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Russian Journal of Genetics

, Volume 55, Issue 1, pp 1–9 | Cite as

HD-Zip Genes and Their Role in Plant Adaptation to Environmental Factors

  • A. B. ShcherbanEmail author
REVIEWS AND THEORETICAL ARTICLES
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Abstract

This review presents characteristics of the HD-Zip family of homeobox-containing genes unique to plants, and their involvement in molecular mechanisms of resistance to certain adverse environmental factors (such as drought, deficiency of light, and pathogens) is considered. The importance of the HD-Zip genes in modulating and combining the signals from different hormone-dependent genetic cascades controlling the adaptation of plants to various external factors is demonstrated.

Keywords:

transcription factor homeobox leucine zipper HD-Zip gene phytohormones stress 

Notes

ACKNOWLEDGMENTS

This work was supported by the Russian Science Foundation (project no. 14-14-00161).

COMPLIANCE WITH ETHICAL STANDARDS

The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

REFERENCES

  1. 1.
    Garber, R.L., Kuroiwa, A., Gehring, W.J., et al., Genomic and cDNA clones of the homeotic locus Antennapedia in Drosophila, EMBO J., 1983, vol. 2, pp. 2027—2036.  https://doi.org/10.1002/j.1460-2075.1983.tb01696.x CrossRefGoogle Scholar
  2. 2.
    Moens, C.B. and Selleri, L., Hox cofactors in vertebrate development, Dev. Biol., 2006, vol. 291, pp. 193—206.  https://doi.org/10.1016/j.ydbio.2005.10.032 CrossRefGoogle Scholar
  3. 3.
    Vollbrecht, E., Veit, B., Sinha, N., and Hake, S., The developmental gene Knotted-1 is a member of a maize homeobox gene family, Nature, 1991, vol. 350, pp. 241—243.  https://doi.org/10.1038/350241a0 CrossRefGoogle Scholar
  4. 4.
    Bharathan, G., Janssen, B.-J., Kellogg, E.A., and Sinha, N., Did homeodomain proteins duplicate before the origin of angiosperms, fungi, and metazoa?, Proc. Natl. Acad. Sci. U.S.A., 1997, vol. 94, pp. 13749—13753.CrossRefGoogle Scholar
  5. 5.
    Sessa, G., Morelli, G., and Ruberti, I., The Athb-1 and -2 HD-Zip domains homodimerize forming complexes of different DNA binding specificities, EMBO J., 1993, vol. 12, pp. 3507—3517.CrossRefGoogle Scholar
  6. 6.
    Schena, M. and Davis, R.W., HD-Zip protein members of Arabidopsis homeodomain protein superfamily, Proc. Natl. Acad. Sci. U.S.A., 1992, vol. 89, pp. 3894—3898.CrossRefGoogle Scholar
  7. 7.
    Zhong, R. and Ye, Z.-H., IFL1, a gene regulating interfascicular fiber differentiation in Arabidopsis, encodes a homeodomain-leucine zipper protein, Plant Cell. 1999, vol. 11, pp. 2139—2152.  https://doi.org/10.1105/tpc.11.11.2139.CrossRefGoogle Scholar
  8. 8.
    McConnell, J.R., Emery, J., Eshed, Y., et al., Role of PHABULOSA and PHAVOLUTA in determining radial patterningin shoots, Nature, 2001, vol. 411, pp. 709—713.  https://doi.org/10.1038/35079635 CrossRefGoogle Scholar
  9. 9.
    Ohashi-Ito, K. and Fukuda, H., HD-Zip III homeobox genes that include a novel member, ZeHB-13 (Zinnia)/ATHB-15 (Arabidopsis), are involved in procambium and xylem cell differentiation, Plant Cell Physiol., 2003, vol. 44, pp. 1350—1358.  https://doi.org/10.1093/pcp/pcg164.CrossRefGoogle Scholar
  10. 10.
    Rerie, W.G., Feldmann, K.A., and Marks, M.D., The glabra2 gene encodes a homeodomain protein required for normal trichome development in Arabidopsis, Genes Dev., 1994, vol. 8, pp. 1388—1399.  https://doi.org/10.1101/gad.8.12.1388 CrossRefGoogle Scholar
  11. 11.
    Di Cristina, M., Sessa, G., Dolan, L., et al., The Arabidopsis Athb-10 (GLABRA2) is an HD-Zip protein required for regulation of root hair development, Plant J., 1996, vol. 10, pp. 393—402.  https://doi.org/10.1046/j.1365-313X.1996.10030393.x CrossRefGoogle Scholar
  12. 12.
    Masucci, J., Rerie, W., Foreman, D., et al., The homeobox gene GLABRA2 is required for position-dependent cell differentiation in the root epidermis of Arabidopsis thaliana, Development, 1996, vol. 122, pp. 1253—1260.Google Scholar
  13. 13.
    Ohashi, Y., Oka, A., Ruberti, I., et al., Ectopically additive expression of GLABRA2 alters the frequency and spacing of trichome initiation, Plant J., 2002, vol. 29, pp. 359—369.  https://doi.org/10.1046/j.0960-7412.2001.01214.x CrossRefGoogle Scholar
  14. 14.
    Abe, M., Katsumata, H., Komeda, Y., and Takahashi, T., Regulation of shoot epidermal cell differentiation by a pair of homeodomain proteins in Arabidopsis, Development, 2003, vol. 130, pp. 635—643.  https://doi.org/10.1242/dev.00292 CrossRefGoogle Scholar
  15. 15.
    Chan, R.L., Gago, G.M., Palena, C.M., and Gonzalez, D.H., Homeoboxes in plant development, Biochim. Biophys. Acta, 1998, vol. 1442, pp. 1—19.  https://doi.org/10.1016/S0167-4781(98)00119-5.CrossRefGoogle Scholar
  16. 16.
    Aoyama, T., Dong, C., Wu, Y., et al., Ectopic expression of the Arabidopsis transcriptional activator Athb-1 alters leaf cell fate in tobacco, Plant Cell, 1995, vol. 7, pp. 1773—1785.  https://doi.org/10.1105/tpc.7.11.1773. CrossRefGoogle Scholar
  17. 17.
    Hanson, J., Johannesson, H., and Engstrom, P., Sugar-dependent alterations in cotyledon and leaf development in transgenic plants expressing the HDZip gene ATHB13, Plant Mol. Biol., 2001, vol. 45, pp. 247—262.CrossRefGoogle Scholar
  18. 18.
    Li, G., Yu, M., Fang, T., et al., Vernalization requirement duration in winter wheat is controlled by TaVRN-A1 at the protein level, Plant J., 2013, vol. 76, pp. 742—753.  https://doi.org/10.1111/tpj.12326 CrossRefGoogle Scholar
  19. 19.
    Brandt, R., Cabedo, M., Xie, Y., and Wenkel, S., Homeodomain leucine-zipper proteins and their role in synchronizing growth and development with the environment, J. Integr. Plant Biol., 2014, vol. 56, pp. 518—526.  https://doi.org/10.1111/jipb.12185 CrossRefGoogle Scholar
  20. 20.
    Ariel, F.D., Manavella, P.A., Dezar, C.A., and Chan, R.L., The true story of the HD-Zip family, Trends Plant Sci., 2007, vol. 12, no. 9, pp. 419—426.  https://doi.org/10.1016/j.tplants.2007.08.003 CrossRefGoogle Scholar
  21. 21.
    Henriksson, E., Olsson, A.S.B., Johannesson, H., et al., Homeodomain leucine zipper class I genes in Arabidopsis: expression patterns and phylogenetic relationships, Plant Physiol., 2005, vol. 139, pp. 509—518.  https://doi.org/10.1104/pp.105.063461.CrossRefGoogle Scholar
  22. 22.
    Agalou, A., Purwantomo, S., Overnaes, E., et al., A genome-wide survey of HD-Zip genes in rice and analysis of drought responsive family members, Plant Mol. Biol., 2008, vol. 66, pp. 87—103.  https://doi.org/10.1007/s11103-007-9255-7 CrossRefGoogle Scholar
  23. 23.
    Tron, A.E., Bertoncini, C.W., Chan, R.L., and Gonzalez, D.H., Redox regulation of plant homeodomain transcription factors, J. Biol. Chem., 2002, vol. 277, pp. 34800—34807.  https://doi.org/10.1074/jbc.M203297200 CrossRefGoogle Scholar
  24. 24.
    Tron, A.E., Comelli, R.N., and Gonzalez, D.H., Structure of homeodomain-leucine zipper/DNA complexes studied using hydroxyl radical cleavage of DNA and methylation interference, Biochemistry, 2005, vol. 44, pp. 16796—16803.  https://doi.org/10.1021/bi0513150 CrossRefGoogle Scholar
  25. 25.
    Palena, C.M., Tron, A.E., Bertoncinim, C.W., et al., Positively charged residues at the N-terminal arm of the homeodomain are required for efficient DNA binding by homeodomain-leucine zipper proteins, J. Mol. Biol., 2001, vol. 308, pp. 39—47.  https://doi.org/10.1006/jmbi.2001.4563.CrossRefGoogle Scholar
  26. 26.
    Tron, A.E., Welchen, E., and Gonzalez, D.H., Engineering the loop region of a homeodomain-leucine zipper protein promotes efficient binding to a monomeric DNA binding site, Biochemistry, 2004, vol. 43, pp. 15845—15851.  https://doi.org/10.1021/bi048254a CrossRefGoogle Scholar
  27. 27.
    Ponting, C.P. and Aravind, L., START: a lipid-binding domain in StAR, HD-ZIP and signaling proteins, Trends Biochem. Sci., 1999, vol. 24, pp. 130—132.  https://doi.org/10.1016/S0968-0004(99)01362-6.CrossRefGoogle Scholar
  28. 28.
    Schrick, K., Nguyen, D., Karlowski, W.M., and Mayer, K.F., START lipid/sterol-binding domains are amplified in plants and are predominantly associated with homeodomain transcription factors, Genome Biol., 2004, vol. 5, no. 6. R41.  https://doi.org/10.1186/gb-2004-5-6-r41 CrossRefGoogle Scholar
  29. 29.
    Ohashi, Y., Oka, A., Rodrigues-Pousada, R., et al., Modulation of phospholipid signaling by GLABRA2 in root-hair pattern formation, Science, 2003, vol. 300, pp. 1427—1430.  https://doi.org/10.1126/science.1083695 CrossRefGoogle Scholar
  30. 30.
    Kumar, R. and Thompson, E.B., Gene regulation by the glucocorticoid receptor: structure: function relationship, J. Steroid Biochem. Mol. Biol., 2005, vol. 94, pp. 383—394.  https://doi.org/10.1016/j.jsbmb.2004.12.046.CrossRefGoogle Scholar
  31. 31.
    Zhang, F., Zuo, K., Zhang, J., et al., An L1 box binding protein, GbML1, interacts with GbMYB25 to control cotton fibre development, J. Exp. Bot., 2010, vol. 61, pp. 3599—3613.  https://doi.org/10.1093/jxb/erq173 CrossRefGoogle Scholar
  32. 32.
    Mukherjee, K. and Bürglin, T.R., MEKHLA, a novel domain with similarity to PAS domains, is fused to plant homeodomain-leucine zipper III proteins, Plant Physiol., 2006, vol. 140, pp. 1142—1150.  https://doi.org/10.1104/pp.105.073833.CrossRefGoogle Scholar
  33. 33.
    Skirycz, A. and Inzé, D., More from less: plant growth under limited water, Curr. Opin. Biotechnol., 2010, vol. 21, pp. 197—203.  https://doi.org/10.1016/j.copbio.2010.03.002.CrossRefGoogle Scholar
  34. 34.
    Shinozaki, K. and Yamaguchi-Shinozaki, K., Gene networks involved in drought stress response and tolerance, J. Exp. Bot., 2007, vol. 58, pp. 221—227.  https://doi.org/10.1093/jxb/erl164 CrossRefGoogle Scholar
  35. 35.
    Manavella, P.A., Arce, A.L., Dezar, C.A., et al., Cross-talk between ethylene and drought signalling pathways is mediated by the sunflower Hahb-4 transcription factor, Plant J., 2006, vol. 48, no. 1, pp. 125—137.  https://doi.org/10.1111/j.1365-313X.2006.02865.x CrossRefGoogle Scholar
  36. 36.
    Harris, J.C., Sornaraj, P., Taylor, M., et al., Molecular interactions of the γ-clade homeodomain-leucine zipper class I transcription factors during the wheat response to water deficit, Plant Mol. Biol., 2016, vol. 90, pp. 435—452.  https://doi.org/10.1007/s11103-015-0427-6 CrossRefGoogle Scholar
  37. 37.
    Dezar, C.A., Gago, G.M., Gonzalez, D.H., and Chan, R.L., Hahb-4, a sunflower homeobox-leucine zipper gene, is a developmental regulator and confers drought tolerance to Arabidopsis thaliana plants, Transgenic Res., 2005, vol. 14, pp. 429—440.CrossRefGoogle Scholar
  38. 38.
    Yang, S.F. and Hoffman, N.E., Ethylene biosynthesis and its regulation in higher-plants, Annu. Rev. Plant Physiol. Mol. Biol., 1984, vol. 35, pp. 155—189.CrossRefGoogle Scholar
  39. 39.
    Chao, Q., Rothenberg, M., Solano, R., et al., Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSITIVE3 and related proteins, Cell, 1997, vol. 89, pp. 1133—1144.  https://doi.org/10.1016/S0092-8674(00)80300-1.CrossRefGoogle Scholar
  40. 40.
    Sakamoto, A. and Murata, N., Genetic engineering of glycinebetaine synthesis in plants: current status and implications for enhancement of stress tolerance, J. Exp. Bot., 2000, vol. 51, pp. 81—88.CrossRefGoogle Scholar
  41. 41.
    Capell, T., Bassie, L., and Christou, P., Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress, Proc. Natl. Acad. Sci. U.S.A., 2004, vol. 101, pp. 9909—9914.  https://doi.org/10.1073/pnas.0306974101.CrossRefGoogle Scholar
  42. 42.
    Yu, H., Chen, X., Hong, Y.-Y., et al., Activated expression of an Arabidopsis HD-START protein confers drought tolerance with improved root system and reduced stomatal density, Plant Cell, 2008, vol. 20, pp. 1134—1151.  https://doi.org/10.1105/tpc.108.058263.CrossRefGoogle Scholar
  43. 43.
    Chen, M., Chory, J., and Fankhauser, C., Light signal transduction in higher plants, Annu. Rev. Genet., 2004, vol. 38, pp. 87—117.CrossRefGoogle Scholar
  44. 44.
    Salter, M.G., Franklin, K.A., and Whitelam, G.C., Gating of the rapid shade avoidance response by the circadian clock in plants, Nature, 2003, vol. 426, pp. 680—683.  https://doi.org/10.1038/nature02174 CrossRefGoogle Scholar
  45. 45.
    Carabelli, M., Morelli, G., Whitelam, G., and Ruberti, I., Twilight zone and canopy shade induction of the ATHB-2 homeobox gene in green plants, Proc. Natl. Acad. Sci. U.S.A., 1996, vol. 93, pp. 3530—3535.CrossRefGoogle Scholar
  46. 46.
    Sessa, G., Carabelli, M., Sassi, M., et al., A dynamic balance between gene activation and repression regulates the shade avoidance response in Arabidopsis, Genes Dev., 2005, vol. 19, pp. 2811—2815.  https://doi.org/10.1101/gad.364005 CrossRefGoogle Scholar
  47. 47.
    Iglesias, M.J., Sellaro, R., Zurbriggen, M.D., et al., Multiple links between shade avoidance and auxin networks, J. Exp. Bot., 2017, vol. 69, pp. 213—218.  https://doi.org/10.1093/jxb/erx295 CrossRefGoogle Scholar
  48. 48.
    Chapman, E.J. and Estelle, M., Mechanism of auxin-regulated gene expression in plants, Annu. Rev. Genet., 2009, vol. 43, pp. 265—285.  https://doi.org/10.1146/annurev-genet-102108-134148 CrossRefGoogle Scholar
  49. 49.
    Hornitschek, P., Lorrain, S., Zoete, V., et al., Inhibition of the shade avoidance response by formation of non-DNA binding bHLH heterodimers, EMBO J., 2009, vol. 28, pp. 3893—3902.  https://doi.org/10.1038/emboj.2009.306 CrossRefGoogle Scholar
  50. 50.
    Lau, O.S. and Deng, X.W., The photomorphogenic repressors COP1 and DET1: 20 years later, Trends Plant Sci., 2012, vol. 17, pp. 584—593.  https://doi.org/10.1016/j.tplants.2012.05.004 CrossRefGoogle Scholar
  51. 51.
    Pacín, M., Semmoloni, M., Legris, M., et al., Convergence of CONSTITUTIVE PHOTOMORPHOGENESIS 1 and PHYTOCHROME INTERACTING FACTOR signalling during shade avoidance, New Phytol., 2016, vol. 211, pp. 967—979.  https://doi.org/10.1111/nph.13965 CrossRefGoogle Scholar
  52. 52.
    Ariel, F., Diet, A., Verdenaud, M., et al., Environmental regulation of lateral root emergence in Medicago truncatula requires the HD-Zip I transcription factor HB1, Plant Cell, 2010, vol. 22, pp. 2171—2183.  https://doi.org/10.1105/tpc.110.074823.CrossRefGoogle Scholar
  53. 53.
    Chen, X., Chen, Z., Zhao, H., et al., Genome-wide analysis of soybean HD-Zip gene family and expression profiling under salinity and drought treatments, PLoS One, 2014, vol. 9. e87156.  https://doi.org/10.1371/journal.pone.0087156.CrossRefGoogle Scholar
  54. 54.
    Jeffree, C.E., The fine structure of the plant cuticle, in Annual Plant Reviews, vol. 23: Biology of the Plant Cuticle, Oxford, UK: Blackwell, 2007, pp. 11—125.Google Scholar
  55. 55.
    Wu, R., Li, S., He, S., et al., CFL1, aWW domain protein, regulates cuticle development by modulating the function of HDG1, a class IV homeodomain transcription factor, in rice and Arabidopsis, Plant Cell, 2011, vol. 23, pp. 3392—3411.  https://doi.org/10.1105/tpc.111.088625 CrossRefGoogle Scholar
  56. 56.
    Javelle, M., Vernoud, V., Depege-Fargeix, N., et al., Overexpression of the epidermis-specific homeodomain-leucine zipper IV transcription factor Outer Cell Layer1 in maize identifies target genes involved in lipid metabolism and cuticle biosynthesis, Plant Physiol., 2010, vol. 154, pp. 273—286.  https://doi.org/10.1104/pp.109 CrossRefGoogle Scholar
  57. 57.
    DeBono, A., Yeats, T.H., Rose, J.K.C., et al., Arabidopsis LTPG is a glycosyl phosphatidylinositol-anchored lipid transfer protein required for export of lipids to the plant surface, Plant Cell, 2009, vol. 21, pp. 1230—1238.  https://doi.org/10.1105/tpc.108.064451 CrossRefGoogle Scholar
  58. 58.
    Zottich, U., Cunha, M., Carvalho, A.O., et al., Purification, biochemical characterization and antifungal activity of a new lipid transfer protein (LTP) from Coffea canephora seeds with alpha-amylase inhibitor properties, Biochim. Biophys. Acta, 2011, vol. 4, pp. 375—383.  https://doi.org/10.1016/j.bbagen.2010.12.002 CrossRefGoogle Scholar
  59. 59.
    Boutrot, F., Chantret, N., and Gautier, M.-F., Genome-wide analysis of the rice and Arabidopsis non-specific lipid transfer protein (nsLtp) gene families and identification of wheat nsLtp genes by EST data mining, BMC Genomics, 2008, vol. 9(86), pp. 1—19.  https://doi.org/10.1186/1471-2164-9-86 CrossRefGoogle Scholar
  60. 60.
    Molina, A. and Garcia-Olmedo, F., Enhanced tolerance to bacterial pathogens caused by the transgenic expression of barley lipid transfer protein LTP2, Plant J., 1997, vol. 12, pp. 669—675.  https://doi.org/10.1046/j.1365-313X.1997.00605.x CrossRefGoogle Scholar
  61. 61.
    Lee, S.B., Go, Y.S., Bae, H.J., et al., Disruption of glycosylphosphatidylinositol-anchored lipid transfer protein gene altered cuticular lipid composition, increased plastoglobules, and enhanced susceptibility to infection by the fungal pathogen Alternaria brassicicola, Plant Physiol., 2009, vol. 150, pp. 42—54.  https://doi.org/10.1104/pp.109.137745 CrossRefGoogle Scholar
  62. 62.
    Thomma, B.P., Cammue, B.P., and Thevissen, K., Plant defensins, Planta, 2002, vol. 216, no. 2, pp. 193—202.  https://doi.org/10.1007/s00425-002-0902-6 CrossRefGoogle Scholar
  63. 63.
    Kovalchuk, N., Li, M., Wittek, F., et al., Defensin promoters as potential tools for engineering disease resistance in cereal grains, Plant Biotech. J., 2010, vol. 8, p. 47—64.  https://doi.org/10.1111/j.1467-7652.2009.00465.x CrossRefGoogle Scholar

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© Pleiades Publishing, Inc. 2019

Authors and Affiliations

  1. 1.Federal Research Center Institute of Cytology and Genetics, Siberian Branch, Russian Academy of SciencesNovosibirskRussia

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