Cellulose synthase complexes display distinct dynamic behaviors during xylem transdifferentiation

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 115; no. 27; pp. E6366 - E6374
• Main Authors: Watanabe, Yoichiro, Schneider, Rene, Barkwill, Sarah, Gonzales-Vigil, Eliana, Hill, Joseph L., Samuels, A. Lacey, Persson, Staffan, Mansfield, Shawn D.
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 03.07.2018; Proceedings of the National Academy of Sciences
• Series: From the Cover
• Subjects: Arabidopsis - enzymology; Arabidopsis - genetics; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; BASIC BIOLOGICAL SCIENCES; bio-inspired; biofuels (including algae and biomass); Biological Sciences; carbon sequestration; Cell Transdifferentiation - physiology; Cell walls; Cellulase; Cellulose; cellulose biosynthesis; Cellulose synthase; CesA protein; Chemical synthesis; Domains; Glucosyltransferases - genetics; Glucosyltransferases - metabolism; Golgi apparatus; Isoxaben; Localization; materials and chemistry by design; membrane; Membranes; Plant growth; PNAS Plus; Polymers; primary cell wall; Proteins; secondary cell wall; synthesis (self-assembly); Thickening; Vacuoles; Xylem; Xylem - enzymology; Xylem - genetics; xylem transdifferentiation; xylem transdifferentiation; secondary cell wall; cellulose; primary cell wall; cellulose biosynthesis
• ISSN: 0027-8424; 1091-6490; 1091-6490
• DOI: 10.1073/pnas.1802113115

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 to be delivered to the plasma membrane and were gradually removed from both the plasma membrane and the Golgi. For a brief transition period, both primary wall- and secondary wall-specific CESAs coexisted in banded domains of the plasma membrane where secondary wall synthesis is concentrated. During this transition, primary and secondary wall CESAs displayed discrete dynamic behaviors and sensitivities to the inhibitor isoxaben. As secondary wall-specific CESAs were delivered and inserted into the plasma membrane, the primary wall CESAs became concentrated in prevacuolar compartments and lytic vacuoles. 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.