Microbial volatiles organic compounds (mVOCs) play diverse roles in modulating plant growth and stress tolerance. However, the molecular responses of plants to mVOCs are largely undescribed. In this study, we examined the early transcriptomic response of Arabidopsis thaliana to two plant growth-promoting mVOCs (PGPVs) and one plant growth-inhibiting mVOC (PGIV). Our phenotype analysis showed that PGPVs from Fusarium verticillioides and Simplicillium sympodiophorum promote plant growth by affecting different organs. In particular, F. verticillioides mVOCs promote plant growth in whole seedlings, while S. sympodiophorum mVOCs increase leaf surface area. Moreover, Arabidopsis treated with the two PGPVs exhibited different growth-associated molecular responses, which corresponded to the phenotype analysis results. For instance, the FAR1 family (regulates light-associated plant development) was upregulated by F. verticillioides mVOCs, while the LBD family (regulates leaf size and shape) was enriched among S. sympodiophorum mVOC-upregulated genes. Hierarchical clustering analysis further indicated that PGPVs induced expression of growth-associated genes and suppressed expression of defense-associated genes. In contrast to the PGPV-induced transcriptional effects, PGIVs caused downregulation of growth-associated genes with coincident upregulation of defense-associated genes. Furthermore, a transcription factor (TF) enrichment analysis suggested that HSFs, NACs and WRKYs might be core regulators in the plant response towards mVOCs. In particular, WRKYs might serve as integrating nodes to regulate salicylic acid- and jasmonic acid-mediated defense responses and growth-defense trade-offs. Overall, this study provides insights into the early molecular responses of plants after mVOC exposure and suggests that these molecular responses contribute to different phenotypic responses.
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