Targeted-metabolome and transcriptome analysis revealed the mechanisms by which jasmonate and flavonoids regulate Ginkgo biloba adaptation to high-dose NaCl stress

Abstract

Ginkgo biloba L. has attracted much attention due to containing important compounds such as flavonoids. Our previous results ensured exogenous methyl jasmonate (MJ) could improve salt tolerance and flavonoid (Fla) synthesis in Ginkgo, while its intrinsic mechanism was still unclear. To elucidate the relationship between jasmonate acid (JA), Fla, and salinity stress, we performed integrated transcriptomic (Tr) and wild-targeted metabolomic (Me) analysis in ginkgo seedlings under MJ (250 μM MJ), Na (150 mM NaCl), Na+MJ (150 mM NaCl+250 μM MJ) treatments. The Na+MJ treatment enhanced the enzyme activities of POD and 4CL, elevated quercetin and total Fla levels, and reduced MDA and H₂O₂ levels compared to the Na treatment. Most of the differential expression genes (DEGs) were up-regulated in antioxidant enzymes (GST, APX), biosynthesis of Fla (FLS, F3’H) and JA (LOX, AOC), and phytohormone signal transduction (transcription factor (TF) family JAZ, MYC2, SAUR, and bHLH related genes) under the MJ or Na+MJ treatment. Na treatment also upregulated some gene (CCR), and SAUR and bHLH genes expressions. Correspondently, 252 differentially accumulated metabolites (DAMs) were enriched in 601 detected metabolites by KEGG analysis. The DAMs involved in flavonoids (isosakuranetin and sakuranetin), JA, and JA-Ile were significantly upregulated in the three treatments, and these changes coincided with the DEGs expressions of FLS, F3’H, JAZ, and MYC2 genes. However, Na treatment downregulated most of the DAMs in fatty acid and polyamine synthesis, and Na+MJ treatment could alleviate the decrease of these DAMs. These results suggest ginkgo seedlings have a degree of salt tolerance via promoting gene expressions and metabolite accumulations in the Fla and JA synthesis pathway. The MJ application enhanced ginkgo’s resistance ability to salinity stress. The JA signaling cascades such as MYC2 and bHLH induce flavonoid synthesis and the latter feedback to stimulate JA synthesis. Spraying MJ could be a sustainable strategy to promote flavonoid biosynthesis and enhance the salinity resistance of ginkgo in saline-alkali soil.