Conservation and divergence of APETALA1/FRUITFULL-like gene function in grasses: Evidence from gene expression analyses

Plant Journal

Volumn 52, Issue 1, 2007, Pages 69-81

  Preston, Jill C ^a   Kellogg, Elizabeth A ^a  

^a UNIVERSITY OF MISSOURI ST LOUIS   (United States)

Author keywords

APETALA1; FRUITFULL; Gene duplication; Grasses; MADS box

Indexed keywords

APETALA1; GENE DUPLICATION; MADS BOX;

BIOLOGICAL ORGANS; MOLECULAR INTERACTIONS; PLANTS (BOTANY);

GENE EXPRESSION;

PRIMER DNA; VEGETABLE PROTEIN;

ARTICLE; CLASSIFICATION; GENE EXPRESSION; GENETICS; IN SITU HYBRIDIZATION; MOLECULAR EVOLUTION; NUCLEOTIDE SEQUENCE; PHYLOGENY; POACEAE; SOUTHERN BLOTTING;

BASE SEQUENCE; BLOTTING, SOUTHERN; DNA PRIMERS; EVOLUTION, MOLECULAR; GENE EXPRESSION; IN SITU HYBRIDIZATION; PHYLOGENY; PLANT PROTEINS; POACEAE;

ARABIDOPSIS; LOLIUM; LOLIUM TEMULENTUM; ORYZA SATIVA; PALEA; POACEAE;

EID: 34748881306     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2007.03209.x     Document Type: Article

References (80)

1. Ambrose, B.A., Lerner, D.R., Ciceri, P., Padilla, C.M., Yanofsky, M.F. Schmidt, R.J. (2000) Molecular and genetic analyses of the Silky1 gene reveal conservation in floral organ specification between eudicots and monocots. Mol. Cell, 5, 569 579.
2. Becker, A. Theissen, G. (2003) The major clades of MADS-box genes and their role in the development and evolution of flowering plants. Mol. Phylogenet. Evol. 29, 464 489.
3. Benlloch, R., d'Erfurth, I., Ferrándiz, C., Cosson, V., Beltrán, J.P., Cañas, L.A., Kondorosi, A., Madueño, F. Ratet, P. (2006) Isolation of mtpim proves Tnt1 a useful reverse genetics tool in Medicago truncatula and uncovers new aspects of AP1-like functions in legumes. Plant Physiol. 142, 972 983.
4. Berbel, A., Navarro, C., Ferrándiz, C., Cañas, L.A., Madueño, F. Beltrán, J.P. (2001) Analysis of PEAM4, the pea AP1 functional homologue, supports a model for AP1-like genes controlling both floral meristem and floral organ identity in different plant species. Plant J. 25, 441 451.
5. Blázquez, M.A., Soowal, L., Lee, I. Weigel, D. (1997) LEAFY expression and flower initiation in Arabidopsis. Development, 124, 3835 3844.
6. Bowman, J.L., Smyth, D.R. Meyerowitz, E.M. (1989) Genes directing flower development in Arabidopsis. Plant Cell, 1, 37 52.
7. Cacharrón, J., Saedler, H. Theissen, G. (1999) Expression of MADS box genes ZMM8 and ZMM14 during inflorescence development of Zea mays discriminates between the upper and the lower floret of each spikelet. Dev. Genes Evol. 209, 411 420.
8. Carpenter, R., Copsey, L., Vincent, C., Doyle, S., Magath, R. Coen, E. (1995) Control of flower development and phyllotaxy by meristem identity genes in Antirrhinum. Plant Cell, 7, 2001 2011.
9. Clifford, H.T. (1987) Spikelet and floral morphology. In Grass Systematics and Evolution (Soderstrom, T.R., Hilu, K.W., Campbell, C.S. Barkworth, M.E., eds). Washington, DC : Smithsonian Institute, pp. 21 30.
10. Coen, E.S. Meyerowitz, E.M. (1991) The war of the whorls: genetic interactions controlling flower development. Nature, 353, 31 37.
11. Cooper, B., Clarke, J.D., Budworth, P. et al. (2003) A network of rice genes associated with stress response and seed development. Proc. Natl Acad. Sci. USA, 100, 4945 4950.
12. Danyluk, J., Kane, N.A., Breton, G., Limin, A.E., Fowler, D.B. Sarhan, F. (2003) TaVRT-1, a putative transcription factor associated with vegetative to reproductive transition in cereals. Plant Physiol. 132, 1849 1860.
13. 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.
14. Doust, A.N. Kellogg, E.A. (2002) Inflorescence diversification in the panicoid 'bristle grass' clade (Paniceae, Poaceae): evidence from molecular phylogenies and developmental morphology. Am. J. Bot. 89, 1203 1222.
15. Doyle, J.J. Doyle, J.L. (1987) A rapid DNA isolation procedure for small quantities of fresh leaf material. Phytochem. Bull. 19, 11 15.
16. Egea-Cortines, M., Saedler, H. Sommer, H. (1999) Ternary complex formation between the MADS-box proteins SQUAMOSA, DEFICIENS and GLOBOSA is involved in the control of floral architecture in Antirrhinum majus. EMBO J. 18, 5370 5379.
17. Ferrándiz, C., Gu, Q., Martienssen, R. Yanofsky, M.F. (2000) Redundant regulation of meristem identity and plant architecture by FRUITFULL, APETALA1 and CAULIFLOWER. Development, 127, 725 734.
18. Gocal, G.F.W., King, R.W., Blundell, C.A., Schwartz, O.M., Andersen, C.H. Weigel, D. (2001) Evolution of floral meristem identity genes. Analyses of Lolium temulentum genes related to APETALA1 and LEAFY of Arabidopsis. Plant Physiol. 125, 1788 1801.
19. Greco, R., Stagi, L., Colombo, L., Angenent, G.C., Sari-Gorla, M. Pe, M.E. (1997) MADS box genes expressed in developing inflorescences of rice and sorghum. Mol. Gen. Genet. 253, 615 623.
20. Heuer, S., Hansen, S., Bantin, J., Brettschneider, R., Kranz, E., Lorz, H. Dresselhaus, T. (2001) The maize MADS box gene ZmMADS3 affects node number and spikelet development and is co-expressed with ZmMADS1 during flower development in egg cells, and early embryogenesis. Plant Physiol. 127, 33 45.
21. Honma, T. Goto, K. (2001) Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature, 409, 525 529.
22. Huijser, P., Klein, J., Lonnig, W.E., Saedler, H. Sommer, H. (1992) Bracteomania, an inflorescence anomaly, is caused by the loss of function of the MADS-box gene squamosa in Antirrhinum majus. EMBO J. 11, 1239 1249.
23. Immink, R.G.H., Gadella, T.W.J., Ferrario, S., Busscher, M. Angenent, G.C. (2002) Analysis of MADS box protein-protein interactions in living plant cells. Proc. Natl Acad. Sci. USA, 99, 2416 2421.
24. Irish, V.F. Sussex, I.M. (1990) Function of the apetala-1 gene during Arabidopsis floral development. Plant Cell, 2, 741 753.
25. Jackson, D. (1991) In situ hybridization in plants. In Molecular Plant Pathology: A Practical Approach (Bowles, D.J., Gurr, S.J. McPherson, M., eds). Oxford : Oxford University Press, pp. 163 174.
26. Jackson, D., Veit, B. Hake, S. (1994) Expression of maize KNOTTED1 related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot. Development, 120, 405 413.
27. Jeon, J.S., Jang, S., Lee, S.H., Chung, Y.Y., Kim, S.R., Lee, Y.H., Cho, Y.G. An, G. (2000) leafy hull sterile1 is a homeotic mutation in a rice MADS box gene affecting rice flower development. Plant Cell, 12, 871 884.
28. Kaufmann, K., Melzer, R. Theissen, G. (2005) MIKC-type MADS-domain proteins: structural modularity, protein interactions and network evolution in land plants. Gene, 347, 183 198.
29. Kellogg, E.A. (2000) A model of inflorescence development. In Monocots: Systematics and Evolution (Wilson, K.L. Morrison, D.A., eds). Melbourne, Victoria, Australia : CSIRO Publishing, pp. 84 88.
30. Kempin, S., Savidge, B. Yanofsky, M.F. (1995) Molecular basis of the cauliflower phenotype in Arabidopsis. Science, 267, 522 525.
31. Kim, S., Koh, J., Yoo, M.J., Kong, H., Hu, Y., Ma, H., Soltis, P.S. Soltis, D.E. (2005) Expression of floral MADS-box genes in basal angiosperms: implications for the evolution of floral regulation. Plant J. 43, 724 744.
32. Krizek, B.A. Meyerowitz, E.M. (1996) Mapping the protein regions responsible for the functional specificities of the Arabidopsis MADS domain organ-identity proteins. Proc. Natl Acad. Sci. USA, 93, 4063 4070.
33. Laurie, D.A., Pratchett, N., Devos, K.M., Leitch, I.J. Gale, M.D. (1993) The distribution of RFLP markers on chromosome 2 (2H) of barley in relation to the physical and genetic location of 5S rDNA. Theor. Appl. Genet. 87, 177 183.
34. Lim, J., Moon, Y.H., An, G. Yang, S.K. (2000) Two rice MADS domain proteins interact with OsMADS1. Plant Mol. Biol. 44, 513 527.
35. Litt, A. (2007) An evaluation of A-function: evidence from the Apetala1 and Apetala2 gene lineages. Int. J. Plant Sci. 168, 73 91.
36. Litt, A. Irish, V.F. (2003) Duplication and diversification in the APETALA1/FRUITFULL floral homeotic gene lineage: implications for the evolution of floral development. Genetics, 165, 821 833.
37. Loukoianov, A., Yan, L., Blechl, A., Sanchez, A. Dubcovsky, J. (2005) Regulation of VRN-1 vernalization genes in normal and transgenic polyploid wheat. Plant Physiol. 138, 2364 2373.
38. Maddison, D.R. Maddison, W.P. (2003) MacClade: Analysis of Phylogeny and Character Evolution. Sunderland : Sinauer Associates.
39. Malcomber, S.T. Kellogg, E.A. (2004) Heterogeneous expression patterns and separate roles of the SEPALLATA gene LEAFY HULL STERILE1 in grasses. Plant Cell, 16, 1692 1706.
40. Malcomber, S.T. Kellogg, E.A. (2005) SEPALLATA gene diversification: brave new whorls. Trends Plant Sci. 10, 427 435.
41. Malcomber, S.T., Preston, J.C., Reinheimer, R., Kossuth, J. Kellogg, E.A. (2006) Developmental gene evolution and the origin of grass inflorescence diversity. Adv. Bot. Res. 44, 426 481.
42. Mandel, M.A. Yanofsky, M.F. (1995) A gene triggering flower formation in Arabidopsis flowers. Genes Dev. 15, 3355 3364.
43. Mandel, M.A., Gustafson-Brown, C., Savidge, B. Yanofsky, M.F. (1992) Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature, 360, 273 277.
44. Mena, M., Mandel, M.A., Lerner, D.R., Yanofsky, M.F. Schmidt, R.J. (1995) A characterization of the MADS-box gene family in maize. Plant J. 8, 845 854.
45. Moon, Y.H., Kang, H.G., Jung, J.Y., Joen, J.S., Sung, S.K. An, G. (1999) Determination of the motif responsible for interaction between the rice APETALA1/AGAMOUS-LIKE9 family proteins using a yeast two-hybrid system. Plant Physiol. 120, 1193 1204.
46. Murai, K., Miyamae, M., Kato, H., Takumi, S. Ogihara, Y. (2003) WAP1, a wheat APETALA1 homolog, plays a central role in the phase transition from vegetative to reproductive growth. Plant Cell Physiol. 44, 1255 1265.
47. Onouchi, H., Igeno, M.I., Perilleux, C., Graves, K. Coupland, G. (2000) Mutagenesis of plants overexpressing CONSTANS demonstrates novel interactions among Arabidopsis flowering-time genes. Plant Cell, 12, 885 900.
48. Paterson, A.H., Bowers, J.E. Chapman, B.A. (2004) Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics. Proc. Natl Acad. Sci. USA, 101, 9903 9908.
49. Pelaz, S., Ditta, G.S., Baumann, E., Wisman, E. Yanofksy, M.F. (2000) B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature, 405, 200 203.
50. Pelaz, S., Gustafson-Brown, C., Kohalmi, S.E., Crosby, W.L. Yanofsky, M.F. (2001) APETALA1 and SEPALLATA3 interact to promote flower development. Plant J. 26, 385 394.
51. Pelucchi, N., Fornara, F., Favalli, C., Masiero, S., Lago, C., Pè, M.E., Colombo, L. Kater, M.M. (2002) Comparative analysis of rice MADS-box genes expressed during flower development. Sex. Plant Reprod. 15, 113 122.
52. Petersen, K., Didion, T., Andersen, C.H. Nielsen, K.K. (2004) MADS-box genes from perennial ryegrass differentially expressed during transition from vegetative to reproductive growth. J. Plant Physiol. 161, 439 447.
53. Petersen, K., Kolmos, E., Folling, M., Salchert, K., Storgaard, M., Jensen, C.S., Didion, T. Nielsen, K.K. (2006) Two MADS-box genes from perennial ryegrass are regulated by vernalization and involved in the floral transition. Physiol. Plant. 126, 268 278.
54. Prasad, K., Sriram, P., Kumar, C.S., Kushalappa, K. Vijayraghavan, U. (2001) Ectopic expression of rice OsMADS1 reveals a role in specifying the lemma and palea, grass floral organs analogous to sepals. Dev. Genes Evol. 211, 281 290.
55. Prasad, K., Parameswaran, S. Vijayraghavan, U. (2005) OsMADS1, a rice MADS-box factor, controls differentiation of specific cell types in the lemma and palea and is an early-acting regulator of inner floral organs. Plant J. 43, 915 928.
56. Preston, J.C. Kellogg, E.A. (2006) Reconstructing the evolutionary history of paralogous APETALA1/FRUITFULL-like genes in grasses (Poaceae). Genetics, 174, 421 437.
57. Purugganan, M.D., Rounsley, S.D., Schmidt, R.J. Yanofsky, M.F. (1995) Molecular evolution of flower development: diversification of the plant MADS-box regulatory gene family. Genetics, 140, 345 356.
58. Reinheimer, R., Malcomber, S.T. Kellogg, E.A. (2006) Evidence for distinct roles of the SEPALLATA gene LEAFY HULL STERILE1 in Eleusine indica and Megathyrsus maximus (Poaceae). Evol. Dev. 8, 293 303.
59. Riechmann, J.L. Meyerowitz, E.M. (1997) Determination of floral organ identity by Arabidopsis MADS domain homeotic proteins AP1, AP3, PI, and AG is independent of their DNA-binding specificity. Mol. Biol. Cell, 8, 1243 1259.
60. Samach, A., Onouchi, H., Gold, S.E., Ditta, G.S., Schwarz-Sommer, Z., Yanofsky, M.F. Coupland, G. (2000) Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science, 288, 1613 1616.
61. Schwarz-Sommer, Z., Huijser, P., Nacken, W., Saedler, H. Sommer, H. (1990) Genetic control of flower development by homeotic genes in Antirrhinum majus. Science, 250, 931 936.
62. Shan, H., Zhang, N., Cuijing, L., Xu, G., Zhang, J., Chen, Z. Kong, H. (2007) Patterns of gene duplication and functional diversification during the evolution of the AP11/SQUA subfamily of plant MADS-box genes. Mol. Phylogenet. Evol. 44, 26 41.
63. Shitsukawa, N., Takagishi, A., Ikari, C., Takumi, S. Murai, K. (2006) WFL, a wheat FLORICAULA/LEAFY ortholog, is associated with spikelet formation as lateral branch of the inflorescence meristem. Genes Genet. Syst. 81, 13 20.
64. Simpson, G.G. Dean, C. (2002) Arabidopsis, the Rosetta stone of flowering time? Science, 296, 285 289.
65. Theissen, G. (2001) Development of floral organ identity: stories from the MADS house. Curr. Opin. Plant Biol. 4, 75 85.
66. Theissen, G. Saedler, H. (2001) Floral quartets. Nature, 409, 469 471.
67. Theissen, G., Kim, J.T. Saedler, H. (1996) Classification and phylogeny of the MADS-box multigene family suggest defined roles of MADS-box gene subfamilies in the morphological evolution of eukaryotes. J. Mol. Evol. 43, 484 516.
68. Theissen, G., Becker, A., Di Rosa, A., Kanno, A., Kim, J.T., Münster, T., Winter, K.U. Saedler, H. (2000) A short history of MADS box genes in plants. Plant Mol. Biol. 42, 115 149.
69. Trevaskis, B., Bagnall, D.J., Ellis, M.H., Peacock, W.J. Dennis, E.S. (2003) MADS box genes control vernalization-induced flowering in cereals. Proc. Natl Acad. Sci. USA, 100, 13099 13104.
70. Trevaskis, B., Hemming, M.N., Peacock, W.J. Dennis, E.S. (2006) HvVRN2 responds to daylength whereas HvVRN1 is regulated by vernalization and developmental status. Plant Physiol. 140, 1397 1405.
71. Von Zitzewitz, J., Szucs, P., Dubcovsky, J., Yan, L., Francia, E., Pecchioni, N., Casa, A., Chen, T.H., Hayes, P.M. Skinner, J.S. (2005) Molecular and structural characterization of barley vernalization genes. Plant Mol. Biol. 59, 449 467.
72. Weigel, D. Meyerowitz, E.M. (1994) The ABCs of floral homeotic genes. Cell, 78, 203 209.
73. Whipple, C.J. Schmidt, R.J. (2006) Genetics of grass flower development. Adv. Bot. Res. 44, 426 481.
74. Whipple, C.J., Ciceri, P., Padilla, C.M., Ambrose, B.A., Bandong, S.L. Schmidt, R.J. (2004) Conservation of B-class floral homeotic gene function between maize and Arabidopsis. Development, 131, 6083 6091.
75. Whipple, C.J., Zanis, M., Kellogg, E.A. Schmidt, R.J. (2007) Conservation of B class MADS-box gene expression in the second whorl of a basal grass and outgroups links the origin of lodicules and petals. Proc. Natl Acad. Sci. USA, 104, 1081 1086.
76. Wolfe, K.H., Gouy, M., Yang, Y.W., Sharp, P.M. Li, W.H. (1987) Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast and nuclear DNAs. Proc. Natl Acad. Sci. USA, 84, 9054 9058.
77. Yan, L., Loukoianov, A., Tranquilli, G., Helguera, M., Fahima, T. Dubcovksy, J. (2003) Positional cloning of the wheat vernalization gene VRN1. Proc. Natl Acad. Sci. USA, 100, 6263 6268.
78. Yanofsky, M.F., Ma, H., Bowman, J.L., Drews, G.N., Feldmann, K.A. Meyerowitz, E.M. (1990) The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature, 346, 35 39.
79. Yu, H. Goh, C.J. (2000) Identification and characterization of three orchid MADS-box genes of the AP1/AGL9 subfamily during floral transition. Plant Physiol. 123, 1325 1336.
80. Yu, J., Wang, J., Lin, W. et al. (2005) The genomes of Oryza sativa: a history of duplications. PLoS Biol. 3, e38.