Cellulose synthase complexes act in a concerted fashion to synthesize highly aggregated cellulose in secondary cell walls of plants

Abstract

Cellulose, often touted as the most abundant biopolymer on Earth, is a critical component of the plant cell wall and is synthesized by plasma membrane-spanning cellulose synthase (CESA) enzymes, which in plants are organized into rosette-like CESA complexes (CSCs). Plants construct two types of cell walls, primary cell walls (PCWs) and secondary cell walls (SCWs), which differ in composition, structure, and purpose. Cellulose in PCWs and SCWs is chemically identical but has different physical characteristics. During PCW synthesis, multiple dispersed CSCs move along a shared linear track in opposing directions while synthesizing cellulose microfibrils with low aggregation. In contrast, during SCW synthesis, we observed swaths of densely arranged CSCs that moved in the same direction along tracks while synthesizing cellulose microfibrils that became highly aggregated. Our data support a model in which distinct spatiotemporal features of active CSCs during PCW and SCW synthesis contribute to the formation of cellulose with distinct structure and organization in PCWs and SCWs of Arabidopsis thaliana. This study provides a foundation for understanding differences in the formation, structure, and organization of cellulose in PCWs and SCWs.

Two Complementary Mechanisms Underpin Cell Wall Patterning during Xylem Vessel Development

“…For example, the speeds significantly increased during the mid stages of transition ( Figure 2H). These data are very similar to what has independently been reported for the secondary wall CesA7 (Watanabe et al, 2015), but contrast those of Li et al (2016b). Assuming that the speed of the CSCs represents catalytic activity, these findings support a scenario in which an increase in speed of tracking and CesA abundance leads to a major boost in cellulose synthesis, which is compatible with the rapid development and subsequent death of the xylem vessels.…”

“…Assuming that the speed of the CSCs represents catalytic activity, these findings support a scenario in which an increase in speed of tracking and CesA abundance leads to a major boost in cellulose synthesis, which is compatible with the rapid development and subsequent death of the xylem vessels. Li et al (2016b) also studied secondary wall CesA behavior in the VND7-inducible system and concluded that the CSCs moved unidirectionally as "swarms" (referred to as "directionally coherent movement"; Li et al, 2016b) during xylem vessel development. Our data support this report, but it is important to note that the unidirectional movement apparent in CSI1/POM2 was observed both during primary wall synthesis (DMSO treatment; Figure 4) and xylem vessel development and appears to depend on local versus global cell wall synthesis.…”

Secondary cell wall biosynthesis

“…The importance of cortical microtubules in cellulose microfibril deposition was demonstrated by disruption of cortical microtubules by pharmacological drugs or genetic mutations, which results in alterations in the patterned secondary wall thickening, the localized cellulose synthase accumulation and the normal cellulose microfibril deposition (Burk & Ye, 2002;Roberts et al, 2004;Oda et al, 2005;Wightman & Turner, 2008). Imaging of the fluorescence protein-tagged Arabidopsis secondary wall CESA7 revealed that clusters of CESA complexes moved in the same direction along the cortical microtubule tracks in Arabidopsis epidermal cells induced to undergo transdifferentiation into xylem cells, leading to the suggestion that the coalescence of cellulose microfibrils into macrofibrils in secondary walls is attributed to the clustering of CESA complexes (Watanabe et al, 2015;Li et al, 2016). The alignment of CESAs with the underlying cortical microtubules is mediated by CSI1, a cellulose synthase-interactive protein, which was first discovered as a link between primary wall CESAs and cortical microtubules and subsequently shown to be required for the alignment of secondary wall CESAs with cortical microtubules during the early phase of xylem secondary wall thickening (Li et al, 2015;Schneider et al, 2017).…”

KTN80 confers precision to microtubule severing by specific targeting of katanin complexes in plant cells

“…Plant cells establish cortical microtubule (MT) arrays that are independent of centrosomes and closely aligned with the plasma membrane in a two-dimensional layer (Ehrhardt, 2008;Wasteneys & Ambrose, 2009;Shaw, 2013). During cell morphogenesis, plant cortical MTs play a crucial role by providing tracks for cellulose synthase complexes in cellulose biosynthesis (Paredez et al, 2006;McFarlane et al, 2014;Watanabe et al, 2015;Li et al, 2016). Additionally, plant cortical MTs are also thought to act as sensors that respond to developmental and environmental stimuli via their dynamic reorganization (Nick, 2013).…”