The plant microbiome

Turner et al. Genome Biology 2013, 14:209 http://genomebiology.com/2013/14/6/209 REVIEW The plant microbiome Thomas R Turner1, Euan K James2 and Philip S Poole1* Abstract Plant genomes contribute to the structure and function of the plant microbiome, a key determinant of plant health and productivity. High-throughput technologies are revealing interactions between these complex communities and their hosts in unprecedented detail. Keywords: Endophyte, microbiome, phyllosphere, rhizosphere Introduction Microbes are fundamental to the maintenance of life on Earth, yet we understand little about the majority of microbes in environments such as soils, oceans, the atmosphere and even those living on and in our own bodies. Culture-based techniques have allowed isolated microbes to be studied in detail, and molecular techniques such as metagenomics are increasingly allowing the identification of microbes in situ. The microbial communities, or microbiomes, of diverse environments have been studied in this way, with the goal of understanding their ecological function [1,2]. The plant microbiome is a key determinant of plant health and productivity [3] and has received substantial attention in recent years [4,5]. A testament to the importance of plant-microbe interactions are the mycorrhizal fungi. Molecular evidence suggests that their associations with green algae were fundamental to the evolution of land plants about 700 million years ago [6]. Most plants, although notably not Arabidopsis thaliana and other Brassicaceae, have maintained this symbiosis, which assists root uptake of mineral nutrients such as phosphate [7]. Plant-associated microbes are also key players in global biogeochemical cycles [8]. A significant amount, 5 to 20%, of the products of photosynthesis (the photosynthate) is released, mainly into the rhizosphere (the *Correspondence: 1 John Innes Centre, Norwich Research Park, Norwich NR4 7UH, UK Full list of author information is available at the end of the article © 2010 BioMed Central Ltd © 2013 BioMed Central Ltd soil-root interface) through roots [9]. In addition, 100 Tg of methanol and 500 Tg of isoprene are released into the atmosphere by plants annually [10,11]. For methanol this corresponds to between 0.016% and 0.14% of photosynthate depending on plant type [10]. Both are potential sources of carbon and energy for microorganisms. In agricultural soils in particular, plants stimulate microbial denitrification and methanogenesis, which contribute to emissions of N2O and methane, respectively [12,13]. These gases represent a loss of carbon and nitrogen from the system and contribute to the greenhouse effect. Manipulation of the plant microbiome has the potential to reduce the incidence of plant disease [14,15], increase agricultural production [16], reduce chemical inputs [17] and reduce emissions of greenhouse gases [18], resulting in more sustainable agricultural practices. This goal is seen as vital for sustaining the world’s growing population. Virtually all tissues of a plant host a microbial community. Here, we focus on the rhizosphere, phyllosphere (plant aerial surfaces) and endosphere (internal tissues). The rhizosphere is a region of rich, largely soilderived, microbial diversity, influenced by deposition of plant mucilage and root exudates [19]. By contrast, the phyllosphere is relatively nutrient poor and subject to extremes of temperature, radiation and moisture [20]. Microbial inhabitants of the rhizosphere and phyllosphere (those near or on plant tissue) are considered epiphytes, whereas microbes residing within plant tissues (the endosphere), whether in leaves, roots or stems, are considered endophytes. Microbes in these niches can establish beneficial, neutral or detrimental associations of varying intimacy with their host plants. Specific interactions between microbes and model plants, such as in Rhizobium-legume symbioses [21], are well understood, but the majority of the plant microbiome, and its contribution to the extended phenotype of the host, is not yet well defined. Importantly, the microbiome is strongly influenced by the plant genome and may be considered as an extension to form a second genome or collectively to form a pan-genome. Approaches for studying the plant microbiome Classic microbiology involves isolating and culturing microbes from an environment using different nutrient media and growth conditions depending on the target Turner et al. Genome Biology 2013, 14:209 http://genomebiology.com/2013/14/6/209 organisms. Although obtaining a pure culture of an organism is required for detailed studies of its genetics and physiology, culture-dependent techniques miss the vast majority of microbial diversity in an environment. Numerous culture-independent, molecular techniques are used in microbial ecology. For studying prokaryotes, PCR amplification of the ubiquitous 16S ribosomal RNA (rRNA) gene is commonly used. Sequencing the variable regions of this gene allows precise (species- and strainlevel) taxonomic identification. The use of high-through put sequencing technologies [22,23] has been widely adopted as they allow identification of thousands to millions of sequences in a sample, revealing the abun dances of even rare microbial species. For studying eukaryotic microbes such as fungi, the equivalent rRNA gene (18S) may not provide sufficient taxonomic discri mination so the hypervariable internally transcribed spacer is often used. A limitation of this is that PCR amplification of genomic DNA is inherently biased by primer design [24,25] and generally only identifies the target organisms. Complex environments are inhabited by organisms from all domains of life. Eukaryotes, including fungi, protozoa, oomycetes and nematodes, are ubiquitous in soils and can be important plant pathogens or symbionts, whereas others are bacterial grazers. The archaea carry out important biochemical reactions, particularly in agricul tural soils, such as ammonia oxidation [26] and methano genesis [13]. Viruses too are abundant and widespread and can affect the metabolism and population dynamics of their hosts [27]. Microbes in a community interact with each other and the host plant [28], so it is important to capture as much of the diversity of a microbiome as possible. To do so requires the use of global analyses such as metagenomics, metatranscriptomics and metaproteo mics, which allow simultaneous assessment and com parison of microbial populations across all domains of life. Metagenomics can reveal the functional potential of a microbiome (the abundance of genes involved in particular metabolic processes), whereas metatranscrip tomics and metaproteomics provide snapshots of community-wide gene expression and protein abundance, respectively. Metatranscriptomics has revealed kingdom-level changes in the structure of crop-plant rhizosphere microbiomes [29]. The relative abundance of eukaryotes in pea and oat rhizospheres was five (...truncated)