TRM4 is essential for cellulose deposition in Arabidopsis seed mucilage by maintaining cortical microtubule organization and interacting with CESA3

Abstract

Summary The differentiation of the seed coat epidermal ( SCE ) cells in Arabidopsis thaliana leads to the production of a large amount of pectin‐rich mucilage and a thick cellulosic secondary cell wall. The mechanisms by which cortical microtubules are involved in the formation of these pectinaceous and cellulosic cell walls are still largely unknown. Using a reverse genetic approach, we found that TONNEAU 1 ( TON 1) recruiting motif 4 ( TRM 4 ) is implicated in cortical microtubule organization in SCE cells, and functions as a novel player in the establishment of mucilage structure. TRM 4 is preferentially accumulated in the SCE cells at the stage of mucilage biosynthesis. The loss of TRM 4 results in compact seed mucilage capsules, aberrant mucilage cellulosic structure, short cellulosic rays and disorganized cellulose microfibrils in mucilage. The defects could be rescued by transgene complementation of trm4 alleles. Probably, this is a consequence of a disrupted organization of cortical microtubules, observed using fluorescently tagged tubulin proteins in trm4 SCE cells. Furthermore, TRM 4 proteins co‐aligned with microtubules and interacted directly with CELLULOSE SYNTHASE 3 in two independent assays. Together, the results indicate that TRM 4 is essential for microtubule array organization and therefore correct cellulose orientation in the SCE cells, as well as the establishment of the subsequent mucilage architecture.

Plant Cell Walls Tackling Climate Change: Biotechnological Strategies to Improve Crop Adaptations and Photosynthesis in Response to Global Warming

“…Developmental defects have been observed in cases of cellulose synthesis, and deposition is affected in seeds, roots, embryos, and among many other tissues [16][17][18][19]. The CW matrix is formed by other glucans, such as Xyloglucan (XG), a hemicellulose.…”

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“…Recent reviews sequentially reported 54 genes (Francoz et al, 2015) and 82 genes (Phan & Burton, 2018). Since then, 12 additional genes have been characterized (Fabrissin et al, 2019;Kunieda, Hara-Nishimura, Demura, & Haughn, 2019;Li et al, 2018;Shimada et al, 2018;Šola, Gilchrist, et al, 2019;Takenaka et al, 2018;van Wijk et al, 2018;Voiniciuc et al, 2018;Wang et al, 2019;Yang et al, 2019) bringing the list to 94 genes so far. They constitute the continuously growing MSC toolbox that participate to a proper seed mucilage production and release in A. thaliana (Francoz et al, 2015;Voiniciuc, Yang, Schmidt, Günl, & Usadel, 2015).…”

Mapping and Dynamics of Regulatory DNA in Maturing Arabidopsis thaliana Siliques

“…Previous studies have identified at least 59 genes affecting seed coat cell differentiation and maturation when disrupted in A. thaliana (North et al, 2014; Rautengarten et al, 2014; Francoz et al, 2015; Voiniciuc et al, 2015a; Voiniciuc et al, 2015b; Griffiths et al, 2016; Ralet et al, 2016; Wardhan et al, 2016; Saez-Aguayo et al, 2017; Polko et al, 2018; Takenaka et al, 2018; Voiniciuc et al, 2018; Yu et al, 2018; Šola et al, 2019; Yang et al, 2019). These genes fall into roughly three functional categories: epidermal cell differentiation, mucilage synthesis and secretion, and secondary cell wall synthesis ( Supplemental Table 1 ).…”