The plant microbiome explored: implications for experimental botany

Abstract

The importance of microbial root inhabitants for plant growth and health was recognized as early as 100 years ago. Recent insights reveal a close symbiotic relationship between plants and their associated microorganisms, and high structural and functional diversity within plant microbiomes. Plants provide microbial communities with specific habitats, which can be broadly categorized as the rhizosphere, phyllosphere, and endosphere. Plant-associated microbes interact with their host in essential functional contexts. They can stimulate germination and growth, help plants fend off disease, promote stress resistance, and influence plant fitness. Therefore, plants have to be considered as metaorganisms within which the associated microbes usually outnumber the cells belonging to the plant host. The structure of the plant microbiome is determined by biotic and abiotic factors but follows ecological rules. Metaorganisms are co-evolved species assemblages. The metabolism and morphology of plants and their microbiota are intensively connected with each other, and the interplay of both maintains the functioning and fitness of the holobiont. Our study of the current literature shows that analysis of plant microbiome data has brought about a paradigm shift in our understanding of the diverse structure and functioning of the plant microbiome with respect to the following: (i) the high interplay of bacteria, archaea, fungi, and protists; (ii) the high specificity even at cultivar level; (iii) the vertical transmission of core microbiomes; (iv) the extraordinary function of endophytes; and (v) several unexpected functions and metabolic interactions. The plant microbiome should be recognized as an additional factor in experimental botany and breeding strategies.

Keywords: Endosphere; holobiont; microbiome; phyllosphere; plant-microbe interaction; rhizosphere..

Fig. 1

The plant as a natural metaorganism visualized by fluorescence in situ hybridization (A-C) and confocal laser scanning microscopy. (A) Phyllosphere of a Sphagnum leave, (B) bacteria on pumpkin pollen, (C) bacteria in the rhizosphere of lettuce, and (D) root of an oilseed rape inoculated with the DsRed-labelled biocontrol agent Pseudomonas trivialis 3Re2-7.

Fig. 2

Taxonomic composition and Venn diagrams of the 16S rRNA and nifH gene communities inhabiting the rhizosphere of medicinal plants (German chamomile [Matricaria chamomilla L.] and African nightshade [Solanum distichum Schumach. and Thonn.]). Both plants were cultivated in direct proximity to each other under field conditions (loamy sand soil) and were investigated in four independent replicate samples by amplicon sequencing. Singletons, operational taxonomic units defined by only a single observation, were removed and not considered in either dataset.

Fig. 3

Controversial Paenibacillus–plant interaction depends on the plant growth conditions. The images to the left show how the interaction with Paenibacillus spp. may improve plant health when plants are grown in soil, while the images on the right side illustrate the destructive behaviour of Paenibacillus spp. in soil-free conditions. (A) The Paenibacillus–plant interaction in non-sterile soil where the growth of pathogens is reduced by the secondary metabolites produced by the Paenibacillus spp.; the access of pathogens to the plant root cells is blocked by the biofilm produced by Paenibacillus spp. (B) Illustration of plant growth promotion (PGP) by secondary metabolites produced by Paenibacillus spp. in the absence of other bacteria when plants are grown in sterile soil. (C) Possible scenarios of how Paenibacillus spp. can damage plant cells by local overproduction of toxic secondary metabolites (e.g. nonribosomal peptides [NRPs] and polyketides [PKs]). Stunting of the root system and inhibition of plant growth may also result from degradation of the plant root cells by Paenibacillus spp. in the absence of other competing microorganisms and a low nutrient environment.

Fig. 4

Model visualizing the interplay within the plant holobiont.