The WOX13 homeobox gene promotes replum formation in the Arabidopsis thaliana fruit

Plant Journal

Volumn 73, Issue 1, 2013, Pages 37-49

  Romera Branchat, Maida ^a   Ripoll, Juan José ^b   Yanofsky, Martin F ^b   Pelaz, Soraya ^a,c  

^a CSIC   (Spain)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

Arabidopsis thaliana; Carpel development; Fruit dehiscence; Fruit patterning; JAG FIL activity; WOX genes

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; CARPEL DEVELOPMENT; HOMEOBOX GENES; REGULATORY NETWORK; SHOOT APICAL MERISTEMS; LATERAL AXIS; LATERAL POSITIONS; VALVE MARGINS;

FRUITS; GENES; HISTOLOGY; STEM CELLS; TISSUE;

PLANTS (BOTANY);

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ARABIDOPSIS PROTEIN; HOMEODOMAIN PROTEIN; WOX13 PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; FRUIT; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOMEOBOX; MERISTEM; PHYSIOLOGY; PLANT GENE;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; FRUIT; GENE EXPRESSION REGULATION, PLANT; GENES, HOMEOBOX; GENES, PLANT; HOMEODOMAIN PROTEINS; MERISTEM;

EID: 84871939837     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12010     Document Type: Article

References (81)

1. 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.
2. Arnaud, N., Girin, T., Sorefan, K., Fuentes, S., Wood, T.A., Lawrenson, T., Sablowski, R. and Ostergaard, L. (2010) Gibberellins control fruit patterning in Arabidopsis thaliana. Genes Dev. 24, 2127-2132.
3. 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.
4. Bao, X., Franks, R.G., Levin, J.Z. and Liu, Z. (2004) Repression of AGAMOUS by BELLRINGER in floral and inflorescence meristems. Plant Cell, 16, 1478-1489.
5. Bellaoui, M., Pidkowich, M.S., Samach, A., Kushalappa, K., Kohalmi, S.E., Modrusan, Z., Crosby, W.L. and Haughn, G.W. (2001) The Arabidopsis BELL1 and KNOX TALE homeodomain proteins interact through a domain conserved between plants and animals. Plant Cell, 13, 2455-2470.
6. Bensmihen, S., To, A., Lambert, G., Kroj, T., Giraudat, J. and Parcy, F. (2004) Analysis of an activated ABI5 allele using a new selection method for transgenic Arabidopsis seeds. FEBS Lett. 561, 127-131.
7. Bhatt, A.M., Etchells, J.P., Canales, C., Lagodienko, A. and Dickinson, H. (2004) VAAMANA-a BEL1-like homeodomain protein, interacts with KNOX proteins BP and STM and regulates inflorescence stem growth in Arabidopsis. Gene, 328, 103-111.
8. Blazquez, M.A., Soowal, L.N., Lee, I. and Weigel, D. (1997) LEAFY expression and flower initiation in Arabidopsis. Development, 124, 3835-3844.
9. Breuninger, H., Rikirsch, E., Hermann, M., Ueda, M. and Laux, T. (2008) Differential expression of WOX genes mediates apical-basal axis formation in the Arabidopsis embryo. Dev. Cell, 14, 867-876.
10. Byrne, M.E., Simorowski, J. and Martienssen, R.A. (2002) ASYMMETRIC LEAVES1 reveals knox gene redundancy in Arabidopsis. Development, 129, 1957-1965.
11. Byrne, M.E., Groover, A.T., Fontana, J.R. and Martienssen, R.A. (2003) Phyllotactic pattern and stem cell fate are determined by the Arabidopsis homeobox gene BELLRINGER. Development, 130, 3941-3950.
12. Carles, C.C. and Fletcher, J.C. (2003) Shoot apical meristem maintenance: The art of a dynamic balance. Trends Plant Sci. 8, 394-401.
13. Castillejo, C. and Pelaz, S. (2008) The balance between CONSTANS and TEMPRANILLO activities determines FT expression to trigger flowering. Curr. Biol. 18, 1338-1343.
14. Chandler, J., Nardmann, J. and Werr, W. (2008) Plant development revolves around axes. Trends Plant Sci. 13, 78-84.
15. Chen, Q., Atkinson, A., Otsuga, D., Christensen, T., Reynolds, L. and Drews, G.N. (1999) The Arabidopsis FILAMENTOUS FLOWER gene is required for flower formation. Development, 126, 2715-2726.
16. Chuck, G., Lincoln, C. and Hake, S. (1996) KNAT1 induces lobed leaves with ectopic meristems when overexpressed in Arabidopsis. Plant Cell, 8, 1277-1289.
17. Chung, M.Y., Vrebalov, J., Alba, R., Lee, J., McQuinn, R., Chung, J.D., Klein, P. and Giovannoni, J. (2010) A tomato (Solanum lycopersicum) APET-ALA2/ERF gene, SlAP2a, is a negative regulator of fruit ripening. Plant J. 6, 936-947.
18. 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.
19. Cole, M., Nolte, C. and Werr, W. (2006) Nuclear import of the transcription factor SHOOT MERISTEMLESS depends on heterodimerization with BLH proteins expressed in discrete sub-domains of the shoot apical meristem of Arabidopsis thaliana. Nucleic Acids Res. 34, 1281-1292.
20. Dai, M., Hu, Y., Zhao, Y., Liu, H. and Zhou, D.X. (2007) A WUSCHEL-LIKE HOMEOBOX gene represses a YABBY gene expression required for rice leaf development. Plant Physiol. 144, 380-390.
21. Deveaux, Y., Toffano-Nioche, C., Claisse, G., Thareau, V., Morin, H., Laufs, P., Moreau, H., Kreis, M. and Lecharny, A. (2008) Genes of the most conserved WOX clade in plants affect root and flower development in Arabidopsis. BMC Evol. Biol. 8, 291.
22. Dinneny, J.R., Yadegari, R., Fischer, R.L., Yanofsky, M.F. and Weigel, D. (2004) The role of JAGGED in shaping lateral organs. Development, 131, 1101-1110.
23. Dinneny, J.R., Weigel, D. and Yanofsky, M.F. (2005) A genetic framework for fruit patterning in Arabidopsis thaliana. Development, 132, 4687-4696.
24. Ditta, G., Pinyopich, A., Robles, P., Pelaz, S. and Yanofsky, M.F. (2004) The SEP4 gene of Arabidopsis thaliana functions in floral organ and meristem identity. Curr. Biol. 14, 1935-1940.
25. Douglas, S.J., Chuck, G., Dengler, R.E., Pelecanda, L. and Riggs, C.D. (2002) KNAT1 and ERECTA regulate inflorescence architecture in Arabidopsis. Plant Cell, 14, 547-558.
26. Endrizzi, K., Moussian, B., Haecker, A., Levin, J.Z. and Laux, T. (1996) The SHOOT MERISTEMLESS gene is required for maintenance of undifferentiated cells in Arabidopsis shoot and floral meristems and acts at a different regulatory level than the meristem genes WUSCHEL and ZWILLE. Plant J. 10, 967-979.
27. Ferrandiz, C., Liljegren, S.J. and Yanofsky, M.F. (2000) Negative regulation of the SHATTERPROOF genes by FRUITFULL during Arabidopsis fruit development. Science, 289, 436-438.
28. Ferrandiz, C., Gu, Q., Martienssen, R. and Yanofsky, M.F. (2000) Redundant regulation of meristem identity and plant architecture by FRUITFULL, APETALA1 and CAULIFLOWER. Development, 127, 725-734.
29. Girin, T., Sorefan, K. and Ostergaard, L. (2009) Meristematic sculpting in fruit development. J. Exp. Bot. 60, 1493-1502.
30. Girin, T., Stephenson, P., Goldsack, C.M., Kempin, S.A., Perez, A., Pires, N., Sparrow, P.A., Wood, T.A., Yanofsky, M.F. and Ostergaard, L. (2010) Brassicaceae INDEHISCENT genes specify valve margin cell fate and repress replum formation. Plant J. 63, 329-338.
31. van der Graaff, E., Laux, T. and Rensing, S.A. (2009) The WUS homeoboxcontaining (WOX) protein family. Genome Biol. 10, 248.
32. Groszmann, M., Paicu, T. and Smyth, D.R. (2008) Functional domains of SPATULA, a bHLH transcription factor involved in carpel and fruit development in Arabidopsis. Plant J. 55, 40-52.
33. Gu, Q., Ferrandiz, C., Yanofsky, M.F. and Martienssen, R. (1998) The FRUITFULL MADS-box gene mediates cell differentiation during Arabidopsis fruit development. Development, 125, 1509-1517.
34. Guo, M., Thomas, J., Collins, G. and Timmermans, M.C. (2008) Direct repression of KNOX loci by the ASYMMETRIC LEAVES1 complex of Arabidopsis. Plant Cell, 20, 48-58.
35. Ha, C.M., Jun, J.H. and Fletcher, J.C. (2010) Control of Arabidopsis leaf morphogenesis through regulation of the YABBY and KNOX families of transcription factors. Genetics, 186, 197-206.
36. Hackbusch, J., Richter, K., Muller, J., Salamini, F. and Uhrig, J.F. (2005) A central role of Arabidopsis thaliana ovate family proteins in networking and subcellular localization of 3-aa loop extension homeodomain proteins. Proc. Natl Acad. Sci. USA, 102, 4908-4912.
37. Haecker, A., Gross-Hardt, R., Geiges, B., Sarkar, A., Breuninger, H., Herrmann, M. and Laux, T. (2004) Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development, 131, 657-668.
38. Honma, T. and Goto, K. (2001) Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature, 409, 525-529.
39. Hruz, T., Laule, O., Szabo, G., Wessendorp, F., Bleuler, S., Oertle, L., Widmayer, P., Gruissem, W. and Zimmermann, P. (2008) Genevestigator v3: A reference expression database for the meta-analysis of transcriptomes. Adv. Bioinformatics, 2008, 420747.
40. Ji, J., Strable, J., Shimizu, R., Koenig, D., Sinha, N. and Scanlon, M.J. (2010) WOX4 promotes procambial development. Plant Physiol. 152, 1346-1356.
41. Kanrar, S., Onguka, O. and Smith, H.M. (2006) Arabidopsis inflorescence architecture requires the activities of KNOX-BELL homeodomain heterodimers. Planta, 224, 1163-1173.
42. Karlova, R., Rosin, F.M., Busscher-Lange, J., Parapunova, V., Do, P.T., Fernie, A.R., Fraser, P.D., Baxter, C., Angenent, G.C. and de Maagd, R. A. (2011) Transcriptome and metabolite profiling show that APETALA2a is a major regulator of tomato fruit ripening. Plant Cell, 3, 923-941.
43. Kumaran, M.K., Bowman, J.L. and Sundaresan, V. (2002) YABBY polarity genes mediate the repression of KNOX homeobox genes in Arabidopsis. Plant Cell, 14, 2761-2770.
44. Liljegren, S.J., Ditta, G.S., Eshed, Y., Savidge, B., Bowman, J.L. and Yanofsky, M.F. (2000) SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature, 404, 766-770.
45. Liljegren, S.J., Roeder, A.H., Kempin, S.A., Gremski, K., Ostergaard, L., Guimil, S., Reyes, D.K. and Yanofsky, M.F. (2004) Control of fruit patterning in Arabidopsis by INDEHISCENT. Cell, 116, 843-853.
46. Lincoln, C., Long, J., Yamaguchi, J., Serikawa, K. and Hake, S. (1994) A knotted1-like homeobox gene in Arabidopsis is expressed in the vegetative meristem and dramatically alters leaf morphology when overexpressed in transgenic plants. Plant Cell, 6, 1859-1876.
47. 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.
48. Martinez-Laborda, A. and Vera, A. (2009) Fruit development and seed dispersal. In Fruit Development and Seed Dispersal (Østergaard, L., ed.). Cambridge: Wiley-Blackwell, pp. 172-203.
49. Matsumoto, N. and Okada, K. (2001) A homeobox gene, PRESSED FLOWER, regulates lateral axis-dependent development of Arabidopsis flowers. Genes Dev. 15, 3355-3364.
50. 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.
51. Nakata, M., Matsumoto, N., Tsugeki, R., Rikirsch, E., Laux, T. and Okada, K. (2012) Roles of the middle domain-specific WUSCHEL-RELATED HOMEOBOX genes in early development of leaves in Arabidopsis. Plant Cell, 24, 519-535.
52. Nardmann, J., Reisewitz, P. and Werr, W. (2009) Discrete shoot and root stem cell-promoting WUS/WOX5 functions are an evolutionary innovation of angiosperms. Mol. Biol. Evol. 26, 1745-1755.
53. Ohno, C.K., Reddy, G.V., Heisler, M.G. and Meyerowitz, E.M. (2004) The Arabidopsis JAGGED gene encodes a zinc finger protein that promotes leaf tissue development. Development, 131, 1111-1122.
54. Ori, N., Eshed, Y., Chuck, G., Bowman, J.L. and Hake, S. (2000) Mechanisms that control knox gene expression in the Arabidopsis shoot. Development, 127, 5523-5532.
55. Park, S.O., Zheng, Z., Oppenheimer, D.G. and Hauser, B.A. (2005) The PRETTY FEW SEEDS2 gene encodes an Arabidopsis homeodomain protein that regulates ovule development. Development, 132, 841-849.
56. Pelaz, S., Tapia-Lopez, R., Alvarez-Buylla, E.R. and Yanofsky, M.F. (2001) Conversion of leaves into petals in Arabidopsis. Curr. Biol. 11, 182-184.
57. Ragni, L., Belles-Boix, E., Gunl, M. and Pautot, V. (2008) Interaction of KNAT6 and KNAT2 with BREVIPEDICELLUS and PENNYWISE in Arabi dopsis inflorescences. Plant Cell, 20, 888-900.
58. Rajani, S. and Sundaresan, V. (2001) The Arabidopsis myc/bHLH gene ALCATRAZ enables cell separation in fruit dehiscence. Curr. Biol. 11, 1914-1922.
59. Ripoll, J.J., Roeder, A.H., Ditta, G.S. and Yanofsky, M.F. (2011) A novel role for the floral homeotic gene APETALA2 during Arabidopsis fruit development. Development, 138, 5167-5176.
60. Robles, P. and Pelaz, S. (2005) Flower and fruit development in Arabidopsis thaliana. Int. J. Dev. Biol. 49, 633-643.
61. Roeder, A.H. and Yanofsky, M.F. (2006) Fruit development in Arabidopsis. Arabidopsis Book, 4, e0075.
62. Roeder, A.H., Ferrandiz, C. and Yanofsky, M.F. (2003) The role of the REPLUMLESS homeodomain protein in patterning the Arabidopsis fruit. Curr. Biol. 13, 1630-1635.
63. Rutjens, B., Bao, D., van Eck-Stouten, E., Brand, M., Smeekens, S. and Proveniers, M. (2009) Shoot apical meristem function in Arabidopsis requires the combined activities of three BEL1-like homeodomain proteins. Plant J. 58, 641-654.
64. Sarkar, A.K., Luijten, M., Miyashima, S., Lenhard, M., Hashimoto, T., Nakajima, K., Scheres, B., Heidstra, R. and Laux, T. (2007) Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature, 446, 811-814.
65. Savidge, B., Rounsley, S.D. and Yanofsky, M.F. (1995) Temporal relationship between the transcription of two Arabidopsis MADS box genes and the floral organ identity genes. Plant Cell, 7, 721-733.
66. Sawa, S., Ito, T., Shimura, Y. and Okada, K. (1999) FILAMENTOUS FLOWER controls the formation and development of Arabidopsis inflorescences and floral meristems. Plant Cell, 11, 69-86.
67. Schmid, M., Davison, T.S., Henz, S.R., Pape, U.J., Demar, M., Vingron, M., Scholkopf, B., Weigel, D. and Lohmann, J.U. (2005) A gene expression map of Arabidopsis thaliana development. Nat. Genet. 37, 501-506.
68. Scofield, S., Dewitte, W. and Murray, J.A. (2007) The KNOX gene SHOOT MERISTEMLESS is required for the development of reproductive meristematic tissues in Arabidopsis. Plant J. 50, 767-781.
69. Siegfried, K.R., Eshed, Y., Baum, S.F., Otsuga, D., Drews, G.N. and Bowman, J.L. (1999) Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. Development, 126, 4117-4128.
70. Skylar, A., Hong, F., Chory, J., Weigel, D. and Wu, X. (2010) STIMPY mediates cytokinin signaling during shoot meristem establishment in Arabidopsis seedlings. Development, 137, 541-549.
71. Smith, H.M. and Hake, S. (2003) The interaction of two homeobox genes, BREVIPEDICELLUS and PENNYWISE, regulates internode patterning in the Arabidopsis inflorescence. Plant Cell, 15, 1717-1727.
72. Smith, H.M., Campbell, B.C. and Hake, S. (2004) Competence to respond to floral inductive signals requires the homeobox genes PENNYWISE and POUND-FOOLISH. Curr. Biol. 14, 812-817.
73. Suer, S., Agusti, J., Sanchez, P., Schwarz, M. and Greb, T. (2011) WOX4 imparts auxin responsiveness to cambium cells in Arabidopsis. Plant Cell, 23, 3247-3259.
74. Ueda, M., Zhang, Z. and Laux, T. (2011) Transcriptional activation of Arabidopsis axis patterning genes WOX8/9 links zygote polarity to embryo development. Dev. Cell, 20, 264-270.
75. Vandenbussche, M., Horstman, A., Zethof, J., Koes, R., Rijpkema, A.S. and Gerats, T. (2009) Differential recruitment of WOX transcription factors for lateral development and organ fusion in Petunia and Arabidopsis. Plant Cell, 21, 2269-2283.
76. Venglat, S.P., Dumonceaux, T., Rozwadowski, K., Parnell, L., Babic, V., Keller, W., Martienssen, R., Selvaraj, G. and Datla, R. (2002) The homeobox gene BREVIPEDICELLUS is a key regulator of inflorescence architecture in Arabidopsis. Proc. Natl Acad. Sci. USA, 99, 4730-4735.
77. Vrebalov, J., Pan, I.L., Arroyo, A.J. et al. (2009) Fleshy fruit expansion and ripening are regulated by the tomato SHATTERPROOF gene TAGL1. Plant Cell, 10, 3041-3062.
78. Wu, X., Dabi, T. and Weigel, D. (2005) Requirement of homeobox gene STIMPY/WOX9 for Arabidopsis meristem growth and maintenance. Curr. Biol. 15, 436-440.
79. Wu, X., Chory, J. and Weigel, D. (2007) Combinations of WOX activities regulate tissue proliferation during Arabidopsis embryonic development. Dev. Biol. 309, 306-316.
80. Zhao, Y., Hu, Y., Dai, M., Huang, L. and Zhou, D.X. (2009) The WUSCHELrelated homeobox gene WOX11 is required to activate shoot-borne crown root development in rice. Plant Cell, 21, 736-748.
81. Zhu, H.L., Zhu, B.Z., Shao, Y., Lin, X.J., Wang, X.G., Gao, H.Y., Xie, Y.H., Li, Y.C. and Luo, Y.B. (2007) Molecular cloning and characterization of ETHYLENE OVERPRODUCER 1-LIKE 1 gene, LeEOL1, from tomato (Lycopersicon esculentum Mill.) fruit. DNA Seq. 18, 131-137.