Multifunctional fungal plant symbionts: new tools to enhance plant growth and productivity (2011)

A number of fungi are known to colonize plant roots but do not cause disease. These include mycorrhizas, binucleate Rhizoctonia spp., Piriformaspora indica, various plant growth-promoting rhizobacteria and, the subject of this commentary, Trichoderma spp. (Shoresh et al., 2010). Many of these organisms have been known for decades as agents that biocontrol plant diseases, but recent studies have demonstrated that they have many other useful attributes. These organisms are very clearly endophytic plant symbionts; this was, only recently, first described for Trichoderma strains (Harman et al., 2004). The first step for any of these microorganisms is for them to colonize roots. In this issue of New Phytologist, Vargas and colleagues (pp. 777–789), together with another recent paper (Vargas et al., 2009), demonstrate that plant-derived sucrose is an important resource and is critical for plant root colonization by Trichoderma virens. A fungal invertase is key to initiation of the mechanisms of root colonization (Vargas et al., 2009). The fungal genome includes a plant-like sucrose transporter: the specific sucrose/H2 symporter is induced during the early stages of root colonization. Furthermore, the results suggested the presence of a sucrose-independent network in the fungal cells that regulates the symbiotic association (Vargas et al., 2010). ‘…results suggested the presence of a sucrose-independent network in the fungal cells that regulates the symbiotic association.’ The next step in establishment of the symbiotic relationship is physical penetration and colonization of the plant roots (Yedidia et al., 1999; Harman et al., 2004; Bae et al., 2011). Typically, the fungi penetrate the outer layers of the epidermis and plant cortex, and establish chemical communication with the plant. An initial result is that the fungi are walled off by the plant, but not killed. A relatively large number of the chemical communicants (effectors/elicitors) released by the fungi are now known; these include small proteins, peptides and other metabolites, including volatile ones. These have been recently reviewed, as has signal transduction in plants (Harman et al., 2004; Lorito et al., 2010; Shoresh et al., 2010). Once the interaction has been initiated, the beneficial responses to plants can last for at least the growing season for an annual plant because the fungi grow and continue to colonize the roots as they, in turn, also grow and increase (Harman, 2000). The signalling induces systemic effects in plants, so that while only roots are typically colonized, the effects also occur in leaves and in stems. The proteome and transcriptome of plants change as a consequence of the interaction of Trichoderma metabolites (Marra et al., 2006) or plant colonization (Alfano et al., 2007; Segarra et al., 2007; Shoresh & Harman, 2008; Bae et al., 2011). Thus, the fungi reprogramme plant gene expression, resulting in alteration of plant responses to their environment. A list of the benefits conferred follow, but it must be emphasized that only highly effective strains selected will be efficient. With these, the addition of even a small amount as a seed treatment (c. 500 mg of concentrated formulation per hectare) confers significant advantages on a wide variety of crops, including both monocots and dicots. The following advantages are conferred (see Fig. 1). Diagram of the overall effects of Trichoderma strains, and of other root-colonizing plant symbiotic microbes on plants and plant productivity. A somewhat similar diagram has been published previously (Shoresh et al., 2010). LRR, leucine-rich-repeat; MAPK, mitogen-activated protein kinase; MW, molecular weight; P. indica, Piriformaspora indica. Increased plant growth, especially of roots, and especially under stress (Harman, 2000; Shoresh et al., 2010). Systemic resistance to diseases, at least in part through processes other than standard induced systemic resistance and systemic acquired resistance; both jasmonate and salicylate signalling may be involved (Lorito et al., 2010; Bae et al., 2011). Systemic resistance to plant stresses, including water deficit (drought), salt and temperature (Mastouri et al., 2010; Shoresh et al., 2010). Enhancement of the vigor of poor-quality seeds (Mastouri et al., 2010; Shoresh et al., 2010). Improved nitrogen use efficiency (NUE) by plants (Harman & Mastouri, 2010; Shoresh et al., 2010). All of these plant responses require energy, although energy requirements may be reduced by the phenomenon of priming, in which response systems are activated, but gene expression does not occur until the pathogen or stress is present (van Loon et al., 1998). However, with some strains there is constant expression of resistance factors (Shoresh & Harman, 2008). Logically, the only way that all of the plant advantages just noted can occur is if the plant energy pool increases through enhanced photosynthetic capabilities. Trichoderma strains increase photosynthetic rates/efficiency in plants whose roots are measured by several different parameters (Vargas et al., 2009; Mastouri, 2010; Shoresh et al., 2010). Clearly, plants are induced to operate more efficiently and to be better able to resist biotic and abiotic stresses if their roots are colonized by highly effective Trichoderma strains. At least part of the stress resistance, and probably the increased photosynthetic efficiency, is because the fungi improve the redox status of the plant. When plants are under stress, the content of reactive oxygen species may increase to toxic concentrations. Several pathways in plants convert oxidized glutathione and ascorbate to the reduced form (Mittler, 2002) and Trichoderma strains enhance the activity of these pathways, in part by enhanced expression of genes encoding the component enzymes (Mastouri, 2010; Mastouri et al., 2010). Enhancement of these pathways in chloroplasts would logically be expected to increase photosynthetic efficiency by reducing damage by the superoxide anion and other reactive species involved in photosynthesis. The ability of the strains to induce NUE is important. Only a small proportion of the nitrogen fertilizers applied to plants is actually taken up; the remainder leaches into water, causing pollution and eutrophication, including the development of ‘dead zones’ in bays and at the mouth of rivers. In addition, nitrous oxide is released from soils by microbial action, and is an important greenhouse gas. Data obtained from commercial and academic field trials with several monocots indicate that the amount of nitrogen fertilizer applied can be reduced by 40–50% in the presence of Trichoderma, with no reduction in yield. This attribute may be even more important to ensure an adequate supply of food in developing countries (see Fig. 2 for an example), where the costs of fertilizers (as well as of irrigation and pest-control products) are too expensive, especially for smallholders. Several different economic models are being used to provide effective strains and formulations for these growers. A considerable advantage of Trichoderma spp. is that benefits can be obtained across a wide variety of crops without extensive modification of varieties. White maize crop at the end of the season in the Democratic Republic of the Congo from seeds treated with the beneficial fungi (right) or without treatment (left). Plants were more robust and greener, probably largely as a result of enhanced nitrogen use efficiency (NUE). High-quality strains and products were produced in the USA and provided through a faith-based nongovernmental organization (NGO). The formulated products are cheaper than other inputs such as nitrogen fertilizer. It also is remarkable that qualitatively similar effects are induced in plants by a variety of plant-associated root-colonizing microbes, including plant growth-promoting rhizobacteria, P. indica and mycorrhizal fungi, as summarized in Shoresh et al. (2010). This is, apparently, an example of convergent evolution by very dissimilar organisms. Presumably, the ability of these microbes to induce changes in plants, resulting in a large number of healthy roots in which they live, provides a competitive advantage.