogens. Further, we prioritized the candidate secretory effectors proteins (CSEPs) of all the studied pathogens by combining various effector mining parameters to highlight the candidates with potential effector features. A novel WAxR motif in conjugation with the Y/F/WxC (FGC) motif was identified in the effectors of various P. striiformis races present globally. The WAxR/WAxR like motifs ( WxxR, WAxx, xAxR) containing effectors were also found in the secretome of other rust fungi. Further, the functional validation of two candidate effectors with WAxR motif from P. striiformis Yr9 showed that these effectors localize to the nucleus as well as cytoplasm, and are able to suppress BAX induced cell death in Nicotiana benthamiana. The mutation analysis of individual residues of the WAxR motif (W, A, R ) however did not affect the cell death suppression nor subcellular localization of these effectors. Overall, the current study reports the presence of novel motifs in large numbers of effectors of rust fungi with cell death suppression features.

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mRNA inventory of extracellular vesicles from Ustilago maydis

10.20944/preprints202106.0257.v1 ◽

2021 ◽

Author(s):

Seomun Kwon ◽

Oliver Rupp ◽

Andreas Brachmann ◽

Alexander Goesmann ◽

Michael Feldbrügge

Keyword(s):

Extracellular Vesicles ◽

Plant Pathogen ◽

Ustilago Maydis ◽

Metabolic Enzyme ◽

Plant Pathogen Interaction ◽

Intercellular Signalling ◽

Animal Hosts ◽

Initial Survey ◽

Plant Pathogen Interactions ◽

Maize Smut

Extracellular vesicles (EVs) can transfer diverse RNA cargo for intercellular signalling. EV-associated RNAs have been found in diverse fungi and were proposed to be relevant for pathogenesis in animal hosts. In plant-pathogen interactions, small RNAs are exchanged in a cross-kingdom RNAi warfare and EVs were considered to be a delivery mechanism. To extend the search for EV-associated molecules involved in plants-pathogen communication, we have characterised the repertoire of EV-associated mRNAs secreted by the maize smut pathogen, Ustilago maydis. For this initial survey, EVs were isolated from axenic filamentous cultures that mimic infectious hyphae. The EV-associated RNAs were resistant to degradation by RNases and the presence of intact mRNAs was evident. The set of mRNAs enriched inside EVs relative to the fungal cells are functionally distinct from those that are depleted from EVs, particularly overrepresented in metabolic enzyme activities. Intriguingly, mRNAs of some known effectors and other proteins linked to virulence were found in EVs. Furthermore, several mRNAs enriched in EVs are also upregulated during infection, suggesting that EV-associated mRNAs may participate in plant-pathogen interaction.

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Convergent Adaptation to Quantitative Host Resistance in a Major Plant Pathogen

mBio ◽

10.1128/mbio.03129-20 ◽

2021 ◽

Vol 12 (1) ◽

Author(s):

Jean Carlier ◽

François Bonnot ◽

Véronique Roussel ◽

Sébastien Ravel ◽

Reina Teresa Martinez ◽

...

Keyword(s):

Plant Pathogen ◽

Genetic Basis ◽

Plant Pathogens ◽

Quantitative Resistance ◽

Biological Data ◽

Content Type ◽

A Genome ◽

Genomic Regions ◽

Plant Pathogen Interactions ◽

Pseudocercospora Fijiensis

ABSTRACT Plant pathogens can adapt to quantitative resistance, eroding its effectiveness. The aim of this work was to reveal the genomic basis of adaptation to such a resistance in populations of the fungus Pseudocercospora fijiensis, a major devastating pathogen of banana, by studying convergent adaptation on different cultivars. Samples from P. fijiensis populations showing a local adaptation pattern on new banana hybrids with quantitative resistance were compared, based on a genome scan approach, with samples from traditional and more susceptible cultivars in Cuba and the Dominican Republic. Whole-genome sequencing of pools of P. fijiensis isolates (pool-seq) sampled from three locations per country was conducted according to a paired population design. The findings of different combined analyses highly supported the existence of convergent adaptation on the study cultivars between locations within but not between countries. Five to six genomic regions involved in this adaptation were detected in each country. An annotation analysis and available biological data supported the hypothesis that some genes within the detected genomic regions may play a role in quantitative pathogenicity, including gene regulation. The results suggested that the genetic basis of fungal adaptation to quantitative plant resistance is at least oligogenic, while highlighting the existence of specific host-pathogen interactions for this kind of resistance. IMPORTANCE Understanding the genetic basis of pathogen adaptation to quantitative resistance in plants has a key role to play in establishing durable strategies for resistance deployment. In this context, a population genomic approach was developed for a major plant pathogen (the fungus Pseudocercospora fijiensis causing black leaf streak disease of banana) whereby samples from new resistant banana hybrids were compared with samples from more susceptible conventional cultivars in two countries. A total of 11 genomic regions for which there was strong evidence of selection by quantitative resistance were detected. An annotation analysis and available biological data supported the hypothesis that some of the genes within these regions may play a role in quantitative pathogenicity. These results suggested a polygenic basis of quantitative pathogenicity in this fungal pathogen and complex molecular plant-pathogen interactions in quantitative disease development involving several genes on both sides.

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