Patterns of MADS-box gene expression mark flower-type development in Gerbera hybrida (Asteraceae)

BMC Plant Biology

Volumn 6, Issue , 2006, Pages

  Laitinen, Roosa A E ^a   Broholm, Suvi ^a   Albert, Victor A ^b   Teeri, Teemu H ^a   Elomaa, Paula ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF OSLO   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

ASTERACEAE; GERBERA; GERBERA HYBRID CULTIVAR;

MADS DOMAIN PROTEIN; TRANSCRIPTION FACTOR;

ASTERACEAE; BIOLOGICAL MODEL; CLASSIFICATION; CYTOLOGY; FLOWER; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROARRAY ANALYSIS; MOLECULAR GENETICS; PLANT GENE; ULTRASTRUCTURE;

ASTERACEAE; FLOWERS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; MADS DOMAIN PROTEINS; MICROARRAY ANALYSIS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; TRANSCRIPTION FACTORS;

EID: 33746690360     PISSN: 14712229     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-6-11     Document Type: Article

References (74)

1. Kotilainen M, Elomaa P, Uimari A, Albert VA, Yu D, Teeri TH: GRCD1, an AGL2-like MADS box gene, participates in the C function during stamen development in Gerbera hybrida. Plant Cell 2000, 12:1893-1902.
2. Kloos WE, George CG, Sorge LK: Inheritance of the flowertypes of Gerbera hybrida. J Am Soc Hortic Sci 2004, 129:802-810.
3. Albert VA, Gustafsson MHG, Di Laurenzio L: Ontogenetic systematics, molecular developmental genetics, and the angiosperm petal. In Molecular Systematics of Plants II Edited by: Soltis P, Soltis D, Doyle J. Boston: Kluwer Academic Publishers; 1998:349-374.
4. Coen E, Nugent JM: Evolution of flowers and inflorescences. Development 1994:107-116.
5. Bremer K: Asteraceae: Cladistics and classification. Portland, OR: Timber Press; 1994.
6. Gillies ACM, Cubas P, Coen ES, Abbott RJ: Making rays in the Asteraceae: genetics and evolution of radiate versus discoid flower heads. In Developmental Genetics and Plant Evolution Edited by: Cronk QCB, Bateman RM, Hawkins JA. London: Taylor & Francis; 2002:233-246.
7. Baldwin BG: Origin of the serpentine-endemic herb Layia discoidea from the widespread L. glandulosa (Compositae). Evolution 2005, 59:2473-2479.
8. Abbott RJ, Ashton PA, Forbes DG: Introgressive origin ofthe radiate groundsel Senecio vulgaris var hibernicus Syme: Aat-3 evidence. Heredity 1992, 68:425-435.
9. Comes HP: Major gene effects during weed evolution: phenotypic characters cosegregate with alleles at the ray floret locus in Senecio vulgaris L. (Asteraceae). J Hered 1998, 89:54-61.
10. Andersson S: Fitness consequences of floral variation in Senecio jacobaea (Asteraceae): Evidence from a segregating hybrid population and a resource manipulation experiment. Biol J Linn Soc Lond 2001, 74:17-24.
11. Abbott RJ, James JK, Milne RI, Gillies AC: Plant introductions, hybridization and gene flow. Philos Trans R Soc Lond B Biol Sci 2003, 358:1123-1132.
12. Luo D, Carpenter R, Vincent C, Copsey L, Coen E: Origin of floral asymmetry in Antirrhinum. Nature 1996, 383:794-799.
13. Cubas P, Lauter N, Doebley J, Coen E: The TCP domain: a motif found in proteins regulating plant growth and development. Plant J 1999, 18:215-222.
14. Citerne HL, Moller M, Cronk QCB: Diversity of cycloidea-like genes in Gesneriaceae in relation to floral symmetry. Ann Bot (Lond) 2000, 86:167-176.
15. Hegarty MJ, Jones JM, Wilson ID, Barker GL, Coghill JA, Sanchez-Baracaldo P, Liu G, Buggs RJA, Abbott JA, Edwards KJ, Hiscock SJ: Development of anonymous cDNA microarrays to study changes tothe Senecio floral transcriptome during hybrid speciation. Mol Ecol 2005, 14:2493-2510.
16. Buzgo M, Soltis DE, Soltis PS, Ma H: Towards a comprehensive integration of morphological and genetic studies of floral development. Trends Plant Sci 2004, 9:164-173.
17. Irish VF, Litt A: Flower development and evolution: gene duplication, diversification and redeployment. Curr Opin Genet Dev 2005, 15:454-60.
18. Jack T: Molecular and genetic mechanisms of floral control. Plant Cell 2004, 16:S1-S17.
19. Doebley J, Stec A, Hubbard L: The evolution of apical dominance in maize. Nature 1997, 386:485-488.
20. He C, Saedler H: Heterotopic expression of MPF2 is the key to the evolution of the Chinese lantern of Physalis, a morphological novelty in Solanaceae. Proc Natl Acad Sci U S A 2005, 102:5779-84.
21. Jaramillo MA, Kramer EM: APETALA3 and PISTILLATA homologs exhibit novel expression patterns in the unique perianth of Aristolochia (Aristolochiaceae). Evol Dev 2004, 6:449-458.
22. Laitinen RAE, Immanen J, Auvinen P, Rudd S, Alatalo E, Paulin L, Ainasoja M, Kotilainen M, Koskela S, Teeri TH, Elomaa P: Analysis of the floral transcriptome uncovers new regulators or organ determination and gene families related to flower organ differentiation in Gerbera hybrida (Asteraceae). Genome Res 2005, 15:475-486.
23. Helariutta Y, Kotilainen M, Elomaa P, Teeri TH: Gerbera hybrida (Asteraceae) imposes regulation at several anatomical levels during inflorescence development on the gene for dihydroflavonol-4-reductase. Plant Mol Biol 1995, 28:935-941.
24. Utsugi S, Sakamoto W, Murata M, Motoyoshi F: Arabidopsis thaliana vegetative storage protein (VSP) genes: gene organization and tissue-specific expression. Plant Mol Biol 1998, 38:565-576.
25. Hu W, Wang Y, Bowers C, Ma H: Isolation, sequence analysis, and expression studies on florally expressed cDNAs in Arabidopsis. Plant Mol Biol 2003, 53:545-563.
26. Nakayama N, Arroyo JM, Simorowski J, May B, Martienssen R, Fukuchi-Mizutani M, Ueda T, Nakao M, Tanaka Y, Kusumi T, Nishino T: Gene trap lines define domains of gene regulation in Arabidopsis petals and stamens. Plant Cell 2005, 17:2486-2506.
27. van Doorn WG, Balk PA, van Houwelingen AM, van Houwelingen, Hoeberichts FA, Hall RD, Vorst O, van der Schoot C, van Wordragen MF: Gene expression during anthesis and senescence in Irish flowers. Plant Mol Biol 2003, 53:845-863.
28. Li Y, Jones L, McQueen-Mason S: Expansins and cellgrowth. Curr Op Plant Biol 2003, 6:603-610.
29. Choi D, Lee Y, Cho HT, Kende H: Regulation of expansin gene expression affects growth and development in transgenic rice plants. Plant Cell 2003, 15:1386-1398.
30. Nakayama T, Yonekura-Sakakibara K, Sato T, Kikuchi S, Fukui Y, Fukuchi-Mizutani M, Ueda T, Nakao M, Tanaka Y, Kusumi T, Nishino T: Aureusidin synthase: a polyphenol oxidase homolog responsible for flower coloration. Science 2000, 10:1163-1166.
31. Jensen RB, Jensen KL, Jespersen HM, Skriver K: Widespread occurence of a highly conserved RING-H2 zinc finger motif in themodel plant Arabidopsis thaliana. FEBS Lett 1998, 436:283-287.
32. Greve K, La Cour T, Jensen MK, Poulsen FM, Skriver K: Interactions between plant RING-H2 and plant specific NAC (NAM/ATAF1/2/CUC2) proteins: RING-H2 molecular specificity and cellular localization. Biochem J 2003, 371:97-108.
33. Ohashi-Ito K, Demura T, Fukuda H: Promotion of transcript accumulation of novel Zinnia immature xylem-specific HD-Zip III homeobox genes by brassinosteroids. Plant Cell Physiol 2002, 43:1146-1153.
34. Green KA, Prigge MJ, Katzman RB, Clark SE: CORONA, a member of the class III homeodomain-leucine zipper gene family in Arabidopsis, regulates stem cell specification and organogenesis. Plant Cell 2005, 17:691-704.
35. Prigge MJ, Otsuga D, Alonso JM, Ecker JR, Drews GN, Clark SE: Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. Plant Cell 2005, 17:61-76.
36. Engström EM, Izhaki A, Bowman JL: Promoter bashing, microRNAs, and Knox genes. New insights, regulators, and targetsof-regulation in the establishment of lateral organ polarity in Arabidopsis. Plant Physiol 2004, 135:685-694.
37. Cardon G, Höhmann S, Nettesheim K, Saedler H, Huijser P: Functional analysis of the Arabidopsis thaliana SBP-box gene SPL3: a novel gene involved in the floral transition. Plant J 1997, 12:367-377.
38. Cardon G, Höhmann S, Klein J, Nettesheim K, Saedler H, Huijser P: Molecular characterization of the Arabidopsis SBP-box genes. Gene 1999, 237:91-104.
39. Unte US, Sorensen A-M, Pesaresi P, Gandikota M, Leister D, Saedler H, Huijser P: SPL8, an SBP-box gene that affects pollen sac development in Arabidopsis. Plant Cell 2003, 15:1009-1019.
40. Takatsuji H: Zinc-finger transcription factors in plants. Cell Mol Life Sci 1998, 54:582-596.
41. Kozaki A, Hake S, Colasanti J: The maize ID1 flowering time regulator is a zinc finger protein with novel DNA binding properties. Nucl Acids Res 2004, 32:1710-1720.
42. Eliasson A, Gass N, Mundel C, Baltz R, Krauter R, Evrard JL, Steinmetz A: Molecular and expression analysis of a LIM protein gene family from flowering plants. Mol Gen Genet 2000, 264:257-267.
43. Mundel C, Baltz R, Eliasson Å, Bronner R, Grass N, Kräuter R, Evrard J-L, Steinmetz A: A LIM-domain protein from sunflower is localized to the cytoplasm and/or nucleus in a wide variety of tissues and is associated with the phragmoplast in dividing cells. Plant Mol Biol 2000, 42:291-302.
44. Elomaa P, Mehto M, Kotilainen M, Helariutta Y, Nevalainen L, Teeri TH: A bHLH transcription factor mediates organ, region and flower type specific signals on dihydroflavonol-4-reductase (dfr) geneexpression in the inflorescence of Gerbera hybrida (Asteraceae). Plant J 1998, 16:93-100.
45. Teeri TH, Albert VA, Elomaa P, Hämäläinen J, Kotilainen M, Pöllänen E, Uimari A: Involvement of non-ABC MADS-box genes indetermining stamen and carpel identity in Gerbera hybrida (Asteraceae). In Developmental Genetics and Plant Evolution Edited by: Cronk QCB, Bateman RM, Hawkins JA. London: Taylor & Francis; 2002:220-232.
46. Teeri TH, Kotilainen M, Uimari A, Ruokolainen S, Ng YP, Malm U, Pöllänen E, Broholm S, Laitinen R, Elomaa P, Albert VA: Floral-developmental genetics of Gerbera (Asteraceae). Adv Bot Res in press.
47. Yu D, Kotilainen M, Pöllänen E, Mehto M, Elomaa P, Helariutta Y, Albert VA, Teeri TH: Organ identity genes and modified patterns of flower development in Gerbera hybrida (Asteraceae). Plant J 1999, 17:51-62.
48. Kim S, Yoo M-J, Albert VA, Farris JS, Soltis PS, Soltis DE: Phylogeny and diversification of B-function MADS-box genes in angiosperms: evolutionary and functional implications of a 260-million-year-old duplication. Am J Bot 2004, 91:2102-2118.
49. Uimari A, Kotilainen M, Elomaa P, Yu D, Albert VA, Teeri TH: Integration of reproductive meristem fates by a SEPALLATA-like MADS-box gene. Proc Natl Acad Sci U S A 2004, 101:15817-15822.
50. Shchennikova AV, Shulga OA, Immink R, Skryabin KG, Angenent GC: Identification and characterization of four chrysanthemum MADS-box genes, belonging to the APETALA1/FRUITFULL and SEPALLATA3 subfamilies. Plant Physiol 2004, 134:1632-1641.
51. Angenent GC, Busscher M, Franken J, Mol JNM, Van Tunen AJ: Differential Expression of Two MADS Box Genes in Wild-Type and Mutant Petunia Flowers. Plant Cell 1992, 8:983-993.
52. Zahn LM, Kong H, Leebens-Mack JH, Kim S, Soltis PS, Landherr LL, Soltis DE, DePamphilis CW, Ma H: The evolution of the SEPALLATA subfamily of MADS-box genes: a preangiosperm origin with multiple duplications throughout angiosperm history. Genetics 2005, 4:2209-2223.
53. Egea-Cortines M, Saedler H, Sommer H: 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 1999, 18:5370-5379.
54. Honma T, Goto K: Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 2001, 409:525-529.
55. Immink RGH, Ferrario S, Busscher-Lange J, Kooiker M, Busscher M, Angenent GC: Analysis of the petunia MADS-box transcription factor family. Mol Genet Genomics 2003, 268:598-606.
56. de Folter S, Immink RGH, Kieffer M, Paøenicová L, Henz SR, Weigel D, Busscher M, Kooiker M, Colombo L, Kater MM, Davies B, Angenent GC: Comprehensive interaction map of the arabidopsis MADS box transcription factors. Plant Cell 2005, 17:1424-1433.
57. Uimari A, Strommer J: Myb26: a MYB-like protein in pea flowers with affinity for promoters of phenylpropanoid genes. Plant J 1997, 12:1273-1284.
58. Grant S, Houben A, Vyskot B, Siroky J, Pan W-H, Macas J, Saedler H: Genetics of sex determination in flowering plants. Dev Genet 1994, 15:214-230.
59. Coen ES, Meyerowitz EM: The warof the whorls:genetic interactions controlling flower development. Nature 1991, 353:31-37.
60. Hardenack S, Ye D, Saedler H, Grant S: Comparison of MADS box gene expression in developing male and female flowers of the dioecious plant white campion. Plant Cell 1994, 6:1775-1787.
61. Perl-Treves R, Kahana A, Rosenman N, Xiang Y, Silberstein L: Expression of multiple AGAMOUS-like genes in male and female flowers of cucumber (Cucumis sativus L.). Plant Cell Physiol 1998, 39:701-710.
62. Kater MM, Franken J, Carney KJ, Colombo L, Angenent GC: Sex determination in the monoecious species cucumber is confined to specific floral whorls. Plant Cell 2001, 13:481-493.
63. Park JH, Ishikawa Y, Yoshida R, Kanno A, Kameya T: Expression of AODEF, a B-functional MADS-box gene, in stamens and inner tepals of the dioecious species Asparagusofficinalis L. Plant Mol Biol 2003, 51:867-875.
64. Ainsworth C, Rahman A, Parker J, Edwards G: Intersex inflorescences of Rumex acetosa demonstrate that sex determination is unique to each flower. New Phytol 2005, 165:711-720.
65. Malcomber ST, Kellogg EA: Heterogeneous expression patterns and separate roles of the SEPALLATA gene LEAFY HULL STERILE1 in grasses. Plant Cell 2004, 16:1692-1706.
66. Vandenbussche M, Zethof J, Royaert S, Weterings K, Gerats T: The duplicated B-class heterodimer model: whorl-specific effects and complex genetic interactions in Petunia hybrida flower development. Plant Cell 2004, 16:741-754.
67. Hernandez LF, Palmer JH: Regeneration of the sunflower capitulum after cylindrical wounding of the receptacle. Am J Bot 1998, 75:1253-1261.
68. Palmer JH, Marc J: Wound-induced initiation of involucral bracts and florets in the developing sunflower inflorescence. Plant Cell Physiol 1982, 23:1401-1409.
69. Bachmann K: Evolutionary genetics and the genetic-control of morphogenesis in flowering plants. Evol Biol 1983, 16:157-208.
70. Mauthe S, Bachmann K, Chambers KL, Price HJ: Independent responses of two fruit characters to developmental regulation in Microseris douglasii (Asteraceae, Lactuceae). Experientia 1984, 40:1280-1281.
71. Meinhardt H: Space-dependent cell determination under the control of a morphogen gradient. J Theor Biol 1978, 74:307-321.
72. Perbal M-C, Haughn G, Saedler H, Schwarz-Sommer Z: Non-cell-autonomous function of the Antirrhinum floral homeotic proteins DEFICIENS and GLOBOSA is exerted by their polar cell-to-cell trafficking. Development 1996, 122:3433-3441.
73. Sessions A, Yanofsky MF, Weigel D: Cell-cell signaling and movement by the floral transcription factors LEAFY and APETALA1. Science 2000, 289:779-781.
74. Theiâen G: Development of floral organ identity:stories from the MADS house. Curr Opin Plant Biol 2001, 4:75-85.