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Role of PtrXTH1 and PnXTH1 Genes Encoding Xyloglucan Endo-Transglycosylases in Regulation of Growth and Adaptation of Plants to Stress Factors

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Abstract

The expression level of the gene PtrXTH1 encoding xyloglucan endo-transglycosylase in the leaves of Populus tremula L. of wild-type and in response to exogenous phytohormones treatment was analyzed. The highest level of transcripts of PtrXTH1 was detected in young, intensively growing leaves of aspen. In young aspen leaves, the expression of PtrXTH1 was induced by cytokinins, auxins, and brassinosteroids. The content of PtrXTH1 transcripts increased under the constitutive expression of the PnARGOS-LIKE gene. Bioinformatic analysis of PtXTH1 putative promoter region in P. trichocarpa Torr. and A. Gray ex. Hook showed the presence of cis-regulatory elements associated with the regulation of growth and stress resistance. To determine the role of the gene under study, we also created transgenic tobacco plants with constitutive expression of the PnXTH1 gene (the ortholog of PtrXTH1 from the black poplar P. nigra). Transgenic tobacco plants were characterized by an increase in leaf size and fresh and dry weight of the aboveground part under normal growth conditions. When grown under conditions of salinization and drought, transgenic plants were distinguished by increased stress resistance due to the maintenance of cell expansion in roots and stems at a higher level and the ability to more effectively retain water in leaves compared with wild-type plants.

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References

  1. Gonzalez, N., Vanhaeren, H., and Inze, D., Leaf size control: complex coordination of cell division and expansion, Trends Plant Sci., 2012, vol. 17, pp. 332–340.

    Article  CAS  PubMed  Google Scholar 

  2. Inouhe, M. and Nevins, D.J., Inhibition of auxininduced cell elongation of maize coleoptiles by antibodies specific for cell wall glucanases, Plant Physiol., 1991, vol. 96, pp. 426–431.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Eklof, J.M. and Brumer, H., The XTH gene family: an update on enzyme structure, function, and phylogeny in xyloglucan remodeling, Plant Physiol., 2010, vol. 153, pp. 456–466.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Dal Santo, S., Fasoli, M., Cavallini, E., Tornielli, G.B., Pezzotti, M., and Zenoni, S., PhEXPA1, a Petunia hybrida expansin, is involved in cell wall metabolism and in plant architecture specification, Plant Signal. Behav., 2011, vol. 6, pp. 2031–2034.

    Article  Google Scholar 

  5. Smith, R.C. and Fry, S.C., Endotransglycosylation of xyloglucans in plant cell suspension cultures, Biochem. J., 1991, vol. 15, pp. 529–535.

    Article  Google Scholar 

  6. Nishitani, K. and Tominaga, R., In vitro molecular weight increase in xyloglucan by an apoplastic enzyme preparation from epicotyls of Vigna angularis, Physiol. Plant., 1991, vol. 82, pp. 490–497.

    Article  CAS  Google Scholar 

  7. Rose, J.K.C., Braam, J., Fry, S.C., and Nishitani, K., The XTH family of enzymes involved in xyloglucan endotransglucosylation and endohydrolysis: current perspectives and a new unifying nomenclature, Plant Cell Physiol., 2002, vol. 43, pp. 1421–1435.

    Article  CAS  PubMed  Google Scholar 

  8. Yokoyama, R. and Nishitani, K., A comprehensive expression analysis of all members of a gene family encoding cell-wall enzymes allowed us to predict cisregulatory regions involved in cell-wall construction in specific organs of Arabidopsis, Plant Cell Physiol., 2001, vol. 42, pp. 1025–1033.

    Article  CAS  PubMed  Google Scholar 

  9. Yokoyama, R., Rose, J.K., and Nishitani, K., A surprising diversity and abundance of xyloglucan endotransglucosylase/hydrolases in rice. Classification and expression analysis, Plant Physiol., 2004, vol. 134, pp. 1088–1099.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Geisler-Lee, J., Geisler, M., Coutinho, P.M., Segerman, B., Nishikubo, N., Takahashi, J., Aspeborg, H., Djerbi, S., Master, E., Andersson-Gunnerås, S., Sundberg, B., Karpinski, S., Teeri, T.T., Kleczkowski, L.A., Henrissat, B., et al., Poplar carbohydrate–active enzymes. Gene identification and expression analyses, Plant Physiol., 2006, vol. 140, pp. 946–962.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Miedes, E., Zarra, I., Hoson, T., Herbers, K., Sonnewald, U., and Lorences, E.P., Xyloglucan endotransglucosylase and cell wall extensibility, Plant Physiol., 2011, vol. 168, pp. 196–203.

    Article  CAS  Google Scholar 

  12. Chen, F., Nonogaki, H., and Bradford, K.J., A gibberellin-regulated xyloglucan endotransglycosylase gene is expressed in the endosperm cap during tomato seed germination, J. Exp. Bot., 2002, vol. 53, pp. 215–223.

    Article  CAS  PubMed  Google Scholar 

  13. Catala, C., Rose, J.K.C., and Bennett, A.B., Auxinregulated genes encoding cell wall-modifying proteins are expressed during early tomato fruit growth, Plant Physiol., 2000, vol. 122, pp. 527–534.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Choi, J.Y., Seo, Y.S., Kim, S.J., Kim, W.T., and Shin, J.S., Constitutive expression of CaXTH3, a hot pepper xyloglucan endotransglucosylase/hydrolase, enhanced tolerance to salt and drought stresses without phenotypic defects in tomato plants (Solanum lycopersicum cv. Dotaerang), Plant Cell Rep., 2011, vol. 30, pp. 867–877.

    Article  CAS  PubMed  Google Scholar 

  15. Kuluev, B.R., Knyazev, A.V., Mikhaylova, E.V., Ermoshin, A.A., Nikonorov, Y.M., and Chemeris, A.V., The poplar ARGOS-LIKE gene promotes leaf initiation and cell expansion, and controls organ size, Biol. Plant., 2016, vol. 60, pp. 513–522.

    Article  CAS  Google Scholar 

  16. Zhang, H., Yin, W., and Xia, X., Calcineurin B-Like family in Populus: comparative genome analysis and expression pattern under cold, drought and salt stress treatment, Plant Growth Regul., 2008, vol. 56, pp. 129–140.

    Article  CAS  Google Scholar 

  17. Schmidt, G.W. and Delaney, S.K., Stable internal reference genes for normalization of real-time RT-PCR in tobacco (Nicotiana tabacum) during development and abiotic stress, Mol. Genet. Genomics, 2010, vol. 283, pp. 233–241.

    Article  CAS  PubMed  Google Scholar 

  18. Wang, Y., Chen, Y., Ding, L., Zhang, J., Wei, J., and Wang, H., Validation of reference genes for gene expression by quantitative real-time RT-PCR in stem segments spanning primary to secondary growth in Populus tomentosa, PLoS One, 2016, vol. 14: e0157370. doi 10.1371/journal.pone.0157370

    Article  Google Scholar 

  19. Kuluev, B.R., Safiullina, M.G., Knyazev, A.V., and Chemeris, A.V., Morphological analysis of transgenic tobacco plants expressing the PnEXPA3 gene of black poplar (Populus nigra), Russ. J. Dev. Biol., 2013, vol. 44, pp. 129–134.

    Article  CAS  Google Scholar 

  20. Bourquin, V., Nishikubo, N., Abe, H., Brumer, H., Denman, S., Eklund, M., Christiernin, M., Teeri, T.T., Sundberg, B., and Mellerowicz, E.J., Xyloglucan endotransglycosylases have a function during the formation of secondary cell walls of vascular tissues, Plant Cell, 2002, vol. 14, pp. 3073–3088.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Behringer, C. and Schwechheimer, C., B-GATA transcription factors—insights into their structure, regulation, and role in plant development, Front. Plant Sci., 2015, vol. 6. doi 10.3389/fpls.2015.00090

    Google Scholar 

  22. Bao, X., Franks, R.G., Levin, J.G., and Liu, Z., Repression of AGAMOUS by BELLRINGER in floral and inflorescence meristems, Plant Cell, 2004, vol. 16, pp. 1478–1489.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Yu, D., Chen, C., and Chen, Z., Evidence for an important role of WRKY DNA binding proteins in the regulation of NPR1 gene expression, Plant Cell, 2001, vol. 13, pp. 1527–1540.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Abe, H., Yamaguchi-Shinozaki, K., Urao, T., Iwasaki, T., Hosokawa, D., and Shinozaki, K., Role of Arabidopsis MYC and MYB homologs in droughtand abscisic acid-regulated gene expression, Plant Cell, 1997, vol. 9, pp. 1859–1868.

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Hu, Y., Poh, H., and Chua, N., The Arabidopsis ARGOS-LIKE gene regulates cell expansion during organ growth, Plant J., 2006, vol. 47, pp. 1–9.

    Article  CAS  PubMed  Google Scholar 

  26. Etchells, J.P., Moore, L., Jiang, W.Z., Prescott, H., Capper, R., Saunders, N.J., Bhatt, A.M., and Dickinson, H.G., A role for BELLRINGER in cell wall development is supported by loss-of-function phenotypes, BMC Plant Biol., 2012, vol. 13. doi 10.1186/1471-2229-12-212

    Google Scholar 

  27. Yang, Y., Chi, Y., Wang, Z., Zhou, Y., Fan, B., and Chen, Z., Functional analysis of structurally related soybean GmWRKY58 and GmWRKY76 in plant growth and development, J. Exp. Bot., 2016, vol. 21. doi 10.1093/jxb/erw252

    Google Scholar 

  28. Shinozaki, K. and Yamaguchi-Shinozaki, K., Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways, Curr. Opin. Plant Biol., 2000, vol. 3, pp. 217–223.

    Article  CAS  PubMed  Google Scholar 

  29. Ron’zhina, E.S., Cytokinin-regulated mesophyll cell division and expansion during development of Cucurbita pepo leaves, Russ. J. Plant Physiol., 2003, vol. 50, pp. 646–655.

    Article  Google Scholar 

  30. Kuluev, B.R., Knyazev, A.V., Nikonorov, Yu.M., and Chemeris, A.V., Role of the expansin genes NtEXPA1 and NtEXPA4 in the regulation of cell extension during tobacco leaf growth, Russ. J. Genet., 2014, vol. 50, no. 5, pp. 489–497.

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Institute of Biochemistry and Genetics, Ufa Scientific Centre, Russian Academy of Sciences, Ufa, Bashkortostan, 450054, Russia

    B. R. Kuluev, Z. A. Berezhneva, A. V. Knyazev, Yu. M. Nikonorov & A. V. Chemeris

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  1. B. R. Kuluev
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  2. Z. A. Berezhneva
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  3. A. V. Knyazev
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  4. Yu. M. Nikonorov
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  5. A. V. Chemeris
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Correspondence to B. R. Kuluev.

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Original Russian Text © B.R. Kuluev, Z.A. Berezhneva, A.V. Knyazev, Yu.M. Nikonorov, A.V. Chemeris, 2018, published in Fiziologiya Rastenii, 2018, Vol. 65, No. 1, pp. 26–37.

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Kuluev, B.R., Berezhneva, Z.A., Knyazev, A.V. et al. Role of PtrXTH1 and PnXTH1 Genes Encoding Xyloglucan Endo-Transglycosylases in Regulation of Growth and Adaptation of Plants to Stress Factors. Russ J Plant Physiol 65, 38–48 (2018). https://doi.org/10.1134/S1021443718010065

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  • DOI: https://doi.org/10.1134/S1021443718010065

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