Mutations in the Pectin Methyltransferase QUASIMODO2 Influence Cellulose Biosynthesis and Wall Integrity in Arabidopsis

Overview

Journal Plant Cell

Publisher Oxford University Press

Specialties Biology
Cell Biology

Date 2020 Sep 5

PMID 32883711

Citations 40

Authors

Juan Du

Alex Kirui

Shixin Huang

Lianglei Wang

William J Barnes

Sarah N Kiemle

Yunzhen Zheng

Yue Rui

Mei Ruan

Shiqian Qi

Seong H Kim

Tuo Wang

Daniel J Cosgrove

Charles T Anderson

Chaowen Xiao

Affiliations

Soon will be listed here.

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 () , and 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.

Citing Articles

A cell fractionation and quantitative proteomics pipeline to enable functional analyses of cotton fiber development.

Lee Y, Rani H, Mallery E, Szymanski D Plant J. 2025; 121(4):e17246.

PMID: 39970036 PMC: 11838819. DOI: 10.1111/tpj.17246.

A Fresh Look at Celery Collenchyma and Parenchyma Cell Walls Through a Combination of Biochemical, Histochemical, and Transcriptomic Analyses.

Mokshina N, Sautkina O, Gorshkov O, Mikshina P Int J Mol Sci. 2025; 26(2).

PMID: 39859452 PMC: 11765706. DOI: 10.3390/ijms26020738.

Understanding pectin cross-linking in plant cell walls.

Obomighie I, Prentice I, Lewin-Jones P, Bachtiger F, Ramsay N, Kishi-Itakura C Commun Biol. 2025; 8(1):72.

PMID: 39825091 PMC: 11748717. DOI: 10.1038/s42003-025-07495-0.

Heterogeneity in Mechanical Properties of Plant Cell Walls.

Zhang H, Xiao L, Qin S, Kuang Z, Wan M, Li Z Plants (Basel). 2025; 13(24.

PMID: 39771259 PMC: 11678144. DOI: 10.3390/plants13243561.

Antioxidant activity and comparative RNA-seq analysis support mitigating effects of an algae-based biostimulant on drought stress in tomato plants.

Cerruti P, Campobenedetto C, Montrucchio E, Agliassa C, Contartese V, Acquadro A Physiol Plant. 2024; 176(6):e70007.

PMID: 39703136 PMC: 11659800. DOI: 10.1111/ppl.70007.

References

Peaucelle A, Wightman R, Hofte H . The Control of Growth Symmetry Breaking in the Arabidopsis Hypocotyl. Curr Biol. 2015; 25(13):1746-52. DOI: 10.1016/j.cub.2015.05.022. View

Caffall K, Mohnen D . The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydr Res. 2009; 344(14):1879-900. DOI: 10.1016/j.carres.2009.05.021. View

Rajangam A, Kumar M, Aspeborg H, Guerriero G, Arvestad L, Pansri P . MAP20, a microtubule-associated protein in the secondary cell walls of hybrid aspen, is a target of the cellulose synthesis inhibitor 2,6-dichlorobenzonitrile. Plant Physiol. 2008; 148(3):1283-94. PMC: 2577246. DOI: 10.1104/pp.108.121913. View

Wang T, Park Y, Cosgrove D, Hong M . Cellulose-Pectin Spatial Contacts Are Inherent to Never-Dried Arabidopsis Primary Cell Walls: Evidence from Solid-State Nuclear Magnetic Resonance. Plant Physiol. 2015; 168(3):871-84. PMC: 4741345. DOI: 10.1104/pp.15.00665. View

Atmodjo M, Sakuragi Y, Zhu X, Burrell A, Mohanty S, Atwood 3rd J . Galacturonosyltransferase (GAUT)1 and GAUT7 are the core of a plant cell wall pectin biosynthetic homogalacturonan:galacturonosyltransferase complex. Proc Natl Acad Sci U S A. 2011; 108(50):20225-30. PMC: 3250160. DOI: 10.1073/pnas.1112816108. View

Korolev A, Buschmann H, Doonan J, Lloyd C . AtMAP70-5, a divergent member of the MAP70 family of microtubule-associated proteins, is required for anisotropic cell growth in Arabidopsis. J Cell Sci. 2007; 120(Pt 13):2241-7. DOI: 10.1242/jcs.007393. View

Amos R, Pattathil S, Yang J, Atmodjo M, Urbanowicz B, Moremen K . A two-phase model for the non-processive biosynthesis of homogalacturonan polysaccharides by the GAUT1:GAUT7 complex. J Biol Chem. 2018; 293(49):19047-19063. PMC: 6295712. DOI: 10.1074/jbc.RA118.004463. View

Hsiao K, Zegzouti H, Goueli S . Methyltransferase-Glo: a universal, bioluminescent and homogenous assay for monitoring all classes of methyltransferases. Epigenomics. 2016; 8(3):321-39. DOI: 10.2217/epi.15.113. View

Refregier G, Pelletier S, Jaillard D, Hofte H . Interaction between wall deposition and cell elongation in dark-grown hypocotyl cells in Arabidopsis. Plant Physiol. 2004; 135(2):959-68. PMC: 514130. DOI: 10.1104/pp.104.038711. View

10.

Voiniciuc C, Engle K, Gunl M, Dieluweit S, Schmidt M, Yang J . Identification of Key Enzymes for Pectin Synthesis in Seed Mucilage. Plant Physiol. 2018; 178(3):1045-1064. PMC: 6236597. DOI: 10.1104/pp.18.00584. View

11.

Park Y, Cosgrove D . A revised architecture of primary cell walls based on biomechanical changes induced by substrate-specific endoglucanases. Plant Physiol. 2012; 158(4):1933-43. PMC: 3320196. DOI: 10.1104/pp.111.192880. View

12.

Perez Garcia M, Zhang Y, Hayes J, Salazar A, Zabotina O, Hong M . Structure and interactions of plant cell-wall polysaccharides by two- and three-dimensional magic-angle-spinning solid-state NMR. Biochemistry. 2011; 50(6):989-1000. DOI: 10.1021/bi101795q. View

13.

Miedes E, Suslov D, Vandenbussche F, Kenobi K, Ivakov A, Van Der Straeten D . Xyloglucan endotransglucosylase/hydrolase (XTH) overexpression affects growth and cell wall mechanics in etiolated Arabidopsis hypocotyls. J Exp Bot. 2013; 64(8):2481-97. DOI: 10.1093/jxb/ert107. View

14.

Gao P, Xin Z, Zheng Z . The OSU1/QUA2/TSD2-encoded putative methyltransferase is a critical modulator of carbon and nitrogen nutrient balance response in Arabidopsis. PLoS One. 2008; 3(1):e1387. PMC: 2148111. DOI: 10.1371/journal.pone.0001387. View

15.

Xu S, Rahman A, Baskin T, Kieber J . Two leucine-rich repeat receptor kinases mediate signaling, linking cell wall biosynthesis and ACC synthase in Arabidopsis. Plant Cell. 2008; 20(11):3065-79. PMC: 2613664. DOI: 10.1105/tpc.108.063354. View

16.

Cornuault V, Manfield I, Ralet M, Knox J . Epitope detection chromatography: a method to dissect the structural heterogeneity and inter-connections of plant cell-wall matrix glycans. Plant J. 2014; 78(4):715-22. DOI: 10.1111/tpj.12504. View

17.

Zheng Y, Wang X, Chen Y, Wagner E, Cosgrove D . Xyloglucan in the primary cell wall: assessment by FESEM, selective enzyme digestions and nanogold affinity tags. Plant J. 2017; 93(2):211-226. DOI: 10.1111/tpj.13778. View

18.

Clough S, Bent A . Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1999; 16(6):735-43. DOI: 10.1046/j.1365-313x.1998.00343.x. View

19.

Baskin T, Beemster G, Judy-March J, Marga F . Disorganization of cortical microtubules stimulates tangential expansion and reduces the uniformity of cellulose microfibril alignment among cells in the root of Arabidopsis. Plant Physiol. 2004; 135(4):2279-90. PMC: 520797. DOI: 10.1104/pp.104.040493. View

20.

Ambrose J, Shoji T, Kotzer A, Pighin J, Wasteneys G . The Arabidopsis CLASP gene encodes a microtubule-associated protein involved in cell expansion and division. Plant Cell. 2007; 19(9):2763-75. PMC: 2048705. DOI: 10.1105/tpc.107.053777. View