The microbe-free plant: fact or artifact?

Laila P Partida-Martínez,Martin Heil

doi:10.3389/fpls.2011.00100

Abstract

Plant–microbe interactions are ubiquitous. Plants are threatened by pathogens, but they are even more commonly engaged in neutral or mutualistic interactions with microbes: belowground microbial plant associates are mycorrhizal fungi, Rhizobia, and plant-growth promoting rhizosphere bacteria, aboveground plant parts are colonized by internally living bacteria and fungi (endophytes) and by microbes in the phyllosphere (epiphytes). We emphasize here that a completely microbe-free plant is an exotic exception rather than the biologically relevant rule. The complex interplay of such microbial communities with the host–plant affects multiple vital parameters such as plant nutrition, growth rate, resistance to biotic and abiotic stressors, and plant survival and distribution. The mechanisms involved reach from direct ones such as nutrient acquisition, the production of plant hormones, or direct antibiosis, to indirect ones that are mediated by effects on host resistance genes or via interactions at higher trophic levels. Plant-associated microbes are heterotrophic and cause costs to their host plant, whereas the benefits depend on the current environment. Thus, the outcome of the interaction for the plant host is highly context dependent. We argue that considering the microbe-free plant as the “normal” or control stage significantly impairs research into important phenomena such as (1) phenotypic and epigenetic plasticity, (2) the “normal” ecological outcome of a given interaction, and (3) the evolution of plants. For the future, we suggest cultivation-independent screening methods using direct PCR from plant tissue of more than one fungal and bacterial gene to collect data on the true microbial diversity in wild plants. The patterns found could be correlated to host species and environmental conditions, in order to formulate testable hypotheses on the biological roles of plant endophytes in nature. Experimental approaches should compare different host–endophyte combinations under various relevant environmental conditions and study at the genetic, epigenetic, transcriptional, and physiological level the parameters that cause the interaction to shift along the mutualism–parasitism continuum.

Highlights

Considering the fact that nowadays more than 80% of all terrestrial plants are associated with mycorrhizal fungi it is tempting to state provocatively that an un-mycorrhized plant does not exist, neither nor in the history of land plants
Realizing that it is impossible to assess the net balance of a certain host–microbe interaction for all possible sets of environmental conditions, we suggest that endophytes whose presence under the average conditions causes negative effects on host fitness should be termed “pathogens,”whereas endophytes with generally neutral or positive effects on host fitness represent the “classical” endophytes
Some microorganisms will usually have negative effects on the fitness of their hosts and should be termed pathogens, whereas other microorganisms that colonize the tissue of plants usually have positive effects and represent mutualistic endophytes

Summary

Introduction

The phenotype of most plants in nature is the product of the concerted and highly co-regulated expression of both plant and microbial genes. Mutualistic plant–microbe interactions were originally considered as interesting, but specific, cases, which are of relevance only for some selected species or families. Most plant-infecting microorganisms were considered pathogens with detrimental effects on plant development, in crop plants and much less so in wild plants under natural conditions. Mutualistic fungal endophytes, mycorrhiza, nodulating and other plant-associated N-fixing bacteria, as well as microorganisms in the rhizosphere and phyllosphere (see Glossary). Many of these microorganisms develop within living plant tissue and represent endophytes (see below)

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Conclusion