Control of Cellulose Synthase Complex Localization in Developing Xylem

Abstract

Cellulose synthesis in the developing xylem vessels of Arabidopsis requires three members of the cellulose synthase (CesA) gene family. In young vessels, these three proteins localize within the cell, whereas in older vessels, all three CesA proteins colocalize with bands of cortical microtubules that mark the sites of secondary cell wall deposition. In the absence of one subunit, however, the remaining two subunits are retained in the cell, demonstrating that all three CesA proteins are required to assemble a functional complex. CesA proteins with altered catalytic activity localize normally, suggesting that cellulose synthase activity is not required for this localization. Cortical microtubule arrays are required continually to maintain normal CesA protein localization. By contrast, actin microfilaments do not colocalize with the CesA proteins and are unlikely to play a direct role in their localization. Green fluorescent protein-tagged CesA reveals a novel process in which the structure and/or local environment of the cellulose synthase complex is altered rapidly.

A Structural Study of CESA1 Catalytic Domain of Arabidopsis Cellulose Synthesis Complex: Evidence for CESA Trimers

“…Since the scattering data showed no indications of oligomer forms beyond a trimer, we can conclude that this domain of ATCESA1 has determinants that contribute to lobe formation, but likely makes no direct contribution to the assembly of lobes into CSCs. Genetic and biochemical studies have shown that in Arabidopsis CESA1, -3, and -6 and CESA4, -7, and -8 isoforms are required for primary and secondary wall cellulose synthesis, respectively (Gardiner et al, 2003;Taylor et al, 2003;Persson et al, 2007). Other CESAs that play roles in tissue-specific processes are partially redundant with CESA6, as described in the introduction (Gardiner et al, 2003;Taylor et al, 2003;Somerville, 2006;Persson et al, 2007).…”

“…Genetic and biochemical studies have shown that in Arabidopsis CESA1, -3, and -6 and CESA4, -7, and -8 isoforms are required for primary and secondary wall cellulose synthesis, respectively (Gardiner et al, 2003;Taylor et al, 2003;Persson et al, 2007). Other CESAs that play roles in tissue-specific processes are partially redundant with CESA6, as described in the introduction (Gardiner et al, 2003;Taylor et al, 2003;Somerville, 2006;Persson et al, 2007). Furthermore, the stoichiometry of the CESA isoforms responsible for primary and secondary cell wall synthesis in Arabidopsis has recently been reported to be 1:1:1 (Gonneau et al, 2014; Hill et al, 2014).…”

“…The different CESA isoforms play specific roles in cellulose synthesis during plant development. In Arabidopsis, CESA1, CESA3, and CESA6 are required for primary cell wall synthesis, while CESA4, CESA7, and CESA8 are required for secondary cell wall synthesis (Gardiner et al, 2003;Taylor et al, 2003;Persson et al, 2007). CESA2, CESA5, and CESA9 play roles in tissue-specific processes and are partially redundant with CESA6, whereas CESA10 is closely related to AtCESA1 but evidently has a minor role in plant development (Somerville, 2006).…”

Disorganization of Cortical Microtubules Stimulates Tangential Expansion and Reduces the Uniformity of Cellulose Microfibril Alignment among Cells in the Root of Arabidopsis

“…A role for microtubules in aligning microfibrils is supported by a substantial body of evidence (Baskin, 2001;Burk and Ye, 2002;Gardiner et al, 2003). Nevertheless, some have argued that the parallelism between microtubules and microfibrils represents a correlated response to an unknown polarizing principle rather than a causal relation (Emons et al, 1992).…”

“…A potent role for selfassembly is reasonable, given that cellulose microfibrils are well ordered even when assembled in vitro (Whitney et al, 1995). In some cells, self-assembly may suffice entirely, for example root hairs with helicoidal cell walls (Emons and Mulder, 1998); whereas in others, microtubule guidance may be paramount, for example in developing xylem, where parallel bands of a cellulose synthase subunit, observed as a green fluorescent protein-fusion, spread out immediately upon oryzalin treatment (Gardiner et al, 2003). However, most cells may lie between these extremes.…”