Figure 11.

Overview of the responses observed in Arabidopsis seedlings exposed to Serendipita VOCs or 1500 ppm CO₂ (A) and a tentative model explaining these observations (B). (A) Morphological and physiological changes in roots (supposedly the primary target of rhizofungal VOCs) and shoots upon VOC (purple color) and CO₂ (blue) treatment. The illustration of the Arabidopsis plant is modified from figshare.com. (B) Model summarizing the biological processes that might be affected in VOC-exposed plants, based on our own observations combined with transcriptome/proteome data from other studies (especially García-Gómez et al., 2019). Serendipita VOCs stimulate the photosynthetic reactions (both the light-dependent reactions (e.g., effect on photosystem proteins) and the Calvin Cycle), interfere with hormone signaling pathways, and induce gene expression (see purple markings). The resulting elevated sugar levels, altered hormonal crosstalk, and modified proteome (see asterisks) contribute to plant growth modulation in a direct or indirect way. Augmentation of photosynthetic activity induced by Serendipita VOCs and respiratory CO₂ is associated with a rise in the production of the Calvin cycle intermediate glyceraldehyde 3‐phosphate (GAP). The increase in GAP leads to higher sugar levels and stimulates the accumulation of plastidial MEP pathway-derived isoprenoid compounds, including hormones (e.g., CK, ABA), resulting in changes in the expression of genes involved in many different processes. The impact of elevated CO₂ is especially linked to an enhanced photosynthetic CO₂ fixation through maximization of the carboxylation rates of RuBP by Rubisco. At the same time, the non-productive oxygenation side-reaction in which Rubisco uses O₂ as a substrate to oxygenate RuBP is competitively inhibited, preventing the formation of 2‐phosphoglycollate, which is recycled in the energy-demanding photorespiratory pathway instead of the Calvin cycle (Ainsworth and Rogers, 2007). Feedback inhibition of photosynthesis due to elevated carbohydrate levels via a hexokinase-dependent mechanism of glucose sensing (Rolland et al., 2006) does not occur in the VOC-exposed plants, possibly implicating the downregulation of ABA signal transduction (Zhang et al., 2008b) and increased cytokinin levels (Sánchez-López et al., 2016b). The increased sucrose and cytokinin levels due to volatile treatment induce the expression of anthocyanin biosynthesis genes through the activation of specific transcription factors of the MYB-bHLH-WD40 (MBW) regulatory complexes, exemplifying the intimate interplay between photosynthesis, carbohydrate-phytohormone metabolism/signaling and gene expression. CK, cytokinin; IAA, indole-3-acetic acid; GAP, glyceraldehyde 3‐phosphate; MEP, methylerythritol 4‐phosphate; ROS, reactive oxygen species; RuBP, ribulose-1,5-biphosphate.