528 Scientia Agricola http://dx.doi.org/10.1590/0103-9016-2014-0195 Review Exploring interactions of plant microbiomes Fernando Dini Andreote*, Thiago Gumiere, Ademir Durrer University of São Paulo/ESALQ – Dept. of Soil Science, C.P. ABSTRACT: A plethora of microbial cells is present in every gram of soil, and microbes are found 09 – 13418-900 – Piracicaba, SP – Brazil. extensively in plant and animal tissues. The mechanisms governed by microorganisms in the *Corresponding author <[email protected]> regulation of physiological processes of their hosts have been extensively studied in the light of recent findings on microbiomes. In plants, the components of these microbiomes may form Edited by: Paulo Cesar Sentelhas distinct communities, such as those inhabiting the plant rhizosphere, the endosphere and the phyllosphere. In each of these niches, the “microbial tissue” is established by, and responds to, specific selective pressures. Although there is no clear picture of the overall role of the plant mi- crobiome, there is substantial evidence that these communities are involved in disease control, enhance nutrient acquisition, and affect stress tolerance. In this review, we first summarize fea- tures of microbial communities that compose the plant microbiome and further present a series of studies describing the underpinning factors that shape the phylogenetic and functional plant- associated communities. We advocate the idea that understanding the mechanisms by which plants select and interact with their microbiomes may have a direct effect on plant development and health, and further lead to the establishment of novel microbiome-driven strategies, that can Received May 30, 2014 cope with the development of a more sustainable agriculture. Accepted July 22, 2014 Keywords: microbial communities, rhizosphere, endophytes, phyllosphere Introduction space in our body” (Lederberg and McCray, 2001). Hence, the human body is a great reservoir of microbes, recent- Surveys performed on interactions between plants ly broadly studied by the Human Microbiome project, and microbes are numerous, and have traditionally fo- which linked several features of the host to the presence cused on pathogenic interactions. However, after several of specific sets of microbial groups (Turnbaugh et al., descriptions and attempts to assess the occurrence and 2006; Djikeng et al., 2011; The Human Microbiome Proj- the role of microbial diversity associated with plants, ect Consortium, 2012). More recently, the use of this term it is assumed that only a minor fraction of plant-inter- has been broadly applied to different sets of microbes acting microbes are pathogenic. Most microbes inhabit- found in specific hosts or inhabiting a given environment ing plant-related niches have neutral or beneficial roles (Boon et al., 2014; Ofek et al., 2014). Boon et al. (2014) in plant health and development (Beattie and Lindow, proposed that the best definition of ‘microbiome’ would 1995; Hallmann et al., 1997; Mendes et al., 2013; Philip- relate to the set of genes encountered in association with pot et al., 2013). the host or a defined environment, thus diminishing the Microorganisms can affect agricultural produc- importance of the link between taxonomy and functional- tivity, for instance by assisting and controlling nutrient ity of the microbial community members. These assump- availability/acquisition and promoting stress tolerance tions made feasible the application of the microbiome (Doornbos et al., 2011; Ferrara et al., 2012; Kavamura concept to plants, which carry out several essential func- et al., 2013). Most of the research on this topic has fo- tions in association with distinct microbial groups. Some cused on the functional roles of single microbial groups authors have addressed this issue, such as Bulgarelli et al. (e.g., specific species or organisms from the same genera) (2013), Turner et al. (2013a) and Rout (2014). associated with plants, mostly because of methodologi- In this review article, we focus on the description cal limitations to assess non-culturable microbial groups of plant microbiomes by not only describing the compart- (Amann et al., 1995; Andreote et al., 2009). Examples of ments where the microbes live (rhizosphere, endosphere these inferences are related to specific microbial groups and phyllosphere) but by also discussing the importance able to promote plant growth, such as nitrogen-fixing of interactions between plants and microorganisms. Due bacteria (Raymond et al., 2004) and mycorrhiza-forming to the availability of data, most examples focus on bacte- fungi (Chagnon et al., 2013). However, a holistic view rial fractions of the microbiome or the bacteriome. How- of this system highlights the importance of interactions ever, data and discussions on fungal communities are occurring amongst distinct microbial groups, resulting in also presented. This review was organized to offer an the coining of the term ‘microbiome’. overview of the plant-associated microbial communities, The word ‘microbiome’ was first used by Joshua followed by a description of the role played by plant mi- Lederberg as the “ecological community of commensal mi- crobiomes, and finally a portrayal of microbiome-related croorganisms, symbionts or pathogens, that literally occupy a initiatives underway in Brazil. Sci. Agric. v.71, n.6, p.528-539, November/December 2014 529 Scientia Agricola Plant-associated microbial communities The soil matrix is the major reservoir of microbes that interact with plants, being described as the most bio- diverse ecosystem on Earth (Vogel et al., 2009). The soil microbiome is responsible for important processes occur- ring in this environment, which directly relate to plant health. For instance, the soil microbiome suppresses plant diseases by imposing physiological restrictions on patho- gens establishing and infecting plant tissues (Weller et al., 2002; Mendes et al., 2011). Equally, the soil microbiome also imparts a certain degree of resistance to the system against “invaders”, thereby linking the diversity of the mi- crobiome to its intrinsic ability to restrict or inhibit the survival of exogenous organisms (Elsas et al., 2012). Although the presence of microbes in plants ini- tially related to the occurrence of diseases, it is now rec- ognized that the vast majority of microbial organisms are not causal agents of damage in plants (Mendes et al., Figure 1 − Schematic representation of the major sources for 2013). Several functions have been attributed to micro- microbes that compose the plant-associated communities: the bial cells in close association with plants, for instance, rhizosphere, endosphere and phyllosphere. Thickness and fill of their ability to provide nutrients, such as (i) phosphorus connections indicate the contribution of environmental sources solubilization and nitrogen fixation; (ii) their support of for the composition of microbial communities in plant-harboring nutrient uptake from the soil, as described for the mycor- niches. rhiza; and (iii) their capacity to promote plant protection by hindering agents of plant stresses, such as infection by pathogens and pests (Halmann et al., 1997; Mendes sphere is composed of those organisms that intimately et al., 2011; Mendes et al., 2013; Quecine et al., 2014). interact with the host and inhabit inner plant tissues as- Despite the substantial progress allowed by culti- ymptomatically (Hallmann et al., 1997; Hardoim et al., vation-dependent methods, due to “the great plate count 2008), and the phyllosphere is defined by microbial cells anomaly,” only a small fraction of the microbes in nature that are able to colonize plant surfaces (Lambais et al., (ca. 1 to 5 %) are represented by standard cultivation 2006; Lindow and Brandl, 2003). methods for communities retrieved from natural envi- The richness of species and diversity of microbial ronments (Amann et al., 1995). Hence, an exploration communities that comprise the plant microbiome, as of plant microbiomes that encompasses the whole set well as the factors affecting it and their performance, are of microorganisms interacting with plants might lead to mostly unknown. It is likely that one single plant species the description of numerous other functions that the as- has thousands of epiphytic and endophytic microbial sociated “microbial tissue” exerts when interacting with species, and the interactions between these microorgan- the host plant. Some authors claim that a co-evolution isms might regulate several physiological processes in process occurs between plants and its associated micro- the host. In combination with these factors, the influ- biome, resulting in a strong genomic interdependency, ence of abiotic drivers, such as soil characteristics or the leading to the “metaorganism” concept (Bosch and Mc- edaphoclimatic area where the plant is cultivated, may Fall-Ngai, 2011). play a role. In the following discussion, we character- Considering the microbiome as an active compo- ize each of these “microbial compartments” and provide nent of the host, being also responsive to changes in en- examples of studies addressing the functional roles of vironmental (biotic and abiotic) conditions, is important these communities in plant health and development. to a better understanding of the most important drivers of the composition of plant microbiomes. In order to un- Plant selection for the rhizosphere microbial com- derstand the factors that influence this assembly and the munities dynamics from a phylogenetic