Involvement of the MADS-box gene ZMM4 in floral induction and inflorescence development in maize

Plant Physiology

Volumn 147, Issue 4, 2008, Pages 2054-2069

  Danilevskaya, Olga N ^a   Meng, Xin ^a   Selinger, David A ^a   Deschamps, Stéphane ^a   Hermon, Pedro ^a   Vansant, Gordon ^b   Gupta, Rajeev ^a   Ananiev, Evgueni V ^a   Muszynski, Michael G ^a,c  

^a DUPONT COMPANY   (United States)

^b Althea Technologies   (United States)

^c IOWA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRITICUM AESTIVUM; TRITICUM MONOCOCCUM; ZEA MAYS;

BETA GLUCURONIDASE; HYBRID PROTEIN; MADS DOMAIN PROTEIN; MESSENGER RNA; VEGETABLE PROTEIN;

ARTICLE; CHROMOSOME MAP; FLOWER; GENE DUPLICATION; GENE EXPRESSION PROFILING; GENETICS; GROWTH, DEVELOPMENT AND AGING; IN SITU HYBRIDIZATION; MAIZE; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; PLANT CHROMOSOME; REPRODUCTION; SYNTENY; TRANSGENIC PLANT; WHEAT;

CHROMOSOME MAPPING; CHROMOSOMES, PLANT; FLOWERS; GENE DUPLICATION; GENE EXPRESSION PROFILING; GLUCURONIDASE; IN SITU HYBRIDIZATION; MADS DOMAIN PROTEINS; MOLECULAR SEQUENCE DATA; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; RECOMBINANT FUSION PROTEINS; REPRODUCTION; RNA, MESSENGER; SYNTENY; TRITICUM; ZEA MAYS;

EID: 53749085134     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.107.115261     Document Type: Article

References (87)

1. Abe M, Kobayashi Y, Yamamoto S, Daimon Y, Yamaguchi A, Ikeda Y, Ichinoki H, Notaguchi M, Goto K, Araki T (2005) FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science 309: 1052-1056
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. Becker A, Winter KU, Meyer B, Saedler H, Theissen G (2000) MADS-Box gene diversity in seed plants 300 million years ago. Mol Biol Evol 17: 1425-1434
4. Bernier G, Perilleux C (2005) A physiological overview of the genetics of flowering time control. Plant Biotechnol J 3: 3-16
5. Blazquez MA, Soowal LN, Lee I, Weigel D (1997) LEAFY expression and flower initiation in Arabidopsis. Development 124: 3835-3844
6. Blazquez MA, Weigel D (2000) Integration of floral inductive signals in Arabidopsis. Nature 404: 889-892
7. Bomblies K, Doebley JF (2005) Pleiotropic effects of the duplicate maize FLORICAULA/LEAFY genes zfl1 and zfl2 on traits under selection during maize domestication. Genetics 172: 519-531
8. Bomblies K, Wang RL, Ambrose BA, Schmidt RJ, Meeley RB, Doebley J (2003) Duplicate FLORICAULA/LEAFY homologs zfl1 and zfl2 control inflorescence architecture and flower patterning in maize. Development 130: 2385-2395
9. Borner R, Kampmann G, Chandler J, Gleissner R, Wisman E, Apel K, Melzer S (2000) A MADS domain gene involved in the transition to flowering in Arabidopsis. Plant J 24: 591-599
10. Boss PK, Bastow RM, Mylne JS, Dean C (2004) Multiple pathways in the decision to flower: enabling, promoting, and resetting. Plant Cell (Suppl) 16: S18-S31
11. Bradley D, Carpenter R, Sommer H, Hartley N, Coen E (1993) Complementary floral homeotic phenotypes result from opposite orientations of a transposon at the plena locus of Antirrhinum. Cell 72: 85-95
12. Brenner S, Johnson M, Bridgham J, Golda G, Lloyd DH, Johnson D, Luo S, McCurdy S, Foy M, Ewan M et al (2000) Gene expression analysis by massively parallel signature sequencing (MPSS) on microbead arrays. Nat Biotechnol 18: 630-634
13. Bruggmann R, Bharti AK, Gundlach H, Lai J, Young S, Pontaroli AC, Wei F, Haberer G, Fuks G, Du C et al (2006) Uneven chromosome contraction and expansion in the maize genome. Genome Res 16: 1241-1251
14. Brunner S, Fengler K, Morgante M, Tingey S, Rafalski A (2005) Evolution of DNA sequence nonhomologies among maize inbreds. Plant Cell 17: 343-360
15. Cardon GH, Höhmann S, Nettesheim K, Saedler H, Huijser P (1997) Functional analysis of the Arabidopsis thaliana SBP-box gene SPL3: a novel gene involved in the floral transition. Plant J 12: 367-377
16. Chen Q-R, Vansant G, Oades K, Pickering M, Wei JS, Song YK, Monforte J, Khan J (2007) Diagnosis of the small round blue cell tumors using multiplex polymerase chain reaction. J Mol Diagn 9: 80-88
17. Cigan AM, Unger-Wallace E, Haug-Collet K (2005) Transcriptional gene silencing as a tool for uncovering gene function in maize. Plant J 43: 929-940
18. Colasanti J, Sundaresan V (2000) 'Florigen' enters the molecular age: long-distance signals that cause plants to flower. Trends Biochem Sci 25: 236-240
19. Colasanti J, Tremblay R, Wong AY, Coneva V, Kozaki A, Mable BK (2006) The maize INDETERMINATE1 flowering time regulator defines a highly conserved zinc finger protein family in higher plants. BMC Genomics 7: 158
20. Colasanti J, Yuan Z, Sundaresan V (1998) The indeterminate gene encodes a zinc finger protein and regulates a leaf-generated signal required for the transition to flowering in maize. Cell 93: 593-603
21. Corbesier L, Vincent C, Jang S, Fornara F, Fan Q, Searle I, Giakountis A, Farrona S, Gissot L, Turnbull C, et al (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316: 1030-1033
22. Danyluk J, Kane NA, Breton G, Limin AE, Fowler DB, Sarhan F (2003) TaVRT-1, a putative transcription factor associated with vegetative to reproductive transition in cereals. Plant Physiol 132: 1849-1860
23. Ferrandiz C, Gu Q, Martienssen R, Yanofsky MF (2000) Redundant regulation of meristem identity and plant architecture by FRUITFULL, APETALA1 and CAULIFLOWER. Development 127: 725-734
24. Gaut BS (2001) Patterns of chromosomal duplication in maize and their implications for comparative maps of the grasses. Genome Res 11: 55-66
25. Gaut BS, Doebley JF (1997) DNA sequence evidence for the segmental allotetraploid origin of maize. Proc Natl Acad Sci USA 94: 6809-6814
26. Hartmann U, Hohmann S, Nettesheim K, Wisman E, Saedler H, Huijser P (2000) Molecular cloning of SVP: a negative regulator of the floral transition in Arabidopsis. Plant J 21: 351-360
27. Ilic K, SanMiguel PJ, Bennetzen JL (2003) A complex history of rearrangement in an orthologous region of the maize, sorghum, and rice genomes. Proc Natl Acad Sci USA 100: 12265-12270
28. Immink RG, Hannapel DJ, Ferrario S, Busscher M, Franken J, Lookeren Campagne MM, Angenent GC (1999) A petunia MADS box gene involved in the transition from vegetative to reproductive development. Development 126: 5117-5126
29. Irish EE, Nelson TM (1991) Identification of multiple stages in the conversion of maize meristems from vegetative to floral development. Development 112: 891-898
30. Izawa T, Takahashi Y, Yano M (2003) Comparative biology comes into bloom: genomic and genetic comparison of flowering pathways in rice and Arabidopsis. Curr Opin Plant Biol 6: 113-120
31. Jackson D (1991) In situ hybridization in plants. In DJ Bowles, SJ Gurr, M McPherson, eds, Molecular Plant Pathology: A Practical Approach. Oxford University Press, Oxford, pp 163-174
32. Jang S, An K, Lee S, An G (2002) Characterization of tobacco MADS-box genes involved in floral initiation. Plant Cell Physiol 43: 230-238
33. Kang HG, Jang S, Chung JE, Cho YG, An G (1997) Characterization of two rice MADS box genes that control flowering time. Mol Cells 7: 559-566
34. Kempin SA, Savidge B, Yanofsky MF (1995) Molecular basis of the cauliflower phenotype in Arabidopsis. Science 267: 522-525
35. Kozaki A, Hake S, Colasanti J (2004) The maize ID1 flowering time regulator is a zinc finger protein with novel DNA binding properties. Nucleic Acids Res 32: 1710-1720
36. Lai J, Ma J, Swigonova Z, Ramakrishna W, Linton E, Llaca V, Tanyolac B, Park YJ, Jeong OY, Bennetzen JL, et al (2004) Gene loss and movement in the maize genome. Genome Res 14: 1924-1931
37. Lee H, Suh SS, Park E, Cho E, Ahn JH, Kim SG, Lee JS, Kwon YM, Lee I (2000) The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes Dev 14: 2366-2376
38. Litt A, Irish VF (2003) Duplication and diversification in the APETALA1/FRUITFULL floral homeotic gene lineage: implications for the evolution of floral development. Genetics 165: 821-833
39. Liu C, Zhou J, Bracha-Drori K, Yalovsky S, Ito T, Yu H (2007) Specification of Arabidopsis floral meristem identity by repression of flowering time genes. Development 134: 1901-1910
40. 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
41. Malcomber ST, Kellogg EA (2005) SEPALLATA gene diversification: brave new whorls. Trends Plant Sci 10: 427-435
42. Malcomber ST, Preston JC, Reinheimer R, Kossuth J, Kellogg EA (2006) Developmental gene evolution and the origin of grass inflorescence diversity. Adv Bot Res 44: 426-481
43. Mandel MA, Gustafson-Brown C, Savidge B, Yanofsky MF (1992) Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 360: 273-277
44. Mandel MA, Yanofsky MF (1995) A gene triggering flower formation in Arabidopsis. Nature 377: 522-524
45. McElroya D, Brettell RIS (1994) Foreign gene expression in transgenic cereals. Trends Biotechnol 12: 62-68
46. McSteen P, Hake S (2001) barren inflorescence2 regulates axillary meristem development in the maize inflorescence. Development 128: 2881-2891
47. McSteen P, Laudencia-Chingcuanco D, Colasanti J (2000) A floret by any other name: control of meristem identity in maize. Trends Plant Sci 5: 61-66
48. Messing J, Bharti AK, Karlowski WM, Gundlach H, Kim HR, Yu Y, Wei F, Fuks G, Soderlund CA, Mayer KF, et al (2004) Sequence composition and genome organization of maize. Proc Natl Acad Sci USA 101: 14349-14354
49. Messing J, Dooner HK (2006) Organization and variability of the maize genome. Curr Opin Plant Biol 9: 157-163
50. Michaels SD, Himelblau E, Kim SY, Schomburg FM, Amasino RM (2005) Integration of flowering signals in winter-annual Arabidopsis. Plant Physiol 137: 149-156
51. Moon J, Suh SS, Lee H, Choi KR, Hong CB, Paek NC, Kim SG, Lee I (2003) The SOC1 MADS-box gene integrates vernalization and gibberellin signals for flowering in Arabidopsis. Plant J 35: 613-623
52. Mouradov A, Cremer F, Coupland G (2002) Control of flowering time: interacting pathways as a basis for diversity. Plant Cell (Suppl) 14: S111-S130
53. 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
54. Muszynski MG, Dam T, Li B, Shirbroun DM, Hou Z, Bruggemann E, Archibald R, Ananiev EV, Danilevskaya ON (2006) delayed flowering1 encodes a basic leucine zipper protein that mediates floral inductive signals at the shoot apex in maize. Plant Physiol 142: 1523-1536
55. Neuffer MG, Coe EH, Wessler SR (1997) Mutants of Maize. CSHL Press, Cold Spring Harbor, NY
56. Parcy F, Nilsson O, Busch MA, Lee I, Weigel D (1998) A genetic framework for floral patterning. Nature 395: 561-566
57. Parenicova L, de Folter S, Kieffer M, Horner DS, Favalli C, Busscher J, Cook HE, Ingram RM, Kater MM, Davies B, et al (2003) Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis: new openings to the MADS world. Plant Cell 15: 1538-1551
58. Pelaz S, Ditta GS, Baumann E, Wisman E, Yanofsky MF (2000) B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature 405: 200-203
59. Petersen K, Didion T, Andersen CH, Nielsen KK (2004) MADS-box genes from perennial ryegrass differentially expressed during transition from vegetative to reproductive growth. J Plant Physiol 161: 439-447
60. Petersen K, Kolmos E, Folling M, Salchert K, Storgaard M, Jensen CS, Didion T, Nielsen KK (2006) Two MADS-box genes from perennial ryegrass are regulated by vernalization and involved in the floral transition. Physiol Plant 126: 268-278
61. Preston JC, Kellogg EA (2006) Reconstructing the evolutionary history of paralogous APETALA1/FRUITFULL-like genes in grasses (Poaceae). Genetics 174: 421-437
62. Preston JC, Kellogg EA (2007) Conservation and divergence of APETALA1/FRUITFULL-like gene function in grasses: evidence from gene expression analyses. Plant J 52: 69-81
63. Preston JC, Kellogg EA (2008) Discrete developmental roles for temperate cereal grass VRN1/FUL-like genes in flowering competency and the transition to flowering. Plant Physiol 146: 265-276
64. Razem FA, El-Kereamy A, Abrams SR, Hill RD (2006) The RNA-binding protein FCA is an abscisic acid receptor. Nature 439: 290-294
65. Reinartz J, Bruyns E, Lin JZ, Burcham T, Brenner S, Bowen B, Kramer M, Woychik R (2002) Massively parallel signature sequencing (MPSS) as a tool for in-depth quantitative gene expression profiling in all organisms. Brief Funct Genomics Proteomics 1: 95-104
66. Ritchie SW, Hanway JJ, Benson GO (1997) How a Corn Plant Develops. Special Report No. 48, Vol 48. Iowa State University of Science and Technology Cooperative Extension Service, Ames, IA
67. Saddic LA, Huvermann B, Bezhani S, Su Y, Winter CM, Kwon CS, Collum RP, Wagner D (2006) The LEAFY target LMI1 is a meristem identity regulator and acts together with LEAFY to regulate expression of CAULIFLOWER. Development 133: 1673-1682
68. Samach A, Onouchi H, Gold SE, Ditta GS, Schwarz-Sommer Z, Yanofsky MF, Coupland G (2000) Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288: 1613-1616
69. Schmid M, Uhlenhaut NH, Godard F, Demar M, Bressan R, Weigel D, Lohmann JU (2003) Dissection of floral induction pathways using global expression analysis. Development 130: 6001-6012
70. 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
71. Stangeland B, Salehian Z (2002) An improved clearing method for GUS assay in Arabidopsis endosperm and seeds. Plant Mol Biol Rep 20: 107-114
72. Stolovitzky GA, Kundaje A, Held GA, Duggar KH, Haudenschild CD, Zhou D, Vasicek TJ, Smith KD, Aderem A, Roach JC (2005) Statistical analysis of MPSS measurements: application to the study of LPS-activated macrophage gene expression. Proc Natl Acad Sci USA 102: 1402-1407
73. Swigonova Z, Lai J, Ma J, Ramakrishna W, Llaca V, Bennetzen JL, Messing J (2004) Close split of sorghum and maize genome progenitors. Genome Res 14: 1916-1923
74. Teper-Bamnolker P, Samach A (2005) The flowering integrator FT regulates SEPALLATA3 and FRUITFULL accumulation in Arabidopsis leaves. Plant Cell 17: 2661-2675
75. Trevaskis B, Bagnall DJ, Ellis MH, Peacock WJ, Dennis ES (2003) MADS box genes control vernalization-induced flowering in cereals. Proc Natl Acad Sci USA 100: 13099-13104
76. Trevaskis B, Hemming MN, Peacock WJ, Dennis ES (2006) HvVRN2 responds to daylength, whereas HvVRN1 is regulated by vernalization and developmental status. Plant Physiol 140: 1397-1405
77. Unger E, Betz S, Xu R, Cigan AM (2001) Selection and orientation of adjacent genes influences DAM-mediated male sterility in transformed maize. Transgenic Res 10: 409-422
78. Vijayraghavan U, Prasad K, Meyerowitz EM (2005) Specification and maintenance of the floral meristem: interactions between positively-acting promoters of flowering and negative regulators. Curr Sci 89: 1835-1843
79. von Zitzewitz J, Szucs P, Dubcovsky J, Yan L, Francia E, Pecchioni N, Casas A, Chen TH, Hayes PM, Skinner JS (2005) Molecular and structural characterization of barley vernalization genes. Plant Mol Biol 59: 449-467
80. Walsh B (2003) Population-genetic models of the fates of duplicate genes. Genetica 118: 279-294
81. Wigge PA, Kim MC, Jaeger KE, Busch W, Schmid M, Lohmann JU, Weigel D (2005) Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309: 1056-1059
82. Yan L, Loukoianov A, Blechl A, Tranquilli G, Ramakrishna W, SanMiguel P, Bennetzen JL, Echenique V, Dubcovsky J (2004) The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science 303: 1640-1644
83. Yan L, Loukoianov A, Tranquilli G, Helguera M, Fahima T, Dubcovsky J (2003) Positional cloning of the wheat vernalization gene VRN1. Proc Natl Acad Sci USA 100: 6263-6268
84. Yan L, von Zitzewitz J, Skinner JS, Hayes PM, Dubcovsky J (2005) Molecular characterization of the duplicated meristem identity genes HvAP1a and HvAP1b in barley. Genome 48: 905-912
85. Yano M, Kojima S, Takahashi Y, Lin H, Sasaki T (2001) Genetic control of flowering time in rice, a short-day plant. Plant Physiol 127: 1425-1429
86. Yanofsky MF (1995) Floral meristems to floral organs: genes controlling early events in Arabidopsis flower development. Annu Rev Plant Physiol Plant Mol Biol 46: 167-188
87. Yu H, Xu Y, Tan EL, Kumar PP (2002) AGAMOUS-LIKE 24, a dosage-dependent mediator of the flowering signals. Proc Natl Acad Sci USA 99: 16336-16341