The NTT transcription factor promotes replum development in Arabidopsis fruits

Plant Journal

Volumn 80, Issue 1, 2014, Pages 69-81

  Marsch Martínez, Nayelli ^a   Zúñiga Mayo, Victor M ^b   Herrera Ubaldo, Humberto ^b   Ouwerkerk, Pieter B F ^c   Pablo Villa, Jeanneth ^b   Lozano Sotomayor, Paulina ^b   Greco, Raffaella ^d   Ballester, Patricia ^e   Balanzá, Vicente ^e   Kuijt, Suzanne J H ^c   Meijer, Annemarie H ^c   Pereira, Andy ^f   Ferrándiz, Cristina ^e   De Folter, Stefan ^b  

^a DEPARTAMENTO DE INGENIERÍA GENÉTICA   (Mexico)

^b DEPARTAMENTO DE FÍSICA   (Mexico)

^c LEIDEN UNIVERSITY   (Netherlands)

^d PARCO TECNOLOGICO PADANO   (Italy)

^e Ciudad Politécnica de la Innovación   (Spain)

^f UNIVERSITY OF ARKANSAS   (United States)

Author keywords

Arabidopsis thaliana; Fruit development; Fruit patterning; NO TRANSMITTING TRACT; Replum; Transcription factors

Indexed keywords

FRUITS; PROTEINS; SEED; TRANSCRIPTION FACTORS; YEAST;

ARABIDOPSIS; ARABIDOPSIS THALIANA; COMPLEX PLANTS; FRUIT DEVELOPMENT; GENETIC INTERACTION; HOMEOBOX GENES; REPLUM; ZINC FINGER TRANSCRIPTION FACTOR;

TRANSCRIPTION;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ARABIDOPSIS PROTEIN; NTT PROTEIN, ARABIDOPSIS; TRANSCRIPTION FACTOR; ZINC FINGER PROTEIN;

ANTIBODY SPECIFICITY; ARABIDOPSIS; BIOLOGICAL MODEL; CYTOLOGY; FRUIT; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; PHENOTYPE; PLANT SEED; PROMOTER REGION; REPORTER GENE;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; FRUIT; GENE EXPRESSION REGULATION, PLANT; GENES, REPORTER; MODELS, BIOLOGICAL; MUTATION; ORGAN SPECIFICITY; PHENOTYPE; PROMOTER REGIONS, GENETIC; SEEDS; TRANSCRIPTION FACTORS; ZINC FINGERS;

EID: 84924759919     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12617     Document Type: Article

References (54)

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. 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.
3. Belda-Palazon, B., Ruiz, L., Marti, E., Tarraga, S., Tiburcio, A.F., Culianez, F., Farras, R., Carrasco, P. and Ferrando, A. (2012) Aminopropyltransferases involved in polyamine biosynthesis localize preferentially in the nucleus of plant cells. PLoS One, 7, e46907.
4. 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.
5. 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.
6. 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.
7. 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.
8. 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.
9. Chalfun-Junior, A., Franken, J., Mes, J.J., Marsch-Martinez, N., Pereira, A. and Angenent, G.C. (2005) ASYMMETRIC LEAVES2-LIKE1 gene, a member of the AS2/LOB family, controls proximal-distal patterning in Arabidopsis petals. Plant Mol. Biol. 57, 559-575.
10. Chuck, G., Lincoln, C. and Hake, S. (1996) KNAT1 induces lobed leaves with ectopic meristems when overexpressed in Arabidopsis. Plant Cell, 8, 1277-1289.
11. Chung, K., Lee, J., Lee, J. and Ahn, J. (2013) Fruit indehiscence caused by enhanced expression of NO TRANSMITTING TRACT in Arabidopsis thaliana. Mol. Cells, 35, 519-525.
12. 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.
13. Crawford, B.C. and Yanofsky, M.F. (2008) The formation and function of the female reproductive tract in flowering plants. Curr. Biol. 18, R972-R978.
14. Crawford, B.C. and Yanofsky, M.F. (2011) HALF FILLED promotes reproductive tract development and fertilization efficiency in Arabidopsis thaliana. Development, 138, 2999-3009.
15. Crawford, B.C., Ditta, G. and Yanofsky, M.F. (2007) The NTT gene is required for transmitting-tract development in carpels of Arabidopsis thaliana. Curr. Biol. 17, 1101-1108.
16. Dinneny, J.R., Weigel, D. and Yanofsky, M.F. (2005) A genetic framework for fruit patterning in Arabidopsis thaliana. Development, 132, 4687-4696.
17. Engelen, F.A., Molthoff, J.W., Conner, A.J., Nap, J.P., Pereira, A. and Stiekema, W.J. (1995) pBINPLUS: an improved plant transformation vector based on pBIN19. Transgenic Res. 4, 288-290.
18. Ferrandiz, C. (2002) Regulation of fruit dehiscence in Arabidopsis. J. Exp. Bot. 53, 2031-2038.
19. 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.
20. 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, NY: Springer, pp. 145-165.
21. 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.
22. 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.
23. Girin, T., Sorefan, K. and Ostergaard, L. (2009) Meristematic sculpting in fruit development. J. Exp. Bot. 60, 1493-1502.
24. Gonzalez-Reig, S., Ripoll, J.J., Vera, A., Yanofsky, M.F. and Martinez-Laborda, A. (2012) Antagonistic gene activities determine the formation of pattern elements along the mediolateral axis of the Arabidopsis fruit. PLoS Genet. 8, e1003020.
25. 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.
26. 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.
27. 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.
28. Kuijt, S.J.H., Lamers, G.E.M., Rueb, S., Scarpella, E., Ouwerkerk, P.B.F., Spaink, H.P. and Meijer, A.H. (2004) Different subcellular localization and trafficking properties of KNOX class 1 homeodomain proteins from rice. Plant Mol. Biol. 55, 781-796.
29. 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, 805-814.
30. 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.
31. 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.
32. 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.
33. 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, 3654-3670.
34. Longabaugh, W.J., Davidson, E.H. and Bolouri, H. (2005) Computational representation of developmental genetic regulatory networks. Dev. Biol. 283, 1-16.
35. Marsch-Martinez, N., Greco, R., Van Arkel, G., Herrera-Estrella, L. and Pereira, A. (2002) Activation tagging using the En-I maize transposon system in Arabidopsis. Plant Physiol. 129, 1544-1556.
36. Meijer, A.H., Ouwerkerk, P.B.F. and Hoge, J.H.C. (1998) Vectors for transcription factor isolation and target gene identification by means of genetic selection in yeast. Yeast, 14, 1407-1416.
37. Meijer, A.H., Schouten, J., Ouwerkerk, P.B.F. and Hoge, J.H.C. (2000) Yeast as versatile tool in transcription factor research. In Plant Molecular Biology Manual (Gelvin, S.B. and Schilperoort, R.A., eds). Dordrecht: Kluwer Academic Publishers, pp. E3: 1-28.
38. Ori, N., Eshed, Y., Chuck, G., Bowman, J. and Hake, S. (2000) Mechanisms that control knox gene expression in the Arabidopsis shoot. Development, 127, 5523-5532.
39. Ouwerkerk, P.B.F. and Meijer, A.H. (2001) Yeast one-hybrid screening for DNA-protein interactions. Curr. Protoc. Mol. Biol., 11-22. DOI: 10.1002/0471142727.mb1212s55.
40. 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.
41. Ragni, L., Belles-Boix, E., Gunl, M. and Pautot, V. (2008) Interaction of KNAT6 and KNAT2 with BREVIPEDICELLUS and PENNYWISE in Arabidopsis inflorescences. Plant Cell, 20, 888-900.
42. Reyes-Olalde, J.I., Zuniga-Mayo, V.M., Chavez Montes, R.A., Marsch-Martinez, N. and de Folter, S. (2013) Inside the gynoecium: at the carpel margin. Trends Plant Sci. 18, 644-655.
43. Roeder, A.H.K. and Yanofsky, M.F. (2006) Fruit development in Arabidopsis. Arabidopsis Book, 4, e0075.
44. 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.
45. Romera-Branchat, M., Ripoll, J.J., Yanofsky, M.F. and Pelaz, S. (2013) The WOX13 homeobox gene promotes replum formation in the Arabidopsis thaliana fruit. Plant J. 73, 37-49.
46. Sagasser, M., Lu, G.-H., Hahlbrock, K. and Weisshaar, B. (2002) A. thaliana TRANSPARENT TESTA 1 is involved in seed coat development and defines the WIP subfamily of plant zinc finger proteins. Genes Dev. 16, 138-149.
47. 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.
48. 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.
49. 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.
50. Sundberg, E. and Ferrandiz, C. (2009) Gynoecium patterning in Arabidopsis: a basic plan behind a complex structure. In Annual Plant Reviews Volume 38 (Østergaard, L., ed.). Hoboken, NJ: Wiley-Blackwell, pp. 35-69. Doi: 10.1002/9781444314557.ch2.
51. Tissier, A., Marillonnet, S., Klimyuk, V., Patela, K., Torres, M.A., Murphy, G. and Jones, J.D.G. (1999) Multiple independent defective suppressor-mutator transposon insertions in Arabidopsis: a tool for functional genomics. Plant Cell, 11, 1841-1852.
52. Urbanus, S., de Folter, S., Shchennikova, A., Kaufmann, K., Immink, R. and Angenent, G. (2009) In planta localisation patterns of MADS domain proteins during floral development in Arabidopsis thaliana. BMC Plant Biol. 9, 5.
53. 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.
54. Zuniga Mayo, V.M., Marsch Martinez, N. and de Folter, S. (2012) 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 J. 71, 314-326.