Location via proxy:   [ UP ]  
[Report a bug]   [Manage cookies]                
Skip to main content

Advertisement

Tuning of pectin methylesterification: consequences for cell wall biomechanics and development

  • Review
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

Recent publications have increased our knowledge of how pectin composition and the degree of homogalacturonan methylesterification impact the biochemical and biomechanical properties of plant cell walls, plant development, and plants’ interactions with their abiotic and biotic environments. Experimental observations have shown that the relationships between the DM, the pattern of de-methylesterificaton, its effect on cell wall elasticity, other biomechanical parameters, and growth are not straightforward. Working towards a detailed understanding of these relationships at single cell resolution is one of the big tasks of pectin research.

Pectins are highly complex polysaccharides abundant in plant primary cell walls. New analytical and microscopy techniques are revealing the composition and mechanical properties of the cell wall and increasing our knowledge on the topic. Progress in plant physiological research supports a link between cell wall pectin modifications and plant development and interactions with the environment. Homogalacturonan pectins, which are major components of the primary cell wall, have a potential for modifications such as methylesterification, as well as an ability to form cross-linked structures with divalent cations. This contributes to changing the mechanical properties of the cell wall. This review aims to give a comprehensive overview of the pectin component homogalacturonan, including its synthesis, modification, regulation and role in the plant cell wall.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Alonso-Simón A, García-Angulo P, Mélida H, Encina A, Álvarez JM, Acebes JL (2011) The use of FTIR spectroscopy to monitor modifications in plant cell wall architecture caused by cellulose biosynthesis inhibitors. Plant Signal Behav 6:1104–1110

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • An SH, Sohn KH, Choi HW, Hwang IS, Lee SC, Hwang BK (2008) Pepper pectin methylesterase inhibitor protein CaPMEI1 is required for antifungal activity, basal disease resistance and abiotic stress tolerance. Planta 228:61–78

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Atmodjo MA, Sakuragi Y, Zhu X, Burrell AJ, Mohanty SS, Atwood 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Baldwin L, Domon J-M, Klimek JF, Fournet F, Sellier H, Gillet F, Pelloux J, Lejeune-Hénaut I, Carpita NC, Rayon C (2014) Structural alteration of cell wall pectins accompanies pea development in response to cold. Phytochemistry 104:37–47

    Article  CAS  PubMed  Google Scholar 

  • Bethke G, Grundman RE, Sreekanta S, Truman W, Katagiri F, Glazebrook J (2014) Arabidopsis pectin methylesterases contribute to immunity against pseudomonas syringae. Plant Physiol 164:1093–1107

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bordenave M, Goldberg R (1993) Purification and characterization of pectin methylesterases from mung bean hypocotyl cell walls. Phytochemistry 33:999–1003

    Article  CAS  Google Scholar 

  • Bordenave M, Goldberg R, Huet JC, Pernollet JC (1995) A novel protein from mung bean hypocotyl cell walls with acetyl esterase activity. Phytochemistry 38:315–319

    Article  CAS  PubMed  Google Scholar 

  • Bosch M, Hepler PK (2005) Pectin methylesterases, a regulator of pollen tube growth. Plant Phys 38:1334–1346

    Article  CAS  Google Scholar 

  • Bouton S (2002) Quasimodo1 encodes a putative membrane-bound glycosyltransferase required for normal pectin synthesis and cell adhesion in arabidopsis. Plant Cell Online 14:2577–2590

    Article  CAS  Google Scholar 

  • Bowling AJ, Vaughn KC (2011) Leaf abscission in Impatiens (Balsaminaceae) is due to loss of highly de-esterified homogalacturonans in the middle lamellae. Am J Bot 98:619–629

    Article  PubMed  Google Scholar 

  • Braybrook SA, Peaucelle A (2013) Mechano-chemical aspects of organ formation in Arabidopsis thaliana: the relationship between auxin and pectin. PLoS One 8:e57813

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Braybrook SA, Hofte H, Peaucelle A (2012) Probing the mechanical contributions of the pectin matrix: insights for cell growth. Plant Signal Behav 7:1037–1041

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Burgert I, Keplinger T (2013) Plant micro- and nanomechanics: experimental techniques for plant cell-wall analysis. J Exp Bot 64:4635–4649

    Article  CAS  PubMed  Google Scholar 

  • Cabrera JC, Boland A, Messiaen J, Cambier P, Van Cutsem P (2008) Egg box conformation of oligogalacturonides: the time-dependent stabilization of the elicitor-active conformation increases its biological activity. Glycobiology 18:473–482

    Article  CAS  PubMed  Google Scholar 

  • Caffall KH, Mohnen D (2009) The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydr Res 344:1879–1900

    Article  CAS  PubMed  Google Scholar 

  • Cantu D, Vicente AR, Labavitch JM, Bennett AB, Powell ALT (2008) Strangers in the matrix: plant cell walls and pathogen susceptibility. Trends Plant Sci 13:610–617

    Article  CAS  PubMed  Google Scholar 

  • Catoire L, Pierron M, Morvan C, du Penhoat CH, Goldberg R (1998) Investigation of the action patterns of pectinmethylesterase isoforms through kinetic analyses and NMR spectroscopy. Implications In cell wall expansion. J Biol Chem 273:33150–33156

    Article  CAS  PubMed  Google Scholar 

  • Chatterjee M, Tabi Z, Galli M, Malcomber S, Buck A, Muszynski M, Gallavotti A (2014) The boron efflux transporter ROTTEN EAR is required for maize inflorescence development and fertility. Plant Cell 26:2962–2977

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chebli Y, Kaneda M, Zerzour R, Geitmann A (2012) The cell wall of the Arabidopsis pollen tube–spatial distribution, recycling, and network formation of polysaccharides. Plant Physiol 160:1940–1955

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chen M-H, Citovsky V (2003) Systemic movement of a tobamovirus requires host cell pectin methylesterase. Plant J 35:386–392

    Article  CAS  PubMed  Google Scholar 

  • Chormova D, Messenger DJ, Fry SC (2014a) Boron bridging of rhamnogalacturonan-II, monitored by gel electrophoresis, occurs during polysaccharide synthesis and secretion but not post-secretion. Plant J 77:534–546

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chormova D, Messenger DJ, Fry SC (2014b) Rhamnogalacturonan-II cross-linking of plant pectins via boron bridges occurs during polysaccharide synthesis and/or secretion. Plant Signal Behav, 9

  • Christensen TMIE, Nielsen JE, Mikkelsen JD (1996) Pectins and Pectinases, Proceedings of an International Symposium. Prog Biotechnol 14: 723–730

  • Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861

    Article  CAS  PubMed  Google Scholar 

  • Cosgrove DJ, Jarvis MC (2012) Comparative structure and biomechanics of plant primary and secondary cell walls. Front Plant Sci 3:204

    Article  PubMed Central  PubMed  Google Scholar 

  • Coutinho PM, Stam M, Blanc E, Henrissat B (2003) Why are there so many carbohydrate-active enzyme-related genes in plants? Trends Plant Sci 8:563–565

    Article  CAS  PubMed  Google Scholar 

  • Dardelle F, Lehner A, Ramdani Y, Bardor M, Lerouge P, Driouich A, Mollet J-C (2010) Biochemical and immunocytological characterizations of Arabidopsis pollen tube cell wall. Plant Physiol 153:1563–1576

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • De Souza A, Hull PA, Gille S, Pauly M (2014) Identification and functional characterization of the distinct plant pectin esterases PAE8 and PAE9 and their deletion mutants. Planta 240:1123–1138

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Dean GH, Zheng H, Tewari J, Huang J, Young DS, Hwang YT, Western TL, Carpita NC, McCann MC, Mansfield SD et al (2007) The Arabidopsis MUM2 gene encodes a beta-galactosidase required for the production of seed coat mucilage with correct hydration properties. Plant Cell 19:4007–4021

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Denès JM, Baron A, Renard CM, Péan C, Drilleau JF (2000) Different action patterns for apple pectin methylesterase at pH 7.0 and 4.5. Carbohydr Res 327:385–393

    Article  PubMed  Google Scholar 

  • Deng W, Iannetta PPM, Hallett PD, Toorop PE, Squire GR, Jeng D-S (2013) The rheological properties of the seed coat mucilage of Capsella bursa-pastoris L. Medik. (shepherd’s purse). Biorheology 50:57–67

    PubMed  Google Scholar 

  • Derbyshire P, McCann MC, Roberts K (2007) Restricted cell elongation in Arabidopsis hypocotyls is associated with a reduced average pectin esterification level. BMC Plant Biol 7:31

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Di Matteo A, Giovane A, Raiola A, Camardella L, Bonivento D, De Lorenzo G, Cervone F, Bellincampi D, Tsernoglou D (2005) Structural basis for the interaction between pectin methylesterase and a specific inhibitor protein. Plant Cell 17:849–858

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Diaz-Cacho P, Moral R, Encina A, Luis Acebes J, Alvarez J (1999) Cell wall modifications in bean (Phaseolus vulgaris) callus cultures tolerant to isoxaben. Physiol Plant 107:54–59

    Article  CAS  Google Scholar 

  • Dixit S, Upadhyay SK, Singh H, Sidhu OP, Verma PC (2013) Enhanced methanol production in plants provides broad spectrum insect resistance. PLoS One 8:79664

    Article  CAS  Google Scholar 

  • Dorokhov YL, Komarova TV, Petrunia IV, Frolova OY, Pozdyshev DV, Gleba YY (2012) Airborne signals from a wounded leaf facilitate viral spreading and induce antibacterial resistance in neighboring plants. PLoS Pathog 8:e1002640

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Driouich A, Follet-Gueye M-L, Bernard S, Kousar S, Chevalier L, Vicré-Gibouin M, Lerouxel O (2012) Golgi-mediated synthesis and secretion of matrix polysaccharides of the primary cell wall of higher plants. Front Plant Sci 3:79

    Article  PubMed Central  PubMed  Google Scholar 

  • Durand C, Vicré-Gibouin M, Follet-Gueye ML, Duponchel L, Moreau M, Lerouge P, Driouich A (2009) The organization pattern of root border-like cells of Arabidopsis is dependent on cell wall homogalacturonan. Plant Physiol 150:1411–1421

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Durbak AR, Phillips KA, Pike S, O’Neill MA, Mares J, Gallavotti A, Malcomber ST, Gassmann W, McSteen P (2014) Transport of boron by the tassel-less1 aquaporin is critical for vegetative and reproductive development in maize. Plant Cell 26:2978–2995

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Espino JJ, Gutiérrez-Sánchez G, Brito N, Shah P, Orlando R, González C (2010) The Botrytis cinerea early secretome. Proteomics 10:3020–3034

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Eticha D, Stass A, Horst WJ (2005) Cell-wall pectin and its degree of methylation in the maize root-apex: significance for genotypic differences in aluminium resistance. Plant Cell Environ 28:1410–1420

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fry SC (2004) Primary cell wall metabolism: tracking the careers of wall polymers in living plant cells. New Phytol 161:641–675

    Article  CAS  Google Scholar 

  • Gendre D, McFarlane HE, Johnson E, Mouille G, Sjödin A, Oh J, Levesque-Tremblay G, Watanabe Y, Samuels L, Bhalerao RP (2013) Trans-Golgi network localized ECHIDNA/Ypt interacting protein complex is required for the secretion of cell wall polysaccharides in Arabidopsis. Plant Cell 25:2633–2646

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gille S, de Souza A, Xiong G, Benz M, Cheng K, Schultink A, Reca I-B, Pauly M (2011) O-acetylation of Arabidopsis hemicellulose xyloglucan requires AXY4 or AXY4L, proteins with a TBL and DUF231 domain. Plant Cell 23:4041–4053

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gjetting KSK, Ytting CK, Schulz A, Fuglsang AT (2012) Live imaging of intra- and extracellular pH in plants using pHusion, a novel genetically encoded biosensor. J Exp Bot 63:3207–3218

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gou J-Y, Miller LM, Hou G, Yu X-H, Chen X-Y, Liu C-J (2012) Acetylesterase-mediated deacetylation of pectin impairs cell elongation, pollen germination, and plant reproduction. Plant Cell 24:50–65

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Guénin S, Mareck A, Rayon C, Lamour R, Assoumou Ndong Y, Domon J-M, Sénéchal F, Fournet F, Jamet E, Canut H et al (2011) Identification of pectin methylesterase 3 as a basic pectin methylesterase isoform involved in adventitious rooting in Arabidopsis thaliana. New Phytol 192:114–126

    Article  PubMed  CAS  Google Scholar 

  • Ha MA, Apperley DC, Jarvis MC (1997) Molecular Rigidity in Dry and Hydrated Onion Cell Walls. Plant Physiol 115:593–598

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hall H, Ellis B (2013) Transcriptional programming during cell wall maturation in the expanding Arabidopsis stem. BMC Plant Biol 13:14

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Harpaz-Saad S, Western TL, Kieber JJ (2012) The FEI2-SOS5 pathway and CELLULOSE SYNTHASE 5 are required for cellulose biosynthesis in the Arabidopsis seed coat and affect pectin mucilage structure. Plant Signal Behav 7:285–288

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Haughn G, Chaudhury A (2005) Genetic analysis of seed coat development in Arabidopsis. Trends Plant Sci 10:472–477

    Article  CAS  PubMed  Google Scholar 

  • Haughn GW, Western TL (2012) Arabidopsis seed coat mucilage is a specialized cell wall that can be used as a model for genetic analysis of plant cell wall structure and function. Front Plant Sci 3:64

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hayot CM, Forouzesh E, Goel A, Avramova Z, Turner JA (2012) Viscoelastic properties of cell walls of single living plant cells determined by dynamic nanoindentation. J Exp Bot 63:2525–2540

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hewezi T, Howe P, Maier TR, Hussey RS, Mitchum MG, Davis EL, Baum TJ (2008) Cellulose binding protein from the parasitic nematode Heterodera schachtii interacts with Arabidopsis pectin methylesterase: cooperative cell wall modification during parasitism. Plant Cell 20:3080–3093

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hongo S, Sato K, Yokoyama R, Nishitani K (2012) Demethylesterification of the primary wall by PECTIN METHYLESTERASE35 provides mechanical support to the Arabidopsis stem. Plant Cell 24:2624–2634

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hothorn M, Wolf S, Aloy P, Greiner S, Scheffzek K (2004) Structural insights into the target specificity of plant invertase and pectin methylesterase inhibitory proteins. Plant Cell 16:3437–3447

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ishii T (1997) O-acetylated oligosaccharides from pectins of potato tuber cell walls. Plant Physiol 113:1265–1272

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Iwai H, Masaoka N, Ishii T, Satoh S (2002) A pectin glucuronyltransferase gene is essential for intercellular attachment in the plant meristem. Proc Natl Acad Sci USA 99:16319–16324

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Iwai H, Hokura A, Oishi M, Chida H, Ishii T, Sakai S, Satoh S (2006) The gene responsible for borate cross-linking of pectin Rhamnogalacturonan-II is required for plant reproductive tissue development and fertilization. Proc Natl Acad Sci USA 103:16592–16597

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jiang L, Yang S-L, Xie L-F, Puah CS, Zhang X-Q, Yang W-C, Sundaresan V, Ye D (2005) Vanguard1 encodes a pectin methylesterase that enhances pollen tube growth in the Arabidopsis style and transmitting tract. Plant Cell 17:584–596

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kierzkowski D, Nakayama N, Routier-Kierzkowska A-L, Weber A, Bayer E, Schorderet M, Reinhardt D, Kuhlemeier C, Smith RS (2012) Elastic domains regulate growth and organogenesis in the plant shoot apical meristem. Science 335:1096–1099

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Komarova TV, Sheshukova EV, Dorokhov YL (2014) Cell wall methanol as a signal in plant immunity. Front Plant Sci 5:101

    Article  PubMed Central  PubMed  Google Scholar 

  • Körner E, von Dahl CC, Bonaventure G, Baldwin IT (2009) Pectin methylesterase NaPME1 contributes to the emission of methanol during insect herbivory and to the elicitation of defence responses in Nicotiana attenuata. J Exp Bot 60:2631–2640

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Krupková E, Immerzeel P, Pauly M, Schmülling T (2007) The tumorous shoot development2 gene of Arabidopsis encoding a putative methyltransferase is required for cell adhesion and co-ordinated plant development. Plant J 50:735–750

    Article  PubMed  CAS  Google Scholar 

  • Lau JM, McNeil M, Darvill AG, Albersheim P (1985) Structure of the backbone of rhamnogalacturonan I, a pectic polysaccharide in the primary cell walls of plants. Carbohydr Res 137:111–125

    Article  CAS  Google Scholar 

  • Leboeuf E, Guillon F, Thoiron S, Lahaye M (2005) Biochemical and immunohistochemical analysis of pectic polysaccharides in the cell walls of Arabidopsis mutant QUASIMODO 1 suspension-cultured cells: implications for cell adhesion. J Exp Bot 56:3171–3182

    Article  CAS  PubMed  Google Scholar 

  • Lehner A, Dardelle F, Soret-Morvan O, Lerouge P, Driouich A, Mollet J-C (2010) Pectins in the cell wall of Arabidopsis thaliana pollen tube and pistil. Plant Signal Behav 5:1282–1285

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Leroux C, Bouton S, Kiefer-Meyer M-C, Fabrice TN, Mareck A, Guénin S, Fournet F, Ringli C, Pelloux J, Driouich A et al (2015) Pectin methylesterase48 Is Involved in Arabidopsis Pollen Grain Germination. Plant Physiol 167:367–380

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Levesque-Tremblay G, Müller K, Mansfield SD, Haughn GW (2015) Highly methyl esterified seeds is a pectin methyl esterase involved in embryo development. Plant Physiol 167:725–737

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Liners F, Letesson JJ, Didembourg C, Van Cutsem P (1989) Monoclonal Antibodies against pectin: recognition of a conformation induced by calcium. Plant Physiol 91:1419–1424

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lionetti V, Raiola A, Camardella L, Giovane A, Obel N, Pauly M, Favaron F, Cervone F, Bellincampi D (2007) Overexpression of pectin methylesterase inhibitors in Arabidopsis restricts fungal infection by Botrytis cinerea. Plant Physiol 143:1871–1880

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lionetti V, Cervone F, Bellincampi D (2012) Methyl esterification of pectin plays a role during plant-pathogen interactions and affects plant resistance to diseases. J Plant Physiol 169:1623–1630

    Article  CAS  PubMed  Google Scholar 

  • Lionetti V, Raiola A, Cervone F, Bellincampi D (2014) Transgenic expression of pectin methylesterase inhibitors limits tobamovirus spread in tobacco and Arabidopsis. Mol Plant Pathol 15:265–274

    Article  CAS  PubMed  Google Scholar 

  • Lionetti V, Cervone F, De Lorenzo G (2015) A lower content of de-methylesterified homogalacturonan improves enzymatic cell separation and isolation of mesophyll protoplasts in Arabidopsis. Phytochemistry 112:188–194

    Article  CAS  PubMed  Google Scholar 

  • Lord EM, Mollet J-C (2002) Plant cell adhesion: a bioassay facilitates discovery of the first pectin biosynthetic gene. Proc Natl Acad Sci USA 99:15843–15845

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Louvet R, Cavel E, Gutierrez L, Guénin S, Roger D, Gillet F, Guerineau F, Pelloux J (2006) Comprehensive expression profiling of the pectin methylesterase gene family during silique development in Arabidopsis thaliana. Planta 224:782–791

    Article  CAS  PubMed  Google Scholar 

  • Ma L, Jiang S, Lin G, Cai J, Ye X, Chen H, Li M, Li H, Takác T, Samaj J et al (2013) Wound-induced pectin methylesterases enhance banana (Musa spp. AAA) susceptibility to Fusarium oxysporum f. sp. cubense. J Exp Bot 64:2219–2229

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Macarisin D, Wisniewski ME, Bassett C, Thannhauser TW (2009) Proteomic analysis of β-aminobutyric acid priming and abscisic acid—induction of drought resistance in crabapple (Malus pumila): effect on general metabolism, the phenylpropanoid pathway and cell wall enzymes. Plant Cell Environ 32:1612–1631

    Article  CAS  Google Scholar 

  • Manabe Y, Nafisi M, Verhertbruggen Y, Orfila C, Gille S, Rautengarten C, Cherk C, Marcus SE, Somerville S, Pauly M et al (2011) Loss-of-function mutation of reduced wall acetylation2 in Arabidopsis leads to reduced cell wall acetylation and increased resistance to Botrytis cinerea. Plant Physiol 155:1068–1078

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Manfield IW, Orfila C, McCartney L, Harholt J, Bernal AJ, Scheller HV, Gilmartin PM, Mikkelsen JD, Paul Knox J, Willats WGT (2004) Novel cell wall architecture of isoxaben-habituated Arabidopsis suspension-cultured cells: global transcript profiling and cellular analysis. Plant J 40:260–275

    Article  CAS  PubMed  Google Scholar 

  • Markovic O, Kohn R (1984) Mode of pectin deesterification by trichoderma reseei pectinesterase. Experientia 40:842–843

    Article  CAS  Google Scholar 

  • McFarlane HE, Watanabe Y, Gendre D, Carruthers K, Levesque-Tremblay G, Haughn GW, Bhalerao RP, Samuels L (2013) Cell wall polysaccharides are mislocalized to the Vacuole in echidna mutants. Plant Cell Physiol 54:1867–1880

    Article  CAS  PubMed  Google Scholar 

  • Micheli F (2001) Pectin methylesterases: cell wall enzymes with important roles in plant physiology. Trends Plant Sci 6:414–419

    Article  CAS  PubMed  Google Scholar 

  • Milani P, Braybrook SA, Boudaoud A (2013) Shrinking the hammer: micromechanical approaches to morphogenesis. J Exp Bot 64:4651–4662

    Article  CAS  PubMed  Google Scholar 

  • Mohnen D (2008) Pectin structure and biosynthesis. Curr Opin Plant Biol 11:266–277

    Article  CAS  PubMed  Google Scholar 

  • Mouille G, Ralet M-C, Cavelier C, Eland C, Effroy D, Hématy K, McCartney L, Truong HN, Gaudon V, Thibault J-F et al (2007) Homogalacturonan synthesis in Arabidopsis thaliana requires a Golgi-localized protein with a putative methyltransferase domain. Plant J 50:605–614

    Article  CAS  PubMed  Google Scholar 

  • Moulia B (2013) Plant biomechanics and mechanobiology are convergent paths to flourishing interdisciplinary research. J Exp Bot 64:4617–4633

    Article  CAS  PubMed  Google Scholar 

  • Moustacas AM, Nari J, Borel M, Noat G, Ricard J (1991) Pectin methylesterase, metal ions and plant cell-wall extension. The role of metal ions in plant cell-wall extension. Biochem J 279 (Pt 2: 351–4

  • Müller K, Tintelnot S, Leubner-Metzger G (2006) Endosperm-limited Brassicaceae seed germination: abscisic acid inhibits embryo-induced endosperm weakening of Lepidium sativum (cress) and endosperm rupture of cress and Arabidopsis thaliana. Plant Cell Physiol 47:864–877

    Article  PubMed  CAS  Google Scholar 

  • Müller K, Levesque-Tremblay G, Fernandes A, Wormit A, Bartels S, Usadel B, Kermode AR (2013a) Overexpression of a pectin methylesterase inhibitor in Arabidopsis thaliana leads to altered growth morphology of the stem and defective organ separation. Plant Signal Behav 8:e26464

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Müller K, Levesque-Tremblay G, Bartels S, Weitbrecht K, Wormit A, Usadel B, Haughn G, Kermode AR (2013b) Demethylesterification of cell wall pectins in Arabidopsis plays a role in seed germination. Plant Physiol 161:305–316

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Nakamura A, Furuta H, Maeda H, Takao T, Nagamatsu Y (2002) Structural studies by stepwise enzymatic degradation of the main backbone of soybean soluble polysaccharides consisting of galacturonan and rhamnogalacturonan. Biosci Biotechnol Biochem 66:1301–1313

    Article  CAS  PubMed  Google Scholar 

  • Neumetzler L, Humphrey T, Lumba S, Snyder S, Yeats TH, Usadel B, Vasilevski A, Patel J, Rose JKC, Persson S et al (2012) The FRIABLE1 gene product affects cell adhesion in Arabidopsis. PLoS ONE 7:e42914

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ogawa M, Kay P, Wilson S, Swain SM (2009) ARABIDOPSIS DEHISCENCE ZONE POLYGALACTURONASE1 (ADPG1), ADPG2, and QUARTET2 are Polygalacturonases required for cell separation during reproductive development in Arabidopsis. Plant Cell 21:216–233

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Osorio S, Castillejo C, Quesada MA, Medina-Escobar N, Brownsey GJ, Suau R, Heredia A, Botella MA, Valpuesta V (2008) Partial demethylation of oligogalacturonides by pectin methyl esterase 1 is required for eliciting defence responses in wild strawberry (Fragaria vesca). Plant J 54:43–55

    Article  CAS  PubMed  Google Scholar 

  • Parre E, Geitmann A (2005) Pectin and the role of the physical properties of the cell wall in pollen tube growth of Solanum chacoense. Planta 220:582–592

    Article  CAS  PubMed  Google Scholar 

  • Pauly M, Scheller HV (2000) O-Acetylation of plant cell wall polysaccharides: identification and partial characterization of a rhamnogalacturonan O-acetyl-transferase from potato suspension-cultured cells. Planta 210:659–667

    Article  CAS  PubMed  Google Scholar 

  • Peaucelle A, Louvet R, Johansen JN, Höfte H, Laufs P, Pelloux J, Mouille G (2008) Arabidopsis phyllotaxis is controlled by the methyl-esterification status of cell-wall pectins. Curr Biol 18:1943–1948

    Article  CAS  PubMed  Google Scholar 

  • Peaucelle A, Braybrook SA, Le Guillou L, Bron E, Kuhlemeier C, Höfte H (2011a) Pectin-induced changes in cell wall mechanics underlie organ initiation in Arabidopsis. Curr Biol 21:1720–1726

    Article  CAS  PubMed  Google Scholar 

  • Peaucelle A, Louvet R, Johansen JN, Salsac F, Morin H, Fournet F, Belcram K, Gillet F, Höfte H, Laufs P et al (2011b) The transcription factor BELLRINGER modulates phyllotaxis by regulating the expression of a pectin methylesterase in Arabidopsis. Development 138:4733–4741

    Article  CAS  PubMed  Google Scholar 

  • Pelletier S, Van Orden J, Wolf S, Vissenberg K, Delacourt J, Ndong YA, Pelloux J, Bischoff V, Urbain A, Mouille G et al (2010) A role for pectin de-methylesterification in a developmentally regulated growth acceleration in dark-grown Arabidopsis hypocotyls. New Phytol 188:726–739

    Article  CAS  PubMed  Google Scholar 

  • Pelloux J, Rustérucci C, Mellerowicz EJ (2007) New insights into pectin methylesterase structure and function. Trends Plant Sci 12:267–277

    Article  CAS  PubMed  Google Scholar 

  • Qu T, Liu R, Wang W, An L, Chen T, Liu G, Zhao Z (2011) Brassinosteroids regulate pectin methylesterase activity and AtPME41 expression in Arabidopsis under chilling stress. Cryobiology 63:111–117

    Article  CAS  PubMed  Google Scholar 

  • Raiola A, Lionetti V, Elmaghraby I, Immerzeel P, Mellerowicz EJ, Salvi G, Cervone F, Bellincampi D (2011) Pectin methylesterase is induced in Arabidopsis upon infection and is necessary for a successful colonization by necrotrophic pathogens. Mol Plant Microbe Interact 24:432–440

    Article  CAS  PubMed  Google Scholar 

  • Ralet M-C, Crépeau M-J, Lefèbvre J, Mouille G, Höfte H, Thibault J-F (2008) Reduced number of homogalacturonan domains in pectins of an Arabidopsis mutant enhances the flexibility of the polymer. Biomacromolecules 9:1454–1460

    Article  CAS  PubMed  Google Scholar 

  • Rautengarten C, Usadel B, Neumetzler L, Hartmann J, Büssis D, Altmann T (2008) A subtilisin-like serine protease essential for mucilage release from Arabidopsis seed coats. Plant J 54:466–480

    Article  CAS  PubMed  Google Scholar 

  • Rautengarten C, Ebert B, Moreno I, Temple H, Herter T, Link B, Doñas-Cofré D, Moreno A, Saéz-Aguayo S, Blanco F et al (2014) The Golgi localized bifunctional UDP-rhamnose/UDP-galactose transporter family of Arabidopsis. Proc Natl Acad Sci U S A 111:11563–11568

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ren C, Kermode AR (2000) An increase in pectin methyl esterase activity accompanies dormancy breakage and germination of yellow cedar seeds. Plant Physiol 124:231–242

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ridley BL, O’Neill MA, Mohnen D (2001) Pectins: structure, biosynthesis, and oligogalacturonide-related signaling. Phytochemistry 57:929–967

    Article  CAS  PubMed  Google Scholar 

  • Rocchi V, Janni M, Bellincampi D, Giardina T, D’Ovidio R (2012) Intron retention regulates the expression of pectin methyl esterase inhibitor (Pmei) genes during wheat growth and development. Plant Biol (Stuttg) 14:365–373

    Article  CAS  Google Scholar 

  • Röckel N, Wolf S, Kost B, Rausch T, Greiner S (2008) Elaborate spatial patterning of cell-wall PME and PMEI at the pollen tube tip involves PMEI endocytosis, and reflects the distribution of esterified and de-esterified pectins. Plant J 53:133–143

    Article  PubMed  CAS  Google Scholar 

  • Saez-Aguayo S, Ralet M-C, Berger A, Botran L, Ropartz D, Marion-Poll A, North HM (2013) Pectin methylesterase inhibitor6 promotes Arabidopsis mucilage release by limiting methylesterification of homogalacturonan in seed coat epidermal cells. Plant Cell 25:308–323

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Scheler C, Weitbrecht K, Pearce SP, Hampstead A, Büttner-Mainik A, Lee K, Voegele A, Oracz K, Dekkers B, Wang X et al (2014) Promotion of Testa Rupture during Lepidium sativum Germination Involves Seed Compartment-Specific Expression and Activity of Pectin Methylesterases. Plant Physiol 167:200–215

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Schmohl N, Pilling J, Fisahn J, Horst WJ (2000) Pectin methylesterase modulates aluminium sensitivity in Zea mays and Solanum tuberosum. Physiol Plant 109:419–427

    Article  CAS  Google Scholar 

  • Schopfer P (2006) Biomechanics of plant growth. Am J Bot 93:1415–1425

    Article  PubMed  Google Scholar 

  • Schuster E, Lundin L, Williams MAK (2012) Investigating the Relationship between Network Mechanics and Single-Chain Extension Using Biomimetic Polysaccharide Gels. Macromolecules 45:4863–4869

    Article  CAS  Google Scholar 

  • Sénéchal F, Graff L, Surcouf O, Marcelo P, Rayon C, Bouton S, Mareck A, Mouille G, Stintzi A, Höfte H et al (2014a) Arabidopsis PECTIN METHYLESTERASE17 is co-expressed with and processed by SBT3.5, a subtilisin-like serine protease. Ann Bot 114:1161–1175

    Article  PubMed  PubMed Central  Google Scholar 

  • Sénéchal F, Wattier C, Rustérucci C, Pelloux J (2014b) Homogalacturonan-modifying enzymes: structure, expression, and roles in plants. J Exp Bot 65:5125–5160

    Article  PubMed  PubMed Central  Google Scholar 

  • Sexton TR, Henry RJ, Harwood CE, Thomas DS, McManus LJ, Raymond C, Henson M, Shepherd M (2012) Pectin methylesterase genes influence solid wood properties of Eucalyptus pilularis. Plant Physiol 158:531–541

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shedletzky E, Shmuel M, Delmer DP, Lamport DT (1990) Adaptation and growth of tomato cells on the herbicide 2,6-dichlorobenzonitrile leads to production of unique cell walls virtually lacking a cellulose-xyloglucan network. Plant Physiol 94:980–987

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Siedlecka A, Wiklund S, Péronne M-A, Micheli F, Lesniewska J, Sethson I, Edlund U, Richard L, Sundberg B, Mellerowicz EJ (2008) Pectin methyl esterase inhibits intrusive and symplastic cell growth in developing wood cells of Populus. Plant Physiol 146:554–565

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Solecka D, Zebrowski J, Kacperska A (2008) Are pectins involved in cold acclimation and de-acclimation of winter oil-seed rape plants? Ann Bot 101:521–530

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Somerville C, Bauer S, Brininstool G, Facette M, Hamann T, Milne J, Osborne E, Paredez A, Persson S, Raab T et al (2004) Toward a systems approach to understanding plant cell walls. Science 306:2206–2211

    Article  CAS  PubMed  Google Scholar 

  • Staehelin LA, Moore I (1995) The Plant Golgi Apparatus: structure, Functional Organization and Trafficking Mechanisms. Annu Rev Plant Physiol Plant Mol Biol 46:261–288

    Article  CAS  Google Scholar 

  • Sterling JD, Quigley HF, Orellana A, Mohnen D (2001) The catalytic site of the pectin biosynthetic enzyme alpha-1,4-galacturonosyltransferase is located in the lumen of the Golgi. Plant Physiol 127:360–371

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tan L, Eberhard S, Pattathil S, Warder C, Glushka J, Yuan C, Hao Z, Zhu X, Avci U, Miller JS et al (2013) An Arabidopsis cell wall proteoglycan consists of pectin and arabinoxylan covalently linked to an arabinogalactan protein. Plant Cell 25:270–287

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tanino KK, Kobayashi S, Hyett C, Hamilton K, Liu J, Li B, Borondics F, Pedersen T, Tse J, Ellis T et al (2013) Physiol Plant 147:101–111

    Article  CAS  PubMed  Google Scholar 

  • Tian G-W, Chen M-H, Zaltsman A, Citovsky V (2006) Pollen-specific pectin methylesterase involved in pollen tube growth. Dev Biol 294:83–91

    Article  CAS  PubMed  Google Scholar 

  • Van Doorn WG, Hiemstra T, Fanourakis D (2011) Hydrogel regulation of xylem water flow: an alternative hypothesis. Plant Physiol 157:1642–1649

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Vicré M, Santaella C, Blanchet S, Gateau A, Driouich A (2005) Root border-like cells of Arabidopsis. Microscopical characterization and role in the interaction with rhizobacteria. Plant Physiol 138:998–1008

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Vincent RR, Williams MAK (2009) Microrheological investigations give insights into the microstructure and functionality of pectin gels. Carbohydr Res 344:1863–1871

    Article  CAS  PubMed  Google Scholar 

  • Voiniciuc C, Dean GH, Griffiths JS, Kirchsteiger K, Hwang YT, Gillett A, Dow G, Western TL, Estelle M, Haughn GW (2013) Flying saucer1 is a transmembrane RING E3 ubiquitin ligase that regulates the degree of pectin methylesterification in Arabidopsis seed mucilage. Plant Cell 25:944–959

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Volpi C, Janni M, Lionetti V, Bellincampi D, Favaron F, D’Ovidio R (2011) The ectopic expression of a pectin methyl esterase inhibitor increases pectin methyl esterification and limits fungal diseases in wheat. Mol Plant Microbe Interact 24:1012–1019

    Article  CAS  PubMed  Google Scholar 

  • Von Dahl CC, Hävecker M, Schlögl R, Baldwin IT (2006) Caterpillar-elicited methanol emission: a new signal in plant-herbivore interactions? Plant J 46:948–960

    Article  CAS  Google Scholar 

  • Vorwerk S, Somerville S, Somerville C (2004) The role of plant cell wall polysaccharide composition in disease resistance. Trends Plant Sci 9:203–209

    Article  CAS  PubMed  Google Scholar 

  • Wakabayashi K, Hoson T, Huber DJ (2003) Methyl de-esterification as a major factor regulating the extent of pectin depolymerization during fruit ripening: a comparison of the action of avocado (Persea americana) and tomato (Lycopersicon esculentum) polygalacturonases. J Plant Physiol 160:667–673

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Wang W, Wang Y-Q, Liu Y-Y, Wang J-X, Zhang X-Q, Ye D, Chen L-Q (2013a) Arabidopsis galacturonosyltransferase (GAUT) 13 and GAUT14 have redundant functions in pollen tube growth. Mol Plant 6:1131–1148

    Article  CAS  PubMed  Google Scholar 

  • Wang M, Yuan D, Gao W, Li Y, Tan J, Zhang X (2013b) A comparative genome analysis of PME and PMEI families reveals the evolution of pectin metabolism in plant cell walls. PLoS ONE 8:e72082

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Weber M, Deinlein U, Fischer S, Rogowski M, Geimer S, Tenhaken R, Clemens S (2013) A mutation in the Arabidopsis thaliana cell wall biosynthesis gene pectin methylesterase 3 as well as its aberrant expression cause hypersensitivity specifically to Zn. Plant J 76:151–164

    CAS  PubMed  Google Scholar 

  • Western TL, Skinner DJ, Haughn GW (2000) Differentiation of mucilage secretory cells of the Arabidopsis seed coat. Plant Physiol 122:345–356

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Western TL, Burn J, Tan WL, Skinner DJ, Martin-McCaffrey L, Moffatt BA, Haughn GW (2001) Isolation and characterization of mutants defective in seed coat mucilage secretory cell development in Arabidopsis. Plant Physiol 127:998–1011

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Whitcombe AJ, O’Neill MA, Steffan W, Albersheim P, Darvill AG (1995) Structural characterization of the pectic polysaccharide, rhamnogalacturonan-II. Carbohydr Res 271:15–29

    Article  CAS  PubMed  Google Scholar 

  • Willats WGT, McCartney L, Mackie W, Knox JP (2001) Pectin: cell biology and prospects for functional analysis. Plant Mol Biol 47:9–27

    Article  CAS  PubMed  Google Scholar 

  • Williamson G (1991) Purification and characterization of pectin acetylesterase from orange peel. Phytochemistry 30:445–449

    Article  CAS  Google Scholar 

  • Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ (2007) An “Electronic Fluorescent Pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS ONE 2:e718

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Wolf S, Mouille G, Pelloux J (2009a) Homogalacturonan methyl-esterification and plant development. Mol Plant 2:851–860

    Article  CAS  PubMed  Google Scholar 

  • Wolf S, Rausch T, Greiner S (2009b) The N-terminal pro region mediates retention of unprocessed type-I PME in the Golgi apparatus. Plant J 58:361–375

    Article  CAS  PubMed  Google Scholar 

  • Wolf S, Mravec J, Greiner S, Mouille G, Höfte H (2012) Plant cell wall homeostasis is mediated by brassinosteroid feedback signaling. Curr Biol 22:1732–1737

    Article  CAS  PubMed  Google Scholar 

  • Wu H-C, Hsu S-F, Luo D-L, Chen S-J, Huang W-D, Lur H-S, Jinn T-L (2010) Recovery of heat shock-triggered released apoplastic Ca2 + accompanied by pectin methylesterase activity is required for thermotolerance in soybean seedlings. J Exp Bot 61:2843–2852

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Xiong G, Cheng K, Pauly M (2013) Xylan O-acetylation impacts xylem development and enzymatic recalcitrance as indicated by the Arabidopsis mutant tbl29. Mol Plant 6:1373–1375

    Article  CAS  PubMed  Google Scholar 

  • Yang JL, Li YY, Zhang YJ, Zhang SS, Wu YR, Wu P, Zheng SJ (2008) Cell wall polysaccharides are specifically involved in the exclusion of aluminum from the rice root apex. Plant Physiol 146:602–611

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yang JL, Zhu XF, Zheng C, Zhang YJ, Zheng SJ (2011) Genotypic differences in Al resistance and the role of cell-wall pectin in Al exclusion from the root apex in Fagopyrum tataricum. Ann Bot 107:371–378

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yoneda A, Higaki T, Kutsuna N, Kondo Y, Osada H, Hasezawa S, Matsui M (2007) Chemical genetic screening identifies a novel inhibitor of parallel alignment of cortical microtubules and cellulose microfibrils. Plant Cell Physiol 48:1393–1403

    Article  CAS  PubMed  Google Scholar 

  • Yoneda A, Ito T, Higaki T, Kutsuna N, Saito T, Ishimizu T, Osada H, Hasezawa S, Matsui M, Demura T (2010) Cobtorin target analysis reveals that pectin functions in the deposition of cellulose microfibrils in parallel with cortical microtubules. Plant J 64:657–667

    Article  CAS  PubMed  Google Scholar 

  • Zablackis E, Huang J, Müller B, Darvill AG, Albersheim P (1995) Characterization of the cell-wall polysaccharides of Arabidopsis thaliana leaves. Plant Physiol 107:1129–1138

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zerzour R, Kroeger J, Geitmann A (2009) Polar growth in pollen tubes is associated with spatially confined dynamic changes in cell mechanical properties. Dev Biol 334:437–446

    Article  CAS  PubMed  Google Scholar 

  • Zhang GF, Staehelin LA (1992) Functional compartmentation of the Golgi apparatus of plant cells : immunocytochemical analysis of high-pressure frozen- and freeze-substituted sycamore maple suspension culture cells. Plant Physiol 99:1070–1083

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zwieniecki MA, Melcher PJ, Michele Holbrook NM (2001) Hydrogel control of xylem hydraulic resistance in plants. Science 291:1059–1062

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Sam Taylor for his help with this manuscript. The financial support from the NSERC Postgraduate Scholarships (to G.L.-T.), the Institut Universitaire de France (IUF) to J.P. and a Marie Curie International Outgoing Fellowship to K.M. is gratefully acknowledged.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kerstin Müller.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Levesque-Tremblay, G., Pelloux, J., Braybrook, S.A. et al. Tuning of pectin methylesterification: consequences for cell wall biomechanics and development. Planta 242, 791–811 (2015). https://doi.org/10.1007/s00425-015-2358-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-015-2358-5

Keywords