The Microbe-Free Plant: Fact or Artifact?

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.

Relationships between phyllosphere bacterial communities and plant functional traits in a neotropical forest

“…Bacteria are also important to their plant hosts. Leaf-associated bacteria represent a widespread and ancient symbiosis (3,4) that can influence host growth and function in many ways, including the production of growth-promoting nutrients and hormones (5,6) and protection of hosts against pathogen infection (7,8). Phyllosphere bacteria have the potential to influence plant biogeography and ecosystem function through their influence on plant performance under different environmental conditions (9)(10)(11), but the drivers of variation in leaf-associated bacterial biodiversity among host plants are not well understood.…”

“…Numerous studies of host-associated microbiomes have shown that microbial biodiversity is a trait (13) that forms part of the extended phenotype of the host organism (4,14,15) with important effects on the health and fitness (16)(17)(18) and evolution (19)(20)(21) of the host. Because of the importance of the microbiome for host fitness and function, there is a growing desire to model and manage hostmicrobiome interactions (22,23), and understanding the drivers of host-associated microbial community assembly has thus become a cornerstone of microbiome research (24).…”

Host and tissue preferences of Enterobacter cloacae and Bacillus amyloliquefaciens for endophytic colonization

“…These organisms secrete proteins and other metabolites called 'effectors' that interfere with plant defenses, allowing them to colonize host plants (Corradi and Bonfante, 2012). Nevertheless, the fact that plant-associated microorganisms are the rule in nature, their multi-faceted interactions can lead to beneficial, neutral or detrimental effects to the host, depending clearly on the environmental status of the surroundings (Partida-Martinez and Heil, 2011). In fact, the recent view of a 'holobiont' (the combination of a host and all its interacting microbial cells) serving as the genetic unit subjected to evolutionary forces (Zilber-Rosenberg and Rosenberg, 2008) brings an alternative theoretical framework for hypothesis-driven research and data interpretation regarding plant-microorganisms association.…”

An evolutionary ecology perspective to address forest pathology challenges of today and tomorrow

“…By comparison, trees are expected to adapt more slowly and to experience a phenotype-environment mismatch (Carroll et al 2014). There is, however, one facet of the tree phenotype that may evolve as quickly as the pathogens: the tree microbiota, which belongs to the extended phenotype of a tree (Dawkins 1999;Whitham et al 2006;Partida-Martínez and Heil 2011). Indeed, virtually, all tissues of trees are colonized by microorganisms (Turner et al 2013).…”