Rapid evolution in plant-microbe interactions - an evolutionary genomics perspective.
TL;DR: This work has shown that host jumps and shifts may be more pervasive than once believed and hybridization and horizontal gene transfer likely play important roles in the emergence of genetic novelty.
Abstract: Access to greater genomic resolution through new sequencing technologies is transforming the field of plant pathology. As scientists embrace these new methods, some overarching patterns and observations come into focus. Evolutionary genomic studies are used to determine not only the origins of pathogen lineages and geographic patterns of genetic diversity, but also to discern how natural selection structures genetic variation across the genome. With greater and greater resolution, we can now pinpoint the targets of selection on a large scale. At multiple levels, crypsis and convergent evolution are evident. Host jumps and shifts may be more pervasive than once believed, and hybridization and horizontal gene transfer (HGT) likely play important roles in the emergence of genetic novelty.
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TL;DR: This article presents cases where multi-omics technologies salient to pathology including metabolomics, genomics, metagenomics, volatilomics, and spectranomics have been successfully used for plant disease ecology, and discusses additional limitations and pitfalls to be wary of.
Abstract: The swift rise of omics-approaches allows for investigating microbial diversity and plant-microbe interactions across diverse ecological communities and spatio-temporal scales. The environment, however, is rapidly changing. The introduction of invasive species and the effects of climate change have particular impact on emerging plant diseases and managing current epidemics. It is critical, therefore, to take a holistic approach to understand how and why pathogenesis occurs in order to effectively manage for diseases given the synergies of changing environmental conditions. A multi-omics approach allows for a detailed picture of plant-microbial interactions and can ultimately allow us to build predictive models for how microbes and plants will respond to stress under environmental change. This article is designed as a primer for those interested in integrating -omic approaches into their plant disease research. We review -omics technologies salient to pathology including metabolomics, genomics, metagenomics, volatilomics, and spectranomics, and present cases where multi-omics have been successfully used for plant disease ecology. We then discuss additional limitations and pitfalls to be wary of prior to conducting an integrated research project as well as provide information about promising future directions.
38 citations
Cites background from "Rapid evolution in plant-microbe in..."
...The types of questions addressed include genome-wide evolutionary and demographic processes affecting population structure, evolutionary processes affecting speciation and the divergence of closely related taxa, and locus-specific effects, acting on specific genes or chromosomes that affect adaptation or defined phenotypes [26, 29, 30]....
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TL;DR: In this article, the authors showed that SCOOP peptides trigger immune responses and altered root development in a MIK2-dependent manner with a sub-nanomolar sensitivity.
Abstract: Sessile plants encode a large number of small peptides and cell surface-resident receptor kinases, most of which have unknown functions. Here, we report that the Arabidopsis receptor kinase MALE DISCOVERER 1-INTERACTING RECEPTOR-LIKE KINASE 2 (MIK2) recognizes the conserved signature motif of SERINE-RICH ENDOGENOUS PEPTIDEs (SCOOPs) from Brassicaceae plants as well as proteins present in fungal Fusarium spp. and bacterial Comamonadaceae, and elicits various immune responses. SCOOP signature peptides trigger immune responses and altered root development in a MIK2-dependent manner with a sub-nanomolar sensitivity. SCOOP12 directly binds to the extracellular leucine-rich repeat domain of MIK2 in vivo and in vitro, indicating that MIK2 is the receptor of SCOOP peptides. Perception of SCOOP peptides induces the association of MIK2 and the coreceptors SOMATIC EMBRYOGENESIS RECEPTOR KINASE 3 (SERK3) and SERK4 and relays the signaling through the cytosolic receptor-like kinases BOTRYTIS-INDUCED KINASE 1 (BIK1) and AVRPPHB SUSCEPTIBLE1 (PBS1)-LIKE 1 (PBL1). Our study identifies a plant receptor that bears a dual role in sensing the conserved peptide motif from phytocytokines and microbial proteins via a convergent signaling relay to ensure a robust immune response. Peptide signals generated during plant microbe interactions can trigger immune responses in plants. Here the authors show that SCOOP12, a member of a family of peptides present in Brassicaceae plants, and SCOOP12-like motifs in Fusarium fungi, can trigger immune responses following perception by the MIK2 receptor kinase.
37 citations
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TL;DR: In this article, the importance of indigenous microbial communities in improving plant health under pathogen-induced stress is highlighted and potential solutions leading towards commercialization of proficient bioformulations for sustainable and improved crop production are also described.
Abstract: Plants host diverse but taxonomically structured communities of microorganisms, called microbiome, which colonize various parts of host plants. Plant-associated microbial communities have been shown to confer multiple beneficial advantages to their host plants, such as nutrient acquisition, growth promotion, pathogen resistance, and environmental stress tolerance. Systematic studies have provided new insights into the economically and ecologically important microbial communities as hubs of core microbiota and revealed their beneficial impacts on the host plants. Microbiome engineering, which can improve the functional capabilities of native microbial species under challenging agricultural ambiance, is an emerging biotechnological strategy to improve crop yield and resilience against variety of environmental constraints of both biotic and abiotic nature. This review highlights the importance of indigenous microbial communities in improving plant health under pathogen-induced stress. Moreover, the potential solutions leading towards commercialization of proficient bioformulations for sustainable and improved crop production are also described.
23 citations
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TL;DR: In this article , the authors focus on the biological control of plant diseases, aiming to elucidate the contribution and key roles of endophytes and their metabolites in this field with the latest research information.
Abstract: Endophytes represent a ubiquitous and magical world in plants. Almost all plant species studied by different researchers have been found to harbor one or more endophytes, which protect host plants from pathogen invasion and from adverse environmental conditions. They produce various metabolites that can directly inhibit the growth of pathogens and even promote the growth and development of the host plants. In this review, we focus on the biological control of plant diseases, aiming to elucidate the contribution and key roles of endophytes and their metabolites in this field with the latest research information. Metabolites synthesized by endophytes are part of plant disease management, and the application of endophyte metabolites to induce plant resistance is very promising. Furthermore, multi-omics should be more fully utilized in plant–microbe research, especially in mining novel bioactive metabolites. We believe that the utilization of endophytes and their metabolites for plant disease management is a meaningful and promising research direction that can lead to new breakthroughs in the development of more effective and ecosystem-friendly insecticides and fungicides in modern agriculture.
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TL;DR: A spatially explicit dynamic model is presented that separates the effects of microbial mutualists and pathogens, thereby presenting a testable mechanistic framework to reconcile previously puzzling observations of the strength and direction of PSF with diversity maintenance.
Abstract: Empirical studies show that plant-soil feedbacks (PSF) can generate negative density dependent (NDD) recruitment capable of maintaining plant community diversity at landscape scales. However, the observation that common plants often exhibit relatively weaker NDD than rare plants at local scales is difficult to reconcile with the maintenance of overall plant diversity. We develop a spatially explicit simulation model that tracks the community dynamics of microbial mutualists, pathogens, and their plant hosts. We find that net PSF effects vary as a function of both host abundance and key microbial traits (e.g., host affinity) in ways that are compatible with both common plants exhibiting relatively weaker local NDD, while promoting overall species diversity. The model generates a series of testable predictions linking key microbial traits and the relative abundance of host species, to the strength and scale of PSF and overall plant community diversity.
17 citations
References
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TL;DR: Evidence that a gene encoding a critical virulence factor was transferred from one species of fungal pathogen to another probably occurred just before 1941, creating a pathogen population with significantly enhanced virulence and leading to the emergence of a new damaging disease of wheat.
Abstract: New diseases of humans, animals and plants emerge regularly. Enhanced virulence on a new host can be facilitated by the acquisition of novel virulence factors. Interspecific gene transfer is known to be a source of such virulence factors in bacterial pathogens (often manifested as pathogenicity islands in the recipient organism) and it has been speculated that interspecific transfer of virulence factors may occur in fungal pathogens. Until now, no direct support has been available for this hypothesis. Here we present evidence that a gene encoding a critical virulence factor was transferred from one species of fungal pathogen to another. This gene transfer probably occurred just before 1941, creating a pathogen population with significantly enhanced virulence and leading to the emergence of a new damaging disease of wheat.
676 citations
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TL;DR: Here, TE-induced variation is viewed from three evolutionary perspectives that are not mutually exclusive and possible coadaptations between elements and their hosts that appear to have evolved to reduce the deleterious effects of new insertions on host fitness are described.
Abstract: A tremendous wealth of data is accumulating on the variety and distribution of transposable elements (TEs) in natural populations. There is little doubt that TEs provide new genetic variation on a scale, and with a degree of sophistication, previously unimagined. There are many examples of mutations and other types of genetic variation associated with the activity of mobile elements. Mutant phenotypes range from subtle changes in tissue specificity to dramatic alterations in the development and organization of tissues and organs. Such changes can occur because of insertions in coding regions, but the more sophisticated TE-mediated changes are more often the result of insertions into 5' flanking regions and introns. Here, TE-induced variation is viewed from three evolutionary perspectives that are not mutually exclusive. First, variation resulting from the intrinsic parasitic nature of TE activity is examined. Second, we describe possible coadaptations between elements and their hosts that appear to have evolved because of selection to reduce the deleterious effects of new insertions on host fitness. Finally, some possible cases are explored in which the capacity of TEs to generate variation has been exploited by their hosts. The number of well documented cases in which element sequences appear to confer useful traits on the host, although small, is growing rapidly.
564 citations
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TL;DR: The genome sequence of the phytopathogenic ascomycete Leptosphaeria maculans is reported and its repertoire of protein effectors is characterized, revealing an unusual bipartite structure that underpins the evolutionary potential of the fungus to adapt rapidly to novel host-derived constraints.
Abstract: Fungi are of primary ecological, biotechnological and economic importance. Many fundamental biological processes that are shared by animals and fungi are studied in fungi due to their experimental tractability. Many fungi are pathogens or mutualists and are model systems to analyse effector genes and their mechanisms of diversification. In this study, we report the genome sequence of the phytopathogenic ascomycete Leptosphaeria maculans and characterize its repertoire of protein effectors. The L. maculans genome has an unusual bipartite structure with alternating distinct guanine and cytosine-equilibrated and adenine and thymine (AT)-rich blocks of homogenous nucleotide composition. The AT-rich blocks comprise one-third of the genome and contain effector genes and families of transposable elements, both of which are affected by repeat-induced point mutation, a fungal-specific genome defence mechanism. This genomic environment for effectors promotes rapid sequence diversification and underpins the evolutionary potential of the fungus to adapt rapidly to novel host-derived constraints.
471 citations
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TL;DR: A group of papers analyzes pathogen genomes to find the roots of virulence, opportunism, and life-style determinants, demonstrating that dynamic repeat-rich genome compartments underpin accelerated gene evolution following host jumps in this pathogen lineage.
Abstract: Many plant pathogens, including those in the lineage of the Irish potato famine organism Phytophthora infestans, evolve by host jumps followed by specialization. However, how host jumps affect genome evolution remains largely unknown. To determine the patterns of sequence variation in the P. infestans lineage, we resequenced six genomes of four sister species. This revealed uneven evolutionary rates across genomes with genes in repeat-rich regions showing higher rates of structural polymorphisms and positive selection. These loci are enriched in genes induced in planta, implicating host adaptation in genome evolution. Unexpectedly, genes involved in epigenetic processes formed another class of rapidly evolving residents of the gene-sparse regions. These results demonstrate that dynamic repeat-rich genome compartments underpin accelerated gene evolution following host jumps in this pathogen lineage.
409 citations
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TL;DR: Key examples from fungal plant pathogen genomics are summarized and evolutionary processes in pathogenic fungi are discussed in the context of molecular evolution, population genomics and agriculture.
Abstract: The fungal kingdom comprises some of the most devastating plant pathogens. Sequencing the genomes of fungal pathogens has shown a remarkable variability in genome size and architecture. Population genomic data enable us to understand the mechanisms and the history of changes in genome size and adaptive evolution in plant pathogens. Although transposable elements predominantly have negative effects on their host, fungal pathogens provide prominent examples of advantageous associations between rapidly evolving transposable elements and virulence genes that cause variation in virulence phenotypes. By providing homogeneous environments at large regional scales, managed ecosystems, such as modern agriculture, can be conducive for the rapid evolution and dispersal of pathogens. In this Review, we summarize key examples from fungal plant pathogen genomics and discuss evolutionary processes in pathogenic fungi in the context of molecular evolution, population genomics and agriculture.
280 citations