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Biologia Plantarum

, Volume 62, Issue 4, pp 763–774 | Cite as

In vitro regeneration of two Populus hybrid clones. The role of pectin domains in cell processes underlying shoot organogenesis induction

  • P. García-Angulo
  • I. Villar
  • L. Giner-Robles
  • M. L. Centeno
Original papers
  • 36 Downloads

Abstract

An efficient plant regeneration protocol has been established for two commercial Populus hybrid clones, MC (Populus × euramericana) and UNAL (Populus × interamericana). The culture of internode segments on Murashige and Skoog (MS) medium with 0.5 μM α-naphthalene acetic acid (NAA) and 4 μM N6-benzyladenine for 7 weeks (2 weeks in absence of activated charcoal and 5 weeks in its presence) resulted in the highest frequency of shoot regeneration (100 % for MC and 82 % for UNAL). All regenerated shoots longer than 2 cm rooted on half-strength MS medium, independent of the addition of 0.1 μM NAA. Nevertheless, shoots developed better-formed roots in NAA-free medium, which had a positive effect on the acclimatization of plants. In order to know the cellular processes underlying in vitro shoot organogenesis, a histological study was made in UNAL internode-explants. Results revealed that in vitro culture caused swelling around the cut-off zones in all explants, but only those undergoing organogenesis formed proliferation centers under subepidermal cells, which led to formation of bud primordia. Moreover, in vivo tissues and explants with different in vitro response showed different immunolabelling patterns when they were treated with fluorescentmonoclonal antibodies directed to several pectin-polysaccharides of the cell wall. Results allow us to assign a predominant role of homogalacturonan with a low degree of methyl-esterification in the initiation of bud primordia, a role of β-1,4-D-galactan side chains of rhamnogalacturonan-I in the cellular differentiation, ra ole of α-1,5-L-arabinan side chains of rhamnogalacturonan-I and of homogalacturonan with a high degree of methyl-esterification in cell division and growth.

Additional key words

cell wall homogalacturonan immunohistochemistry micropropagation poplar rhamnogalacturonan-I 

Abbreviations

AC

activated charcoal

BA

N6-benzyladenine

HG

homogalacturonan

NAA

a-naphthalene acetic acid

PBS

phosphate-buffered saline

PFD

photon flux density

PGR

plant growth regulator

RG-I

rhamnogalacturonan-I.

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Supplementary material

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References

  1. Arancibia, R.A., Motsenbocker, C.E.: Pectin methylesterase activity in vivo differs from activity in vitro and enhances polygalacturonase-mediated pectin degradation in tabasco pepper. - J. Plant Physiol. 163: 488–496, 2006.CrossRefPubMedGoogle Scholar
  2. Bao, Y., Dharmawardhana, P., Mockler, T.C., Strauss S.H.: Genome scale transcriptome analysis of shoot organogenesis in Populus. - BMC Plant Biol. 9: 132–154, 2009.CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bidhendi, A.J., Geitmann, A.: Relating the mechanics of the primary plant cell wall to morphogenesis. - J. exp. Bot. 67: 449–461, 2016.CrossRefPubMedGoogle Scholar
  4. Bosch, M., Hepler, P.K.: Pectin methylesterases and pectin dynamics in pollen tubes. - Plant Cell 17: 3219–3226, 2005.CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bush, M.S., Marry, M., Huxham, I.M., Jarvis, M.C., McCann, M.C.: Developmental regulation of pectic epitopes during potato tuberisation. - Planta 213: 869–880, 2001.CrossRefPubMedGoogle Scholar
  6. Caffall, K.H., Mohnen, D.: The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. - Carbohydr. Res. 344: 1879–1900, 2009.CrossRefPubMedGoogle Scholar
  7. Chaturvedi, H.C., Sharma, A.K., Agha, V.Q., Jain, M., Sharma, M.: Production of cloned trees of Populus deltoides through in vitro regeneration of shoots from leaf, stem and root explants and their field cultivation. - Indian J. Biotechnol. 2: 203–208, 2004.Google Scholar
  8. Chebli, Y., Geitmann, A.: Cellular growth in plants requires regulation of cell wall biochemistry. - Curr. Opin. cell. Biol. 44: 28–35, 2017.CrossRefPubMedGoogle Scholar
  9. Christianson, M.L., Warnick, D.A.: Temporal requirement for phytohormone balance in the control of organogenesis in vitro. - Dev. Biol. 112: 494–497, 1985.CrossRefGoogle Scholar
  10. Confalonieri, M., Balestrazzi, A., Bisoffi, S., Carbonera, D.: in vitro culture and genetic engineering of Populus spp.: synergy for forest tree improvement. - Plant Cell Tissue Organ Cult. 72: 109–138, 2003.CrossRefGoogle Scholar
  11. Cui, H.Y., Lee, H.S., Oh, Ch.Y., Han, S.H., Lee, K.J., Lee, H.J., Kang, K.S., Park, S.Y.: High-frequency regeneration by stem disc culture in selected clones of Populus - euramericana. - J. Plant Biotechnol. 41: 236–241, 2014.CrossRefGoogle Scholar
  12. Dong, N.G., Yin, W.L., Gao, Y., Pei, D.: Indole-3-acetic acid accumulation during poplar rhizogenesis revealed by immunohistochemistry. - Biol. Plant. 53: 581–584, 2012.CrossRefGoogle Scholar
  13. Duclercq, J., Sangwan-Norreel, B., Catterou, M., Sangwzn, R.S.: De novo shoot organogenesis: from art to science. - Trends Plant Sci. 16: 597–606, 2011.CrossRefPubMedGoogle Scholar
  14. Ferreira, S., Batista, D., Serrazina, S., Pais, M.S.: Morphogenesis induction and organogenic nodule differentiation in Populus euphratica Oliv. leaf explants. - Plant Cell Tissue Organ Cult. 72: 109–138, 2009.Google Scholar
  15. Gaur, A., Kumar, P., Thakur, A.K., Srivastava, D.K.: in vitro plant regeneration studies and their potential applications in Populus spp.: a review. - Israel J. Plant Sci. 63: 77–84, 2016.CrossRefGoogle Scholar
  16. Giri, C.C., Shyamkumar, B., Anjaneyulu, C.: Progress in tissue culture, genetic transformation and applications of biotechnology to trees: an overview. - Trees 18: 115–135, 2004.CrossRefGoogle Scholar
  17. Hoagland, D.R., Arnon, D.I.: The water culture method for growing plants without soil. - California Agr. Exp. Sta. Bull. 347: 32, 1938.Google Scholar
  18. Iordan-Costache, M., Lowe, K.C., Davey, M.R., Power, J.B.: Improved micropropagation of Populus spp. by Pluronic F-68. - Plant Growth Regul. 17: 233–239, 1995.CrossRefGoogle Scholar
  19. Janson, S., Douglas, C.J.: Populus: a model system for plant biology. - Annu. Rev. Plant Biol. 58: 435–458, 2007.CrossRefGoogle Scholar
  20. Jiang, C., Liu, Z., Zheng, Q.: Direct regeneration of plants derived form in vitro cultured shoots tips and leaves of poplar (Populus - euramericana 'Neva'). - J. Life Sci. 9: 366–372, 2015.Google Scholar
  21. Kang, B.G., Osburn, L., Kopsell, D., Tuskan, G.A., Cheng, Z.M.: Micropropagation of Populus trichocarpa 'Nisqually-1': the genotype deriving the Populus reference genome. - Plant Cell Tisue. Organ Cult. 99: 251–257, 2009.CrossRefGoogle Scholar
  22. Kwon, A.R., Cui, H.Y., Lee, H., Shin, H., Kang, K.S., Park, S.Y.: Light quality affects shoot regeneration, cell division, and wood formation in elite clones of Populus euramericana. - Acta Physiol. Plant. 37: 65, 2015.CrossRefGoogle Scholar
  23. Levesque-Tremblay, G., Pelloux, J., Braybrook, S.A.: Tuning of pectin methylesterification: consequences for cell wall biomechanics and development. - Planta 242: 791–811, 2015.CrossRefPubMedGoogle Scholar
  24. Li, S.W., Xue, L., Xu, S., Feng, H., An, L.: Mediators, genes and signalling in adventitious rooting. - Bot. Rev. 75: 230–247, 2009.CrossRefGoogle Scholar
  25. Lup, S.D., Tian, X., Xu, J., Pérez-Pereda, J.M.: Wound signaling of regenerative cell reprogramming. - Plant Sci. 250: 178–187, 2016.CrossRefPubMedGoogle Scholar
  26. Maheshwari, P., Kovalchuk, I.: Efficient shoot regeneration from internodal explants of Populus angustifolia, Populus balsaminifera and Populus deltoides. - New Biotechnol. 28: 778–787, 2011.CrossRefGoogle Scholar
  27. Mingozzi, M., Montello, P., Merkle, S.: Adventitious shoot regeneration from leaf explants of eastern cottonwood (Populus deltoides) cultured under photoautotrophic conditions. - Tree Physiol. 29: 333–343, 2008.CrossRefPubMedGoogle Scholar
  28. Mohnen, D.: Pectin structure and biosynthesis. - Plant Biol. 11: 266–277, 2008.Google Scholar
  29. Motte, H., Vereecke, D., Geelen, D., Werbrouck, S.: The molecular path to in vitro shoot regeneration. - Biotechnol. Adv. 32: 107–121, 2014.CrossRefPubMedGoogle Scholar
  30. Murashige, T., Skoog, F.: A revised medium for rapid growth and bioassays with tobacco tissue culture. - Physiol. Plant. 15: 473–479, 1962.CrossRefGoogle Scholar
  31. Noël, N., Leplé. J.C., Pilate. G.: Optimization of in vitro micropropagation and regeneration for Populus - interamericana and Populus × euramericana hybrids (P. deltoides, P. trichocarpa, and P. nigra). - Plant Cell Rep. 20: 1150–1155, 2002.CrossRefGoogle Scholar
  32. Peaucelle, A., Braybrook, S.A., Le Guillou, L., Bron, E., Kuhlemeier, C., Hofte, H.: Pectin-induced changes in cell wall mechanics underlie organ initiation in Arabidopsis. - Curr. Biol. 21: 1720–1726, 2011.CrossRefPubMedGoogle Scholar
  33. Peaucelle, A., Louvet, R., Johansen, J.N., Hofte, H., Laufs, P., Pelloux, J., Mouille, G.: Arabidopsis phyllotaxis is controlled by the methyl-esterification status of cell-wall pectins. - Curr. Biol. 18: 1943–1948, 2008.CrossRefPubMedGoogle Scholar
  34. Peaucelle, A., Wightman, R., Höfte, H.: The control of growth symmetry breaking in the Arabidopsis hypocotyl. - Curr. Biol. 25: 1746–1752, 2015.CrossRefPubMedGoogle Scholar
  35. Pelloux, J., Rustérucci, C., Mellerowicz, E.J.: New insights into pectin methylesterase structure and function. - Trends Plant Sci. 12: 267–277, 2007.CrossRefPubMedGoogle Scholar
  36. Ridley, B.L., ONeill, M.A., Mohnen, D.: Pectins: structure, biosynthesis, and oligogalacturonide-related signaling. - Phytochemistry 57: 929–967, 2001.CrossRefPubMedGoogle Scholar
  37. Scheller, H.V., Ulvskov, P.: Hemicelluloses. - Annu. Rev. Plant Biol. 61: 263–289, 2010.CrossRefPubMedGoogle Scholar
  38. Serpe, M.D., Muir, A.J., Keidel, A.M.: Localization of cell wall polysaccharides in non-articulated laticifers of Asclepias speciosa Torr. - Protoplasma 216: 215–226, 2001.CrossRefPubMedGoogle Scholar
  39. Sugimoto, K., Gordon, S.P., Meyerowitz.: Regeneration in plants and animals: dedifferentiation, transdifferentiation, or just differentiation? - Trends Cell Biol. 21: 212–218, 2011.CrossRefPubMedGoogle Scholar
  40. Thakur, A.K., Saraswat, A., Srivastava, D.K.: in vitro plant regeneration through direct organogenesis in Populus deltoides clone G48 from petiole explants. - J. Plant Biochem. Biotechnol. 21: 23–29, 2012.CrossRefGoogle Scholar
  41. Willats, W.G.T., McCartney, L., Mackie, W., Knox, P.: Pectin: cell biology for functional analysis. - Plant mol. Biol. 47: 9–27, 2001.CrossRefPubMedGoogle Scholar
  42. 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.CrossRefPubMedGoogle Scholar
  43. Wolf, S., Hématy, K., Höfte, H.: Growth control and cell wall signaling in plants. - Annu. Rev. Plant Biol. 63: 381–407, 2012.CrossRefPubMedGoogle Scholar
  44. Wolf, S., Mouille, G., Pelloux, J.: Homogalacturonan methylesterification and plant development. - Mol. Plant 2: 851–860, 2009.CrossRefPubMedGoogle Scholar
  45. Yadav, R., Arora, P., Kumar, D., Katlay, D., Dilbaghi, N., Chaudhury, A.: High frequency direct plant regeneration from leaf, internode, and root segments of eastern cottonwood (Populus deltoides). - Plant Biotechnol. Rep. 3: 175–182, 2009.CrossRefGoogle Scholar
  46. Zhao, X.Y., Su, Y.H., Cheng, Z.J., Zhang, X.S.: Cell fate switch during in vitro plant organogenesis. - J. Integr. Plant Biol. 50: 816–824, 2008.CrossRefPubMedGoogle Scholar
  47. Zykwinska, A.W., Ralet, M.C., Garnier, C.D., Thibault, J.F.: Evidence for in vitro binding of pectin side chains to cellulose. - Plant Physiol. 139: 397–407, 2005.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© The Institute of Experimental Botany 2018

Authors and Affiliations

  • P. García-Angulo
    • 1
  • I. Villar
    • 2
  • L. Giner-Robles
    • 3
  • M. L. Centeno
    • 1
  1. 1.Plant Physiology Laboratory, Department of Plant Engineering and SciencesUniversity of LeónLeónSpain
  2. 2.Experimental Centre of Aula Dei (CSIC)ZaragozaSpain
  3. 3.Biomedical and Biotechnological Institute of Cantabria Albert EinsteinSantanderSpain

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