scholarly journals Convergent Adaptation to Quantitative Host Resistance in a Major Plant Pathogen

mBio ◽  
2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Jean Carlier ◽  
François Bonnot ◽  
Véronique Roussel ◽  
Sébastien Ravel ◽  
Reina Teresa Martinez ◽  
...  

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.

Author(s):  
Thomas Dumartinet ◽  
Sébastien Ravel ◽  
Véronique Roussel ◽  
Luis Pérez Vicente ◽  
Jaime Aguayo ◽  
...  

Plant pathogens often adapt to plant genetic resistance so characterization of the architecture under-lying such an adaptation is required to understand the adaptive potential of pathogen populations. Erosion of banana quantitative resistance to a major leaf disease caused by polygenic adaptation of the causal agent, the fungus Pseudocercospora fijiensis, was recently identified in the northern Caribbean region. Genome scan and quantitative genetics approaches were combined to investigate the adaptive architecture underlying this adaptation. Thirty-two genomic regions showing host se-lection footprints were identified by pool sequencing of isolates collected from seven plantation pairs of two cultivars with different levels of quantitative resistance. Individual sequencing and phenotyping of isolates from one pair revealed significant and variable levels of correlation be-tween haplotypes in 17 of these regions with a quantitative trait of pathogenicity (the diseased leaf area). The multilocus pattern of haplotypes detected in the 17 regions was found to be highly varia-ble across all the population pairs studied. These results suggest complex adaptive architecture un-derlying plant pathogen adaptation to quantitative resistance with a polygenic basis, redundancy, and a low level of parallel evolution between pathogen populations. Candidate genes involved in quantitative pathogenicity and host adaptation of P. fijiensis were highlighted in genomic regions combining annotation analysis with available biological data.


Author(s):  
McKinlee M. Salazar ◽  
Mônica T. Pupo ◽  
Amanda M. V. Brown

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.


2020 ◽  
Vol 11 ◽  
Author(s):  
Ya Li ◽  
Yijuan Han ◽  
Mengyu Qu ◽  
Jia Chen ◽  
Xiaofeng Chen ◽  
...  

mSystems ◽  
2018 ◽  
Vol 3 (6) ◽  
Author(s):  
Irina M. Velsko ◽  
Brinta Chakraborty ◽  
Marcelle M. Nascimento ◽  
Robert A. Burne ◽  
Vincent P. Richards

ABSTRACTHealth-associated oralStreptococcusspecies are promising probiotic candidates to protect against dental caries. Ammonia production through the arginine deiminase system (ADS), which can increase the pH of oral biofilms, and direct antagonism of caries-associated bacterial species are desirable properties for oral probiotic strains. ADS and antagonistic activities can vary dramatically among individuals, but the genetic basis for these differences is unknown. We sequenced whole genomes of a diverse set of clinical oralStreptococcusisolates and examined the genetic basis of variability in ADS and antagonistic activities. A total of 113 isolates were included and represented 10 species:Streptococcus australis, A12-like,S. cristatus,S. gordonii,S. intermedius,S. mitis,S. oralisincludingS. oralissubsp.dentisani,S. parasanguinis,S. salivarius, andS. sanguinis. Mean ADS activity and antagonism onStreptococcus mutansUA159 were measured for each isolate, and each isolate was whole genome shotgun sequenced on an Illumina MiSeq. Phylogenies were built of genes known to be involved in ADS activity and antagonism. Several approaches to correlate the pan-genome with phenotypes were performed. Phylogenies of genes previously identified in ADS activity and antagonism grouped isolates by species, but not by phenotype. A genome-wide association study (GWAS) identified additional genes potentially involved in ADS activity or antagonism across all the isolates we sequenced as well as within several species. Phenotypic heterogeneity in oral streptococci is not necessarily reflected by genotype and is not species specific. Probiotic strains must be carefully selected based on characterization of each strain and not based on inclusion within a certain species.IMPORTANCERepresentative type strains are commonly used to characterize bacterial species, yet species are phenotypically and genotypically heterogeneous. Conclusions about strain physiology and activity based on a single strain therefore may be inappropriate and misleading. When selecting strains for probiotic use, the assumption that all strains within a species share the same desired probiotic characteristics may result in selection of a strain that lacks the desired traits, and therefore makes a minimally effective or ineffective probiotic. Health-associated oral streptococci are promising candidates for anticaries probiotics, but strains need to be carefully selected based on observed phenotypes. We characterized the genotypes and anticaries phenotypes of strains from 10 species of oral streptococci and demonstrate poor correlation between genotype and phenotype across all species.


mBio ◽  
2019 ◽  
Vol 10 (4) ◽  
Author(s):  
Jacob L. Steenwyk ◽  
Xing-Xing Shen ◽  
Abigail L. Lind ◽  
Gustavo H. Goldman ◽  
Antonis Rokas

ABSTRACT The filamentous fungal family Aspergillaceae contains >1,000 known species, mostly in the genera Aspergillus and Penicillium. Several species are used in the food, biotechnology, and drug industries (e.g., Aspergillus oryzae and Penicillium camemberti), while others are dangerous human and plant pathogens (e.g., Aspergillus fumigatus and Penicillium digitatum). To infer a robust phylogeny and pinpoint poorly resolved branches and their likely underlying contributors, we used 81 genomes spanning the diversity of Aspergillus and Penicillium to construct a 1,668-gene data matrix. Phylogenies of the nucleotide and amino acid versions of this full data matrix as well as of several additional data matrices were generated using three different maximum likelihood schemes (i.e., gene-partitioned, unpartitioned, and coalescence) and using both site-homogenous and site-heterogeneous models (total of 64 species-level phylogenies). Examination of the topological agreement among these phylogenies and measures of internode certainty identified 11/78 (14.1%) bipartitions that were incongruent and pinpointed the likely underlying contributing factors, which included incomplete lineage sorting, hidden paralogy, hybridization or introgression, and reconstruction artifacts associated with poor taxon sampling. Relaxed molecular clock analyses suggest that Aspergillaceae likely originated in the lower Cretaceous and that the Aspergillus and Penicillium genera originated in the upper Cretaceous. Our results shed light on the ongoing debate on Aspergillus systematics and taxonomy and provide a robust evolutionary and temporal framework for comparative genomic analyses in Aspergillaceae. More broadly, our approach provides a general template for phylogenomic identification of resolved and contentious branches in densely genome-sequenced lineages across the tree of life. IMPORTANCE Understanding the evolution of traits across technologically and medically significant fungi requires a robust phylogeny. Even though species in the Aspergillus and Penicillium genera (family Aspergillaceae, class Eurotiomycetes) are some of the most significant technologically and medically relevant fungi, we still lack a genome-scale phylogeny of the lineage or knowledge of the parts of the phylogeny that exhibit conflict among analyses. Here, we used a phylogenomic approach to infer evolutionary relationships among 81 genomes that span the diversity of Aspergillus and Penicillium species, to identify conflicts in the phylogeny, and to determine the likely underlying factors of the observed conflicts. Using a data matrix comprised of 1,668 genes, we found that while most branches of the phylogeny of the Aspergillaceae are robustly supported and recovered irrespective of method of analysis, a few exhibit various degrees of conflict among our analyses. Further examination of the observed conflict revealed that it largely stems from incomplete lineage sorting and hybridization or introgression. Our analyses provide a robust and comprehensive evolutionary genomic roadmap for this important lineage, which will facilitate the examination of the diverse technologically and medically relevant traits of these fungi in an evolutionary context.


2019 ◽  
Author(s):  
Paula Maria Moreira Martins ◽  
Andre da Silva Xavier ◽  
Marco Aurelio Takita ◽  
Poliane Alfemas-Zerbini ◽  
Alessandra Alves de Souza

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.


2019 ◽  
Vol 109 (8) ◽  
pp. 1324-1330 ◽  
Author(s):  
E. Kosman ◽  
X. Chen ◽  
A. Dreiseitl ◽  
B. McCallum ◽  
A. Lebeda ◽  
...  

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.


mBio ◽  
2020 ◽  
Vol 11 (5) ◽  
Author(s):  
Lukas Meile ◽  
Jules Peter ◽  
Guido Puccetti ◽  
Julien Alassimone ◽  
Bruce A. McDonald ◽  
...  

ABSTRACT Dynamic changes in transcription profiles are key for the success of pathogens in colonizing their hosts. In many pathogens, genes associated with virulence, such as effector genes, are located in regions of the genome that are rich in transposable elements and heterochromatin. The contribution of chromatin modifications to gene expression in pathogens remains largely unknown. Using a combination of a reporter gene-based approach and chromatin immunoprecipitation, we show that the heterochromatic environment of effector genes in the fungal plant pathogen Zymoseptoria tritici is a key regulator of their specific spatiotemporal expression patterns. Enrichment in trimethylated lysine 27 of histone H3 dictates the repression of effector genes in the absence of the host. Chromatin decondensation during host colonization, featuring a reduction in this repressive modification, indicates a major role for epigenetics in effector gene induction. Our results illustrate that chromatin modifications triggered during host colonization determine the specific expression profile of effector genes at the cellular level and, hence, provide new insights into the regulation of virulence in fungal plant pathogens. IMPORTANCE Fungal plant pathogens possess a large repertoire of genes encoding putative effectors, which are crucial for infection. Many of these genes are expressed at low levels in the absence of the host but are strongly induced at specific stages of the infection. The mechanisms underlying this transcriptional reprogramming remain largely unknown. We investigated the role of the genomic environment and associated chromatin modifications of effector genes in controlling their expression pattern in the fungal wheat pathogen Zymoseptoria tritici. Depending on their genomic location, effector genes are epigenetically repressed in the absence of the host and during the initial stages of infection. Derepression of effector genes occurs mainly during and after penetration of plant leaves and is associated with changes in histone modifications. Our work demonstrates the role of chromatin in shaping the expression of virulence components and, thereby, the interaction between fungal pathogens and their plant hosts.


2018 ◽  
Vol 31 (1) ◽  
pp. 6-12 ◽  
Author(s):  
Yan Wang ◽  
Yuanchao Wang

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.


2016 ◽  
Vol 198 (6) ◽  
pp. 930-940 ◽  
Author(s):  
Chao Wang ◽  
Desong Tang ◽  
Yong-Gui Gao ◽  
Lian-Hui Zhang

ABSTRACTSuccinic semialdehyde (SSA), an important metabolite of γ-aminobutyric acid (GABA), is a ligand of the repressor AttJ regulating the expression of theattJ-attKLMgene cluster in the plant pathogenAgrobacterium tumefaciens. While the response ofA. tumefaciensto GABA and the function ofattKLMhave been extensively studied, genetic and physiological responses ofA. tumefaciensto SSA remain unknown. In combination with microarray and genetic approaches, this study sets out to explore new roles of the SSA-AttJKLM regulatory mechanism during bacterial infection. The results showed that SSA plays a key role in regulation of several bacterial activities, including C4-dicarboxylate utilization, nitrate assimilation, and resistance to oxidative stress. Interestingly, while the SSA relies heavily on the functional AttKLM in mediating nitrate assimilation and oxidative stress resistance, the compound could regulate utilization of C4-dicarboxylates independent of AttJKLM. We further provide evidence that SSA controls C4-dicarboxylate utilization through induction of an SSA importer and that disruption ofattKLMattenuates the tumorigenicity ofA. tumefaciens. Taken together, these findings indicate that SSA could be a potent plant signal which, together with AttKLM, plays a vital role in promoting the bacterial prosurvival abilities during infection.IMPORTANCEAgrobacterium tumefaciensis a plant pathogen causing crown gall diseases and has been well known as a powerful tool for plant genetic engineering. During the long history of microbe-host interaction,A. tumefacienshas evolved the capabilities of recognition and response to plant-derived chemical metabolites. Succinic semialdehyde (SSA) is one such metabolite. Previous results have demonstrated that SSA functions to activate a quorum-quenching mechanism and thus to decrease the level of quorum-sensing signals, thereby avoiding the elicitation of a plant defense. Here, we studied the effect of SSA on gene expression at a genome-wide level and reported that SSA also promotes bacterial survival during infection. These findings provide a new insight on the biological significance of chemical signaling between agrobacteria and plant hosts.


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