Volatile compounds emitted by diverse phytopathogenic microorganisms promote plant growth and flowering through cytokinin action

Abstract

It is known that volatile emissions from some beneficial rhizosphere microorganisms promote plant growth. Here we show that volatile compounds (VCs) emitted by phylogenetically diverse rhizosphere and non-rhizhosphere bacteria and fungi (including plant pathogens and microbes that do not normally interact mutualistically with plants) promote growth and flowering of various plant species, including crops. In Arabidopsis plants exposed to VCs emitted by the phytopathogen Alternaria alternata, changes included enhancement of photosynthesis and accumulation of high levels of cytokinins (CKs) and sugars. Evidence obtained using transgenic Arabidopsis plants with altered CK status show that CKs play essential roles in this phenomenon, because growth and flowering responses to the VCs were reduced in mutants with CK-deficiency (35S:AtCKX1) or low receptor sensitivity (ahk2/3). Further, we demonstrate that the plant responses to fungal VCs are light-dependent. Transcriptomic analyses of Arabidopsis leaves exposed to A. alternata VCs revealed changes in the expression of light- and CK-responsive genes involved in photosynthesis, growth and flowering. Notably, many genes differentially expressed in plants treated with fungal VCs were also differentially expressed in plants exposed to VCs emitted by the plant growth promoting rhizobacterium Bacillus subtilis GB03, suggesting that plants react to microbial VCs through highly conserved regulatory mechanisms.

Arabidopsis Responds to Alternaria alternata Volatiles by Triggering Plastid Phosphoglucose Isomerase-Independent Mechanisms

“…Moreover, pgi1-2 plants exposed to VCs had higher A n values than controls at all C i levels ( Fig. 3B), reaching values that were comparable to those of VC-treated wild-type plants (Sánchez-López et al, 2016). The maximum rate of carboxylation by Rubisco as well as the maximum electron transport demand for ribulose 1,5-bisphosphate regeneration determined from the A n /C i curves were both significantly higher in leaves of VC-treated pgi1-2 plants than in controls, as was triose phosphate use (Table I).…”

“…The transcriptome changes of plants exposed to VCs emitted by phylogenetically distant microbial species, such as A. alternata and the beneficial plant growth-promoting rhizobacterium Bacillus subtilis GB03, were strikingly similar (Sánchez-López et al, 2016), indicating that plants react to microbial VCs through highly conserved regulatory mechanisms. We have proposed that VC-promoted plant growth and metabolic changes prepare the plant to host the microorganism, which, in the case of phytopathogenic microorganisms, ensures proper continuation into the pathogenic phase (Sánchez-López et al, 2016).…”

“…Furthermore, mutants with reduced CK content or sensitivity responded poorly to VCs (Sánchez-López et al, 2016). Because CKs are major determinants of growth, photosynthesis, and starch accumulation in mature leaves (Riefler et al, 2006;Werner et al, 2008;Kieber and Schaller, 2014;Bahaji et al, 2015b), we postulated that a plant's response to VCs involves CK action (Sánchez-López et al, 2016). The transcriptome changes of plants exposed to VCs emitted by phylogenetically distant microbial species, such as A. alternata and the beneficial plant growth-promoting rhizobacterium Bacillus subtilis GB03, were strikingly similar (Sánchez-López et al, 2016), indicating that plants react to microbial VCs through highly conserved regulatory mechanisms.…”

“…When Arabidopsis (Arabidopsis thaliana) plants were exposed to VCs emitted by the fungal phytopathogen Alternaria alternata, growth promotion was accompanied by enhanced intracellular levels of plastid-type, 2-C-methyl-D-erythritol 4-phosphate (MEP) pathway-derived cytokinins (CKs), augmented photosynthesis, and the accumulation of exceptionally high levels of starch in leaves (Ezquer et al, 2010;Li et al, 2011;Sánchez-López et al, 2016). Furthermore, mutants with reduced CK content or sensitivity responded poorly to VCs (Sánchez-López et al, 2016). Because CKs are major determinants of growth, photosynthesis, and starch accumulation in mature leaves (Riefler et al, 2006;Werner et al, 2008;Kieber and Schaller, 2014;Bahaji et al, 2015b), we postulated that a plant's response to VCs involves CK action (Sánchez-López et al, 2016).…”

“…We recently showed that this action is not only restricted to beneficial microorganisms but extends to pathogens and microbes that do not normally interact mutualistically with plants ( Sánchez-López et al, 2016). When Arabidopsis (Arabidopsis thaliana) plants were exposed to VCs emitted by the fungal phytopathogen Alternaria alternata, growth promotion was accompanied by enhanced intracellular levels of plastid-type, 2-C-methyl-D-erythritol 4-phosphate (MEP) pathway-derived cytokinins (CKs), augmented photosynthesis, and the accumulation of exceptionally high levels of starch in leaves (Ezquer et al, 2010;Li et al, 2011;Sánchez-López et al, 2016). Furthermore, mutants with reduced CK content or sensitivity responded poorly to VCs (Sánchez-López et al, 2016).…”