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  • Review Article
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Microbial genome-enabled insights into plant–microorganism interactions

Nature Reviews Genetics volume 15, pages 797–813 (2014)Cite this article

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Key Points

  • Next-generation genomic technology has enabled comparative genomics of pathogen species and populations to be examined at high resolution. These studies have been particularly useful for identifying genes associated with important disease or immunity phenotypes, such as type III secreted effectors (T3SEs) in Gram-negative bacteria, and distinct effector families in oomycetes and fungi.

  • Comparative genomics of bacterial phytopathogens has revealed that although related pathogens may use similar mechanisms to subvert host immunity, they often achieve similar results through distinct evolutionary paths. For example, independent lineages of Pseudomonas syringae seem to use distinct sets of T3SEs to overcome the immune response of a common host.

  • Microbial genomes are incredibly dynamic. Any single isolate may share <50% of its genome with other isolates of the same species, and the pan genome of the species may be as much as 10 times larger than the size of an individual genome.

  • Genome compartmentalization of pathogenicity-related genes in eukaryotic filamentous phytopathogens seems to allow higher rates of evolution for functions that are relevant to host adaptation while leaving the core genome with basal cellular functions 'protected' against excessive mutation rates.

  • Comparative genomics revealed genome adaptations that are associated with distinctive pathogen lifestyles, including diversification and proliferation of gene families that encode enzymes needed for host cell wall degradation and secondary metabolite biosynthesis to produce an arsenal of small molecules, some of which have host cytotoxic activity. Such an adaptation is a common feature of necrotrophic bacteria and fungi. By contrast, a hallmark of obligate biotrophic pathogens, which derive nutrients only from living host cells, is convergent gene losses in metabolic pathways, which is likely to explain why these parasites became obligate.

  • Culture-independent community profiling methods, coupled with metagenomic and metatranscriptomic studies, are beginning to unveil the principles underlying the establishment of plant-associated microbial communities with distinct taxonomic structures. Discovery of the key microbial functionalities in these assemblies, which comprise mutualistic and commensal members, will require the design of statistically informative experiments with large numbers of replicates, the integrated interpretation of multiple omics data types and the establishment of synthetic model communities that can be manipulated in a targeted manner.

Abstract

Advances in genome-based studies on plant-associated microorganisms have transformed our understanding of many plant pathogens and are beginning to greatly widen our knowledge of plant interactions with mutualistic and commensal microorganisms. Pathogenomics has revealed how pathogenic microorganisms adapt to particular hosts, subvert innate immune responses and change host range, as well as how new pathogen species emerge. Similarly, culture-independent community profiling methods, coupled with metagenomic and metatranscriptomic studies, have provided the first insights into the emerging field of research on plant-associated microbial communities. Together, these approaches have the potential to bridge the gap between plant microbial ecology and plant pathology, which have traditionally been two distinct research fields.

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Figure 1: Whole-genome phylogenetic relationships of three P. syringae pv. avellanae strains responsible for hazelnut decline in Greece and Italy.
Figure 2: Evolutionary and recombination mechanisms driving diversity in effector gene repertoires.

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Change history

  • 03 November 2014

    In the original version of this article, the middle initial of David S. Guttman was omitted. This has been corrected.

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Acknowledgements

The authors thank S. Hacquard in P.S-L's laboratory for the genome comparison underlying the heat map representation embedded in Box 2 and J. Vorholt for comments. We apologize to colleagues whose work could not be cited owing to length considerations. This work was supported by funds to P.S.-L. from the Max Planck Society and a European Research Council advanced grant (ROOTMICROBIOTA).

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Author notes

  1. David S. Guttman, Alice C. McHardy and Paul Schulze-Lefert: All authors contributed equally to this work.

Authors and Affiliations

  1. Center for the Analysis of Genome Evolution and Function, University of Toronto, 25 Willcocks Street, Toronto, M5S3B2, Ontario, Canada

    David S. Guttman

  2. Department for Algorithmic Bioinformatics, Heinrich Heine University Düsseldorf, Universitätsstrasse 1, Düsseldorf, 40225, Germany

    Alice C. McHardy

  3. Cluster of Excellence on Plant Sciences (CEPLAS),

    Alice C. McHardy & Paul Schulze-Lefert

  4. Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, Carl-von-Linné-Weg 10, Köln, D-50829, Germany

    Paul Schulze-Lefert

Authors
  1. David S. Guttman
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Corresponding author

Correspondence to Paul Schulze-Lefert.

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Glossary

Pathogen effector

Any microbial secreted molecule providing a fitness benefit to the pathogen during host colonization, such as by suppressing the host immune system, by extracting nutrients from the host or even by suppressing the growth of microbial competitors in the host environment. Effectors are proteins or secondary metabolites and act in the plant apoplast or inside host cells.

Nucleotide-binding domain and LLR-containing protein

(NLR). 'Resistance proteins' that monitor or guard host proteins that are targeted by pathogen effector proteins. NLRs induce an effector-triggered immunity defence response upon perceiving an effector-mediated modification to the host target protein.

Type III secreted effectors

(T3SEs). Bacterial proteins secreted and translocated directly into the host cell by the bacterial type III secretion system. T3SEs are highly variable (with respect to both presence/absence polymorphisms and nucleotide polymorphisms) among strains of bacteria. Although the specific molecular function of most T3SEs is still unknown, most act to suppress various aspects of plant immunity.

Oomycetes

A distinct phylogenetic lineage of fungus-like (filamentous) eukaryotic microorganisms that can reproduce both sexually and asexually. They are closely related to photosynthetic organisms such as brown algae and diatoms.

Virulence

A pathogen–host interaction in which the pathogen causes disease in the host.

Avirulence

A pathogen–host interaction in which the pathogen inadvertently elicits the host immune system through the action of one or more of its effectors.

Effector-triggered immunity

(ETI). An immune response induced by the recognition of pathogen effector activity by a host nucleotide-binding domain and leucine-rich repeat-containing protein (NLR). The ETI response includes the fortification of the plant cell wall, the generation of reactive oxygen species, the induction of pathogenesis-related proteins and a hypersensitive response.

Co-evolutionary arms race

Iterative, antagonistic cycles of evolution between pathogen, parasite or predator and host or prey, in which one continually drives the evolution of the other to better their chances of surviving or benefitting from the interaction. In the context of phytopathogens, the arms race often manifests in the evolution of new pathogen effectors and host nucleotide-binding domain and leucine-rich repeat-containing proteins (NLRs), which recognize and/or respond to the effectors.

Mutualistic

Pertaining to a mutually beneficial relationship between two organisms.

Commensal

Pertaining to a relationship between two organisms in which one organism benefits without affecting the other.

Microbiota

All microorganisms of a particular habitat.

Avirulence genes

(AVRs). Genes that encode a pathogen effector that is recognized by a host resistance nucleotide-binding domain and leucine-rich repeat-containing protein (NLR). AVR proteins are present in an isolate-specific manner and, together with the cognate NLRs, are the main drivers of the host–pathogen arms race.

Gene-for-gene model

A model of pathogen–host or parasite–host interactions, in which each specific pathogen avirulence factor (that is, effector) interacts with a specific cognate host resistance factor (that is, nucleotide-binding domain and leucine-rich repeat-containing protein (NLR)). The specific combination of avirulence and resistance factors carried by the pathogen and the host, respectively, will determine whether the interaction is compatible (virulent) or incompatible (avirulent). The model was originally developed by Flor in the 1940s to describe rust–flax interactions and was the guiding framework for plant–microorganism interactions for many years.

Hypersensitive response

A programmed cell death response of the host tissue surrounding the site of pathogen infection. It is a component of the overall effector-triggered immunity defence response and is usually induced by pathogen effector activity perceived by nucleotide-binding domain and leucine-rich repeat-containing proteins (NLRs).

Core genome

The set of genes shared by all members of a group of strains being examined. It is an operational definition that changes depending on the set of strains being examined, so the core genome of an entire bacterial species will be smaller than the core genome of a specific lineage of strains. Mathematically, the core genome is the intersection set of the genomes from the strains under study.

Positive selection

Selection that increases the frequency of a beneficial mutation. Positive selection is typically identified by looking for polymorphisms that cause an amino acid substitution with a frequency that is higher than expected.

Paralogues

Homologous genes related through a gene duplication event. They are commonly assumed to diverge in function through neofunctionalization or subfunctionalization.

Homologous

Pertaining to genes related through a common ancestry.

Horizontal gene transfer

(HGT). The movement of genetic material between strains or species through various non-sexual means, as opposed to mother-to-daughter transfer of genetic material. HGT is an important source of genetic novelty in microorganisms.

Parasexual

Pertaining to recombination of DNA that does not involve meiosis. Examples include the fusion of nuclei within a fungal heterokaryon or bacterial conjugation.

Rhizosphere

The region of soil surrounding plant roots in which the chemistry and microbiology are influenced by the roots' growth, respiration and nutrient exchange.

Pan genome

The entire set of genes carried by a group of strains being examined (that is, essentially the total gene pool). Mathematically, the pan genome is the union set of the genomes from the strains under study.

Linkage

Non-independent evolution between two or more loci in a genome due to restricted recombination.

Sympatry

The phenomenon whereby two species or populations exist in the same geographical area and regularly encounter one another.

Endosphere

The microbial habitat inside plant organs.

Phyllosphere

The microbial habitat defined by the surface of aboveground plant organs (mainly leaves).

Microbiome

The collection of the genomes of the microorganisms in a particular habitat.

Operational taxonomic units

(OTUs). A proxy for a microbial taxon defined on the basis of sequence divergence of 'universal' marker genes, such as ribosomal RNA genes.

Methanotrophy

A lifestyle of methane utilization in methylotroph species.

Facultative methylotrophs

Microorganisms that are able to use multicarbon sources in addition to reduced one-carbon substrates, such as methanol or methane.

Neofunctionalization

The acquisition of a new function by one member of a duplicated gene family.

Subfunctionalization

The partitioning of an ancestral function among multiple members of a duplicated gene family. For example, assume the product of an ancestral gene functioned in all plant tissues. If this gene duplicated, one member of the new gene family may now subfunctionalize to only function in root tissues, while another member of the family may subfunctionalize to only function in leaf tissues.

Xenologues

Homologous genes transferred between strains through horizontal gene transfer.

Incomplete lineage sorting

The phenomenon whereby an ancestral species undergoes several speciation events in a short period of time. It is the expected consequence of natural genetic diversity from an ancestral population that sorted itself incompletely into different descendant species.

Genome-wide association studies

(GWASs). Statistical genetic approaches to identify genetic variants that influence traits of interest. This method identifies statistical associations between genetic variants that are segregating in a population under study with phenotypes of interest.

Orthologous genes

Homologous genes related through a speciation event. They are commonly assumed to share a similar function.

Gnotobiotic

Pertaining to a germ-free plant or animal.

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Guttman, D., McHardy, A. & Schulze-Lefert, P. Microbial genome-enabled insights into plant–microorganism interactions. Nat Rev Genet 15, 797–813 (2014). https://doi.org/10.1038/nrg3748

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