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

Abstract

Volatile compounds (VCs) emitted by phylogenetically diverse microorganisms (including plant pathogens and microbes that do not normally interact mutualistically with plants) promote photosynthesis, growth, and the accumulation of high levels of starch in leaves through cytokinin (CK)-regulated processes. In Arabidopsis (Arabidopsis thaliana) plants not exposed to VCs, plastidic phosphoglucose isomerase (pPGI) acts as an important determinant of photosynthesis and growth, likely as a consequence of its involvement in the synthesis of plastidic CKs in roots. Moreover, this enzyme plays an important role in connecting the CalvinBenson cycle with the starch biosynthetic pathway in leaves. To elucidate the mechanisms involved in the responses of plants to microbial VCs and to investigate the extent of pPGI involvement, we characterized pPGI-null pgi1-2 Arabidopsis plants cultured in the presence or absence of VCs emitted by Alternaria alternata. We found that volatile emissions from this fungal phytopathogen promote growth, photosynthesis, and the accumulation of plastidic CKs in pgi1-2 leaves. Notably, the mesophyll cells of pgi1-2 leaves accumulated exceptionally high levels of starch following VC exposure. Proteomic analyses revealed that VCs promote global changes in the expression of proteins involved in photosynthesis, starch metabolism, and growth that can account for the observed responses in pgi1-2 plants. The overall data show that Arabidopsis plants can respond to VCs emitted by phytopathogenic microorganisms by triggering pPGI-independent mechanisms.

Respiratory CO2 Combined With a Blend of Volatiles Emitted by Endophytic Serendipita Strains Strongly Stimulate Growth of Arabidopsis Implicating Auxin and Cytokinin Signaling

“…In fact, these two phytohormones are emerging as the central regulators in the plant growth-modulating mechanisms of many microbial VOCs. Indeed, by using diverse approaches, including screening Arabidopsis mutants and/or reporter lines and interfering with hormone biosynthesis or transport ( Zhang et al, 2007 ; Ortíz-Castro et al, 2008 ; Bhattacharyya et al, 2015 ; Bitas et al, 2015 ; Garnica-Vergara et al, 2016 ; Sánchez-López et al, 2016a ; Pérez-Flores et al, 2017 ; Li et al, 2018 ) as well as transcriptomics ( Zhang et al, 2007 ; Bhattacharyya et al, 2015 ; Sánchez-López et al, 2016a ) and proteomics ( Kwon et al, 2010 ; Sánchez-López et al, 2016b ), it was shown that mainly auxin and cytokinin production and signaling as well as auxin transport were affected by microbial VOCs, indicating that plants react to these volatiles through highly conserved regulatory mechanisms. Interestingly, plant growth promotion due to physical contact between S. indica and Arabidopsis also appeared to be linked to auxin signaling ( Schäfer et al, 2009 ; Lee et al, 2011 ; Dong et al, 2013 ; Ye et al, 2014 ; Hua et al, 2017 ) and cytokinin perception (through CRE1/AHK2; Vadassery et al, 2008 ).…”

Plastidial Phosphoglucose Isomerase Is an Important Determinant of Seed Yield through Its Involvement in Gibberellin-Mediated Reproductive Development and Storage Reserve Biosynthesis in Arabidopsis

“…We have shown that Arabidopsis mutants impaired in PGI1 accumulate low levels of CKs derived from the MEP pathway, display reduced photosynthetic capacity and slow growth phenotypes, and accumulate low levels of transitory starch in leaves, a phenotype that can be reverted to the wild type by supplementation with exogenous CK (Bahaji et al, 2015). Stimulation of photosynthesis and synthesis of active CK forms is accompanied by enhanced growth and the accumulation of exceptionally high levels of starch in the mesophyll cells of PGI1 null pgi1-2 plants (Sánchez-López et al, 2016). Thus, we have proposed that PGI1 is an important determinant of photosynthesis, transitory starch accumulation, and growth, likely due to its involvement in the synthesis of metabolic intermediates, e.g., GAP and pyruvate, required for the synthesis of plastidial isoprenoid-derived molecules (Bahaji et al, 2015).…”

Unraveling the role of transient starch in the response of Arabidopsis to elevated CO2 under long-day conditions

“…It is widely assumed that this reserve polysaccharide is the end product of a metabolic pathway exclusive to the illuminated chloroplast that involves metabolization of fructose-6phosphate from the Calvin-Benson cycle (CBC) by the stepwise reactions of plastidic phosphoglucose isomerase (PGI1), phosphoglucomutase (PGM1), ADP-glucose pyrophosphorylase (AGP) and starch synthase (SS). Recent studies have provided evidence that, in addition to the CBC-PGI1-PGM1-AGP-SS, Arabidopsis plants possess important alternative/additional starch biosynthetic pathways involving the cytosolic and chloroplastic compartments (Bahaji et al, 2014;2015;Sánchez-López et al, 2016;Baslam et al, 2017). Starch breakdown in leaves requires the coordinated actions of a suite of enzymes including glucan, water dikinase (GWD), phosphoglucan, water dikinase, β-amylases, α-amylases, debranching enzymes and disproportionating enzymes (Streb and Zeeman, 2012;Santelia et al 2015).…”