Dissecting lncRNA-mRNA networks underlying physiological alterations in Taxodium hybrid ‘Zhongshanshan’ leaves in acclimation to prolonged partial submergence

Long non-coding RNAs (lncRNAs) play essential roles in plant adaptation to various abiotic stresses. However, lncRNAs-mRNA networks underpinning physiological alterations in trees responding to long-term flooding remain unknown. Here, cuttings of Taxodium hybrid ‘Zhongshanshan 703’ (T. mucronatum × T. distichum; T. ‘Zhongshanshan’), which is highly tolerant to flooding, were irrigated to keep the field capacity (C) or partial-submerged (S) for two months. The leaves above (AL) and below (BL) flooding-water surface were separately harvested. In total, 294 and 975 lncRNAs (DELs) as well as 1503 and 6170 mRNAs (DEMs) were significantly differentially expressed in AL and BL of T. ‘Zhongshanshan’ treated with S than those exposed to C, respectively. 493 DELs were predicted to target 517 DEMs through co-location way, and 906 DEMs were identified as putative target genes of 314 DELs through co-expression way. Furthermore, co-expression networks of DELs and DEMs that are closely correlated with the changes in concentrations of organic acids, sugars, amino acids and phytohormones and activities of anaerobic respiratory enzymes and enzymatic antioxidants were established. For instance, the transcript levels of an lncRNA (TCONS_00030503) and its target gene ADH1 which is involved in alcoholic fermentation were elevated in the BL of T. ‘Zhongshanshan’ exposed to S. This is in line with increased ADH activity in BL due to flooding. Moreover, eight hub DELs and five hub DEMs that are related to photosynthesis, starch metabolism, glycolysis, amino acid metabolism and hormone metabolism were identified. Overall, these results suggest that lncRNA-mRNA networks play significant roles in regulating TCA cycle, fermentation, glycolysis, reactive oxygen species detoxification, and metabolism of carbohydrate, alanine and phytohormone in T. ‘Zhongshanshan’ leaves, and these processes play pivotal roles in acclimation to long-term submergence. •It is the first study about lncRNA in woody plants that adapt to flooding stress.•Flooding induced higher numbers of DELs and DEMs in BL than AL.•Co-expression networks were correlated with physiological alterations under flooding.•LncRNA-mRNA networks play pivotal roles in regulating TCA cycle and fermentation.