Plant Physiology

Geitmann, Anja; Bacic, Antony (Tony)

doi: 10.1093/plphys/kiad537pmid: 37819051

Oliveira, Dyoni M

doi: 10.1093/plphys/kiad442pmid: 37542475

Jarvis, Michael C

doi: 10.1093/plphys/kiad387pmid: 37403192

Environmental influences and differential growth subject plants to mechanical forces. Forces on the whole plant resolve into tensile forces on its primary cell walls and both tensile and compression forces on the secondary cell wall layers of woody tissues. Forces on cell walls are further resolved into forces on cellulose microfibrils and the noncellulosic polymers between them. Many external forces on plants oscillate, with time constants that vary from seconds to milliseconds. Sound waves are a high-frequency example. Forces on the cell wall lead to responses that direct the oriented deposition of cellulose microfibrils and the patterned expansion of the cell wall, leading to complex cell and tissue morphology.Recent experiments have established many of the details of which cell wall polymers associate with one another in both primary and secondary cell walls, but questions remain about which of the interconnections are load bearing, especially in primary cell walls. Direct cellulose–cellulose interactions appear to have a more important mechanical role than was previously thought, and some of the noncellulosic polymers may have a role in keeping microfibrils apart rather than cross-linking them as formerly envisaged.

Domozych, David S; LoRicco, Josephine G

doi: 10.1093/plphys/kiad384pmid: 37399237

Green algae display a wide range of extracellular matrix (ECM) components that include various types of cell walls (CW), scales, crystalline glycoprotein coverings, hydrophobic compounds, and complex gels or mucilage. Recently, new information derived from genomic/transcriptomic screening, advanced biochemical analyses, immunocytochemical studies, and ecophysiology has significantly enhanced and refined our understanding of the green algal ECM. In the later diverging charophyte group of green algae, the CW and other ECM components provide insight into the evolution of plants and the ways the ECM modulates during environmental stress. Chlorophytes produce diverse ECM components, many of which have been exploited for various uses in medicine, food, and biofuel production. This review highlights major advances in ECM studies of green algae.

Hrmova, Maria; Zimmer, Jochen; Bulone, Vincent; Fincher, Geoffrey B

doi: 10.1093/plphys/kiad415pmid: 37594400

Recent breakthroughs in structural biology have provided valuable new insights into enzymes involved in plant cell wall metabolism. More specifically, the molecular mechanism of synthesis of (1,3;1,4)-β-glucans, which are widespread in cell walls of commercially important cereals and grasses, has been the topic of debate and intense research activity for decades. However, an inability to purify these integral membrane enzymes or apply transgenic approaches without interpretative problems associated with pleiotropic effects has presented barriers to attempts to define their synthetic mechanisms. Following the demonstration that some members of the CslF sub-family of GT2 family enzymes mediate (1,3;1,4)-β-glucan synthesis, the expression of the corresponding genes in a heterologous system that is free of background complications has now been achieved. Biochemical analyses of the (1,3;1,4)-β-glucan synthesized in vitro, combined with 3-dimensional (3D) cryogenic-electron microscopy and AlphaFold protein structure predictions, have demonstrated how a single CslF6 enzyme, without exogenous primers, can incorporate both (1,3)- and (1,4)-β-linkages into the nascent polysaccharide chain. Similarly, 3D structures of xyloglucan endo-transglycosylases and (1,3;1,4)-β-glucan endo- and exohydrolases have allowed the mechanisms of (1,3;1,4)-β-glucan modification and degradation to be defined. X-ray crystallography and multi-scale modeling of a broad specificity GH3 β-glucan exohydrolase recently revealed a previously unknown and remarkable molecular mechanism with reactant trajectories through which a polysaccharide exohydrolase can act with a processive action pattern. The availability of high-quality protein 3D structural predictions should prove invaluable for defining structures, dynamics, and functions of other enzymes involved in plant cell wall metabolism in the immediate future.

Quinn, Oliver; Kumar, Manoj; Turner, Simon

doi: 10.1093/plphys/kiad491pmid: 37682865

The plant cell wall is a complex and dynamic extracellular matrix. Plant primary cell walls are the first line of defense against pathogens and regulate cell expansion. Specialized cells deposit a secondary cell wall that provides support and permits water transport. The composition and organization of the cell wall varies between cell types and species, contributing to the extensibility, stiffness, and hydrophobicity required for its proper function. Recently, many of the proteins involved in the biosynthesis, maintenance, and remodeling of the cell wall have been identified as being post-translationally modified with lipids. These modifications exhibit diverse structures and attach to proteins at different sites, which defines the specific role played by each lipid modification. The introduction of relatively hydrophobic lipid moieties promotes the interaction of proteins with membranes and can act as sorting signals, allowing targeted delivery to the plasma membrane regions and secretion into the apoplast. Disruption of lipid modification results in aberrant deposition of cell wall components and defective cell wall remodeling in response to stresses, demonstrating the essential nature of these modifications. Although much is known about which proteins bear lipid modifications, many questions remain regarding the contribution of lipid-driven membrane domain localization and lipid heterogeneity to protein function in cell wall metabolism. In this update, we highlight the contribution of lipid modifications to proteins involved in the formation and maintenance of plant cell walls, with a focus on the addition of glycosylphosphatidylinositol anchors, N-myristoylation, prenylation, and S-acylation.

Kamel, Hiba; Geitmann, Anja

doi: 10.1093/plphys/kiad544pmid: 37819032

Pectin is a major component of the cell wall in land plants. It plays crucial roles in cell wall assembly, cell growth, shaping, and signaling. The relative abundance of pectin in the cell wall is particularly high in rapidly growing organ regions and cell types. Homogalacturonan (HG), a polymer of 1,4-linked α-D-galacturonic acid, is a major pectin constituent in growing and dividing plant cells. In pollen tubes, an extremely rapidly growing cell type, HG is secreted at and inserted into the apical cell wall and is subject to further modification in muro by HG modifying enzymes (HGMEs). These enzymes, including pectin esterases and depolymerases, have multiple isoforms, some of which are specifically expressed in pollen. Given the importance of pectin chemistry for the fitness of pollen tubes, it is of interest to interrogate the potentially crucial roles these isoforms play in pollen germination and elongation. It is hypothesized that different HGME isoforms, through their action on apoplastic HG, may generate differential methylation and acetylation patterns endowing HG polysaccharides with specific, spatially and temporally varying properties that lead to a fine-tuned pattern of cell wall modification. In addition, these isoforms may be differentially activated and/or inhibited depending on the local conditions that may vary at subcellular resolution. In this Update we review the different HGME isoforms identified in recent years in Arabidopsis thaliana and postulate that the multiplicity of these isoforms may allow for specialized substrate recognition and conditional activation, leading to a sophisticated regulation scheme exemplified in the process that governs the dynamic properties of the cell wall in pollen tube growth.

Rodríguez-García, Diana R; Rondón Guerrero, Yossmayer del Carmen; Ferrero, Lucía; Rossi, Andrés Hugo; Miglietta, Esteban A; Aptekmann, Ariel A; Marzol, Eliana; Martínez Pacheco, Javier; Carignani, Mariana; Berdion Gabarain, Victoria; Lopez, Leonel E; Díaz Dominguez, Gabriela; Borassi, Cecilia;

Huss, Jessica C; Antreich, Sebastian J; Felhofer, Martin; Mayer, Konrad; Eder, Michaela; Vieira Dias dos Santos, Ana Catarina; Ramer, Georg; Lendl, Bernhard; Gierlinger, Notburga

doi: 10.1093/plphys/kiad408pmid: 37427803

The water caltrop (Trapa natans) develops unique woody fruits with unusually large seeds among aquatic plants. During fruit development, the inner fruit wall (endocarp) sclerifies and forms a protective layer for the seed. Endocarp sclerification also occurs in many land plants with large seeds; however, in T. natans, the processes of fruit formation, endocarp hardening, and seed storage take place entirely underwater. To identify potential chemical and structural adaptations for the aquatic environment, we investigated the cell-wall composition in the endocarp at a young developmental stage, as well as at fruit maturity. Our work shows that hydrolyzable tannins—specifically gallotannins—flood the endocarp tissue during secondary wall formation and are integrated into cell walls along with lignin during maturation. Within the secondary walls of mature tissue, we identified unusually strong spectroscopic features of ester linkages, suggesting that the gallotannins and their derivatives are cross-linked to other wall components via ester bonds, leading to unique cell-wall properties. The synthesis of large amounts of water-soluble, defensive aromatic metabolites during secondary wall formation might be a fast way to defend seeds within the insufficiently lignified endocarp of T. natans.

Fang, Shuai; Shang, Xiaoguang; He, Qingfei; Li, Weixi; Song, Xiaohui; Zhang, Baohong; Guo, Wangzhen

doi: 10.1093/plphys/kiad407pmid: 37427813

β-1,3-glucanase functions in plant physiological and developmental processes. However, how β-1,3-glucanase participates in cell wall development remains largely unknown. Here, we answered this question by examining the role of GhGLU18, a β-1,3-glucanase, in cotton (Gossypium hirsutum) fibers, in which the content of β-1,3-glucan changes dynamically from 10% of the cell wall mass at the onset of secondary wall deposition to <1% at maturation. GhGLU18 was specifically expressed in cotton fiber with higher expression in late fiber elongation and secondary cell wall (SCW) synthesis stages. GhGLU18 largely localized to the cell wall and was able to hydrolyze β-1,3-glucan in vitro. Overexpression of GhGLU18 promoted polysaccharide accumulation, cell wall reconstruction, and cellulose synthesis, which led to increased fiber length and strength with thicker cell walls and shorter pitch of the fiber helix. However, GhGLU18-suppressed cotton resulted in opposite phenotypes. Additionally, GhGLU18 was directly activated by GhFSN1 (fiber SCW-related NAC1), a NAC transcription factor reported previously as the master regulator in SCW formation during fiber development. Our results demonstrate that cell wall–localized GhGLU18 promotes fiber elongation and SCW thickening by degrading callose and enhancing polysaccharide metabolism and cell wall synthesis.