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Biologia Plantarum

, Volume 57, Issue 3, pp 410–416 | Cite as

Spatio-temporal distribution and methyl-esterification of pectic epitopes provide evidence of developmental regulation of pectins during somatic embryogenesis in Arabidopsis thaliana

  • K. Sala
  • I. Potocka
  • E. Kurczynska
Article

Abstract

The aim of the present study was to describe the occurrence of three pectic epitopes, recognized by JIM7, LM19, and LM5 antibodies, during somatic (SE) and zygotic (ZE) embryogenesis in Arabidopsis thaliana. The epitopes recognized by JIM7 and LM19 antibodies showed different distributions during SE stages. Moreover, in the early stages of somatic embryo development, a cytoplasmic occurrence of LM19 epitope was detected. Distribution of a pectic epitope recognized by LM5 antibody corresponded to a vascular system differentiation pattern. Occurrence of LM5 epitope was the same in both zygotic and somatic embryos and often restricted to newly synthesized walls of two adjacent cells. These data suggest that both low and high methyl-esterified pectins (recognized by LM19 and JIM7 antibodies, respectively) are developmentally regulated during SE stages and (1→4)-β-D-galactan epitope (recognized by LM5 antibody) may play a role in cell cytokinesis.

Additional key words

galactan immunofluorescence microscopy JIM7 LM19 and LM5 antibodies pectin methyl-esterification 

Abbreviations

HG

homogalacturonan

IZE

immature zygotic embryo

MS

Murashige and Skoog

PEGs

cuticular pegs

RG

rhamnogalacturonan

SAM

shoot apical meristem

SE

somatic embryogenesis

ZE

zygotic embryogenesis

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References

  1. Baluska, F., Samaj, J., Wojtaszek, P., Volkmann, D., Menzel, D.: Cytoskeleton-plasma membrane-cell wall continuum in plants. Emerging links revisited. — Plant Physiol. 133: 482–491, 2003.PubMedCrossRefGoogle Scholar
  2. Bobak, M., Samaj, J., Hlinkova, E., Hlavacka, A., Ovecka, M.: Extracellular matrix in early stages of direct somatic embryogenesis in leaves of Drosera spathulata. — Biol. Plant. 47: 161–166, 2003/4.CrossRefGoogle Scholar
  3. Bouton, S., Leboeuf, E., Mouille, G., Leydecker, M.-T., Talbotec, J., Granier, F., Lahaye, M., Höfte, H., Truong, H.-N.: QUASIMODO1 encodes a putative membrane-bound glycosyltransferase required for normal pectin synthesis and cell adhesion in Arabidopsis. — Plant Cell 14: 2577–2590, 2002.PubMedCrossRefGoogle Scholar
  4. Brownlee, C.: Role of the extracellular matrix in cell-cell signalling: paracrine paradigms. — Curr. Opin. Plant Biol. 5: 396–401, 2002.PubMedCrossRefGoogle Scholar
  5. Bush, M.S., McCann, M.C.: Pectic epitopes are differentially distributed in the cell walls of potato (Solanum tuberosum) tubers. — Physiol. Plant. 107: 201–213, 1999.CrossRefGoogle Scholar
  6. Bush, M.S., Marry, M., Huxham, M.I., Jarvis, M.C., McCann, M.C.: Developmental regulation of pectic epitopes during potato tuberisation. — Planta 213: 869–880, 2001.PubMedCrossRefGoogle Scholar
  7. Chapman, A., Blervacq, A.-S., Hendriks, T., Slomianny, C., Vasseur, J., Hilbert, J.-L.: Cell wall differentiation during early somatic embryogenesis in plants. II. Ultrastructural study and pectin immunolocalization on chicory embryos. — Can. J. Bot. 78: 824–831, 2000.Google Scholar
  8. Chen, W., Stoddard, F.L., Baldwin, T.C.: Developmental regulation of mannan, arabinogalactan-protein, and pectic epitopes in pistils of Vicia faba (faba bean). — Int. J. Plant Sci. 167: 919–932, 2006.CrossRefGoogle Scholar
  9. Dobrowolska, I., Majchrzak, O., Baldwin, T.C., Kurczynska, E.U.: Differences in protodermal cell wall structure in zygotic and somatic embryos of Daucus carota (L.) cultured on solid and in liquid media. — Protoplasma 249: 117–129, 2012.PubMedCrossRefGoogle Scholar
  10. Elviana, M., Rohani, E.R., Ismanizan, I., Normah, M.N.: Morphological and histological changes during the somatic embryogenesis of mangosteen. — Biol. Plant. 55: 731–736, 2011.CrossRefGoogle Scholar
  11. Ermel, F.F., Follet-Gueye, M.-L., Cibert, C., Vian, B., Morvan, C., Catesson, A.-M., Goldberg, R.: Differential localization of arabinan and galactan side chains of rhamnogalacturonan 1 in cambial derivatives. — Planta 210: 732–740, 2000.PubMedCrossRefGoogle Scholar
  12. Femenia, A., Garosi, P., Roberts, K., Waldron, K.W., Selvendran, R.R., Robertson, J.A.: Tissue-related changes in methyl-esterification of pectic polysaccharides in cauliflower (Brassica oleracea L. var. botrytis) stems. — Planta 205: 438–444, 1998.PubMedCrossRefGoogle Scholar
  13. Femenia, A., Waldron, K.W., Robertson, J.A., Selvendran, R.R.: Compositional and structural modification of the cell wall of cauliflower (Brassica oleracea L. var botrytis) during tissue development and plant maturation. — Carbohydr. Polymer. 39: 101–108, 1999.CrossRefGoogle Scholar
  14. Freshour, G., Clay, R.P., Fuller, M.S., Albersheim, P., Darvill, A.G., Hahn, M.G.: Developmental and tissue-specific structural alterations of the cell-wall polysaccharides of Arabidopsis thaliana roots. — Plant Physiol. 110: 1413–1429, 1996.PubMedGoogle Scholar
  15. Gaj, M.D.: Direct somatic embryogenesis as a rapid and efficient system for in vitro regeneration of Arabidopsis thaliana. — Plant Cell Tissue Organ Cult. 64: 39–46, 2001.CrossRefGoogle Scholar
  16. Gamborg, O.L., Miller, R.A., Ojima, K.: Nutrient requirements of suspension cultures of soybean root cells. — Exp. Cell Res. 50: 151–158, 1968.PubMedCrossRefGoogle Scholar
  17. Ikeda-Iwai, M., Satoh, S., Kamada, H.: Establishment of a reproducible tissue culture system for the induction of Arabidopsis somatic embryos. — J. exp. Bot. 53: 1575–1580, 2002.PubMedCrossRefGoogle Scholar
  18. Iwai, H., Kikuchi, A., Kobayashi, T., Kamada, H., Satoh, S.: High levels of non-methylesterified pectins and low levels of peripherally located pectins in loosely attached nonembryogenic callus of carrot. — Plant Cell Rep. 18: 561–566, 1999.CrossRefGoogle Scholar
  19. Jarvis, M.C.: Structure and properties of pectin gels in plant cell walls. — Plant Cell Environ. 7: 153–164, 1984.Google Scholar
  20. Jarvis, M.C., Briggs, S.P.H., Knox, J.P.: Intercellular adhesion and cell separation in plants. — Plant Cell Environ. 26: 977–989, 2003.CrossRefGoogle Scholar
  21. Jones, L., Seymour, G.B., Knox, J.P.: Localization of pectic galactan in tomato cell walls using a monoclonal antibody specific to (1→4)-β-D-galactan. — Plant Physiol. 113: 1405–1412, 1997.PubMedGoogle Scholar
  22. Kikuchi, A., Edashige, Y., Ishii, T., Fujii, T., Satoh, S.: Variations in the structure of neutral sugar chains in the pectic polysaccharides of morphologically different carrot calli and correlations with the size of cell clusters. — Planta 198: 634–639, 1996.PubMedCrossRefGoogle Scholar
  23. Knox, J.P.: Cell adhesion, cell separation and plant morphogenesis. — Plant J. 2: 137–141, 1992.CrossRefGoogle Scholar
  24. Knox, J.P., Linstead, P.J., King, J., Cooper, C., Roberts, K.: Pectin esterification is spatially regulated both within cell walls and between developing tissues of root apices. — Planta 181: 512–521, 1990.CrossRefGoogle Scholar
  25. Kohorn, B.D., Kobayashi, M., Johansen, S., Friedman, H.P., Fisher, A., Byers, N.: Wall-associated kinase 1 (WAK1) is crosslinked in endomembranes, and transport to the cell surface requires correct cell-wall synthesis. — J. Cell Sci. 119: 2282–2290, 2006.PubMedCrossRefGoogle Scholar
  26. Lai, K.S., Yusoff, K., Maziah, M.: Extracellular matrix as the early structural marker for Centella asiatica embryogenic tissues. — Biol. Plant. 55: 549–553, 2011.CrossRefGoogle Scholar
  27. Leboeuf, E., Thoiron, S., Lahaye, M.: Physico-chemical characteristics of cell walls from Arabidopsis thaliana microcalli showing different adhesion strengths. — J. exp. Bot. 55: 2087–2097, 2004.PubMedCrossRefGoogle Scholar
  28. Liners, F., Thibault, J.-F., Van Cutsem, P.: Influence of the degree of polymerization of oligogalacturonates and of esterification pattern of pectin on their recognition by monoclonal antibodies. — Plant Physiol. 99: 1099–1104, 1992.PubMedCrossRefGoogle Scholar
  29. McCartney, L., Knox, J.P.: Regulation of pectic polysaccharide domains in relation to cell development and cell properties in the pea testa. — J. exp. Bot. 53: 707–713, 2002.PubMedCrossRefGoogle Scholar
  30. McCartney, L., Ormerod, A.P., Gidley, M.J., Knox, J.P.: 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, 2000.PubMedCrossRefGoogle Scholar
  31. McCartney, L., Steele-King, C.G., Jordan, E., Knox, J.P.: Cell wall pectic (1→4)-β-D-galactan marks the acceleration of cell elongation in the Arabidopsis seedling root meristem. — Plant J. 33: 447–454, 2003.PubMedCrossRefGoogle Scholar
  32. Micheli, F.: Pectin methylesterases: cell wall enzymes with important roles in plant physiology. — Trends Plant Sci. 6: 414–419, 2001.PubMedCrossRefGoogle Scholar
  33. Mingozzi, M., Morini, S., Lucchesini, M., Mensuali-Sodi, A.: Effects of leaf soluble sugars content and net photosynthetic rate of quince donor shoots on subsequent morphogenesis in leaf explants. — Biol. Plant. 55: 237–242, 2011.CrossRefGoogle Scholar
  34. Mohnen, D.: Biosynthesis of pectins and galactomannans. — In: Pinto, B.M. (ed.): Comprehensive Natural Products Chemistry. Vol. 3. Carbohydrates and Their Derivatives Including Tannins, Cellulose, and Related Lignins. Pp. 497–527. Elsevier, Oxford 1999.Google Scholar
  35. Murashige, T., Skoog, F.: A revised medium for rapid growth and bio assays with tobacco tissue cultures. — Physiol. Plant. 15: 473–497, 1962.CrossRefGoogle Scholar
  36. Pan, X., Yang, X., Lin G., Zou, R., Chen, H., Samaj, J., Xu, C.: Ultrastructural changes and the distribution of arabinogalactan proteins during somatic embryogenesis of banana (Musa spp. AAA cv. ‘Yueyoukang 1’). — Physiol. Plant. 142: 372–389, 2011.PubMedCrossRefGoogle Scholar
  37. Pauly, M., Scheller, H.V.: 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, 2000.PubMedCrossRefGoogle Scholar
  38. Pena, M.J., Carpita, N.C.: Loss of highly branched arabinans and debranching of rhamnogalacturonan I accompany loss of firm texture and cell separation during prolonged storage of apple. — Plant Physiol. 135: 1305–1313, 2004.PubMedCrossRefGoogle Scholar
  39. Popielarska-Konieczna, M., Kozieradzka-Kiszkurno, M., Świerczyńska, J., Góralski, G., Ślesak, H., Bohdanowicz, J.: Are extracellular matrix surface network components involved in signalling and protective function? — Plant Signal. Behav. 3: 707–709, 2008.PubMedCrossRefGoogle Scholar
  40. Ramirez, C., Chiancone, B. Testillano, P.S., Garcia-Fojeda, B., Germana, M.-A., Risueno, M.-C.: First embryogenic stages of Citrus microspore-derived embryos. — Acta Biol. cracov. Ser. Bot. 45: 53–58, 2003.Google Scholar
  41. Ridley, B.L., O’Neill, M.A., Mohnen, D.: Pectins: structure, biosynthesis, and oligogalacturonide-related signaling. — Phytochemistry 57: 929–967, 2001.PubMedCrossRefGoogle Scholar
  42. Rose, J.K.C. (ed.): The Plant Cell Wall. — Blackwell, Oxford 2003.Google Scholar
  43. Satiat-Jeunemaitre, B., Hawes, C.: Immunocytochemistry for light microscopy. — In: Hawes, C., Satiat-Jeunemaitre, B. (ed.): Plant Cell Biology. A Practical Approach. Pp. 207–233. Oxford University Press, Oxford 2001.Google Scholar
  44. Siedlecka, A., Wiklund, S., Peronne, M.-A., Micheli, F., Leśniewska, J., Sethson, I., Edlund, U., Richard, L., Sundberg, B., Mellerowicz, E.J.: Pectin methyl esterase inhibits intrusive and symplastic cell growth in developing wood cells of Populus. — Plant Physiol. 146: 554–565, 2008.PubMedCrossRefGoogle Scholar
  45. Sobry, S., Havelange, A., Van Cutsem, P.: Immunocytochemistry of pectins in shoot apical meristems: consequences for intercellular adhesion. — Protoplasma 225: 15–22, 2005.PubMedCrossRefGoogle Scholar
  46. Ulvskov, P., Wium, H., Bruce, D., Jorgensen, B., Qvist, K.B., Skjot, M., Hepworth, D., Borkhardt, B., Sorensen, S.O.: Biophysical consequences of remodeling the neutral side chains of rhamnogalacturonan I in tubers of transgenic potatoes. — Planta 220: 609–620, 2005.PubMedCrossRefGoogle Scholar
  47. Verhertbruggen, Y., Marcus, S.E., Haeger, A., Ordaz-Ortiz, J.J., Knox, J.P.: An extended set of monoclonal antibodies to pectic homogalacturonan. — Carbohydr. Res. 344: 1858–1862, 2009.PubMedCrossRefGoogle Scholar
  48. Vitha, S., Baluska, F., Jasik, J., Volkmann, D., Barlow, P.W.: Steedman’s wax for F-actin visualization. — In: Staiger, C.J., Baluska, F., Volkmann, D., Barlow, P.W. (ed.): Actin: a Dynamic Framework for Multiple Plant Cell Function. Pp. 619–636. Kluwer Academic Publishers, Dordrecht 2000.CrossRefGoogle Scholar
  49. Willats, W.G.T., Knox, J.P., Mikkelsen, J.D.: Pectin: new insights into an old polymer are starting to gel. — Trends Food Sci. Technol. 17: 97–104, 2006.CrossRefGoogle Scholar
  50. Willats, W.G.T., McCartney, L., Mackie, W., Knox, J.P.: Pectin: cell biology and prospects for functional analysis. — Plant mol. Biol. 47: 9–27, 2001.PubMedCrossRefGoogle Scholar
  51. Willats, W.G.T., Steele-King, C.G., Marcus, S.E., Knox, J.P.: Side chains of pectic polysaccharides are regulated in relation to cell proliferation and cell differentiation. — Plant J. 20: 619–628, 1999.PubMedCrossRefGoogle Scholar
  52. Wiśniewska, E., Majewska-Sawka, A.: The differences in cell wall composition in leaves and regenerating protoplasts of Beta vulgaris and Nicotiana tabacum.— Biol. Plant. 52: 634–641, 2008.CrossRefGoogle Scholar
  53. Wolf, S., Mouille, G., Pelloux, J.: Homogalacturonan methyl esterification and plant development. — Mol. Plant 2: 851–860, 2009.PubMedCrossRefGoogle Scholar
  54. Xu, C., Zhao, L., Pan, X., Samaj, J.: Developmental localization and methylesterification of pectin epitopes during somatic embryogenesis of banana (Musa spp. AAA). — PLoS ONE 6: e22992, 2011.PubMedCrossRefGoogle Scholar
  55. Zhang, G.F., Staehelin, L.A.: Functional compartmentation of the Golgi apparatus of plant cells. — Plant Physiol. 99: 1070–1083, 1992.PubMedCrossRefGoogle Scholar
  56. Zimmerman, J.L.: Somatic embryogenesis: a model for early development in higher plants. — Plant Cell 5: 1411–1423, 1993.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Laboratory of Cell Biology, Faculty of Biology and Environmental ProtectionUniversity of SilesiaKatowicePoland

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