Plant-Derived Sucrose Is a Key Element in the Symbiotic Association between Trichoderma virens and Maize Plants    

Abstract

Fungal species belonging to the genus Trichoderma colonize the rhizosphere of many plants, resulting in beneficial effects such as increased resistance to pathogens and greater yield and productivity. However, the molecular mechanisms that govern the recognition and association between Trichoderma and their hosts are still largely unknown. In this report, we demonstrate that plant-derived sucrose (Suc) is an important resource provided to Trichoderma cells and is also associated with the control of root colonization. We describe the identification and characterization of an intracellular invertase from Trichoderma virens (TvInv) important for the mechanisms that control the symbiotic association and fungal growth in the presence of Suc. Gene expression studies revealed that the hydrolysis of plant-derived Suc in T. virens is necessary for the up-regulation of Sm1, the Trichodermasecreted elicitor that systemically activates the defense mechanisms in leaves. We determined that as a result of colonization of maize (Zea mays) roots by T. virens, photosynthetic rate increases in leaves and the functional expression of tvinv is crucial for such effect. In agreement, the steady-state levels of mRNA for Rubisco small subunit and the oxygen-evolving enhancer 3-1 were increased in leaves of plants colonized by wild-type T. virens. We conclude that during the symbiosis, the sucrolytic activity in the fungal cells affects the sink activity of roots, directing carbon partitioning toward roots and increasing the rate of photosynthesis in leaves. A discussion of the role of Suc in controlling the fungal proliferation on roots and its pivotal role in the coordination of plant-microbe associations is provided.

Comparative study of Trichoderma gene expression in interactions with tomato plants using high-density oligonucleotide microarrays

“…In our study, strain T87 had detrimental effects on tomato roots, and the plants also had a smaller leaf area and a lower true leaf number than the controls in three independent experiments. These results are in disagreement with previous studies indicating that strain T87 (Gv29-8) promoted Arabidopsis seedling growth through production of auxin-like compounds (Contreras-Cornejo et al, 2009) and induced higher photosynthetic rates and systemic increases in the uptake of CO 2 in leaves (Vargas et al, 2009). Interestingly, 18-mer peptaibols from this strain elicited systemic defences against a leaf pathogen in cucumber (Viterbo et al, 2007) and the T87-secreted elicitor Sm1 systematically stimulated defence mechanisms in maize (Djonovic et al, 2007).…”

“…It has been demonstrated that plant-derived sucrose is an important nutrient source for Trichoderma and is also involved in the control of root colonization (Vargas et al, 2009). However, little is known about the changes influenced by plants in the transcriptome of Trichoderma.…”

Plant-beneficial effects of Trichoderma and of its genes

“…As indicated above, an auxin-like effect has been observed in etiolated pea stems treated with harzianolide and 6-pentyl-a-pyrone, the major secondary metabolites produced by different Trichoderma strains (Vinale et al, 2008). Maize rhizosphere colonization by T. virens also induces higher photosynthetic rates and systemic increases in the uptake of CO 2 in leaves (Vargas et al, 2009). …”

“…Similarly to the situation with mycorrhizae, the highly hydrated polysaccharides of the root-secreted mucigel layer and the mono-and disaccharides excreted by plant roots into the rhizosphere encourage growth of the fungi. It has been observed that plant-derived sucrose is an important resource provided to Trichoderma cells to facilitate root colonization, the coordination of defence mechanisms, and increased rate of leaf photosynthesis (Vargas et al, 2009). Solute transporters such as a di/tripeptide transporter and a permease/intracellular invertase system involved in the acquisition of root exudates have been described in Trichoderma (Vizcaíno et al, 2006;Vargas et al, 2009).…”

Functional analysis of non-ribosomal peptide synthetases (NRPSs) in Trichoderma virens reveals a polyketide synthase (PKS)/NRPS hybrid enzyme involved in the induced systemic resistance response in maize

“…In this facultative/atypical symbiosis, Trichoderma spp. derive nutrients from the plant host and, in return, provide protection against invading root and foliar pathogens and abiotic stresses (Shoresh et al, 2010;Harman et al, 2004;Vargas et al, 2009Vargas et al, , 2011. The ability of Trichoderma spp.…”