Extensins: Self-Assembly, Crosslinking, and the Role of Peroxidases

Overview

Journal Front Plant Sci

Date 2021 May 31

PMID 34054905

Citations 16

Authors

John W Mishler-Elmore

Yadi Zhou

Abhijit Sukul

Mercedes Oblak

Li Tan

Ahmed Faik

Michael A Held

Affiliations

Soon will be listed here.

Abstract

The extensin (EXT) network is elaborated by the covalent intermolecular crosslinking of EXT glycoprotein monomers, and its proper assembly is important for numerous aspects of basic wall architecture and cellular defense. In this review, we discuss new advances in the secretion of EXT monomers and the molecular drivers of EXT network self-assembly. Many of the functions of EXTs are conferred through covalent crosslinking into the wall, so we also discuss the different types of known intermolecular crosslinks, the enzymes that are involved, as well as the potential for additional crosslinks that are yet to be identified. EXTs also function in wall architecture independent of crosslinking status, and therefore, we explore the role of non-crosslinking EXTs. As EXT crosslinking is upregulated in response to wounding and pathogen infection, we discuss a potential regulatory mechanism to control covalent crosslinking and its relationship to the subcellular localization of the crosslinking enzymes.

Citing Articles

Effects of Different Pretreatments on Wheat Bran and Its Arabinoxylan Obtained by Sequential Extraction with Dilute Alkali and Alkali-Urea Mixture.

Liu A, Zhang S, Wang W, Hou H, Dai Y, Li C Foods. 2025; 14(4).

PMID: 40002139 PMC: 11854628. DOI: 10.3390/foods14040696.

The cell colony development is connected with the accumulation of embryogenesis-related proteins and dynamic distribution of cell wall components in in vitro cultures of Fagopyrum tataricum and Fagopyrum esculentum.

Zaranek M, Pinski A, Skupien-Rabian B, Jankowska U, Godel-Jedrychowska K, Sala-Cholewa K BMC Plant Biol. 2025; 25(1):102.

PMID: 39856552 PMC: 11761224. DOI: 10.1186/s12870-025-06119-3.

The Calicophoron daubneyi genome provides new insight into mechanisms of feeding, eggshell synthesis and parasite-microbe interactions.

Clancy S, Whitehead M, Oliver N, Huson K, Kyle J, Demartini D BMC Biol. 2025; 23(1):11.

PMID: 39800692 PMC: 11727788. DOI: 10.1186/s12915-025-02114-0.

Histidine limitation alters plant development and influences the TOR network.

Guerin A, Levasseur C, Herger A, Renggli D, Sotiropoulos A, Kadler G J Exp Bot. 2024; 76(4):1085-1098.

PMID: 39688839 PMC: 11850971. DOI: 10.1093/jxb/erae479.

Differential prolyl hydroxylation by six Physcomitrella prolyl-4 hydroxylases.

Rempfer C, Hoernstein S, van Gessel N, Graf A, Spiegelhalder R, Bertolini A Comput Struct Biotechnol J. 2024; 23:2580-2594.

PMID: 39021582 PMC: 11252719. DOI: 10.1016/j.csbj.2024.06.014.

References

Tan L, Eberhard S, Pattathil S, Warder C, Glushka J, Yuan C . An Arabidopsis cell wall proteoglycan consists of pectin and arabinoxylan covalently linked to an arabinogalactan protein. Plant Cell. 2013; 25(1):270-87. PMC: 3584541. DOI: 10.1105/tpc.112.107334. View

Bernards M, FLEMING W, Llewellyn D, Priefer R, Yang X, Sabatino A . Biochemical characterization of the suberization-associated anionic peroxidase of potato. Plant Physiol. 1999; 121(1):135-46. PMC: 59361. DOI: 10.1104/pp.121.1.135. View

Jackson P, Galinha C, S Pereira C, Fortunato A, Soares N, Amancio S . Rapid deposition of extensin during the elicitation of grapevine callus cultures is specifically catalyzed by a 40-kilodalton peroxidase. Plant Physiol. 2001; 127(3):1065-76. PMC: 129276. View

Keegstra K, Talmadge K, Bauer W, Albersheim P . The Structure of Plant Cell Walls: III. A Model of the Walls of Suspension-cultured Sycamore Cells Based on the Interconnections of the Macromolecular Components. Plant Physiol. 1973; 51(1):188-97. PMC: 367377. DOI: 10.1104/pp.51.1.188. View

Kieliszewski M . The latest hype on Hyp-O-glycosylation codes. Phytochemistry. 2001; 57(3):319-23. DOI: 10.1016/s0031-9422(01)00029-2. View

Bradley D, Kjellbom P, Lamb C . Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: a novel, rapid defense response. Cell. 1992; 70(1):21-30. DOI: 10.1016/0092-8674(92)90530-p. View

Baumberger N, Ringli C, Keller B . The chimeric leucine-rich repeat/extensin cell wall protein LRX1 is required for root hair morphogenesis in Arabidopsis thaliana. Genes Dev. 2001; 15(9):1128-39. PMC: 312681. DOI: 10.1101/gad.200201. View

Baumberger N, Steiner M, Ryser U, Keller B, Ringli C . Synergistic interaction of the two paralogous Arabidopsis genes LRX1 and LRX2 in cell wall formation during root hair development. Plant J. 2003; 35(1):71-81. DOI: 10.1046/j.1365-313x.2003.01784.x. View

Hematy K, Sado P, van Tuinen A, Rochange S, Desnos T, Balzergue S . A receptor-like kinase mediates the response of Arabidopsis cells to the inhibition of cellulose synthesis. Curr Biol. 2007; 17(11):922-31. DOI: 10.1016/j.cub.2007.05.018. View

10.

Price N, Pinheiro C, Soares C, Ashford D, Pinto Ricardo C, Jackson P . A biochemical and molecular characterization of LEP1, an extensin peroxidase from lupin. J Biol Chem. 2003; 278(42):41389-99. DOI: 10.1074/jbc.M304519200. View

11.

Brady J, Sadler I, Fry S . Di-isodityrosine, a novel tetrametric derivative of tyrosine in plant cell wall proteins: a new potential cross-link. Biochem J. 1996; 315 ( Pt 1):323-7. PMC: 1217189. DOI: 10.1042/bj3150323. 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.

Chen S, Schopfer P . Hydroxyl-radical production in physiological reactions. A novel function of peroxidase. Eur J Biochem. 1999; 260(3):726-35. DOI: 10.1046/j.1432-1327.1999.00199.x. View

14.

Levigne S, Ralet M, Quemener B, Pollet B, Lapierre C, Thibault J . Isolation from sugar beet cell walls of arabinan oligosaccharides esterified by two ferulic acid monomers. Plant Physiol. 2004; 134(3):1173-80. PMC: 389941. DOI: 10.1104/pp.103.035311. View

15.

SHPAK E, Barbar E, Leykam J, Kieliszewski M . Contiguous hydroxyproline residues direct hydroxyproline arabinosylation in Nicotiana tabacum. J Biol Chem. 2001; 276(14):11272-8. DOI: 10.1074/jbc.M011323200. View

16.

Dong W, Kieliszewski M, Held M . Identification of the pI 4.6 extensin peroxidase from Lycopersicon esculentum using proteomics and reverse-genomics. Phytochemistry. 2014; 112:151-9. PMC: 4380809. DOI: 10.1016/j.phytochem.2014.09.015. View

17.

Fry S . Isodityrosine, a new cross-linking amino acid from plant cell-wall glycoprotein. Biochem J. 1982; 204(2):449-55. PMC: 1158371. DOI: 10.1042/bj2040449. View

18.

Zhu X, Li S, Pan S, Xin X, Gu Y . CSI1, PATROL1, and exocyst complex cooperate in delivery of cellulose synthase complexes to the plasma membrane. Proc Natl Acad Sci U S A. 2018; 115(15):E3578-E3587. PMC: 5899483. DOI: 10.1073/pnas.1800182115. View

19.

Merkouropoulos G, Shirsat A . The unusual Arabidopsis extensin gene atExt1 is expressed throughout plant development and is induced by a variety of biotic and abiotic stresses. Planta. 2003; 217(3):356-66. DOI: 10.1007/s00425-003-1002-y. View

20.

Keren-Keiserman A, Tanami Z, Shoseyov O, Ginzberg I . Peroxidase activity associated with suberization processes of the muskmelon (Cucumis melo) rind. Physiol Plant. 2004; 121(1):141-148. DOI: 10.1111/j.0031-9317.2004.00301.x. View