Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, Connecticut, 06520, USA.
Biology Department, University of Massachusetts, 611 N. Pleasant St, Amherst, Massachusetts, 01003, USA.
Plant J. 2023 Nov;116(3):855-870. doi: 10.1111/tpj.16414. Epub 2023 Aug 7.
Plant cells and organs grow into a remarkable diversity of shapes, as directed by cell walls composed primarily of polysaccharides such as cellulose and multiple structurally distinct pectins. The properties of the cell wall that allow for precise control of morphogenesis are distinct from those of the individual polysaccharide components. For example, cellulose, the primary determinant of cell morphology, is a chiral macromolecule that can self-assemble in vitro into larger-scale structures of consistent chirality, and yet most plant cells do not display consistent chirality in their growth. One interesting exception is the Arabidopsis thaliana rhm1 mutant, which has decreased levels of the pectin rhamnogalacturonan-I and causes conical petal epidermal cells to grow with a left-handed helical twist. Here, we show that in rhm1 the cellulose is bundled into large macrofibrils, unlike the evenly distributed microfibrils of the wild type. This cellulose bundling becomes increasingly severe over time, consistent with cellulose being synthesized normally and then self-associating into macrofibrils. We also show that in the wild type, cellulose is oriented transversely, whereas in rhm1 mutants, the cellulose forms right-handed helices that can account for the helical morphology of the petal cells. Our results indicate that when the composition of pectin is altered, cellulose can form cellular-scale chiral structures in vivo, analogous to the helicoids formed in vitro by cellulose nano-crystals. We propose that an important emergent property of the interplay between rhamnogalacturonan-I and cellulose is to permit the assembly of nonbundled cellulose structures, providing plants flexibility to orient cellulose and direct morphogenesis.
植物细胞和器官按照细胞壁的指示生长成各种不同的形状,细胞壁主要由多糖组成,如纤维素和多种结构不同的果胶。允许精确控制形态发生的细胞壁的特性与单个多糖成分的特性不同。例如,纤维素是决定细胞形态的主要因素,它是一种手性大分子,在体外可以自组装成具有一致手性的更大规模结构,但大多数植物细胞在其生长过程中并不显示出一致的手性。一个有趣的例外是拟南芥 rhm1 突变体,它的果胶半乳糖醛酸聚糖 I 水平降低,导致锥形花瓣表皮细胞以左手螺旋方式生长。在这里,我们表明 rhm1 中的纤维素被捆绑成大的微纤维,而不像野生型那样均匀分布的微纤维。这种纤维素捆绑随着时间的推移变得越来越严重,这与纤维素正常合成然后自我组装成微纤维一致。我们还表明,在野生型中,纤维素是横向取向的,而在 rhm1 突变体中,纤维素形成右手螺旋,可以解释花瓣细胞的螺旋形态。我们的结果表明,当果胶的组成发生改变时,纤维素可以在体内形成细胞尺度的手性结构,类似于纤维素纳米晶体在体外形成的螺旋体。我们提出,半乳糖醛酸聚糖 I 和纤维素之间相互作用的一个重要突现性质是允许非捆绑纤维素结构的组装,为植物提供了灵活性,以定向纤维素并指导形态发生。