Planta

, Volume 224, Issue 4, pp 782–791 | Cite as

Comprehensive expression profiling of the pectin methylesterase gene family during silique development in Arabidopsis thaliana

  • Romain Louvet
  • Emilie Cavel
  • Laurent Gutierrez
  • Stéphanie Guénin
  • David Roger
  • Françoise Gillet
  • François Guerineau
  • Jérôme Pelloux
Original Article

Abstract

Pectin methylesterases (PME, EC. 3.1.1.11) are enzymes that demethylesterify plant cell wall pectins in muro. In Arabidopsis thaliana, putative PME proteins are thought to be encoded by a 66-member gene family. This study used real-time RT-PCR to gain an overview of the expression of the entire family at eight silique developmental stages, in flower buds and in vegetative tissue in the Arabidopsis. Only 15% of the PMEs were not expressed at any of the developmental stages studied. Among expressed PMEs, expression data could be clustered into five distinct groups: 19 PMEs highly or uniquely expressed in floral buds, 4 PMEs uniquely expressed at mid-silique developmental stages, 16 PMEs highly or uniquely expressed in silique at late developmental stages, 16 PMEs mostly ubiquitously expressed, and 1 PME with a specific expression pattern, i.e. not expressed during early silique development. Comparison of expression and phylogenetic profiles showed that, within phylogenetic group 2, all but one PME belong to the floral bud expression group. Similar results were shown for a subset of one of the phylogenetic group, which differed from others by containing most of the PMEs that do not possess any PRO part next to their catalytic part. Expression data were confirmed by two promoter:GUS transgenic plant analysis revealing a PME expressed in pollen and one in young seeds. Our results highlight the high diversity of PME expression profiles. They are discussed with regard to the role of PMEs in fruit development and cell growth.

Keywords

Arabidopsis Cell wall Pectin methylesterase Silique Real-time RT-PCR 

Abbreviations

PME

Pectin methylesterase

RT-PCR

Reverse transcription polymerase chain reaction

DAF

Days after flowering

Notes

Acknowledgements

We thank Sylvain Jeandroz, (University of Nancy I, France) for help with the phylogenetic analysis, the CRRBM (Centre de Ressources Régionales en Biologie Moléculaire) for the use of the Roche LightCycler and the French Ministry of Research for the funding of Romain Louvet’s PhD. The technical assistance of Françoise Fournet is gratefully acknowledged.

Supplementary material

425_2006_261_MOESM1_ESM.doc (53 kb)
Supplementary material

References

  1. Alexandre F, Morvan O, Gaffe J, Mareck A, Jauneau A, Dauchel H, Balangé AP, Morvan C (1997) Pectin methylesterase pattern in flax seedlings during their development. Plant Physiol Biochem 35:427–436Google Scholar
  2. Al-Qsous S, Carpentier E, Klein-Eude D, Burel C, Mareck A, Dauchel H, Gomord V, Balangé AP (2004) Identification and isolation of a pectin methylesterase isoform that could be involved in flax cell wall stiffening. Planta 219:369–378PubMedCrossRefGoogle Scholar
  3. Barnavon L, Doco T, Terrier N., Ageorges A, Romieu C, Pellerin P (2001) Involvement of pectin methyl-esterase during the ripening of grape berries: partial cDNA isolation, transcript expression and changes in the degree of methyl-esterification of cell wall pectins. Phytochemistry 58:693–701PubMedCrossRefGoogle Scholar
  4. Baud S, Boutin JP, Miquel M, Lepiniec L, Rochat C (2002) An integrated overview of seed development in Arabidopsis thaliana ecotype WS. Plant Physiol Biochem 40:151–160CrossRefGoogle Scholar
  5. Bosch M, Cheung AY, Hepler PK (2005) Pectin methylesterase, a regulator of pollen tube growth. Plant Physiol 138:1334–1346PubMedCrossRefGoogle Scholar
  6. Castillejo C, Delafuente JI, Iannetta P, Botella MA, Valpuesta V (2004). Pectin esterase gene family in strawberry fruit. Study of FaPE1, a ripening-specific isoform. J Exp Bot 55:909–918PubMedCrossRefGoogle Scholar
  7. Chen MH, Citovsky V (2003) Systemic movement of a tobamovirus requires host cell pectin methylesterase. Plant J 35:386–392PubMedCrossRefGoogle Scholar
  8. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743PubMedCrossRefGoogle Scholar
  9. Cosgrove DJ (2001) Wall structure and wall loosening. A look backwards and forwards. Plant Physiol 125:131–134PubMedCrossRefGoogle Scholar
  10. Coutinho PM, Stam M, Blanc E, Henrissat B (2003) Why are there so many carbohydrate-active enzyme-related genes in plants? Trends Plant Sci 8:563–565PubMedCrossRefGoogle Scholar
  11. Czechowski T, Bari RP, Stitt M, Scheible WR, Udvardi MK (2004) Real-time RT-PCR profiling of over 1400 Arabidopsis transcription factors: unprecedented sensitivity reveals novel root- and shoot-specific genes. Plant J 38:366–379PubMedCrossRefGoogle Scholar
  12. De Folter S, Busscher J, Colombo L, Losa A, Angenent G (2004) Transcript profiling of transcription factor genes during silique development in Arabidopsis. Plant Mol Biol. 56:351–366PubMedCrossRefGoogle Scholar
  13. De Paepe A, Vuylsteke M, Van Hummelen P, Zabeau M, Van Der Straeten D (2004) Transcriptional profiling by cDNA-AFLP and microarray analysis reveals novel insights into the early response to ethylene in Arabidopsis. Plant J 39:537–559PubMedCrossRefGoogle Scholar
  14. Ebbelaar ME, Tucker GA, Laats MM, van Dijk C, Stolle-Smits T, Recourt K (1996) Characterization of pectinases and pectin methylesterase cDNAs in pods of green beans (Phaseolus vulgaris L.). Plant Mol Biol 31:1141–1151PubMedCrossRefGoogle Scholar
  15. Eriksson EM, Bovy A, Manning K, Harrison L, Andrews J, Da Silva J, Tucker GA, Seymour BG (2004) Effects of the colorless non ripening mutation on cell wall biochemistry and gene expression during tomato fruit development and ripening. Plant Physiol 136:4184–4197PubMedCrossRefGoogle Scholar
  16. Ferrandiz C (2002) Regulation of fruit dehiscence in Arabidopsis. J Exp Bot 53:2031–2038PubMedCrossRefGoogle Scholar
  17. Gehrig HH, Winter K, Cushman JC, Borland AM, Taybi T (2000) An improved RNA isolation method for succulent plant species rich in polyphenols and polysaccharides. Plant Mol Biol Rep 18:369–376CrossRefGoogle Scholar
  18. Giovane A, Servillo L, Balestrieri C, Raiola A, D’Avino R, Tamburrini M, Ciardiello MA, Camardella L (2004) Pectin methylesterase inhibitor. Biochim Biophys Acta Proteins Proteomics 1696:245–252CrossRefGoogle Scholar
  19. Goda H, Shimada Y, Asami T, Fujioka S, Yoshida S (2002) Microarray analysis of brassinosteroid-regulated genes in Arabidopsis. Plant Physiol 130:1319–1334PubMedCrossRefGoogle Scholar
  20. Goda H, Sawa S, Asami T, Fujioka S, Shimada Y, Yoshida S (2004) Comprehensive comparison of auxin-regulated and brassinosteroid-regulated genes in Arabidopsis. Plant Physiol 134:1555–1573PubMedCrossRefGoogle Scholar
  21. Jiang L, Yang S, Xie LF, Puah CS, Zhang XQ, Yang WC, Sundaresan V, Ye D (2005) VANGUARD1 encodes a pectin methylesterase that enhances pollen tube growth in the Arabidopsis style and transmitting tract. Plant Cell 17:584–596PubMedCrossRefGoogle Scholar
  22. Johansson K, El-Ahmad M, Friemann R, Jörnvall H, Markovic O, Eklund H (2002) Crystal structure of plant pectin methylesterase. FEBS Lett 514:551–555CrossRefGoogle Scholar
  23. Kim SY, Chung HJ, Thomas TL (1997) Isolation of a novel class of bZIP transcription factor that interact with ABA-responsive and embryo-specification elements in the Dc3 promoter using a modified yeast one-hybrid system. Plant J 11:1237–1251PubMedCrossRefGoogle Scholar
  24. Ko JH, Han KH, Park S, Yang J (2004) Plant body weight-induced secondary growth in Arabidopsis and its transcription phenotype revealed by whole-transcriptome profiling. Plant Physiol 135:1069–1083PubMedCrossRefGoogle Scholar
  25. Koch JL, Horbowicz M, Obendorf RL (1999) Methanol, pectin and pectin esterase changes during soybean seed maturation. Seed Sci Res 9:311–320CrossRefGoogle Scholar
  26. Kreps JA, Wu Y, Chang H-S, Zhu T, Wang X, Harper JH (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic and cold stress. Plant Physiol 130:2129–2141PubMedCrossRefGoogle Scholar
  27. Kumar S, Tamura K, Jakobsen IB, Nei M (2001) MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17:1244–1245PubMedCrossRefGoogle Scholar
  28. Lacoux J, Gutierrez L, Dantin F, Beaudoin B, Roger D, Lainé E (2003) Antisense transgenesis of tobacco with a flax pectin methylesterase affects pollen ornamentation. Protoplasma 222:205–209PubMedCrossRefGoogle Scholar
  29. Loreti E, Poggi A, Novi G, Alpi A, Perata P (2005) A genome-wide analysis of the effects of sucrose on gene expression in Arabidopsis seedlings under anoxia. Plant Physiol 137:1130–1138PubMedCrossRefGoogle Scholar
  30. Manfield IW, Orfila C, McCartney L, Harholt J, Bernal AJ, Vibe Scheller H, Gilmartin PM, Mikkelsen JD, Knox JP, Willats WGT (2004) Novel cell wall architecture of isobaxen-habituated Arabidopsis suspension cultured cells: global transcript profiling and cellular analysis. Plant J 40:260–275PubMedCrossRefGoogle Scholar
  31. Markovic O, Janecek S (2004) Pectin methylesterases: sequence–structural features and phylogenetic relationships. Carbohydr Res 339:2281–2295PubMedCrossRefGoogle Scholar
  32. Micheli F (2001) Pectin methylesterases: cell wall enzymes with important roles in plant physiology. Trends Plant Sci 6:414–419PubMedCrossRefGoogle Scholar
  33. Micheli F, Sundberg B, Goldberg R, Richard L (2000) Radial distribution pattern of pectin methylesterases across the cambial region of hybrid aspen at activity and dormancy. Plant Physiol 124:191–199PubMedCrossRefGoogle Scholar
  34. Nguyen BL, Van Loey A, Fachin D, Verlent I, Hendrickx IM (2002) Purification, characterization, thermal and high-presure inactivation of pectin methylesterase from bananas (cv. Cavendish). Biotechnol Bioeng 78:683–691CrossRefGoogle Scholar
  35. 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 220:582–592PubMedCrossRefGoogle Scholar
  36. Pina C, Pinto F, Jeijo JA, Becker JD (2005) Gene family analysis of the Arabidopsis pollen transcriptome reveals biological implications for cell growth, division control, and gene expression regulation. Plant Physiol 138:744–756PubMedCrossRefGoogle Scholar
  37. Ren C, Kermode AR (2000) An increase in pectin methyl esterase activity accompanies dormancy breakage and germination of yellow cedar seeds. Plant Physiol 124:231–242PubMedCrossRefGoogle Scholar
  38. Roberts JA, Whitelaw CA, Gonzalez-Carranza ZH, McManus MT (2000) Cell separation processes in plants: models, mechanisms and manipulation. Ann Bot 86:223–235CrossRefGoogle Scholar
  39. Rodrıguez-Llorente ID, Perez-Hormaeche J, El Mounadi K, Dary M, Caviedes MA, Cosson V, Kondorosi A, Ratet P, Palomares AJ (2004) From pollen tubes to infection threads: recruitment of Medicago floral pectic genes for symbiosis. Plant J 39:587–598PubMedCrossRefGoogle Scholar
  40. Schenk PM, Kazan K, Manners JM, Anderson JP, Simpson RS, Wilson IW, Somerville SC, Maclean DJ (2003) Systemic gene expression in Arabidopsis during an incompatible interaction with Alternaria brassicicola. Plant Physiol 132:999–1010PubMedCrossRefGoogle Scholar
  41. Stolle-Smits T, Beekhuizen JG, Kok MTC, Pijnenburg M, Recourt K, Derksen J, Voragen AGJ (1999) Changes in cell wall polysaccharides of green bean pods during development. Plant Physiol 121:363–372PubMedCrossRefGoogle Scholar
  42. Sutoh K, Yamauchi D (2003) Two cis-acting elements necessary and sufficient for gibberelin-upregulated proteinase expression in rice seeds. Plant J 34:636–645CrossRefGoogle Scholar
  43. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882CrossRefGoogle Scholar
  44. Verwoerd TC, Dekker BM, Hoekema A (1989). A small-scale procedure for the rapid isolation of plant RNAs. Nucleic Acids Res 17:2362PubMedCrossRefGoogle Scholar
  45. 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 160:667–673PubMedCrossRefGoogle Scholar
  46. Wakeley PR, Rogers HJ, Rozycka M, Greenland AJ, Hussey PJ (1998) A maize pectin methylesterase-like gene, ZmC5, specifically expressed in pollen. Plant Mol Biol 137:187–192CrossRefGoogle Scholar
  47. Willats WG, Orfila C, Limberg G, Buchholt HC, van Alebeek GJ, Voragen AG, Marcus SE, Christensen TM, Mikkelsen JD, Murray BS, Knox JP (2001) Modulation of the degree and pattern of methyl-esterification of pectic homogalacturonan in plant cell walls. Implications for pectin methyl esterase action, matrix properties, and cell adhesion. J Biol Chem 276:19404–19413PubMedCrossRefGoogle Scholar
  48. Wolf S, Grsic-Rausch S, Rausch T, Greiner S (2003) Identification of pollen-expressed pectin methylesterase inhibitors. FEBS Lett 555:551–555PubMedCrossRefGoogle Scholar
  49. Zhao C, Craig JC, Petzold HE, Dickerman AW, Beers E (2005) The xylem and phloem transcriptomes from secondary tissues of the Arabidopsis root-hypocotyl. Plant Physiol 138:803–818PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Romain Louvet
    • 1
  • Emilie Cavel
    • 1
  • Laurent Gutierrez
    • 1
    • 3
  • Stéphanie Guénin
    • 2
  • David Roger
    • 1
  • Françoise Gillet
    • 1
  • François Guerineau
    • 1
  • Jérôme Pelloux
    • 1
  1. 1.Groupe de Génomique Fonctionnelle des PlantesAmiensFrance
  2. 2.Centre de Ressources en Biologie MoléculaireUniversité de Picardie Jules VerneAmiensFrance
  3. 3.Umeå Plant Science CenterSwedish University of Agricultural Sciences (SLU)UmeaSweden

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