Abstract
Pectins are abundant in the cell walls of dicotyledonous plants, but how they interact with other wall polymers and influence wall integrity and cell growth has remained mysterious. Here, we verified that QUASIMODO2 (QUA2) is a pectin methyltransferase and determined that QUA2 is required for normal pectin biosynthesis. To gain further insight into how pectin affects wall assembly and integrity maintenance, we investigated cellulose biosynthesis, cellulose organization, cortical microtubules, and wall integrity signaling in two mutant alleles of Arabidopsis (Arabidopsis thaliana) QUA2, qua2 and tsd2 In both mutants, crystalline cellulose content is reduced, cellulose synthase particles move more slowly, and cellulose organization is aberrant. NMR analysis shows higher mobility of cellulose and matrix polysaccharides in the mutants. Microtubules in mutant hypocotyls have aberrant organization and depolymerize more readily upon treatment with oryzalin or external force. The expression of genes related to wall integrity, wall biosynthesis, and microtubule stability is dysregulated in both mutants. These data provide insights into how homogalacturonan is methylesterified upon its synthesis, the mechanisms by which pectin functionally interacts with cellulose, and how these interactions are translated into intracellular regulation to maintain the structural integrity of the cell wall during plant growth and development.
Highlights
The primary cell walls of plants are mainly composed of cellulose, hemicelluloses, and pectins, which interact to form structural networks and tune wall mechanical strength, regulating cell shape determination and organ morphogenesis (Cosgrove, 2005)
Cellulose is synthesized by cellulose synthase complexes (CSCs) at the plasma membrane (Paredez et al, 2006), and its b-1,4-glucan chains are extruded into the apoplast and coalesce into microfibrils, the patterned deposition of which can be guided by cortical microtubules (Baskin et al, 2004)
Purified maltose binding protein (MBP) or MBP-QUA2 was incubated with SAM and polygalacturonic acid (PGA; the fully demethylated form of HG) for 2 h
Summary
The primary cell walls of plants are mainly composed of cellulose, hemicelluloses, and pectins, which interact to form structural networks and tune wall mechanical strength, regulating cell shape determination and organ morphogenesis (Cosgrove, 2005). In Arabidopsis, multiple glycosyltransferases, methyltransferases, and acetyltransferases are required for pectin biosynthesis (Atmodjo et al, 2013). Arabidopsis GALACTURONOSYLTRANSFERASE1 (GAUT1) displays HG:GalA transferase activity and can form a complex with the homologous GAUT7 to synthesize highmolecular-weight polymeric HG via a “two-phase” mechanism (Sterling et al, 2006; Atmodjo et al, 2011; Amos et al, 2018). QUASIMODO1 (QUA1/GAUT8) encodes a putative glycosyltransferase and is likely required for HG biosynthesis, since qua mutant plants have reduced uronic acid content in their walls and display cell adhesion defects (Bouton et al, 2002; Orfila et al, 2005; Durand et al, 2009; Verger et al, 2018). Either during or soon after polymerization, GalA residues in HG can be acetylated at O2 or O3 positions, and the carboxyl groups of most GalA residues in HG are methylesterified by methyltransferases (Atmodjo et al, 2013), but the proteins that perform these modifications have not yet been positively identified
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