Abstract
Trichoderma spp. are common rhizosphere inhabitants widely used as biological control agents and their role as plant growth promoting fungi has been established. Although soil pH influences several fungal and plant functional traits such as growth and nutrition, little is known about its influence in rhizospheric or mutualistic interactions. The role of pH in the Trichoderma–Arabidopsis interaction was studied by determining primary root growth and lateral root formation, root meristem status and cell viability, quiescent center (QC) integrity, and auxin inducible gene expression. Primary root growth phenotypes in wild type seedlings and STOP1 mutants allowed identification of a putative root pH sensing pathway likely operating in plant–fungus recognition. Acidification by Trichoderma induced auxin redistribution within Arabidopsis columella root cap cells, causing root tip bending and growth inhibition. Root growth stoppage correlated with decreased cell division and with the loss of QC integrity and cell viability, which were reversed by buffering the medium. In addition, stop1, an Arabidopsis mutant sensitive to low pH, was oversensitive to T. atroviride primary root growth repression, providing genetic evidence that a pH root sensing mechanism reprograms root architecture during the interaction. Our results indicate that root sensing of pH mediates the interaction of Trichoderma with plants.
Highlights
Plants are constantly exposed to biotic or abiotic stimuli and adjust their growth and developmental patterns to adapt and survive
We found that in the early stages of the interaction, from 24-to-60 h, primary root growth is unaffected (Figure 1A), and the meristem normally expresses CyCB1:uidA, a marker of mitotic activity, and the quiescent center (QC) marker WOX5:GFP, whose corresponding WT protein is required to maintain the root stem cell niche (SCN) (Figure 1B)
The number of Lateral Root Primordia (LRP) per plant changed slightly at early stages of the interaction (24 and 48 h). Such differences were no longer observed after 60 h (Figure 1D), suggesting that the differences in root branching could be due to an accelerated growth of LRP in response to Trichoderma. This was evidenced by analyzing the LRP developmental stages, where a decrease in the number of LRP still at the early stages of development, those at stages III and IV, and an increase in the number of those more developed and emerged lateral roots (ELR), as early as 24 h of co-cultivation was observed (Figure 1E)
Summary
Plants are constantly exposed to biotic or abiotic stimuli and adjust their growth and developmental patterns to adapt and survive. A complex chemical interaction is established between Trichoderma and their plant hosts comprising volatile and diffusible secondary metabolites, small peptides, and/or antibiotics, which influence root growth, branching and absorptive capacity (Samolski et al, 2012; López-Bucio et al, 2015). Trichoderma-Induced Acidification in Root Growth and Phytostimulation (Contreras-Cornejo et al, 2009), whereas T. atroviride and T. asperellum produce the volatile 6-pentyl-2H-pyran-2-one (6-PP), which modulates plant growth and root system architecture (Kottb et al, 2015; Garnica-Vergara et al, 2016). Trichoderma induces plant defense responses and improves crop performance under different stress conditions (Mastouri et al, 2010, 2012; Contreras-Cornejo et al, 2011, 2014a; Salas-Marina et al, 2011; Rawat et al, 2013; Hashem et al, 2014)
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