Abstract
The genes of α-expansins of woody plants are of great interest for genetic engineering, since they can potentially be used to improve the tree growth parameters. In the flora of Russia, model woody plants for plant biotechnology are aspen (Populus tremula L.) and black poplar (Populus nigra L.). The objective of this study was to determine the role of α-expansin-encoding genes, aspen PtrEXPA3 and black poplar PnEXPA3, in the regulation and maintenance of woody plant growth. To achieve this goal, the PtrEXPA3 expression level were determined upon exogenous phytohormone treatment, the action of stress factors, and constitutive expression of the PnARGOS-LIKE gene. In addition, transgenic aspen plants with constitutive expression of the black poplar PnEXPA3 gene were generated, and their morphological analysis was carried out. The highest PtrEXPA3 mRNA level was detected in young intensely growing aspen leaves, and furthermore, expression of the gene was induced by exogenous cytokinins and auxins. In response to NaCl and constitutive expression of the PnARGOS-LIKE gene, the PtrEXPA3 mRNA level decreased. Transgenic aspen plants with constitutive PnEXPA3 expression were characterized by the decreased size of leaves, petioles, and internodes, as well as the increased size of leaf epidermal cells, while the stem size remained unchanged. Taken together, the data obtained enable the suggestion that the PtrEXPA3 and PnEXPA3 genes encode cytokinin- and auxin-regulated, leaf-specific expansins that are involved in the cell expansion.
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McQueen-Mason, S., Durachko, D.M., and Cosgrove, D.J., Two endogenous proteins that induce cell wall extension in plants, Plant Cell, 1992, vol. 4, pp. 1425–1433. doi 10.2307/3869513
Sampedro, J. and Cosgrove, D.J., The expansin superfamily, Genome Biol., 2005, vol. 6, pp. 242.1—242.11. doi 10.1186/gb-2005-6-12-242
Cosgrove, D.J., Plant expansins: diversity and interactions with plant cell walls, Curr. Opin. Plant Biol., 2015, vol. 25, pp. 162–172. doi 10.1016/j.pbi.2015.05.014
Marowa, P., Ding, A., and Kong, Y., Expansins: roles in plant growth and potential applications in crop improvement, Plant Cell Rep., 2016, vol. 35, pp. 949–965. doi 10.1007/s00299-016-1948-4
Lee, Y. and Kende, H., Expression of beta-expansins is correlated with internodal elongation in deepwater rice, Plant Physiol., 2001, vol. 127, pp. 645–654.
Cho, H.T. and Cosgrove, D.J., Expansins as agents in hormone action in Plant Hormones: Biosynthesis, Signal Transduction, Action!, Davies, P.J., Ed., Dordrecht: Kluwer, 2004, pp. 262–281.
Jung, J., O’Donoghue, E.M., and Dijkwel, P.P., Expression of multiple expansin genes is associated with cell expansion in potato organs, Plant Sci., 2010, vol. 179, pp. 77–85. doi 10.1016/j.plantsci.2010.04.007
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. doi 10.1134/S1022795414040061
Li, X., Zhao, J., Walk, T.C., and Liao, H., Characterization of soybean β-expansin genes and their expression responses to symbiosis, nutrient deficiency, and hormone treatment, Appl. Microbiol. Biotechnol., 2014, vol. 98, pp. 2805–2817. doi 10.1007/s00253-013-5240-z
Park, C.H., Kim, T.W., and Son, S.H., Brassinosteroids control AtEXPA5 gene expression in Arabidopsis thaliana, Phytochemistry, 2010, vol. 71, pp. 380–387. doi 10.1016/j.phytochem.2009.11.003
Azeez, A., Sane, A.P., Tripathi, S.K., et al., The gladiolus GgEXPA1 is a GA-responsive alpha-expansin gene expressed ubiquitously during expansion of all floral tissues and leaves but repressed during organ senescence, Postharvest Biol. Technol., 2010, vol. 58, pp. 48–56. doi 10.1016/j.postharvbio.2010.05.006
Qin, Z., Zhang, X., Zhang, X., et al., The Arabidopsis ORGAN SIZE RELATED 2 is involved in regulation of cell expansion during organ growth, BMC Plant Biol., 2014, vol. 14. doi 10.1186/s12870-014-0349-5
Feng, G., Qin, Z., Yan, J., et al., Arabidopsis ORGAN SIZE RELATED1 regulates organ growth and final organ size in orchestration with ARGOS and ARL, New Phytol., 2011, vol. 191, pp. 635–646. doi 10.1111/j.1469-8137.2011.03710.x
Wang, B., Zhou, X., Xu, F., and Gao, J., Ectopic expression of a Chinese cabbage BrARGOS gene in Arabidopsis increases organ size, Transgenic Res., 2010, vol. 19, pp. 461–472. doi 10.1007/s11248-009-9324-6
Han, Y., Li, A., Li, F., et al., Characterization of a wheat (Triticum aestivum) expansin gene, TaEXPB23, involved in the abiotic stress response and phytohormone regulation, Plant Physiol. Biochem., 2012, vol. 54, pp. 49–58. doi 10.1016/j.plaphy.2012.02.007
Lu, P., Kang, M., and Jiang, X., RhEXPA4, a rose expansin gene, modulates leaf growth and confers drought and salt tolerance to Arabidopsis, Planta, 2013, vol. 237, pp. 1547–1559. doi 10.1007/s00425-013-1867-3
Zhao, M.R., Li, F., Fang, Y., et al., Expansin-regulated cell elongation is involved in the drought tolerance in wheat, Protoplasma, 2011, vol. 248, pp. 313–323. doi 10.1007/s00709-010-0172-2
Xu, Q., Xu, X., Shi, Y., et al., Transgenic tobacco plants overexpressing a grass PpEXP1 gene exhibit enhanced tolerance to heat stress, PLoS One, 2014, vol. 8, e100792. doi 10.1371/journal.pone.0100792
Zorb, C., Muhling, K.H., Kutschera, U., and Geilfus, C.M., Salinity stiffens the epidermal cell walls of salt-stressed maize leaves: is the epidermis growthrestricting?, PLoS One, 2015, vol. 10, e0118406. doi 10.1371/journal.pone.0118406
Kwon, Y.R., Lee, H.J., Kim, K.H., et al., Ectopic expression of Expansin3 or Expansin β 1 causes enhanced hormone and salt stress sensitivity in Arabidopsis, Biotechnol. Lett., 2008, vol. 30, pp. 1281–1288. doi 10.1007/s10529-008-9678-5
Tuskan, G.A., Difazio, S., Jansson, S., et al., The genome of black cottonwood, Populus trichocarpa (Torr. and Gray), Science, 2006, vol. 313, pp. 1596–1604.
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, no. 3, pp. 129–134. doi 10.1134/S106236041303003X
Kuluev, B.R., Knyazev, A.V., Mikhaylova, E.V., et al., The poplar ARGOS-LIKE gene promotes leaf initiation and cell expansion, and controls organ size, Biol. Plant., 2016, vol. 60, pp. 513–522. doi 10.1007/s10535-016-0610-x
Kuluev, B.R., Knyazev, A.V., Lebedev, Ya.P., et al., Construction of hybrid promoters of caulimoviruses and analysis of their activity in transgenic plants, Russ. J. Plant Physiol., 2010, vol. 57, no. 4, pp. 582–589. doi 10.1134/S1021443710040187
Xu, M., Zang, V., Yao, H.S., and Huang, M.R., Isolation of high quality RNA and molecular manipulations with various tissues of Populus, Russ. J. Plant Physiol., 2009, vol. 56, no. 5, pp. 716–719. doi 10.1134/S1021443709050197
Wang, Y., Chen, Y., Ding, L., et al., 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
Zheng, M., Wang, Y., and Liu, K., Protein expression changes during cotton fiber elongation in response to low temperature stress, J. Plant Physiol., 2012, vol. 169, pp. 399–409. doi 10.1016/j.jplph.2011.09.014
Zorb, C., Geilfus, C.M., Muhling, K.H., and Ludwig-Muller, J., The influence of salt stress on ABA and auxin concentrations in two maize cultivars differing in salt resistance, J. Plant Physiol., 2013, vol. 170, pp. 220–224. doi 10.1016/j.jplph.2012.09.012
Gray-Mitsumune, M., Mellerovicz, E.J., Abe, H., et al., Expansins abundant in secondary xylem belong to subgroup A of the α-expansin gene family, Plant Physiol., 2004, vol. 135, pp. 1552–1564. doi 10.1104/pp.104.039321
Cho, H.T. and Cosgrove, D.J., Altered expression of expansin modulates leaf growth and pedicel abscission in Arabidopsis thaliana, Proc. Natl. Acad. Sci. U.S.A., 2000, vol. 97, pp. 9783–9788. doi 10.1073/pnas. 160276997
Kuluev, B.R., Avalbaev, A.M., Mikhaylova, E.V., et al., Expression profiles and hormonal regulation of tobacco expansin genes and their involvement in abiotic stress response, J. Plant Physiol., 2016, vol. 206, pp. 1–12. http://dx.doi.org/. doi 10.1016/j.jplph.2016.09.001
Gao, X., Liu, K., and Lu, Y.T., Specific roles of AtEXPA1 in plant growth and stress adaptation, Russ. J. Plant Physiol., 2010, vol. 57, pp. 241–246. doi 10.1134/S1021443710020111
Fleming, A.J., McQueen-Mason, S., Mandel, T., and Kuhlemeier, C., Induction of leaf primordia by the cell wall protein expansin, Science, 1997, vol. 276, pp. 1415–1418. doi 10.1126/science.276.5317.1415
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Original Russian Text © B.R. Kuluev, A.V. Knyazev, E.V. Mikhaylova, A.V. Chemeris, 2017, published in Genetika, 2017, Vol. 53, No. 6, pp. 663–674.
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Kuluev, B.R., Knyazev, A.V., Mikhaylova, E.V. et al. The role of expansin genes PtrEXPA3 and PnEXPA3 in the regulation of leaf growth in poplar. Russ J Genet 53, 651–660 (2017). https://doi.org/10.1134/S1022795417060084
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DOI: https://doi.org/10.1134/S1022795417060084