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.
Similar content being viewed by others
REFERENCES
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
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
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
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.
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.
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.
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.
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
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.
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
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
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.
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
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
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.
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.
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.
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
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
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
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.
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
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
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
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.
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
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.
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
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
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.
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
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.
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.
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
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
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
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.
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.
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.
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.
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.
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.
Chen, M., Chory, J., and Fankhauser, C., Light signal transduction in higher plants, Annu. Rev. Genet., 2004, vol. 38, pp. 87—117.
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
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.
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
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
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
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
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
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
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.
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.
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.
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
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
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
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
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
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
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
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
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
ACKNOWLEDGMENTS
This work was supported by the Russian Science Foundation (project no. 14-14-00161).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
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.
Additional information
Translated by A. Barkhash
Rights and permissions
About this article
Cite this article
Shcherban, A.B. HD-Zip Genes and Their Role in Plant Adaptation to Environmental Factors. Russ J Genet 55, 1–9 (2019). https://doi.org/10.1134/S1022795419010125
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S1022795419010125