Unraveling plant–microbe interactions: can multi-species transcriptomics help? Peer M. Schenk 1 , Lilia C. Carvalhais 1 and Kemal Kazan 2 1 School of Agriculture and Food Sciences, The University of Queensland, Brisbane, Queensland 4072, Australia 2 CSIRO Plant Industry, Queensland Bioscience Precinct, St Lucia, Queensland 4067, Australia Plants in their natural habitats are surrounded by a large number of microorganisms. Some microbes directly interact with plants in a mutually beneficial manner whereas others colonize the plant only for their own benefit. In addition, microbes can indirectly affect plants by drastically altering their environments. Understand- ing the complex nature of plant–microbe interactions can potentially offer new strategies to enhance plant productivity in an environmentally friendly manner. As briefly reviewed here, the emerging area of multi-species transcriptomics holds the promise to provide knowledge on how this can be achieved. We discuss key aspects of how transcriptome analysis can be used to provide a more comprehensive picture of the complex interactions of plants with their biotic and abiotic environments. Enhancing plant productivity for future food security Environmental conditions including biotic and abiotic stresses undoubtedly play a major role in limiting plant productivity. For example, virtually all crops can be sig- nificantly affected by diseases with the potential to reduce both yield and quality, if not kill the crop. Disease preven- tion by breeding of resistant cultivars is the most effective [1,2] and an environmentally responsible approach to com- bat diseases as opposed to indiscriminate application of pesticides. Another environmentally friendly approach is to utilize the biotic and abiotic environment of a plant to develop sustainable disease management strategies. How- ever, this latter approach requires a better understanding of how plants and microbes intimately interact with one another in an extremely complex environment and how this interaction leads to physiological changes in plants. Furthermore, knowledge is required of how plants priori- tize their needs, such as investing resources into defense at the expense of growth and development, to develop sus- tainable strategies to improve plant health in agriculture. This perspectives article reviews the potential of multi- species transcriptomics to reveal key processes between plants and microbes that can be exploited for biotechno- logical applications. Specifically, we address the question whether the new knowledge to be gained from transcrip- tome analyses of interactions between plants and/or bene- ficial or detrimental microbes can be exploited in such a way that ultimately leads to the development of crop cultivars that are productive under multiple environmen- tal pressures. Plants and their microbial environment Plants in natural environments establish multiple inter- actions with many different microorganisms throughout their lifetime. Despite their potentially paramount impor- tance for plants, these extremely complex microbial com- munities have remained largely uncharacterized. Indeed, it was recently estimated that so far only 7% of all pre- dicted land fungi have been identified [3]; furthermore, it can be predicted that a significant proportion of these unidentified fungal species interact with plants in one way or another. Investigations into complex microbial communities have largely been hampered by the fact that most microbes are not culturable. Microbes that live in the rhizosphere, which is the soil region influenced by plant roots, are of particular importance because this is where most interactions between plants and microbes occur. Various plant–microbe interactions can be broadly cate- gorized as beneficial, detrimental or neutral (Figure 1). Although the effect that most microbes would have on plants appears to be neutral, these microbes may utilize plant- derived organic compounds as substrates for energy produc- tion, and thus may still play key roles in nutrient cycling and modifying plant environments. Beneficial microbes promote plant growth and/or suppress plant diseases via a variety of mechanisms, which include improved nutrient acquisition, production of growth regulators, and biosynthesis of patho- gen-inhibiting compounds (Box 1). Much rarer, but more noticeable because of their detrimental effects, are plant pathogenic fungi, oomycetes, bacteria and viruses that can cause diseases on plants (Box 1). The potential outcome of these plant–microbe interactions is further influenced by abiotic stress factors such as drought, temperature, salinity, soil acidity and waterlogging [4]. Metatranscriptomics Metatranscriptomics is the exploratory gene expression analysis of complex microbial community assemblages with- out the need for cultivation, using RNA extracted directly from an environmental sample such as water, soil or sludge [5,6]. Although interactions of certain plants with patho- gens, mycorrhizae or distinct plant growth-promoting bac- teria have been relatively well studied, it is likely that an Review Corresponding author: Schenk, P.M. (p.schenk@uq.edu.au). 0167-7799/$ – see front matter ß 2011 Published by Elsevier Ltd. doi:10.1016/j.tibtech.2011.11.002 Trends in Biotechnology, March 2012, Vol. 30, No. 3 177