植物果胶的生物合成与功能

doi:10.11983/CBB20179

摘要/Abstract

摘要： 果胶作为植物细胞壁多糖之一, 其结构和功能非常复杂。果胶主要由同型半乳糖醛酸聚糖(HG)、鼠李半乳糖醛酸聚糖I (RGI)和鼠李半乳糖醛酸聚糖II (RGII)组成。果胶类成分在维持细胞壁结构的完整性以及细胞间黏附和信号转导等方面发挥重要作用。研究果胶类成分的结构、分布和功能, 对理解细胞壁高级结构的构建和功能具有重要意义。然而, 3种果胶组分在细胞壁内如何交联形成高级结构并发挥生物学功能, 目前尚不明确。该文重点阐述果胶3种组分(HG、RGI和RGII)的生物合成、功能以及果胶的显微成像, 旨在为植物果胶结构及功能研究提供参考。

关键词: 生物合成, 果胶功能, 显微成像, 果胶组分

Abstract: As one of the plant cell wall polysaccharides, pectin has a very complex structure and function. Pectin is mainly composed by homogalacturonan (HG), rhamngalacturonan I (RGI), rhamngalacturonan II (RGII). Pectin plays an important role in maintaining the integrity of cell wall structure, intercellular adhesion and signal transduction. Therefore, studying the structure, distribution and roles of pectin components is of great significance for understanding the construction and function of cell wall. However, it is not clear how these three components of pectin cross-link to form high structure and perform biological function in the cell wall. This review will focus on the biosynthesis, functions of HG, RGI, RGII as well as the microscopic imaging techniques of pectin, aiming to provide a theoretical basis for the study of the structure and function of plant pectin.

Key words: biosynthesis, function of pectin, microscopic imaging, pectin components

刘佩佩, 张耿, 李晓娟. 植物果胶的生物合成与功能. 植物学报, 2021, 56(2): 191-200.

Peipei Liu, Geng Zhang, Xiaojuan Li. Biosynthesis and Function of Plant Pectin. Chinese Bulletin of Botany, 2021, 56(2): 191-200.

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链接本文: https://www.chinbullbotany.com/CN/10.11983/CBB20179

https://www.chinbullbotany.com/CN/Y2021/V56/I2/191

图/表 2

图1 同型半乳糖醛酸聚糖(HG)多糖与Ca2+交联的“鸡蛋盒”模型(改自Micheli,2001; Braccini and Peréz,2001) 高甲基酯化的HG被果胶甲基酯酶(PME)去甲基酯化, 产生带负电荷的羧基。在Ca2+存在时, 2条HG链的羧基与Ca2+相互作用, 形成“鸡蛋盒”结构。

Figure 1 An “egg-box” model of homogalacturonan (HG) polysaccharide and Ca 2+ cross-linking (modified from Micheli, 2001; Braccini and Peréz,2001) Hypermethylated HG is de-methylated by pectin methylesterase (PME) to produce negatively charged carboxyl groups. In the presence of Ca2+, the carboxyl groups of the two HG chains interact with Ca2+ to form an “egg box” structure.

图2 拟南芥野生型和mur1突变体中的鼠李半乳糖醛酸聚糖II (RGII)二聚体(改自O’Neill et al. 2004; Atmodjo et al. 2013) 野生型植株中的鼠李半乳糖醛酸聚糖II二聚体由侧链A的芹菜糖残基通过硼酸二酯键共价交联而成。MUR1催化GDP-L-岩藻糖从头合成的第一步, MUR1功能缺失导致GDP-L-岩藻糖合成受阻。因此, mur1突变体中的鼠李半乳糖醛酸聚糖II侧链A被截断, 这一缺陷导致鼠李半乳糖醛酸聚糖II二聚体的形成减少。HG: 同型半乳糖醛酸聚糖; Api: 芹菜糖; Rha: L-鼠李糖; Fuc: L-岩藻糖; GlcA: D-葡萄糖醛酸; Gal: L-半乳糖; GalA: D-半乳糖醛酸; Me xyl: 2-O-甲基-D-木糖

Figure 2 Rhamngalacturonan II (RGII) dimer in Arabidopsis wild-type and mur1 mutants (modified from O’Neill et al. 2004; Atmodjo et al. 2013) In wild-type plants, RGII dimers are formed between Apiosyl residue of side chain A which are cross-linked covalently by the diester borate bonds. MUR1 catalyzes the first step in the de novo synthesis of GDP-L-fucose. The loss of MUR1 function leads to the block of GDP-L-fucose synthesis. Therefore, the RGII side chain A was truncated in mur1 mutants which resulted in reduced formation of RG-II dimers. HG: Homogalacturonan; Api: D-apiosyl; Rha: L-rhamnose; Fuc: L-fucose; GlcA: D-glucuronic acid; Gal: L-galactose; GalA: D-galacturonic acid; Me xyl: 2-O-methyl-D-xylose

参考文献 70

[1]	解敏敏, 晁江涛, 孔英珍 (2015). 参与木葡聚糖合成的糖基转移酶基因研究进展. 植物学报 50,644-651. DOI URL
[2]	易建勇, 毕金峰, 刘璇, 吕健, 周沫, 吴昕烨, 赵圆圆, 杜茜茜 (2020). 果胶结构域精细结构研究进展. 食品科学 41,292- 299.
[3]	郁有健, 沈秀萍, 曹家树 (2014). 植物细胞壁同聚半乳糖醛酸的代谢与功能. 中国细胞生物学学报 36,93-98.
[4]	查笑君, 马伯军, 潘建伟, 傅昭娟 (2010). 果胶酯酶的研究进展. 安徽农业科学 38,8293-8295.
[5]	张雨, 赵明洁, 张蔚 (2020). 植物次生细胞壁生物合成的转录调控网络. 植物学报 55,351-368.
[6]	Ahn JW, Verma R, Kim M, Lee JY, Kim YK, Bang JW, Reiter WD, Pai HS (2006). Depletion of UDP-D-apiose/ UDP-D-xylose synthases results in rhamnogalacturonan- II deficiency, cell wall thickening, and cell death in higher plants. J Biol Chem 281,13708-13716. DOI URL
[7]	Amsbury S, Hunt L, Elhaddad N, Baillie A, Lundgren M, Verhertbruggen Y, Scheller HV, Knox JP, Fleming AJ, Gray JE (2016). Stomatal function requires pectin de- methyl-esterification of the guard cell wall. Curr Biol 26,2899-2906. DOI URL
[8]	Anderson CT, Wallace IS, Somerville CR (2012). Metabolic click-labeling with a fucose analog reveals pectin delivery, architecture, and dynamics in Arabidopsis cell walls. Proc Natl Acad Sci USA 109,1329-1334. DOI URL
[9]	Arend M, Muninger M, Fromm J (2008). Unique occurrence of pectin-like fibrillar cell wall deposits in xylem fibres of poplar. Plant Biol (Stuttg) 10,763-770. DOI URL
[10]	Atmodjo MA, Hao ZY, Mohnen D (2013). Evolving views of pectin biosynthesis. Annu Rev Plant Biol 64,747-779. DOI URL
[11]	Atmodjo MA, Sakuragi Y, Zhu X, Burrell AJ, Mohanty SS, Atwood III JA, Orlando R, Scheller HV, Mohnen D (2011). Galacturonosyltransferase (GAUT)1 and GAUT7 are the core of a plant cell wall pectin biosynthetic homogalacturonan: galacturonosyltransferase complex. Proc Natl Acad Sci USA 108,20225-20230. DOI URL
[12]	Bidhendi AJ, Chebli Y, Geitmann A (2020). Fluorescence visualization of cellulose and pectin in the primary plant cell wall. J Microsc 278,164-181. DOI URL
[13]	Biswal AK, Atmodjo MA, Li M, Baxter HL, Yoo CG, Pu YQ, Lee YC, Mazarei M, Black IM, Zhang JY, Ramanna H, Bray AL, King ZR, LaFayette PR, Pattathil S, Donohoe BS, Mohanty SS, Ryno D, Yee K, Thompson OA, Rodriguez M Jr, Dumitrache A, Natzke J, Winkeler K, Collins C, Yang XH, Tan L, Sykes RW, Gjersing EL, Ziebell A, Turner GB, Decker SR, Hahn MG, Davison BH, Udvardi MK, Mielenz JR, Davis MF, Nelson RS, Parrott WA, Ragauskas AJ, Mohnen D, Stewart CN Jr, (2018). Sugar release and growth of biofuel crops are improved by downregulation of pectin biosynthesis. Nat Biotechnol 36,249-257.
[14]	Bosch M, Cheung AY, Hepler PK (2005). Pectin methylesterase, a regulator of pollen tube growth. Plant Physiol 138,1334-1346. DOI URL
[15]	Bouton S, Leboeuf E, Mouille G, Leydecker MT, Talbotec J, Granier F, Lahaye M, Höfte H, Truong HN (2002). QUASIMODO1 encodes a putative membrane-bound glycosyltransferase required for normal pectin synthesis and cell adhesion in Arabidopsis. Plant Cell 14, 2577-2590. DOI URL
[16]	Braccini I, Peréz S (2001). Molecular basis of Ca ²⁺-induced gelation in alginates and pectins: the egg-box model revisited. Biomacromolecules 2,1089-1096. DOI URL
[17]	Brutus A, Sicilia F, Macone A, Cervone F, De Lorenzo G (2010). A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. Proc Natl Acad Sci USA 107,9452- 9457. DOI URL
[18]	Caffall KH, Mohnen D (2009). The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydr Res 344,1879-1900. DOI URL
[19]	Cankar K, Kortstee A, Toonen MAJ, Wolters-Arts M, Houbein R, Mariani C, Ulvskov P, Jorgensen B, Schols HA, Visser RGF, Trindade LM (2014). Pectic arabinan side chains are essential for pollen cell wall integrity during pollen development. Plant Biotechnol J 12,492-502. DOI URL
[20]	Clausen MH, Willats WGT, Knox JP (2003). Synthetic methyl hexagalacturonate hapten inhibitors of anti-homogalacturonan monoclonal antibodies LM7, JIM5 and JIM7. Carbohydr Res 338,1797-1800. DOI URL
[21]	Cosgrove DJ (2005). Growth of the plant cell wall. Nat Rev Mol Cell Biol 6,850-861.
[22]	Cosgrove DJ, Jarvis MC (2012). Comparative structure and biomechanics of plant primary and secondary cell walls. Front Plant Sci 3,204.
[23]	Cui YN, Ling Y, Zhou JH, Li XJ (2015). Interference of the histone deacetylase inhibits pollen germination and pollen tube growth in Picea wilsonii mast. PLoS One 10,e0145661.
[24]	Delmas F, Séveno M, Northey JGB, Hernould M, Lerouge P, McCourt P, Chevalier C (2008). The synthesis of the rhamnogalacturonan II component 3-deoxy-D- manno-2- octulosonic acid (Kdo) is required for pollen tube growth and elongation. J Exp Bot 59,2639-2647.
[25]	Dumont M, Lehner A, Vauzeilles B, Malassis J, Marchant A, Smyth K, Linclau B, Baron A, Pons JM, Anderson CT, Schapman D, Galas L, Mollet JC, Lerouge P (2016). Plant cell wall imaging by metabolic click-mediated labelling of rhamnogalacturonan II using azido 3-deoxy-D- manno-oct-2-ulosonic acid. Plant J 85,437- 447.
[26]	Egelund J, Damager I, Faber K, Olsen CE, Ulvskov P, Petersen BL (2008). Functional characterisation of a putative rhamnogalacturonan II specific xylosyltransferase. FEBS Lett 582,3217-3222.
[27]	Egelund J, Petersen BL, Motawia MS, Damager I, Faik A, Olsen CE, Ishii T, Clausen H, Ulvskov P, Geshi N (2006). Arabidopsis thaliana RGXT1 and RGXT2 encode golgi-localized (1,3)-α-D-xylosyltransferases involved in the synthesis of pectic rhamnogalacturonan-II. Plant Cell 18,2593-2607.
[28]	Ferrari S, Savatin DV, Sicilia F, Gramegna G, Cervone F, De Lorenzo G (2013). Oligogalacturonides: plant damage-associated molecular patterns and regulators of growth and development. Front Plant Sci 4,49.
[29]	Funakawa H, Miwa K (2015). Synthesis of borate cross- linked rhamnogalacturonan II. Front Plant Sci 6,223.
[30]	Glushka JN, Terrell M, York WS, O'Neill MA, Gucwa A, Darvill AG, Albersheim P, Prestegard JH (2003). Primary structure of the 2- O-methyl-α-L-fucose-containing side chain of the pectic polysaccharide, rhamnogalacturonan II. Carbohydr Res 338,341-352.
[31]	Hamann T (2015). The plant cell wall integrity maintenance mechanism—a case study of a cell wall plasma membrane signaling network. Phytochemistry 112,100-109.
[32]	Harholt J, Jensen JK, Sørensen SO, Orfila C, Pauly M, Scheller HV (2006). ARABINAN DEFICIENT 1 is a putative arabinosyltransferase involved in biosynthesis of pectic arabinan in Arabidopsis. Plant Physiol 140,49-58.
[33]	Harholt J, Jensen JK, Verhertbruggen Y, Søgaard C, Bernard S, Nafisi M, Poulsen CP, Geshi N, Sakuragi Y, Driouich A, Knox JP, Scheller HV (2012). ARAD proteins associated with pectic arabinan biosynthesis form complexes when transiently overexpressed in planta. Planta 236,115-128.
[34]	Jiménez-Maldonado M, Tiznado-Hernández M, Rascón- Chu A, Carvajal-Millán E, Lizardi-Mendoza J, Troncoso-Rojas R (2018). Analysis of rhamnogalacturonan I fragments as elicitors of the defense mechanism in tomato fruit. Chil J Agric Res 78,339-349.
[35]	Kohorn BD, Kohorn SL, Saba NJ, Martinez VM (2014). Requirement for pectin methyl esterase and preference for fragmented over native pectins for wall-associated kinase-activated, eds1/pad4-dependent stress response in Arabidopsis. J Biol Chem 289,18978-18986.
[36]	Komarova TV, Sheshukova EV, Dorokhov YL (2014). Cell wall methanol as a signal in plant immunity. Front Plant Sci 5,101.
[37]	Lee KJD, Cornuault V, Manfield IW, Ralet MC, Knox JP (2013). Multi-scale spatial heterogeneity of pectic rhamnogalacturonan I (RG-I) structural features in tobacco seed endosperm cell walls. Plant J 75,1018-1027.
[38]	Li Z, Fernie AR, Persson S (2016). Transition of primary to secondary cell wall synthesis. Sci Bull 61,838-846.
[39]	Liu JP, Hayashi K, Matsuoka K (2015). Membrane topology of golgi-localized probable S-adenosylmethionine- dependent methyltransferase in tobacco ( Nicotiana tabacum) BY-2 cells. Biosci Biotechnol Biochem 79, 2007- 2013.
[40]	Liu XL, Liu LF, Niu QK, Xia CA, Yang KZ, Li R, Chen LQ, Zhang XQ, Zhou YH, Ye D (2011). MALE GAMETOPHYTE DEFECTIVE 4 encodes a rhamnogalacturonan II xylosyltransferase and is important for growth of pollen tubes and roots in Arabidopsis. Plant J 65,647-660.
[41]	Liwanag AJM, Ebert B, Verhertbruggen Y, Rennie EA, Rautengarten C, Oikawa A, Andersen MCF, Clausen MH, Scheller HV (2012). Pectin biosynthesis: GALS1 in Arabidopsis thaliana is a β-1,4-Galactan β-1,4-Galactosyltransferase. Plant Cell 24,5024-5036.
[42]	Logan B, Lei L, Li SD, Gu Y (2014). Cell wall, cytoskeleton, and cell expansion in higher plants. Mol Plant 7,586-600.
[43]	Matsunaga T, Ishii T, Matsumoto S, Higuchi M, Darvill A, Albersheim P, O'Neill MA (2004). Occurrence of the primary cell wall polysaccharide rhamnogalacturonan II in pteridophytes, lycophytes, and bryophytes. Implications for the evolution of vascular plants. Plant Physiol 134,339- 351.
[44]	McCartney L, Ormerod AP, Gidley MJ, Knox JP (2000). Temporal and spatial regulation of pectic (1→4)-β-D-galactan in cell walls of developing pea cotyledons: implications for mechanical properties. Plant J 22,105-113.
[45]	Micheli F (2001). Pectin methylesterases: cell wall enzymes with important roles in plant physiology. Trends Plant Sci 6,414-419.
[46]	Mohnen D (2008). Pectin structure and biosynthesis. Curr Opin Plant Biol 11,266-277.
[47]	Moller I, Marcus SE, Haeger A, Verhertbruggen Y, Verhoef R, Schols H, Ulvskov P, Mikkelsen JD, Knox JP, Willats W (2008). High-throughput screening of monoclonal antibodies against plant cell wall glycans by hierarchical clustering of their carbohydrate microarray binding profiles. Glycoconj J 25,37-48.
[48]	Moore JP, Farrant JM, Driouich A (2008). A role for pectin-associated arabinans in maintaining the flexibility of the plant cell wall during water deficit stress. Plant Signal Behav 3,102-104.
[49]	Mravec J, Kračun SK, Rydahl MG, Westereng B, Miart F, Clausen MH, Fangel JU, Daugaard M, Van Cutsem P, De Fine Licht HH, Hofte H, Malinovsky FG, Domozych DS, Willats WGT (2014). Tracking developmentally regulated post-synthetic processing of homogalacturonan and chitin using reciprocal oligosaccharide probes. Development 141,4841-4850.
[50]	Nebenfuhr A, Staehelin LA (2001). Mobile factories: golgi dynamics in plant cells. Trends Plant Sci 6,160-167.
[51]	O’Neill MA, Eberhard S, Albersheim P, Darvill AG (2001). Requirement of borate cross-linking of cell wall rhamnogalacturonan II for Arabidopsis growth. Science 294,846- 849.
[52]	O’Neill MA, Ishii T, Albersheim P, Darvill AG (2004). RHAMNOGALACTURONAN II: structure and function of a borate cross-linked cell wall pectic polysaccharide. Annu Rev Plant Biol 55,109-139.
[53]	Pabst M, Fischl RM, Brecker L, Morelle W, Fauland A, Köfeler H, Altmann F, Léonard R (2013). Rhamnogalacturonan II structure shows variation in the side chains monosaccharide composition and methylation status within and across different plant species. Plant J 76,61-72.
[54]	Panter PE, Kent O, Dale M, Smith SJ, Skipsey M, Thorlby G, Cummins I, Ramsay N, Begum RA, Sanhueza D, Fry SC, Knight MR, Knight H (2019). MUR1-mediated cell- wall fucosylation is required for freezing tolerance in Arabidopsis thaliana. New Phytol 224, 1518-1531.
[55]	Pattathil S, Avci U, Baldwin D, Swennes AG, McGill JA, Popper Z, Bootten T, Albert A, Davis RH, Chennareddy C, Dong RH, O’Shea B, Rossi R, Leoff C, Freshour G, Narra R, O’Neil M, York WS, Hahn MG (2010). A comprehensive toolkit of plant cell wall glycan-directed monoclonal antibodies. Plant Physiol 153,514-525.
[56]	Ralet MC, Tranquet O, Poulain D, Moïse A, Guillon F (2010). Monoclonal antibodies to rhamnogalacturonan I backbone. Planta 231,1373-1383.
[57]	Reuhs BL, Glenn J, Stephens SB, Kim JS, Christie DB, Glushka JG, Zablackis E, Albersheim P, Darvill AG, O’Neill MA (2004). L-galactose replaces l-fucose in the pectic polysaccharide rhamnogalacturonan II synthesized by the l-fucose-deficient mur1 Arabidopsis mutant. Planta 219,147-157.
[58]	Rostovtsev VV, Green LG, Fokin VV, Sharpless KB (2002). A stepwise huisgen cycloaddition process: copper(I)-catalyzed regioselective "ligation" of azides and terminal alkynes. Angew Chem Int Ed 41,2596-2599.
[59]	Sakamoto S, Somssich M, Nakata MT, Unda F, Atsuzawa K, Kaneko Y, Wang T, Bågman AM, Gaudinier A, Yoshida K, Brady SM, Mansfield SD, Persson S, Mitsuda N (2018). Complete substitution of a secondary cell wall with a primary cell wall in Arabidopsis. Nat Plants 4, 777- 783.
[60]	Scheller HV, Jensen JK, Sørensen SO, Harholt J, Geshi N (2007). Biosynthesis of pectin. Physiol Plant 129,283- 295.
[61]	Sebastian W, Grégory M, Jérome P (2009). Homogalacturonan methyl-esterification and plant development. Mol Plant 2,851-860.
[62]	Sterling JD, Atmodjo MA, Inwood SE, Kolli VSK, Quigley HF, Hahn MG, Mohnen D (2006). Functional identification of an Arabidopsis pectin biosynthetic homogalacturonan galacturonosyltransferase. Proc Natl Acad Sci USA 103,5236-5241.
[63]	Sujkowska-Rybkowska M, Borucki W (2015). Pectins esterification in the apoplast of aluminum-treated pea root nodules. J Plant Physiol 184,1-7.
[64]	Tornøe CW, Christensen C, Meldal M (2002). Peptidotriazoles on solid phase: [1,2,3]-triazoles by regiospecific copper(I)-catalyzed 1,3-dipolar cycloadditions of terminal alkynes to azides. J Org Chem 67,3057-3064.
[65]	Ulvskov P, Wium H, Bruce D, Jørgensen B, Qvist KB, Skjøt M, Hepworth D, Borkhardt B, Sørensen SO (2005). Biophysical consequences of remodeling the neutral side chains of rhamnogalacturonan I in tubers of transgenic potatoes. Planta 220,609-620.
[66]	Willats WGT, Steele-King CG, Marcus SE, Knox JP (1999). Side chains of pectic polysaccharides are regulated in relation to cell proliferation and cell differentiation. Plant J 20,619-628.
[67]	Wormit A, Usadel B (2018). The multifaceted role of pectin methylesterase inhibitors (PMEIs). Int J Mol Sci 19,2878.
[68]	Wu HY, Xu HM, Li HY, Wei DM, Lin JX, Li XJ (2016). Seasonal development of cambial activity in relation to xylem formation in Chinese fir. J Plant Physiol 195,23-30.
[69]	Zhang L, Paasch BC, Chen J, Day B, He SY (2019). An important role of L-fucose biosynthesis and protein fucosylation genes in Arabidopsis immunity. New Phytol 222,981-994.
[70]	Zhong RQ, Ye ZH (2015). Secondary cell walls: biosynthesis, patterned deposition and transcriptional regulation. Plant Cell Physiol 56,195-214.