Cellulose synthase complexes display distinct dynamic behaviors during xylem transdifferentiation

First author: Yoichiro Watanabe; Affiliations: University of British Columbia (不列颠哥伦比亚大学): Vancouver, Canada

Corresponding author: Shawn D. Mansfield

In plants, plasma membrane-embedded CELLULOSE SYNTHASE (CESA) enzyme complexes deposit cellulose polymers into the developing cell wall. Cellulose synthesis requires two different sets of CESA complexes that are active during cell expansion and secondary cell wall thickening, respectively. Hence, developing xylem cells, which first undergo cell expansion and subsequently deposit thick secondary walls, need to completely reorganize their CESA complexes from primary wall- to secondary wall-specific CESAs. Using live-cell imaging, we analyzed the principles underlying this remodeling. At the onset of secondary wall synthesis, the primary wall CESAs ceased (停止) to be delivered to the plasma membrane and were gradually removed from both the plasma membrane and the Golgi (高尔基体). For a brief transition period, both primary wall- and secondary wall-specific CESAs coexisted in banded domains (带状域) of the plasma membrane where secondary wall synthesis is concentrated. During this transition, primary and secondary wall CESAs displayed discrete (离散的) dynamic behaviors and sensitivities to the inhibitor isoxaben (异恶酰草胺). As secondary wall-specific CESAs were delivered and inserted into the plasma membrane, the primary wall CESAs became concentrated in prevacuolar compartments (前液泡区室) and lytic vacuoles (溶解小泡). This adjustment in localization between the two CESAs was accompanied by concurrent decreased primary wall CESA and increased secondary wall CESA protein abundance. Our data reveal distinct and dynamic subcellular trafficking patterns that underpin the remodeling of the cellulose biosynthetic machinery, resulting in the removal and degradation of the primary wall CESA complex with concurrent production and recycling of the secondary wall CESAs.

在植物中，嵌在质膜上的纤维素合酶CESA复合物将纤维素多聚物沉积到发育的细胞壁中。在细胞扩增和次生细胞壁加厚过程中纤维素的合成需要两组不同的CESA复合物。因此，发育中的木质部细胞，首先会经历细胞扩增，然后加厚细胞壁，这个过程需要从CESA复合物的变化，初生细胞壁特异性CESA转变为次生细胞壁特异性CESA。利用活细胞成像技术，作者研究了该生物学过程潜在的机制。在次生细胞壁合成的起始，初生细胞壁CESA就会停止在质膜中积累，并同时逐步从质膜和高尔基体中移除。在短暂的转变时期，初生细胞壁和次生细胞壁特异性的CESA共存与质膜的带状域，该区域是次生细胞壁合成的主要地点。在转变过程中，初生细胞壁和次生细胞壁CESA会呈现出非连续的动态变化模式，并且对于抑制剂异恶酰草胺十分敏感。当次生细胞壁CESA插入到质膜后，初生细胞壁CESA会在前液泡区室和溶解小泡的富集。这两种CESA在空间位置上的调整伴随着初生细胞壁CESA蛋白的降低和次生细胞壁CESA蛋白的增高。本文的结果揭示了不同的动态亚细胞运输模式，共同构成了纤维素生物合成机制的基础，导致了初生细胞壁CESA复合物的移除和降解以及次生细胞壁的合成和再循环。

通讯：Shawn D. Mansfield (http://profiles.forestry.ubc.ca/person/shawn-mansfield/)

研究方向： 林木生物技术、植物代谢、细胞壁发育、纤维素生物合成、木质素生物合成、蔗糖代谢等。

doi: https://doi.org/10.1073/pnas.1802113115

Journal: PNAS

Published online: 05 June, 2018

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