Haodong Huang, Xianpeng Yang, Shiyou Lü and Huayan Zhao
State Key Laboratory of Biocatalysis and Enzyme Engineering, School of Life Sciences, Hubei University, Wuhan, China
College of Life Sciences, Shandong Normal University, Jinan, China
Background: In plants, lipids play key roles as components of cellular membranes and the cuticle (the waxy covering of plant leaves and other organs), and as storage compounds in oil-seed plants. 3-KETOACYL-COA SYNTHASE (KCS) enzymes are classified into two subgroups, with one subgroup displaying fatty acid elongase (FAE) activity and the other lacking enzymatic activity. KCSs with enzymatic activity are components of the FAE complex involved in producing very-long-chain fatty acids with chain length specificity, providing precursors for the synthesis of various lipids, including membrane lipids, surface lipids, and storage lipids. However, the precise function of the non-enzymatic group of KCSs remains to be identified.
Question: Are KCSs lacking canonical FAE activity also involved in lipid synthesis? If so, how do they function?
Findings: Here we report that Arabidopsis KCS3, which was previously shown to lack canonical catalytic activity, functions as a negative regulator of wax metabolism by reducing the enzymatic activity of KCS6, a key KCS involved in wax production. We reveal that the role of KCS3 in regulating KCS6 activity involves physical interactions between KCSs and subunits of the fatty acid elongation (FAE) complex and is essential for maintaining wax homeostasis. We also show that the regulatory role of the KCS3-KCS6 module in wax synthesis is highly conserved across diverse plant taxa from the flowering plant Arabidopsis to the moss Physcomitrium patens.
Next steps: We demonstrated that KCS3 plays a role in regulating wax synthesis, implying that other known KCSs lacking canonical FAE catalytic activity might have similar functions in lipid synthesis. To test this notion, we will examine the roles of additional KCSs lacking FAE activity, seek the possible regulatory targets of these KCSs, and study the interactions of these KCSs with their targets.
Haodong Huang, Xianpeng Yang, Minglü Zheng, Zexi Chen, Zhuo Yang, Pan Wu, Matthew A. Jenks, Guangchao Wang, Tao Feng, Li Liu, Pingfang Yang, Shiyou Lü, Huayan Zhao (2023) An ancestral role for 3-KETOACYL-COA SYNTHASE3 as a negative regulator of plant cuticular wax synthesis. https://doi.org/10.1093/plcell/koad051