J Integr Plant Biol.

• Research Article •    

GhCASPL1 regulates secondary cell wall thickening in cotton fibers by stabilizing the cellulose synthase complex on the plasma membrane

Li Zhang1, Xingpeng Wen1,2,3, Xin Chen4, Yifan Zhou2, Kun Wang2 and Yuxian Zhu1,2,3,4*   

  1. 1. Institute for Advanced Studies, Wuhan University, Wuhan 430072, China
    2. State Key Laboratory of Hybrid Rice, Hubei Hongshan Laboratory, College of Life Sciences, Wuhan University, Wuhan 430072, China
    3. TaiKang Center for Life and Medical Sciences, Wuhan University, Wuhan 430072, China
    4. State Key Laboratory of Protein and Plant Gene Research, College of Life Sciences, Peking University, Beijing 100871, China
    *Correspondence: Yuxian Zhu (zhuyx@whu.edu.cn)
  • Received:2024-02-29 Accepted:2024-08-30 Online:2024-09-24
  • Supported by:
    This work was supported by the grants from STI 2030—Major Project (2023ZD04069), the Natural Science Foundation of China (32388101 and 32200286), Foundation of Hubei Hongshan Laboratory (2021hszd014), Hubei Provincial Natural Science Foundation of China (2021CFA055), and China Postdoctoral Science Foundation (2022TQ0240, 2022M722470).

Abstract: Cotton (Gossypium hirsutum) fibers are elongated single cells that rapidly accumulate cellulose during secondary cell wall (SCW) thickening, which requires cellulose synthase complex (CSC) activity. Here, we describe the CSC-interacting factor CASPARIAN STRIP MEMBRANE DOMAIN-LIKE1 (GhCASPL1), which contributes to SCW thickening by influencing CSC stability on the plasma membrane. GhCASPL1 is preferentially expressed in fiber cells during SCW biosynthesis and encodes a MARVEL domain protein. The ghcaspl1 ghcaspl2 mutant exhibited reduced plant height and produced mature fibers with fewer natural twists, lower tensile strength, and a thinner SCW compared to the wild type. Similarly, the Arabidopsis (Arabidopsis thaliana) caspl1 caspl2 double mutant showed a lower cellulose content and thinner cell walls in the stem vasculature than the wild type but normal plant morphology. Introducing the cotton gene GhCASPL1 successfully restored the reduced cellulose content of the Arabidopsis caspl1 caspl2 mutant. Detergent treatments, ultracentrifugation assays, and enzymatic assays showed that the CSC in the ghcaspl1 ghcaspl2 double mutant showed reduced membrane binding and decreased enzyme activity compared to the wild type. GhCASPL1 binds strongly to phosphatidic acid (PA), which is present in much higher amounts in thickening fiber cells compared to ovules and leaves. Mutating the PA-binding site in GhCASPL1 resulted in the loss of its colocalization with GhCesA8, and it failed to localize to the plasma membrane. PA may alter membrane structure to facilitate protein–protein interactions, suggesting that GhCASPL1 and PA collaboratively stabilize the CSC. Our findings shed light on CASPL functions and the molecular machinery behind SCW biosynthesis in cotton fibers.

Key words: cellulose synthase complex (CSC), cotton fiber, GhCASPL1, plasma membrane (PM), secondary cell wall (SCW)

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