Polygalacturonase activity promotes aberrant cell separation in the quasimodo2 mutant of Arabidopsis thaliana

Barnes, William J.; Zelinsky, Ellen; Anderson, Charles T.

doi:10.1016/j.tcsw.2021.100069

Title: Polygalacturonase activity promotes aberrant cell separation in the quasimodo2 mutant of Arabidopsis thaliana

Journal Article · Thu Dec 01 00:00:00 EST 2022 · The Cell Surface

DOI:https://doi.org/10.1016/j.tcsw.2021.100069· OSTI ID:1835436

Barnes, William J.; Zelinsky, Ellen; Anderson, Charles T.

In plants, cell adhesion relies on balancing the integrity of the pectin-rich middle lamella with wall loosening during tissue expansion. Mutation of QUASIMODO2 (QUA2), a pectin methyltransferase, causes defective hypocotyl elongation and cell adhesion in Arabidopsis thaliana hypocotyls. However, the molecular function of QUA2 in cell adhesion is obscured by complex genetic and environmental interactions. To dissect the role of QUA2 in cell adhesion, we investigated a qua2 loss-of-function mutant and a suppressor mutant with restored cell adhesion, qua2 esmeralda1, using a combination of imaging and biochemical techniques. We found that qua2 hypocotyls have reductions in middle lamellae integrity, pectin methyl-esterase (PME) activity, pectin content and molecular mass, and immunodetected Ca2⁺-crosslinking at cell corners, but increased methyl-esterification and polygalacturonase (PG) activity, with qua2 esmd1 having wild type-like or intermediate phenotypes. Our findings suggest that excessive pectin degradation prevents pectin accumulation and the formation of a sufficiently Ca²⁺-crosslinked network to maintain cell adhesion in qua2 mutants. We propose that PME and PG activities balance tissue-level expansion and cell separation. Together, these data provide insight into the cause of cell adhesion defects in qua2 mutants and highlight the importance of harmonizing pectin modification and degradation during plant growth and development.

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Research Organization:: Pennsylvania State Univ., University Park, PA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: SC0001090

OSTI ID:: 1835436

Alternate ID(s):: OSTI ID: 2204040

Journal Information:: The Cell Surface, Journal Name: The Cell Surface Vol. 8 Journal Issue: C; ISSN 2468-2330

Publisher:: ElsevierCopyright Statement

Country of Publication:: Netherlands

Language:: English

References (38)

Necrotizing activity of five Botrytis cinerea endopolygalacturonases produced in Pichia pastoris: Necrotizing activity of BcPGs Kars, Ilona; Krooshof, Geja H.; Wagemakers, Lia The Plant Journal, Vol. 43, Issue 2 https://doi.org/10.1111/j.1365-313X.2005.02436.x	journal	June 2005
Deesterification mode of pectin by pectin esterases of Aspergillus foetidus, tomatoes and alfalfa Kohn, Rudolf; Markovič, Oskar; Machová, Eva Collection of Czechoslovak Chemical Communications, Vol. 48, Issue 3 https://doi.org/10.1135/cccc19830790	journal	January 1983
PECTATE LYASE LIKE12 patterns the guard cell wall to coordinate turgor pressure and wall mechanics for proper stomatal function in Arabidopsis Chen, Yintong; Li, Wenlong; Turner, Joseph A. The Plant Cell, Vol. 33, Issue 9 https://doi.org/10.1093/plcell/koab161	journal	June 2021
The cell wall-associated kinases, WAKs, as pectin receptors Kohorn, Bruce D.; Kohorn, Susan L. Frontiers in Plant Science, Vol. 3 https://doi.org/10.3389/fpls.2012.00088	journal	January 2012
Post-Synthetic Reduction of Pectin Methylesterification Causes Morphological Abnormalities and Alterations to Stress Response in Arabidopsis thaliana Reem, Nathan T.; Chambers, Lauran; Zhang, Ning Plants, Vol. 9, Issue 11 https://doi.org/10.3390/plants9111558	journal	November 2020
Cytosolic invertases contribute to cellulose biosynthesis and influence carbon partitioning in seedlings of Arabidopsis thaliana Barnes, William J.; Anderson, Charles T. The Plant Journal, Vol. 94, Issue 6 https://doi.org/10.1111/tpj.13909	journal	April 2018
Plant cell wall extensibility: connecting plant cell growth with cell wall structure, mechanics, and the action of wall-modifying enzymes Cosgrove, Daniel J. Journal of Experimental Botany, Vol. 67, Issue 2 https://doi.org/10.1093/jxb/erv511	journal	November 2015
QUASIMODO 3 (QUA3) is a putative homogalacturonan methyltransferase regulating cell wall biosynthesis in Arabidopsis suspension-cultured cells Miao, Yansong; Li, Hong-Ye; Shen, Jinbo Journal of Experimental Botany, Vol. 62, Issue 14 https://doi.org/10.1093/jxb/err211	journal	July 2011
A pectin glucuronyltransferase gene is essential for intercellular attachment in the plant meristem Iwai, H.; Masaoka, N.; Ishii, T. Proceedings of the National Academy of Sciences, Vol. 99, Issue 25 https://doi.org/10.1073/pnas.252530499	journal	November 2002
Plant cell adhesion and growth on artificial fibrous scaffolds as an in vitro model for plant development Calcutt, Ryan; Vincent, Richard; Dean, Derrick Science Advances, Vol. 7, Issue 43 https://doi.org/10.1126/sciadv.abj1469	journal	October 2021
Monoclonal Antibodies against Pectin: Recognition of a Conformation Induced by Calcium Liners, Françoise; Letesson, Jean-Jacques; Didembourg, Christian Plant Physiology, Vol. 91, Issue 4 https://doi.org/10.1104/pp.91.4.1419	journal	December 1989
Etiolated Seedling Development Requires Repression of Photomorphogenesis by a Small Cell-Wall-Derived Dark Signal Sinclair, Scott A.; Larue, Camille; Bonk, Laura Current Biology, Vol. 27, Issue 22 https://doi.org/10.1016/j.cub.2017.09.063	journal	November 2017
Inhibition of pectin methyl esterase activity by green tea catechins Lewis, Kristin C.; Selzer, Tzvia; Shahar, Chen Phytochemistry, Vol. 69, Issue 14 https://doi.org/10.1016/j.phytochem.2008.08.012	journal	October 2008
Reduced Number of Homogalacturonan Domains in Pectins of an Arabidopsis Mutant Enhances the Flexibility of the Polymer Ralet, Marie-Christine; Crépeau, Marie-Jeanne; Lefèbvre, Jacques Biomacromolecules, Vol. 9, Issue 5 https://doi.org/10.1021/bm701321g	journal	May 2008
Homogalacturonan synthesis in Arabidopsis thaliana requires a Golgi-localized protein with a putative methyltransferase domain: Homogalacturonan synthesis in Arabidopsis: Mouille, Grégory; Ralet, Marie-Christine; Cavelier, Céline The Plant Journal, Vol. 50, Issue 4 https://doi.org/10.1111/j.1365-313X.2007.03086.x	journal	April 2007
Galacturonosyltransferase (GAUT)1 and GAUT7 are the core of a plant cell wall pectin biosynthetic homogalacturonan:galacturonosyltransferase complex Atmodjo, M. A.; Sakuragi, Y.; Zhu, X. Proceedings of the National Academy of Sciences, Vol. 108, Issue 50 https://doi.org/10.1073/pnas.1112816108	journal	November 2011
POLYGALACTURONASE INVOLVED IN EXPANSION3 Functions in Seedling Development, Rosette Growth, and Stomatal Dynamics in Arabidopsis thaliana Rui, Yue; Xiao, Chaowen; Yi, Hojae The Plant Cell, Vol. 29, Issue 10 https://doi.org/10.1105/tpc.17.00568	journal	October 2017
POLYGALACTURONASE INVOLVED IN EXPANSION1 Functions in Cell Elongation and Flower Development in Arabidopsis Xiao, Chaowen; Somerville, Chris; Anderson, Charles T. The Plant Cell, Vol. 26, Issue 3 https://doi.org/10.1105/tpc.114.123968	journal	March 2014
Mutations in the Pectin Methyltransferase QUASIMODO2 Influence Cellulose Biosynthesis and Wall Integrity in Arabidopsis Du, Juan; Kirui, Alex; Huang, Shixin The Plant Cell, Vol. 32, Issue 11 https://doi.org/10.1105/tpc.20.00252	journal	September 2020
The Control of Growth Symmetry Breaking in the Arabidopsis Hypocotyl Peaucelle, Alexis; Wightman, Raymond; Höfte, Herman Current Biology, Vol. 25, Issue 13 https://doi.org/10.1016/j.cub.2015.05.022	journal	June 2015
The TUMOROUS SHOOT DEVELOPMENT2 gene of Arabidopsis encoding a putative methyltransferase is required for cell adhesion and co-ordinated plant development: The Arabidopsis TSD2 gene Krupková, Eva; Immerzeel, Peter; Pauly, Markus The Plant Journal, Vol. 50, Issue 4 https://doi.org/10.1111/j.1365-313X.2007.03123.x	journal	April 2007
Tracking developmentally regulated post-synthetic processing of homogalacturonan and chitin using reciprocal oligosaccharide probes Mravec, J.; Kracun, S. K.; Rydahl, M. G. Development, Vol. 141, Issue 24 https://doi.org/10.1242/dev.113365	journal	November 2014
Evolving Views of Pectin Biosynthesis Atmodjo, Melani A.; Hao, Zhangying; Mohnen, Debra Annual Review of Plant Biology, Vol. 64, Issue 1 https://doi.org/10.1146/annurev-arplant-042811-105534	journal	April 2013
The FERONIA Receptor Kinase Maintains Cell-Wall Integrity during Salt Stress through Ca2+ Signaling Feng, Wei; Kita, Daniel; Peaucelle, Alexis Current Biology, Vol. 28, Issue 5 https://doi.org/10.1016/j.cub.2018.01.023	journal	March 2018
Expanding roles for pectins in plant development Saffer, Adam M. Journal of Integrative Plant Biology, Vol. 60, Issue 10 https://doi.org/10.1111/jipb.12662	journal	July 2018
A tension-adhesion feedback loop in plant epidermis Verger, Stéphane; Long, Yuchen; Boudaoud, Arezki eLife, Vol. 7 https://doi.org/10.7554/eLife.34460	journal	April 2018
Absence of arabinan in the side chains of the pectic polysaccharides strongly associated with cell walls of Nicotiana plumbaginifolia non-organogenic callus with loosely attached constituent cells Iwai, Hiroaki; Ishii, Tadashi; Satoh, Shinobu Planta, Vol. 213, Issue 6 https://doi.org/10.1007/s004250100559	journal	October 2001
Arabidopsis Phyllotaxis Is Controlled by the Methyl-Esterification Status of Cell-Wall Pectins Peaucelle, Alexis; Louvet, Romain; Johansen, Jorunn N. Current Biology, Vol. 18, Issue 24 https://doi.org/10.1016/j.cub.2008.10.065	journal	December 2008
The FRIABLE1 Gene Product Affects Cell Adhesion in Arabidopsis Neumetzler, Lutz; Humphrey, Tania; Lumba, Shelley PLoS ONE, Vol. 7, Issue 8 https://doi.org/10.1371/journal.pone.0042914	journal	August 2012
An extended set of monoclonal antibodies to pectic homogalacturonan Verhertbruggen, Yves; Marcus, Susan E.; Haeger, Ash Carbohydrate Research, Vol. 344, Issue 14 https://doi.org/10.1016/j.carres.2008.11.010	journal	September 2009
Growth Control and Cell Wall Signaling in Plants Wolf, Sebastian; Hématy, Kian; Höfte, Herman Annual Review of Plant Biology, Vol. 63, Issue 1 https://doi.org/10.1146/annurev-arplant-042811-105449	journal	June 2012
Activation tagging of Arabidopsis POLYGALACTURONASE INVOLVED IN EXPANSION2 promotes hypocotyl elongation, leaf expansion, stem lignification, mechanical stiffening, and lodging Xiao, Chaowen; Barnes, William J.; Zamil, M. Shafayet The Plant Journal, Vol. 89, Issue 6 https://doi.org/10.1111/tpj.13453	journal	February 2017
Anisotropic growth is achieved through the additive mechanical effect of material anisotropy and elastic asymmetry Bou Daher, Firas; Chen, Yuanjie; Bozorg, Behruz eLife, Vol. 7 https://doi.org/10.7554/eLife.38161	journal	September 2018
Connecting Homogalacturonan-Type Pectin Remodeling to Acid Growth Hocq, Ludivine; Pelloux, Jérôme; Lefebvre, Valérie Trends in Plant Science, Vol. 22, Issue 1 https://doi.org/10.1016/j.tplants.2016.10.009	journal	January 2017
Effects of Arabidopsis wall associated kinase mutations on ESMERALDA1 and elicitor induced ROS Kohorn, Bruce D.; Greed, Bridgid E.; Mouille, Gregory PLOS ONE, Vol. 16, Issue 5 https://doi.org/10.1371/journal.pone.0251922	journal	May 2021
Diversity of Pectin Rhamnogalacturonan I Rhamnosyltransferases in Glycosyltransferase Family 106 Wachananawat, Bussarin; Kuroha, Takeshi; Takenaka, Yuto Frontiers in Plant Science, Vol. 11 https://doi.org/10.3389/fpls.2020.00997	journal	July 2020
Overexpression of Polygalacturonase in Transgenic Apple Trees Leads to a Range of Novel Phenotypes Involving Changes in Cell Adhesion Atkinson, Ross G.; Schröder, Roswitha; Hallett, Ian C. Plant Physiology, Vol. 129, Issue 1 https://doi.org/10.1104/pp.010986	journal	May 2002
PECTOPLATE: the simultaneous phenotyping of pectin methylesterases, pectinases, and oligogalacturonides in plants during biotic stresses Lionetti, Vincenzo Frontiers in Plant Science, Vol. 6 https://doi.org/10.3389/fpls.2015.00331	journal	May 2015

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