CsLUX-CsPME6/CsPMEI8/CsPMEI17 modulates pectin methylesterification to coordinate cold tolerance and growth in tea plants

Abstract Cell wall pectin methylesterification is critical for plant defense and development, yet how it coordinately regulates cold tolerance and growth in perennial crops remains unclear. Here, we demonstrate that cold stress significantly reduces the degree of methylesterification (DM) of pectin in tea plants, concurrent with extensive remodeling of cellular and subcellular structures, including enhanced xylem development, altered mesophyll architecture, and impaired chloroplast morphology. Genome-wide analysis identifies 100 pectin methylesterase (PME) and 42 PME inhibitor (PMEI) genes, among which CsPME6, CsPMEI8, and CsPMEI17 exhibit cold-responsive expression and localize to the nucleus and apoplast. Functional studies demonstrate that CsPME6 positively regulates cold tolerance in tea plants, while CsPMEI8 and CsPMEI17 act as negative regulators. Mechanistically, CsPME6 elevates PME activity to lower pectin DM, whereas CsPMEI8 directly inhibit CsPME6 activity to maintain high pectin DM. Also, CsPMEI17 also negatively enhanced total PME activity to enhance the cold tolerance in tea plants. Notably, our findings suggested that the circadian clock component CsLUX directly binds to the LBS motifs in the promoters of these three genes, activating CsPME6 and repressing CsPMEI8/CsPMEI17 expression, which contributes to pectin methylesterification homeostasis. Besides, CsLUX-CsPME6/CsPMEI8/CsPMEI17 module also promote glutamate/γ-aminobutyric acid metabolism, leaf thickness, plant height, and root elongation in tea plants. Our findings underscore the importance of pectin methylesterification dynamics mediated by CsLUX-CsPME/PMEI involving cold tolerance and growth development in tea plants.