JAIBA, a class-II HD-ZIP transcription factor involved in the regulation of meristematic activity, and important for correct gynoecium and fruit development in Arabidopsis

Plant Journal

Volumn 71, Issue 2, 2012, Pages 314-326

  Zúñiga Mayo, Victor M ^a   Marsch Martínez, Nayelli ^a   De Folter, Stefan ^a  

^a DEPARTAMENTO DE FÍSICA   (Mexico)

Author keywords

class II HD ZIP; gynoecium; indeterminacy; JAIBA; meristematic activity

Indexed keywords

ARABIDOPSIS; CLASS-II HD-ZIP; COMPLEX ORGANS; EMBRYO SAC; FLORAL MERISTEMS; FRUIT DEVELOPMENT; FUNCTIONAL CHARACTERIZATION; GYNOECIUM; HOMEODOMAIN; INDETERMINACY; JAIBA; LEUCINE ZIPPERS; PLANT LIFE; REPRODUCTIVE DEVELOPMENT; TISSUE DEVELOPMENT;

DEFECTS; GENES; PLANTS (BOTANY); TISSUE; TRANSCRIPTION FACTORS;

FRUITS;

ARABIDOPSIS PROTEIN; HOMEODOMAIN PROTEIN; JAIBA PROTEIN, ARABIDOPSIS; LEUCINE ZIPPER PROTEIN; PLANT RNA; TRANSCRIPTION FACTOR;

ALLELE; ARABIDOPSIS; ARTICLE; CYTOLOGY; DOWN REGULATION; FLOWER; FRUIT; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MERISTEM; METABOLISM; MUTATION; PHENOTYPE; PLANT SEED; PROTEIN ANALYSIS; TWO HYBRID SYSTEM;

ALLELES; ARABIDOPSIS; ARABIDOPSIS PROTEINS; DOWN-REGULATION; FLOWERS; FRUIT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; HOMEODOMAIN PROTEINS; LEUCINE ZIPPERS; MERISTEM; MUTATION; PHENOTYPE; PROTEIN INTERACTION MAPPING; RNA, PLANT; SEEDS; TRANSCRIPTION FACTORS; TWO-HYBRID SYSTEM TECHNIQUES;

ARABIDOPSIS; DECAPODA (CRUSTACEA);

EID: 84864402582     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2012.04990.x     Document Type: Article

References (77)

1. Alexander, M.P., (1980) A versatile stain for pollen fungi, yeast and bacteria. Biotech. Histochem. 55, 13-18. (Pubitemid 10022442)
2. Alonso, J.M., Stepanova, A.N., Leisse, T.J., et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science, 301, 653-657. (Pubitemid 36927950)
3. Alonso-Cantabrana, H., Ripoll, J.J., Ochando, I., Vera, A., Ferrandiz, C., and, Martinez-Laborda, A., (2007) Common regulatory networks in leaf and fruit patterning revealed by mutations in the Arabidopsis ASYMMETRIC LEAVES1 gene. Development, 134, 2663-2671. (Pubitemid 47225962)
4. Alvarez, J., and, Smyth, D.R., (1999) CRABS CLAW and SPATULA, two Arabidopsis genes that control carpel development in parallel with AGAMOUS. Development, 126, 2377-2386. (Pubitemid 29299007)
5. Alvarez, J., and, Smyth, D.R., (2002) CRABS CLAW and SPATULA genes regulate growth and pattern formation during gynoecium development in Arabidopsis thaliana. Int. J. Plant Sci. 163, 17-41. (Pubitemid 34063154)
6. Alvarez, J.P., Goldshmidt, A., Efroni, I., Bowman, J.L., and, Eshed, Y., (2009) The NGATHA distal organ development genes are essential for style specification in Arabidopsis. Plant Cell, 21, 1373-1393.
7. Ariel, F.D., Manavella, P.A., Dezar, C.A., and, Chan, R.L., (2007) The true story of the HD-Zip family. Trends Plant Sci. 12, 419-426. (Pubitemid 47362794)
8. Azhakanandam, S., Nole-Wilson, S., Bao, F., and, Franks, R.G., (2008) SEUSS and AINTEGUMENTA mediate patterning and ovule initiation during gynoecium medial domain development. Plant Physiol. 146, 1165-1181. (Pubitemid 352844135)
9. Balanza, V., Navarrete, M., Trigueros, M., and, Ferrandiz, C., (2006) Patterning the female side of Arabidopsis: the importance of hormones. J. Exp. Bot. 57, 3457-3469.
10. Barton, M.K., and, Poethig, R.S., (1993) Formation of the shoot apical meristem in Arabidopsis thaliana: an analysis of development in the wild type and in the shoot meristemless mutant. Development, 119, 823-831. (Pubitemid 23337423)
11. Bartrina, I., Otto, E., Strnad, M., Werner, T., and, Schmulling, T., (2011) Cytokinin regulates the activity of reproductive meristems, flower organ size, ovule formation, and thus seed yield in Arabidopsis thaliana. Plant Cell, 23, 69-80.
12. Blazquez, M.A., Ferrandiz, C., Madueno, F., and, Parcy, F., (2006) How floral meristems are built. Plant Mol. Biol. 60, 855-870. (Pubitemid 43841405)
13. Bowman, J.L., (2004) Class III HD-Zip gene regulation, the golden fleece of ARGONAUTE activity? BioEssays, 26, 938-942. (Pubitemid 39273067)
14. Bowman, J.L., and, Meyerowitz, E.M., (1991) Genetic control of pattern formation during flower development in Arabidopsis. Symp. Soc. Exp. Biol. 45, 89-115.
15. Bowman, J.L., and, Smyth, D.R., (1999) CRABS CLAW, a gene that regulates carpel and nectary development in Arabidopsis, encodes a novel protein with zinc finger and helix-loop-helix domains. Development, 126, 2387-2396. (Pubitemid 29299008)
16. Bowman, J.L., Baum, S.F., Eshed, Y., Putterill, J., and, Alvarez, J., (1999) Molecular genetics of gynoecium development in Arabidopsis. Curr. Top. Dev. Biol. 45, 155-205.
17. Byrne, M.E., (2006) Shoot meristem function and leaf polarity: the role of class III HD-ZIP genes. PLoS Genet. 2, e89.
18. Carabelli, M., Morelli, G., Whitelam, G., and, Ruberti, I., (1996) Twilight-zone and canopy shade induction of the Athb-2 homeobox gene in green plants. Proc. Natl Acad. Sci. USA, 93, 3530-3535. (Pubitemid 26125655)
19. Carabelli, M., Possenti, M., Sessa, G., Ciolfi, A., Sassi, M., Morelli, G., and, Ruberti, I., (2007) Canopy shade causes a rapid and transient arrest in leaf development through auxin-induced cytokinin oxidase activity. Genes Dev. 21, 1863-1868. (Pubitemid 47204926)
20. Carles, C.C., Lertpiriyapong, K., Reville, K., and, Fletcher, J.C., (2004) The ULTRAPETALA1 gene functions early in Arabidopsis development to restrict shoot apical meristem activity and acts through WUSCHEL to regulate floral meristem determinacy. Genetics, 167, 1893-1903. (Pubitemid 39265925)
21. Castrillo, G., Turck, F., Leveugle, M., Lecharny, A., Carbonero, P., Coupland, G., Paz-Ares, J., and, Onate-Sanchez, L., (2011) Speeding cis-trans regulation discovery by phylogenomic analyses coupled with screenings of an arrayed library of Arabidopsis transcription factors. PLoS ONE, 6, e21524.
22. Chuang, C.F., Running, M.P., Williams, R.W., and, Meyerowitz, E.M., (1999) The PERIANTHIA gene encodes a bZIP protein involved in the determination of floral organ number in Arabidopsis thaliana. Genes Dev. 13, 334-344. (Pubitemid 29095804)
23. Chuck, G., Lincoln, C., and, Hake, S., (1996) KNAT1 induces lobed leaves with ectopic meristems when overexpressed in Arabidopsis. Plant Cell, 8, 1277-1289. (Pubitemid 26355018)
24. Ciarbelli, A.R., Ciolfi, A., Salvucci, S., Ruzza, V., Possenti, M., Carabelli, M., Fruscalzo, A., Sessa, G., Morelli, G., and, Ruberti, I., (2008) The Arabidopsis homeodomain-leucine zipper II gene family: diversity and redundancy. Plant Mol. Biol. 68, 465-478.
25. Clark, S., Running, M., and, Meyerowitz, E., (1995) CLAVATA3 is a specific regulator of shoot and floral meristem development affecting the same processes a CLAVATA1. Development, 121, 2057-2067.
26. Clough, S.J., and, Bent, A.F., (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
27. Das, P., Ito, T., Wellmer, F., Vernoux, T., Dedieu, A., Traas, J., and, Meyerowitz, E.M., (2009) Floral stem cell termination involves the direct regulation of AGAMOUS by PERIANTHIA. Development, 136, 1605-1611.
28. Dinneny, J.R., and, Yanofsky, M.F., (2004) Floral development: an ABC gene chips in downstream. Curr. Biol. 14, R840-R841. (Pubitemid 39301152)
29. Fiers, M., Golemiec, E., van der Schors, R., van der Geest, L., Li, K.W., Stiekema, W.J., and, Liu, C.M., (2006) The CLAVATA3/ESR motif of CLAVATA3 is functionally independent from the nonconserved flanking sequences. Plant Physiol. 141, 1284-1292. (Pubitemid 44223281)
30. de Folter, S., and, Immink, R.G., (2011) Yeast protein-protein interaction assays and screens. In Plant Transcription Factors (, Yuan, L., and, Perry, S.E., eds). New York: Springer, pp. 145-165.
31. de Folter, S., Busscher, J., Colombo, L., Losa, A., and, Angenent, G.C., (2004) Transcript profiling of transcription factor genes during silique development in Arabidopsis. Plant Mol. Biol. 56, 351-366. (Pubitemid 40141230)
32. de Folter, S., Immink, R.G.H., Kieffer, M., et al. (2005) Comprehensive interaction map of the Arabidopsis MADS box transcription factors. Plant Cell, 17, 1424-1433. (Pubitemid 43138195)
33. Gremski, K., Ditta, G., and, Yanofsky, M.F., (2007) The HECATE genes regulate female reproductive tract development in Arabidopsis thaliana. Development, 134, 3593-3601. (Pubitemid 350104370)
34. Hay, A., and, Tsiantis, M., (2010) KNOX genes: versatile regulators of plant development and diversity. Development, 137, 3153-3165.
35. Helliwell, C.A., Wesley, S.V., Wielopolska, A.J., and, Waterhouse, P.M., (2002) High-throughput vectors for efficient gene silencing in plants. Funct. Plant Biol. 29, 1217-1225. (Pubitemid 35235561)
36. Henriksson, E., Olsson, A.S.B., Johannesson, H., Johansson, H., Hanson, J., Engstrom, P., and, Soderman, E., (2005) Homeodomain leucine zipper class I genes in Arabidopsis. Expression patterns and phylogenetic relationships. Plant Physiol. 139, 509-518. (Pubitemid 43951633)
37. Hu, J., Mitchum, M.G., Barnaby, N., et al. (2008) Potential sites of bioactive gibberellin production during reproductive growth in Arabidopsis. Plant Cell, 20, 320-336. (Pubitemid 352844015)
38. James, P., Halladay, J., and, Craig, E.A., (1996) Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics, 144, 1425-1436.
39. Jefferson, R.A., Kavanagh, T.A., and, Bevan, M.W., (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6, 3901-3907.
40. Karimi, M., Inze, D., and, Depicker, A., (2002) GATEWAY(TM) vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7, 193-195. (Pubitemid 36725938)
41. Kuusk, S., Sohlberg, J.J., Long, J.A., Fridborg, I., and, Sundberg, E., (2002) STY1 and STY2 promote the formation of apical tissues during Arabidopsis gynoecium development. Development, 129, 4707-4717. (Pubitemid 35277198)
42. Lenhard, M., Bohnert, A., Jurgens, G., and, Laux, T., (2001) Termination of stem cell maintenance in Arabidopsis floral meristems by interactions between WUSCHEL and AGAMOUS. Cell, 105, 805.
43. Liu, X., Kim, Y.J., Muller, R., Yumul, R.E., Liu, C., Pan, Y., Cao, X., Goodrich, J., and, Chen, X., (2011) AGAMOUS terminates floral stem cell maintenance in Arabidopsis by directly repressing WUSCHEL through recruitment of polycomb group proteins. Plant Cell, 23 (10), 3654-3670. doi:.
44. Lohmann, J.U., Hong, R.L., Hobe, M., Busch, M.A., Parcy, F., Simon, R., and, Weigel, D., (2001) A molecular link between stem cell regulation and floral patterning in Arabidopsis. Cell, 105, 793-803. (Pubitemid 32635108)
45. Long, J.A., Moan, E.I., Medford, J.I., and, Barton, M.K., (1996) A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature, 379, 66-69. (Pubitemid 26008135)
46. Maier, A.T., Stehling-Sun, S., Wollmann, H., Demar, M., Hong, R.L., Haubeiss, S., Weigel, D., and, Lohmann, J.U., (2009) Dual roles of the bZIP transcription factor PERIANTHIA in the control of floral architecture and homeotic gene expression. Development, 136, 1613-1620.
47. Marchler-Bauer, A., Lu, S., Anderson, J.B., et al. (2011) CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res. 39, D225-D229.
48. Mayer, K.F., Schoof, H., Haecker, A., Lenhard, M., Jurgens, G., and, Laux, T., (1998) Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell, 95, 805-815. (Pubitemid 29014460)
49. Nakamura, M., Katsumata, H., Abe, M., Yabe, N., Komeda, Y., Yamamoto, K.T., and, Takahashi, T., (2006) Characterization of the class IV homeodomain-leucine zipper gene family in Arabidopsis. Plant Physiol. 141, 1363-1375. (Pubitemid 44223288)
50. Payne, T., Johnson, S.D., and, Koltunow, A.M., (2004) KNUCKLES (KNU) encodes a C2H2 zinc-finger protein that regulates development of basal pattern elements of the Arabidopsis gynoecium. Development, 131, 3737-3749. (Pubitemid 39199381)
51. Paz-Ares, J., and, Consortium, T.R., (2002) REGIA, an EU project on fuctional genomics of transcription factors from Arabidopsis thaliana. Comp. Funct. Genomics, 3, 102-108. (Pubitemid 34521189)
52. Prigge, M.J., and, Clark, S.E., (2006) Evolution of the class III HD-Zip gene family in land plants. Evol. Dev. 8, 350-361. (Pubitemid 43974640)
53. Prunet, N., Morel, P., Thierry, A.-M., Eshed, Y., Bowman, J.L., Negrutiu, I., and, Trehin, C., (2008) REBELOTE, SQUINT, and ULTRAPETALA1 function redundantly in the temporal regulation of floral meristem termination in Arabidopsis thaliana. Plant Cell, 20, 901-919. (Pubitemid 352843969)
54. Prunet, N., Morel, P., Negrutiu, I., and, Trehin, C., (2009) Time to stop: flower meristem termination. Plant Physiol. 150, 1764-1772.
55. Roeder, A.H.K., and, Yanofsky, M.F., (2006) Fruit development in Arabidopsis. In The Arabidopsis Book (, Somerville, C.R., and, Meyerowitz, E.M., eds). Rockville, MD: American Society of Plant Biologists, pp. 1-50.
56. Roig-Villanova, I., Bou, J., Sorin, C., Devlin, P.F., and, Martinez-Garcia, J.F., (2006) Identification of primary target genes of phytochrome signaling. Early transcriptional control during shade avoidance responses in Arabidopsis. Plant Physiol. 141, 85-96. (Pubitemid 43956184)
57. Ruberti, I., Sessa, G., Lucchetti, S., and, Morelli, G., (1991) A novel class of plant proteins containing a homeodomain with a closely linked leucine zipper motif. EMBO J. 10, 1787-1791. (Pubitemid 21905646)
58. Running, M.P., and, Meyerowitz, E.M., (1996) Mutations in the PERIANTHIA gene of Arabidopsis specifically alter floral organ number and initiation pattern. Development, 122, 1261-1269. (Pubitemid 26123901)
59. Sablowski, R., (2007) Flowering and determinacy in Arabidopsis. J. Exp. Bot. 58 (5), 899-907, erm002. (Pubitemid 46623299)
60. Sawa, S., Ohgishi, M., Goda, H., Higuchi, K., Shimada, Y., Yoshida, S., and, 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 J. 32, 1011-1022. (Pubitemid 36108067)
61. Schena, M., and, Davis, R.W., (1992) HD-Zip proteins: members of an Arabidopsis homeodomain protein superfamily. Proc. Natl Acad. Sci. USA, 89, 3894-3898.
62. Schoof, H., Lenhard, M., Haecker, A., Mayer, K.F., Jurgens, G., and, Laux, T., (2000) The stem cell population of Arabidopsis shoot meristems in maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell, 100, 635-644.
63. Scofield, S., Dewitte, W., and, Murray, J.A.H., (2007) The KNOX gene SHOOT MERISTEMLESS is required for the development of reproductive meristematic tissues in Arabidopsis. Plant J. 50, 767-781. (Pubitemid 46855034)
64. Scofield, S., Dewitte, W., and, Murray, J.A., (2008) A model for Arabidopsis class-1 KNOX gene function. Plant Signal. Behav. 3, 257-259. (Pubitemid 351578781)
65. Sessa, G., Morelli, G., and, Ruberti, I., (1993) The Athb-1 and -2 HD-Zip domains homodimerize forming complexes of different DNA binding specificities. EMBO J. 12, 3507-3517. (Pubitemid 23256438)
66. Sessa, G., Carabelli, M., Ruberti, I., Baima, S., Lucchetti, S., and, Morelli, G., (1994) Identification of distinct families of HD-Zip proteins in Arabidopsis thaliana. In Analysis of Plant Development and Metabolism (, Puigdomenech, P., and, Coruzzi, G., eds). Berlin: Springer-Verlag, pp. 411-426.
67. Sessa, G., Morelli, G., and, Ruberti, I., (1997) DNA-binding specificity of the homeodomain-leucine zipper domain. J. Mol. Biol. 274, 303-309. (Pubitemid 27520619)
68. Sessa, G., Carabelli, M., Sassi, M., Ciolfi, A., Possenti, M., Mittempergher, F., Becker, J., Morelli, G., and, Ruberti, I., (2005) A dynamic balance between gene activation and repression regulates the shade avoidance response in Arabidopsis. Genes Dev. 19, 2811-2815. (Pubitemid 41739966)
69. Smyth, D.R., Bowman, J.L., and, Meyerowitz, E.M., (1990) Early flower development in Arabidopsis. Plant Cell, 2, 755-767. (Pubitemid 120015483)
70. Sorin, C., Salla-Martret, M., Bou-Torrent, J., Roig-Villanova, I., and, Martinez-Garcia, J.F., (2009) ATHB4, a regulator of shade avoidance, modulates hormone response in Arabidopsis seedlings. Plant J. 59, 266-277.
71. Steindler, C., Carabelli, M., Borello, U., Morelli, G., and, Ruberti, I., (1997) Phytochrome A, phytochrome B and other phytochrome(s) regulate ATHB-2 gene expression in etiolated and green Arabidopsis plants. Plant, Cell Environ. 20, 759-763. (Pubitemid 27269295)
72. Steindler, C., Matteucci, A., Sessa, G., Weimar, T., Ohgishi, M., Aoyama, T., Morelli, G., and, 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. (Pubitemid 29509339)
73. Sun, B., Xu, Y., Ng, K.-H., and, Ito, T., (2009) A timing mechanism for stem cell maintenance and differentiation in the Arabidopsis floral meristem. Genes Dev. 23, 1791-1804.
74. Sundberg, E., and, Ferrándiz, C., (2010) Gynoecium patterning in Arabidopsis: a basic plan behind a complex structure. In Annual Plant Reviews Volume 38: Fruit Development and Seed Dispersal (, Ostergaard, L., ed). Oxford, UK: Blackwell Publishing Ltd, pp. 35-69. doi:.
75. Trigueros, M., Navarrete-Gomez, M., Sato, S., Christensen, S.K., Pelaz, S., Weigel, D., Yanofsky, M.F., and, Ferrandiz, C., (2009) The NGATHA genes direct style development in the Arabidopsis gynoecium. Plant Cell, 21, 1394-1409.
76. Verwoerd, T.C., Dekker, B.M., and, Hoekema, A., (1989) A small-scale procedure for the rapid isolation of plant RNAs. Nucleic Acids Res. 17, 2362.
77. Yu, L.P., Simon, E.J., Trotochaud, A.E., and, Clark, S.E., (2000) POLTERGEIST functions to regulate meristem development downstream of the CLAVATA loci. Development, 127, 1661-1670. (Pubitemid 30234923)