Modulation of plant growth by HD-Zip class I and II transcription factors in response to environmental stimuli

New Phytologist

Volumn 190, Issue 4, 2011, Pages 823-837

  Harris, John C ^a   Hrmova, Maria ^a   Lopato, Sergiy ^a   Langridge, Peter ^a  

^a Australian Centre for Plant Functional Genomics   (Australia)

Author keywords

Abiotic stress; HD Zip; Phytohormone; Plant development; Transcription factor

Indexed keywords

HELIX LOOP HELIX PROTEIN; HOMEODOMAIN PROTEIN; LEUCINE ZIPPER PROTEIN; PHYTOHORMONE; TRANSCRIPTION FACTOR; VEGETABLE PROTEIN;

ADAPTATION; BIOASSAY; CHEMICAL BINDING; ENVIRONMENTAL CUE; GENE EXPRESSION; GROWTH RATE; GROWTH RESPONSE; HORMONE; TOXIC SUBSTANCE;

ADAPTATION; ARABIDOPSIS; ENVIRONMENT; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIGHT; METABOLISM; PHYLOGENY; PLANT GENE; REVIEW;

ADAPTATION, PHYSIOLOGICAL; ARABIDOPSIS; ENVIRONMENT; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; HELIX-TURN-HELIX MOTIFS; HOMEODOMAIN PROTEINS; LEUCINE ZIPPERS; LIGHT; PHYLOGENY; PLANT GROWTH REGULATORS; PLANT PROTEINS; TRANSCRIPTION FACTORS;

EID: 79955783958     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2011.03733.x     Document Type: Review

References (85)

1. Achard P, Cheng H, De Grauwe L, Decat J, Schoutteten H, Moritz T, Van der Straeten D, Peng JR, Harberd NP. 2006. Integration of plant responses to environmentally activated phytohormonal signals. Science 311: 91-94.
2. Agalou A, Purwantomo S, Overnaes E, Johannesson H, Zhu X, Estiati A, de Kam RJ, Engström P, Slamet-Loedin IH, Zhu Z et al. 2008. A genome-wide survey of HD-Zip genes in rice and analysis of drought-responsive family members. Plant Molecular Biology 66: 87-103.
3. Aoyama T, Dong CH, Wu Y, Carabelli M, Sessa G, Ruberti I, Morelli G, Chua NH. 1995. Ectopic expression of the Arabidopsis transcriptional activator ATHB-1 alters leaf cell fate in tobacco. The Plant Cell 7: 1773-1785.
4. Ariel F, Diet A, Verdenaud M, Gruber V, Frugier F, Chan R, Crespi M. 2010. Environmental regulation of lateral root emergence in Medicago truncatula requires the HD-Zip I transcription factor HB1. The Plant Cell 22: 2171-2183.
5. Ariel FD, Manavella PA, Dezar CA, Chan RL. 2007. The true story of the HD-Zip family. Trends in Plant Science 12: 419-426.
6. Barrero JM, Millar AA, Griffiths J, Czechowski T, Scheible WR, Udvardi M, Reid JB, Ross JJ, Jacobsen JV, Gubler F. 2010. Gene expression profiling identifies two regulatory genes controlling dormancy and ABA sensitivity in Arabidopsis seeds. Plant Journal 61: 611-622.
7. Burglin TR, Finney M, Coulson A, Ruvkun G. 1989. Caenorhabditis elegans has scores of homeobox-containing genes. Nature 341: 239-243.
8. Carabelli M, Morelli G, Whitelam G, Ruberti I. 1996. Twilight-zone and canopy shade induction of the Athb-2 homeobox gene in green plants. Proceedings of the National Academy of Sciences, USA 93: 3530-3535.
9. Casteel DE, Smith-Nguyen EV, Sankaran B, Roh SH, Pilz RB, Kim C. 2010. A crystal structure of the cyclic GMP-dependent Protein Kinase I beta dimerization/docking domain reveals molecular details of isoform-specific anchoring. Journal of Biological Chemistry 285: 32684-32688.
10. Ciarbelli AR, Ciolfi A, Salvucci S, Ruzza V, Possenti M, Carabelli M, Fruscalzo A, Sessa G, Morelli G, Ruberti I. 2008. The Arabidopsis Homeodomain-leucine Zipper II gene family: diversity and redundancy. Plant Molecular Biology 68: 465-478.
11. Dai M, Hu Y, Ma Q, Zhao Y, Zhou DX. 2008. Functional analysis of rice HOMEOBOX4 (Oshox4) gene reveals a negative function in gibberellin responses. Plant Molecular Biology 66: 289-301.
12. Deng X, Phillips J, Bräutigam A, Engström P, Johannesson H, Ouwerkerk PB, Ruberti I, Salinas J, Vera P, Iannacone R et al. 2006. A homeodomain leucine zipper gene from Craterostigma plantagineum regulates abscisic acid responsive gene expression and physiological responses. Plant Molecular Biology 61: 469-489.
13. Deng X, Phillips J, Meijer AH, Salamini F, Bartels D. 2002. Characterization of five novel dehydration-responsive homeodomain leucine zipper genes from the resurrection plant Craterostigma plantagineum. Plant Molecular Biology 49: 601-610.
14. Dezar CA, Gago GM, Gonzalez DH, Chan RL. 2005. Hahb-4, a sunflower homeobox-leucine zipper gene, is a developmental regulator and confers drought tolerance to Arabidopsis thaliana plants. Transgenic Research 14: 429-440.
15. Dezar CA, Giacomelli JI, Manavella PA, Ré DA, Alves-Ferreira M, Baldwin IT, Bonaventure G, Chan RL. 2010. HAHB10, a sunflower HD-Zip II transcription factor, participates in the induction of flowering and in the control of phytohormone-mediated responses to biotic stress. Journal of Experimental Botany 62: 1061-1076.
16. Eckardt NA. 2003. MADS monsters: controlling floral organ identity. The Plant Cell 15: 803-805.
17. Ellenberger TE, Brandl CJ, Struhl K, Harrison SC. 1992. The GCN4 basic region leucine zipper binds DNA as a dimer of uninterrupted α-helices: crystal structure of the protein-DNA complex. Cell 71: 1223-1237.
18. de Folter S, Immink RGH, Kieffer M, Parenicová L, Henz SR, Weigel D, Busscher M, Kooiker M, Colombo L, Kater MM et al. 2005. Comprehensive interaction map of the Arabidopsis MADS box transcription factors. The Plant Cell 17: 1424-1433.
19. Frank W, Phillips J, Salamini F, Bartels D. 1998. Two dehydration-inducible transcripts from the resurrection plant Craterostigma plantagineum encode interacting homeodomain-leucine zipper proteins. Plant Journal 15: 413-421.
20. Franklin KA. 2008. Shade avoidance. New Phytologist 179: 930-944.
21. Franklin KA, Quail PH. 2010. Phytochrome functions in Arabidopsis development. Journal of Experimental Botany 61: 11-24.
22. Gago GM, Almoguera C, Jordano J, Gonzalez DH, Chan RL. 2002. Hahb-4, a homeobox-leucine zipper gene potentially involved in abscisic acid-dependent responses to water stress in sunflower. Plant, Cell & Environment 25: 633-640.
23. Garber RL, Kuroiwa A, Gehring WJ. 1983. Genomic and cDNA clones of the homeotic locus ANTENNAPEDIA in Drosophila. The EMBO Journal 2: 2027-2036.
24. Gehring WJ, Qian YQ, Billeter M, Furukubotokunaga K, Schier AF, Resendez-Perez D, Affolter M, Otting G, Wüthrich K. 1994. Homeodomain-dna recognition. Cell 78: 211-223.
25. Gonzalez DH, Valle EM, Gago G, Chan RL. 1997. Interaction between proteins containing homeodomains associated to leucine zippers from sunflower. Biochimica et Biophysica Acta, Gene Structure and Expression 1351: 137-149.
26. Hake S, Vollbrecht E, Freeling M. 1989. Cloning knotted, the dominant morphological mutant in maize using ds2 as a transposon tag. The EMBO Journal 8: 15-22.
27. Hanson J, Johannesson H, Engström P. 2001. Sugar-dependent alterations in cotyledon and leaf development in transgenic plants expressing the HDZhdip gene ATHB13. Plant Molecular Biology 45: 247-262.
28. Henriksson E, Olsson ASB, Johannesson H, Johansson H, Hanson J, Engström P, Söderman E. 2005. Homeodomain leucine zipper class I genes in Arabidopsis. Expression patterns and phylogenetic relationships. Plant Physiology 139: 509-518.
29. Himmelbach A, Hoffmann T, Leube M, Höhener B, Grill E. 2002. Homeodomain protein ATHB6 is a target of the protein phosphatase ABI1 and regulates hormone responses in Arabidopsis. The EMBO Journal 21: 3029-3038.
30. Hirsch JA, Aggarwal AK. 1995. Structure of even skipped homeodomain complexed to AT rich DNA: New perspectives on homeodomain specificity. The EMBO Journal 14: 6280-6291.
31. Hjellstrom M, Olsson ASB, Engstrom O, Soderman EM. 2003. Constitutive expression of the water deficit-inducible homeobox gene ATHB7 in transgenic Arabidopsis causes a suppression of stem elongation growth. Plant, Cell & Environment 26: 1127-1136.
32. Hofer J, Turner L, Moreau C, Ambrose M, Isaac P, Butcher S, Weller J, Dupin A, Dalmais M, Le Signor C et al. 2009. Tendril-less regulates tendril formation in pea leaves. Plant Cell 21: 420-428.
33. Huang DQ, Wu WR, Abrams SR, Cutler AJ. 2008. The relationship of drought-related gene expression in Arabidopsis thaliana to hormonal and environmental factors. Journal of Experimental Botany 59: 2991-3007.
34. Inoue S, Takemiya A, Shimazaki K. 2010. Phototropin signaling and stomatal opening as a model case. Current Opinion in Plant Biology 13: 587-593.
35. Johannesson H, Wang Y, Engstrom P. 2001. DNA-binding and dimerization preferences of Arabidopsis homeodomain-leucine zipper transcription factors in vitro. Plant Molecular Biology 45: 63-73.
36. Johannesson H, Wang Y, Hanson J, Engström P. 2003. The Arabidopsis thaliana homeobox gene ATHB5 is a potential regulator of abscisic acid responsiveness in developing seedlings. Plant Molecular Biology 51: 719-729.
37. Kissinger CR, Liu BS, Martin-Blanco E, Kornberg TB, Pabo CO. 1990. Crystal-structure of an engrailed homeodomain-dna complex at 2.8-a resolution - a framework for understanding homeodomain-dna interactions. Cell 63: 579-590.
38. Lee YH, Chun JY. 1998. A new homeodomain-leucine zipper gene from Arabidopsis thaliana induced by water stress and abscisic acid treatment. Plant Molecular Biology 37: 377-384.
39. Leung J, Merlot S, Giraudat J. 1997. The Arabidopsis ABSCISIC ACID-INSENSITIVE2 (ABI2) and ABI1 genes encode homologous protein phosphatases 2C involved in abscisic acid signal transduction. The Plant Cell 9: 759-771.
40. Lin CT, Shalitin D. 2003. Cryptochrome structure and signal transduction. Annual Review of Plant Biology 54: 469-496.
41. Liu HJ, Wang SF, Yu XB, Yu J, He XW, Zhang SL, Shou HX, Wu P. 2005. ARL1, a LOB-domain protein required for adventitious root formation in rice. Plant Journal 43: 47-56.
42. Lopato S, Bazanova N, Morran S, Milligan AS, Shirley N, Langridge P. 2006. Isolation of plant transcription factors using a modified yeast one-hybrid system. Plant Methods 2: 3-17.
43. Manavella PA, Arce AL, Dezar CA, Bitton F, Renou JP, Crespi M, Chan RL. 2006. Cross-talk between ethylene and drought signalling pathways is mediated by the sunflower Hahb-4 transcription factor. Plant Journal 48: 125-137.
44. Manavella PA, Dezar CA, Ariel FD, Chan RL. 2008a. Two ABREs, two redundant root-specific and one W-box cis-acting elements are functional in the sunflower HAHB4 promoter. Plant Physiology and Biochemistry 46: 860-867.
45. Manavella PA, Dezar CA, Bonaventure G, Baldwin IT, Chan RL. 2008b. HAHB4, a sunflower HD-Zip protein, integrates signals from the jasmonic acid and ethylene pathways during wounding and biotic stress responses. Plant Journal 56: 376-388.
46. Mattsson J, Ckurshumova W, Berleth T. 2003. Auxin signaling in Arabidopsis leaf vascular development. Plant Physiology 131: 1327-1339.
47. Meijer AH, de Kam RJ, d'Erfurth I, Shen W, Hoge JHC. 2000. HD-Zip proteins of families I and II from rice: interactions and functional properties. Molecular and General Genetics 263: 12-21.
48. Möglich A, Yang XJ, Ayers RA, Moffat K. 2010. Structure and function of plant photoreceptors. Annual Review of Plant Biology 61: 21-47.
49. Mukherjee K, Brocchieri L, Bürglin TR. 2009. A comprehensive classification and evolutionary analysis of plant homeobox genes. Molecular Biology and Evolution 26: 2775-2794.
50. Nakashima K, Ito Y, Yamaguchi-Shinozaki K. 2009. Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiology 149: 88-95.
51. Ohgishi M, Oka A, Morelli G, Ruberti I, Aoyama T. 2001. Negative autoregulation of the Arabidopsis homeobox gene ATHB-2. Plant Journal 25: 389-398.
52. Okushima Y, Fukaki H, Onoda M, Theologis A, Tasaka M. 2007. ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis. The Plant Cell 19: 118-130.
53. Olsson AS, Engström P, Söderman E. 2004. The homeobox genes ATHB12 and ATHB7 encode potential regulators of growth in response to water deficit in Arabidopsis. Plant Molecular Biology 55: 663-677.
54. Palena CM, Gonzalez DH, Chan RL. 1999. A monomer-dimer equilibrium modulates the interaction of the sunflower homeodomain leucine-zipper protein Hahb-4 with DNA. Biochemical Journal 341: 81-87.
55. Palena CM, Tron AE, Bertoncini CW, Gonzalez DH, Chan RL. 2001. Positively charged residues at the N-terminal arm of the homeodomain are required for efficient DNA binding by homeodomain-leucine zipper proteins. Journal of Molecular Biology 308: 39-47.
56. Perrot-Rechenmann C. 2010. Cellular responses to auxin: division versus expansion. Cold Spring Harbor Perspectives in Biology 2: a001446.
57. Qian YQ, Otting G, Billeter M, Müller M, Gehring W, Wüthrich K. 1993. Nuclear-magnetic-resonance spectroscopy of a DNA complex with the uniformly c-13-labeled antennapedia homeodomain and structure determination of the DNA-bound homeodomain. Journal of Molecular Biology 234: 1070-1083.
58. Ré DA, Dezar CA, Chan RL, Baldwin IT, Bonaventure G. 2011. Nicotiana attenuata NaHD20 plays a role in leaf ABA accumulation during water stress, benzylacetone emission from flowers, and the timing of bolting and flower transitions. Journal of Experimental Botany 62: 155-166.
59. Ruberti I, Sessa G, Lucchetti S, Morelli G. 1991. A novel class of plant-proteins containing a homeodomain with a closely linked leucine zipper motif. The EMBO Journal 10: 1787-1791.
60. Rueda EC, Dezar CA, Gonzalez DH, Chan RL. 2005. Hahb-10, a sunflower homeobox-leucine zipper gene, is regulated by light quality and quantity, and promotes early flowering when expressed in Arabidopsis. Plant and Cell Physiology 46: 1954-1963.
61. Santner A, Calderon-Villalobos LIA, Estelle M. 2009. Plant hormones are versatile chemical regulators of plant growth. Nature Chemical Biology 5: 301-307.
62. Sawa S, Ohgishi M, Goda H, Higuchi K, Shimada Y, Yoshida S, Koshiba T. 2002. The HAT2 gene, a member of the HD-Zip gene family, isolated as an auxin inducible gene by DNA microarray screening, affects auxin response in Arabidopsis. Plant Journal 32: 1011-1022.
63. Scarpella E, Rueb S, Boot KJM, Hoge JHC, Meijer AH. 2000. A role for the rice homeobox gene Oshox1 in provascular cell fate commitment. Development 127: 3655-3669.
64. Sessa G, Morelli G, Ruberti I. 1993. The ATHB-1 and -2 HD-Zip domains homodimerize forming complexes of different DNA-binding specificities. The EMBO Journal 12: 3507-3517.
65. Sessa G, Morelli G, Ruberti I. 1997. DNA-binding specificity of the homeodomain leucine zipper domain. Journal of Molecular Biology 274: 303-309.
66. Skinner DJ, Gasser CS. 2009. Expression-based discovery of candidate ovule development regulators through transcriptional profiling of ovule mutants. BMC Plant Biology 9. doi:
67. Skirycz A, Inzé D. 2010. More from less: plant growth under limited water. Current Opinion in Biotechnology 21: 197-203.
68. Söderman E, Hjellström M, Fahleson J, Engström P. 1999. The HD-Zip gene ATHB6 in Arabidopsis is expressed in developing leaves, roots and carpels and up-regulated by water deficit conditions. Plant Molecular Biology 40: 1073-1083.
69. Söderman E, Mattsson J, Svenson M, Borkird C, Engström P. 1994. Expression patterns of novel genes encoding homeodomain leucine-zipper proteins in Arabidopsis thaliana. Plant Molecular Biology 26: 145-154.
70. Son O, Cho HY, Kim MR, Lee H, Lee MS, Song E, Park JH, Nam KH, Chun JY, Kim HJ et al. 2005. Induction of a homeodomain-leucine zipper gene by auxin is inhibited by cytokinin in Arabidopsis roots. Biochemical and Biophysical Research Communications 326: 203-209.
71. Son O, Hur YS, Kim YK, Lee HJ, Kim S, Kim MR, Nam KH, Lee MS, Kim BY, Park J et al. 2010. ATHB12, an ABA-inducible homeodomain-leucine zipper (HD-Zip) protein of arabidopsis, negatively regulates the growth of the inflorescence stem by decreasing the expression of a gibberellin 20-oxidase gene. Plant and Cell Physiology 51: 1537-1547.
72. Sorin C, Salla-Martret M, Bou-Torrent J, Roig-Villanova I, Martinez-Garcia JF. 2009. ATHB4, a regulator of shade avoidance, modulates hormone response in Arabidopsis seedlings. Plant Journal 59: 266-277.
73. Stamm P, Kumar PP. 2010. The phytohormone signal network regulating elongation growth during shade avoidance. Journal of Experimental Botany 61: 2889-2903.
74. Steindler C, Carabelli M, Borello U, Morelli G, Ruberti I. 1997. Phytochrome A, phytochrome B and other phytochrome(s) regulate ATHB-2 gene expression in etiolated and green Arabidopsis plants. Plant, Cell & Environment 20: 759-763.
75. Steindler C, Matteucci A, Sessa G, Weimar T, Ohgishi M, Aoyama T, Morelli G, Ruberti I. 1999. Shade avoidance responses are mediated by the ATHB-2 HD-Zip protein, a negative regulator of gene expression. Development 126: 4235-4245.
76. Sultan SE. 2010. Plant developmental responses to the environment: eco-devo insights. Current Opinion in Plant Biology 13: 96-101.
77. Szilák L, Moitra J, Vinson C. 1997. Design of a leucine zipper coiled coil stabilized 1.4 kcal mol(-1) by phosphorylation of a serine in the e position. Protein Science 6: 1273-1283.
78. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. 1997. The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25: 4876-4882.
79. Tron AE, Bertoncini CW, Chan RL, Gonzalez DH. 2002. Redox regulation of plant homeodomain transcription factors. Journal of Biological Chemistry 277: 34800-34807.
80. Tron AE, Comelli RN, Gonzalez DH. 2005. Structure of homeodomain-leucine zipper/DNA complexes studied using hydroxyl radical cleavage of DNA and methylation interference. Biochemistry 44: 16796-16803.
81. Tron AE, Welchen E, Gonzalez DH. 2004. Engineering the loop region of a homeodomain-leucine zipper protein promotes efficient binding to a monomeric DNA binding site. Biochemistry 43: 15845-15851.
82. Vollbrecht E, Veit B, Sinha N, Hake S. 1991. The developmental gene Knotted-1 is a member of a maize homeobox gene family. Nature 350: 241-243.
83. Wang Y, Henriksson E, Söderman E, Henriksson KN, Sundberg E, Engström P. 2003. The Arabidopsis homeobox gene, ATHB16, regulates leaf development and the sensitivity to photoperiod in Arabidopsis. Developmental Biology 264: 228-239.
84. Wolters H, Jürgens G. 2009. Survival of the flexible: hormonal growth control and adaptation in plant development. Nature Reviews Genetics 10: 305-317.
85. Zanetti ME, Chan RL, Godoy AV, González DH, Casalongué CA. 2004. Homeodomain-leucine zipper proteins interact with a plant homologue of the transcriptional co-activator multiprotein bridging factor 1. Journal of Biochemistry and Molecular Biology 37: 320-324.