Article | . 2017 Vol. 29, Issue. 1
Roles of Pectin Methylesterases and Pectin Methylesterase Inhibitors in Plant Physiology

Graduate School of Biotechnology, Kyung Hee University1

2017.. 1:17


Pectin, an enriched component in primary cell walls and middle lamellae, is an essential polysaccharide in all higher plants. Homogalacturonans (HGs), a major form of pectin, are synthesized and methyl-esterified by enzymes localized in the Golgi apparatus and transported into the cell wall. Depending on cell type, the degree and pattern of pectin methylesterification are strictly regulated by cell wall-localized pectin methylesterases (PMEs) which are governed by multiple pectin methylesterase inhibitors (PMEIs) in vivo. Pectin methylesterases (PMEs, EC, belonging to carbohydrate esterase family 8, cleave the ester bond between a galacturonic acid and an methyl group and the resulting change in pectin methylesterification status from which clearly impacts diverse plant developmental processes and stress responses. PMEs play major roles in modification of pectin properties, such as the stiffening by forming Ca2+-pectate cross-link complexes or loosening by triggering cell wall degrading enzymes (CWDE)s to break out cell wall components including pectin and its interactiors. The action of PMEIs results in opposite consequences to PMEs on pectin properties. Optimal pectin methylesterification status in each cell type is determined by the balance between PME activity and post-translational PME inhibition by PMEIs.

1. Al-Qsous, S., Carpentier, E., Klein-Eude, D., Burel, C., Mareck, A., Dauchel, H., Gomord, V., Balangé, A.P. (2004) Identification and isolation of a pectin methylesterase isoform that could be involved in flax cell wall stiffening. Planta 219:369-378.  

2. Andersson‐Gunnerås, S., Mellerowicz, E. J., Love, J., Segerman, B., Ohmiya, Y., Coutinho, P. M., Nilsson, P., Henrissat, B., Moritz, T., Sundberg, B. (2006) Biosynthesis of cellulose‐enriched tension wood in Populus: global analysis of transcripts and metabolites identifies biochemical and developmental regulators in secondary wall biosynthesis. The Plant Journal 45:144-165.  

3. Balestrieri, C., Castaldo, D., Giovane, A., Quagliuolo, L., Servillo, L. (1990) A glycoprotein inhibitor of pectin methylesterase in kiwi fruit (Actinidia chinensis). European Journal of Biochemistry 193:183-187.  

4. Benen, J., Van Alebeek, G., Voragen, A., Visser, J. (2003) Pectic esterases, Handbook of food enzymology, Dekker. pp. 849-856.  

5. Bewley, J. D. (1997) Seed germination and dormancy. The Plant Cell 9:1055.  

6. Boavida, L., Feijó, J., Becker, J. D. (2005) The making of gametes in higher plants.  

7. Bosch, M., Cheung, A. Y., Hepler, P. K. (2005) Pectin methylesterase, a regulator of pollen tube growth. Plant physiology 138:1334-1346.  

8. Bosch, M., Hepler, P. K. (2006) Silencing of the tobacco pollen pectin methylesterase NtPPME1 results in retarded in vivo pollen tube growth. Planta 223:736-745.  

9. Camardella, L., Carratore, V., Ciardiello, M. A., Servillo, L., Balestrieri, C., Giovane, A. (2000) Kiwi protein inhibitor of pectin methylesterase. European Journal of Biochemistry 267:4561-4565.  

10. Camardella, L., Giovane, A., Servillo, L. (2003) Structure-function of a proteinaceous inhibitor of plant pectin methylesterase, Advances in Pectin and Pectinase Research, Springer. pp. 363-372.  

11. Cantarel, B. L., Coutinho, P. M., Rancurel, C., Bernard, T., Lombard, V., Henrissat, B. (2009) The Carbohydrate- Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic acids research 37:D233-D238.  

12. Chanliaud, E., Gidley, M. J. (1999) In vitro synthesis and properties of pectin/Acetobacter xylinus cellulose composites. The Plant Journal 20:25-35.  

13. Cosgrove, D. J. (2005) Growth of the plant cell wall. Nature reviews molecular cell biology 6:850-861.  

14. Cosgrove, D. J., Jarvis, M. C. (2007) Comparative structure and biomechanics of plant primary and secondary cell walls. CURRENT CHALLENGES IN PLANT CELL WALLS.  

15. Darvill, A., McNeil, M., Albersheim, P., Delmer, D. (1980) The primary cell walls of flowering plants. The biochemistry of plants 1:91-162.  

16. D'Avino, R., Camardella, L., Christensen, T. M., Giovane, A., Servillo, L. (2003) Tomato pectin methylesterase: modeling, fluorescence, and inhibitor interaction studies—comparison with the bacterial (Erwinia chrysanthemi) enzyme. Proteins: Structure, Function, and Bioinformatics 53:830-839.  

17. 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. The Plant Cell 17:849-858.  

18. Dorokhov, Y. L., Skurat, E. V., Frolova, O. Y., Gasanova, T. V., Ivanov, P. A., Ravin, N. V., Skryabin, K. G., Mäkinen, K. M., Klimyuk, V. I., Gleba, Y. Y. (2006) Role of the leader sequence in tobacco pectin methylesterase secretion. FEBS letters 580:3329-3334.  

19. Francis, K. E., Lam, S. Y., Copenhaver, G. P. (2006) Separation of Arabidopsis pollen tetrads is regulated by QUARTET1, a pectin methylesterase gene. Plant physiology 142:1004-1013.  

20. Fry, S. C. (1988) The growing plant cell wall: chemical and metabolic analysis Longman Group Limited.  

21. Fry, S. C. (2004) Primary cell wall metabolism: tracking the careers of wall polymers in living plant cells. New phytologist 161:641-675.  

22. Gainvors, A., Frezier, V., Lemaresquier, H., Lequart, C., Aigle, M., Belarbi, A. (1994) Detection of polygalacturonase, pectin‐lyase and pectin‐esterase activities in a Saccharomyces cerevisiae strain. Yeast 10:1311-1319.  

23. Giovane, A., Balestrieri, C., Quagliuolo, L., Castaldo, D., Servillo, L. (1995) A glycoprotein inhibitor of pectin methylesterase in kiwi fruit. European Journal of Biochemistry 233:926-929.  

24. Giovane, A., Servillo, L., Balestrieri, C., Raiola, A., D'avino, R., Tamburrini, M., Ciardiello, M., Camardella, L. (2004) Pectin methylesterase inhibitor. Biochimica et Biophysica Acta (BBA)-Proteins and Proteomics 1696:245-252.  

25. Goldberg, R., Morvan, C., Jauneau, A., Jarvis, M. (1996) Methyl-esterification, de-esterification and gelation of pectins in the primary cell wall. Progress in biotechnology 14:151-172.  

26. Harriman, R. W., Tieman, D. M., Handa, A. K. (1991) Molecular cloning of tomato pectin methylesterase gene and its expression in Rutgers, ripening inhibitor, nonripening, and never ripe tomato fruits. Plant physiology 97:80-87.  

27. Jeong, H. Y., Nguyen, H. P., Lee, C. (2015) Genome-wide identification and expression analysis of rice pectin methylesterases: Implication of functional roles of pectin modification in rice physiology. Journal of plant physiology 183:23-29.  

28. Jiang, L., Yang, S.-L., Xie, L.-F., San Puah, C., 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. The Plant Cell 17:584-596.  

29. Jolie, R. P., Duvetter, T., Van Loey, A. M., Hendrickx, M. E. (2010) Pectin methylesterase and its proteinaceous inhibitor: a review. Carbohydrate Research 345:2583-2595.  

30. Kars, I., Krooshof, G. H., Wagemakers, L., Joosten, R., Benen, J. A., Van Kan, J. A. (2005) Necrotizing activity of five Botrytis cinerea endopolygalacturonases produced in Pichia pastoris. The Plant Journal 43:213-225.  

31. Keegstra, K. (2010) Plant cell walls. Plant physiology 154:483-486.  

32. Leroux, C., Bouton, S., Kiefer-Meyer, M.-C., Fabrice, T. N., Mareck, A., Guénin, S., Fournet, F., Ringli, C., Pelloux, J., Driouich, A. (2015) PECTIN METHYLESTERASE48 is involved in Arabidopsis pollen grain germination. Plant physiology 167:367-380.  

33. Levesque-Tremblay, G., Müller, K., Mansfield, S. D., Haughn, G. W. (2015a) HIGHLY METHYL ESTERIFIED SEEDS is a pectin methyl esterase involved in embryo development. Plant physiology 167:725-737.  

34. Levesque-Tremblay, G., Pelloux, J., Braybrook, S. A., Müller, K. (2015b) Tuning of pectin methylesterification: consequences for cell wall biomechanics and development. Planta 242:791-811.  

35. Lievens, S., Goormachtig, S., Herman, S., Holsters, M. (2002) Patterns of pectin methylesterase transcripts in developing stem nodules of Sesbania rostrata. Molecular plant-microbe interactions 15:164-168.  

36. Manz, B., Müller, K., Kucera, B., Volke, F., Leubner-Metzger, G. (2005) Water uptake and distribution in germinating tobacco seeds investigated in vivo by nuclear magnetic resonance imaging. Plant physiology 138:1538-1551.  

37. Ma, R., Reese, J. C., Black, W. C., Bramel-Cox, P. (1990) Detection of pectinesterase and polygalacturonase from salivary secretions of living greenbugs, Schizaphis graminum (Homoptera: Aphididae). Journal of Insect Physiology 36:507-512.  

38. Markovič, O., Janeček, Š. (2004) Pectin methylesterases: sequence-structural features and phylogenetic relationships. Carbohydrate Research 339:2281-2295.  

39. Mei, X., Shpigelman, A., Verrijssen, T. A., Kyomugasho, C., Luo, Y., Van Loey, A. M., Michiels, C., Huang, K., Hendrickx, M. E. (2015) Recombinant kiwi pectin methylesterase inhibitor: Purification and characterization of the interaction with plant pectin methylesterase during thermal and high-pressure processing. Innovative Food Science & Emerging Technologies 29:295-301.  

40. Micheli, F. (2001) Pectin methylesterases: cell wall enzymes with important roles in plant physiology. Trends in plant science 6:414-419.  

41. 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 physiology 124:191-200.  

42. Mohnen, D. (2008) Pectin structure and biosynthesis. Current opinion in plant biology 11:266-277.  

43. Moustacas, A.-M., 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. Biochemical journal 279:351-354.  

44. 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 and Cell Physiology 47:864-877.  

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

46. Nguyen, H. P., Jeong, H. Y., Kim, H., Kim, Y. C., Lee, C. (2016) Molecular and biochemical characterization of rice pectin methylesterase inhibitors (OsPMEIs). Plant Physiology and Biochemistry 101:105-112.  

47. Ochoa-Villarreal, M., Aispuro-Hernández, E., Vargas-Arispuro, I., Martínez-Téllez, M. Á. (2012) Plant cell wall polymers: function, structure and biological activity of their derivatives. Polymerization 4:63-86.  

48. Owen, H. A., Makaroff, C. (1995) Ultrastructure of microsporogenesis and microgametogenesis inArabidopsis thaliana (L.) Heynh. ecotype Wassilewskija (Brassicaceae). Protoplasma 185:7-21.  

49. Palin, R., Geitmann, A. (2012) The role of pectin in plant morphogenesis. Biosystems 109:397-402.  

50. 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.  

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

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

53. Pelloux, J., Rusterucci, C., Mellerowicz, E. J. (2007) New insights into pectin methylesterase structure and function. Trends in plant science 12:267-277.  

54. Phan, T. D., Bo, W., West, G., Lycett, G. W., Tucker, G. A. (2007) Silencing of the major salt-dependent isoform of pectinesterase in tomato alters fruit softening. Plant physiology 144:1960-1967.  

55. Pinzón-Latorre, D., Deyholos, M. K. (2013) Characterization and transcript profiling of the pectin methylesterase (PME) and pectin methylesterase inhibitor (PMEI) gene families in flax (Linum usitatissimum). BMC Genomics 14:742.  

56. Preuss, D., Rhee, S. Y., Davis, R. W. (1994) Tetrad analysis possible in Arabidopsis with mutation of the QUARTET (QRT) genes. Science 264:1458-1460.  

57. Reca, I. B., Lionetti, V., Camardella, L., D’Avino, R., Giardina, T., Cervone, F., Bellincampi, D. (2012) A functional pectin methylesterase inhibitor protein (SolyPMEI) is expressed during tomato fruit ripening and interacts with PME-1. Plant molecular biology 79:429-442.  

58. Ren, C., Kermode, A. R. (2000) An increase in pectin methyl esterase activity accompanies dormancy breakage and germination of yellow cedar seeds. Plant physiology 124:231-242.  

59. Rhee, S. Y., Osborne, E., Poindexter, P. D., Somerville, C. R. (2003) Microspore separation in the quartet 3 mutants of Arabidopsis is impaired by a defect in a developmentally regulated polygalacturonase required for pollen mother cell wall degradation. Plant physiology 133:1170-1180.  

60. Ridley, B. L., O'Neill, M. A., Mohnen, D. (2001) Pectins: structure, biosynthesis, and oligogalacturonide-related signaling. Phytochemistry 57:929-967.  

61. 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. The Plant Journal 53:133-143.  

62. Saez-Aguayo, S., Ralet, M.-C., Berger, A., Botran, L., Ropartz, D., Marion-Poll, A., North, H. M. (2013) PECTIN METHYLESTERASE INHIBITOR6 promotes Arabidopsis mucilage release by limiting methylesterification of homogalacturonan in seed coat epidermal cells. The Plant Cell 25:308-323.  

63. Scheler, C., Weitbrecht, K., Pearce, S. P., Hampstead, A., Büttner-Mainik, A., Lee, K. J., Voegele, A., Oracz, K., Dekkers, B. J., Wang, X. (2015) Promotion of testa rupture during garden cress germination involves seed compartment-specific expression and activity of pectin methylesterases. Plant physiology 167:200-215.  

64. Scheller, H. V., Ulvskov, P. (2010) Hemicelluloses. Plant Biology 61:263.  

65. Schmohl, N., Pilling, J., Fisahn, J., Horst, W. J. (2000) Pectin methylesterase modulates aluminium sensitivity in Zea mays and Solanum tuberosum. Physiologia Plantarum 109:419-427.  

66. Sénéchal, F., Mareck, A., Marcelo, P., Lerouge, P., Pelloux, J. (2015a) Arabidopsis PME17 Activity can be Controlled by Pectin Methylesterase Inhibitor4. Plant signaling & behavior 10:e983351.  

67. Sénéchal, F., L'Enfant, M., Domon, J.-M., Rosiau, E., Crépeau, M.-J., Surcouf, O., Esquivel-Rodriguez, J., Marcelo, P., Mareck, A., Guérineau, F. (2015b) Tuning of pectin methylesterification pectin methylesterase inhibitor 7 modulates the processive activity of co-expressed pectin methylesterase 3 in a pH-dependent manner. Journal of Biological Chemistry 290:23320-23335.  

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

69. Srivastava, S., Gupta, S. M., Sane, A. P., Nath, P. (2012) Isolation and characterization of ripening related pectin methylesterase inhibitor gene from banana fruit. Physiology and Molecular Biology of Plants 18:191-195.  

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

71. Tieman, D. M., Handa, A. K. (1994) Reduction in pectin methylesterase activity modifies tissue integrity and cation levels in ripening tomato (Lycopersicon esculentum Mill.) fruits. Plant physiology 106:429-436.  

72. Tucker, G. A., Robertson, N. G., Grierson, D. (1982) Purification and changes in activities of tomato pectinesterase isoenzymes. Journal of the Science of Food and Agriculture 33:396-400.  

73. Turbant, A., Fournet, F., Lequart, M., Zabijak, L., Pageau, K., Bouton, S., Van Wuytswinkel, O. (2016) PME58 plays a role in pectin distribution during seed coat mucilage extrusion through homogalacturonan modification. Journal of experimental botany 67:2177-2190.  

74. Vandevenne, E., Van Buggenhout, S., Duvetter, T., Brouwers, E., Declerck, P. J., Hendrickx, M. E., Van Loey, A., Gils, A. (2009) Development and evaluation of monoclonal antibodies as probes to assess the differences between two tomato pectin methylesterase isoenzymes. Journal of immunological methods 349:18-27.  

75. Wolf, S., Mouille, G., Pelloux, J. (2009) Homogalacturonan methyl-esterification and plant development. Molecular plant 2:851-860.  

76. 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. The Plant Journal 64:657-667.  

77. Zandleven, J., Sørensen, S. O., Harholt, J., Beldman, G., Schols, H. A., Scheller, H. V., Voragen, A. J. (2007) Xylogalacturonan exists in cell walls from various tissues of Arabidopsis thaliana. Phytochemistry 68:1219-1226.  

online submission
online submission
online submission
online submission
Sub Menu
Sub Banner
Sub Banner
Sub Menu
Sub Banner
Sub Banner
Sub Banner
Sub Banner
Sub Menu
Sub Menu