Conservation and diversity in flower land

Current Opinion in Plant Biology

Volumn 7, Issue 1, 2004, Pages 84-91

  Ferrario, Silvia ^a   Immink, Richard G H ^a   Angenent, Gerco C ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; MAGNOLIOPHYTA;

EID: 1642444638     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2003.11.003     Document Type: Review

References (67)

1. Darwin C: More Letters from Charles Darwin: A Record of his Work in a Series of Hitherto Unpublished Letters, vol 2. Edited by Darwin F, Seward AC. Appelton, New York; 1903:20.
2. Theissen G., Becker A., Di Rosa A., Kanno A., Kim J.T., Munster T., Winter K.-U., Saedler H. A short history of MADS-box genes in plants. Plant. Mol. Biol. 42:2000;115-149.
3. Ng M., Yanofsky M.F. Function and evolution of the plant MADS-box gene family. Nat. Rev. Genet. 2:2001;186-195.
4. Shepard K.A., Purugganan M.D. The genetics of plant morphological evolution. Curr. Opin. Plant. Biol. 5:2002;49-55.
5. Lohmann J.U., Weigel D. Building beauty: the genetic control of floral patterning. Dev. Cell. 2:2002;135-142 A recent complete review on floral organ identity in Arabidopsis that pays particular attention to the different levels of regulation of floral homeotic genes and their patterns of expression.
6. Schwarz-Sommer Z., Davies B., Hudson A. An everlasting pioneer: the story of Antirrhinum research. Nat. Rev. Genet. 4:2003;657-664.
7. Fornara F., Marziani G., Mizzi L., Kater M., Colombo L. MADS-box genes controlling flower development in rice. Plant. Biol. 5:2003;16-22.
8. Coen E.S., Meyerowitz E.M. The war of the whorls: genetic interactions controlling flower development. Nature. 353:1991;31-37.
9. Colombo L., Franken J., Koetje E., van Went J.L., Dons H.J.M., Angenent G.C., Van Tunen A.J. The petunia MADS-box gene FBP11 determines ovule identity. Plant. Cell. 7:1995;1859-1868.
10. Pelaz S., Ditta G.S., Baumann E., Wisman E., Yanofsky M.F. B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature. 405:2000;200-203.
11. Theissen G., Saedler H. Floral quartets. Nature. 409:2001;469-471.
12. Keck E., McSteen P., Carpenter R., Coen E. Separation of genetic functions controlling organ identity in flowers. EMBO J. 22:2003;1058-1066 The simultaneous inactivation of the Antirrhinum LIP1 and LIP2 genes are shown to produce defects in the identity and development of the first two whorls of the flower, as well as changes in the identity of ovules. These genes are highly homologous to the Arabidopsis A-class gene AP2. The dual functions of organ identity and repression of C-class genes, which are accomplished by AP2 in Arabidopsis, are carried out separately in Antirrhinum. Using in-situ analysis and triple mutant combinations, the authors show that the LIP genes are not required for the repression of PLE.
13. Angenent G.C., Busscher M., Franken J., Mol J.N.M., Van Tunen A.J. Differential expression of two MADS-box genes in wild-type and mutant petunia flowers. Plant. Cell. 4:1992;983-993.
14. Kush A., Brunelle A., Shevell D., Chua N.-H. The sequence of 2 MADS-box proteins in petunia. J. Plant. Physiol. 102:1993;1051-1052.
15. Van der Krol A.R., Brunelle A., Tsuchimoto S., Chua N.-H. Functional analysis of petunia floral homeotic MADS-box gene pMADS1. Genes Dev. 7:1993;1214-1228.
16. Ferrario S., Immink R.G.H., Shchennikova A., Busscher-Lange J., Angenent G.C. The MADS-box gene FBP2 is required for the SEPALLATA function in petunia. Plant. Cell. 15:2003;914-925 The authors of this paper report a functional analysis of the petunia MADS-box gene FBP2, which encodes a protein that carries out the E function in petunia and is functionally equivalent to the Arabidopsis SEP3 protein. Yeast two-hybrid screens showed that FBP2, as well as its paralogue FBP5, forms heterodimers with at least ten other petunia MADS-box proteins, including class C and D proteins. Furthermore, as in Arabidopsis, C/E heterodimers form higher-order complexes between class-B heterodimers in petunia. Interestingly, duplicated B- and C-class genes are not interchangeable in higher-order complexes in petunia, indicating that they have already diverged with respect to interaction specificity.
17. Kang H.-G., Jeon J.-S., Lee S., An G. Identification of class B and class C floral organ identity genes from rice plants. Plant. Mol. Biol. 38:1998;1021-1029.
18. Ambrose B.A., Lerner D.R., Ciceri P., Padilla C.M., Yanofsky M.F., Schmidt R.J. Molecular and genetic analyses of the Silky1 gene reveal conservation in floral organ specification between eudicots and monocots. Mol. Cell. 5:2000;569-579.
19. Lee S, Jeon J-S, An K, Moon Y-H, Lee S, Chung Y-Y, An G: Alteration of floral organ identity in rice through ectopic expression of OsMADS16. Planta 2003, in press.
20. Nagasawa N., Miyoshi M., Sano Y., Satoh H., Hirano H., Sakai H., Nagato Y. SUPERWOMAN and DROOPING LEAF genes control floral organ identity in rice. Development. 130:2003;705-718 The authors show that spw1, a mutation in the rice AP3 homologue, OsMADS16, is responsible for the homeotic conversion of lodicules and stamens into palea-like organs and carpels, respectively. This evidence supports the hypotheses that the monocot lodicules and the eudicot petals are homologous and that the B function is conserved among angiosperms. The authors also examine the interaction between SPW1 and DROOPING LEAF (DL), a locus that controls midrib formation in leaves and gynoecium development. dl mutants have midrib-less leaves and carpels that are converted into stamens. spw1 dl double mutants show indeterminate growth of organs that are neither carpels nor stamens in whorls 3 and 4. On the basis of genetic interactions and molecular data, the authors propose a model for floral organ identity in rice that involves the action of SPW1 and DL in controlling the identity of whorls 2, 3 and 4.
21. Kramer E.M., Irish V.F. Evolution of genetic mechanisms controlling petal development. Nature. 399:1999;144-148.
22. Kramer E.M., Irish V.F. Evolution of the petal and stamen developmental programs: evidence from comparative studies of the lower eudicots and basal angiosperms. Int. J. Plant. Sci. 161:2000;S29-S40.
23. Johansen B., Pedersen L.B., Skipper M., Frederiksen S. MADS-box gene evolution-structure and transcription patterns. Mol. Phylogenet. Evol. 23:2002;458-480.
24. Kramer E.M., Di Stilio V., Schlüter P.M. Complex patterns of gene duplication in the APETALA3 and PISTILLATA lineages of the Ranunculaceae. Int. J. Plant. Sci. 164:2003;1-11 The identification and phylogenetic analysis of B-class genes from different species of Ranunculaceae reveals that many duplication events have occurred in the AP3 and PI lineages of this family of lower eudicots. The authors speculate, using evidence from expression studies, that different AP3 paralogues may have played a role in the evolution of the diverse perianth morphologies seen in the Ranunculaceae. They also point out that the duplications in the PI lineage, which are more recent than those in the AP3 lineage, might have been retained as a response to the functional specialisation of AP3 paralogues in conjunction with the evolution of novel petal identity. Further studies in this direction will reveal the role that modifications of the ABC programme have played in the evolution and diversification of floral morphology.
25. Purugganan M.D., Rounsley S.D., Schmidt R.J., Yanofsky M. Molecular evolution of flower development: diversification of the plant MADS-box regulatory gene family. Genetics. 140:1995;345-356.
26. Riechmann J.L., Krizek B.A., Meyerowitz E.M. Dimerization specificity of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA, and AGAMOUS. Proc. Natl. Acad. Sci. USA. 93:1996;4793-4798.
27. Winter K.U., Weiser C., Kaufmann K., Bohne A., Kirchner C., Kanno A., Saedler H., Theissen G. Evolution of class B floral homeotic proteins: obligate heterodimerization originated from homodimerization. Mol. Biol. Evol. 19:2002;587-596 The authors investigate the dimerisation ability of a putative B protein from the gymnosperm Gnetum gnemon (GGM2) and of the DEF-like protein LRDEF and the GLO-like proteins LRGLOA and LRGLOB from the monocot lily (Lilium regale). By means of gel retardation and yeast two-hybrid assays, they show that GGM2 undergoes homodimerisation and subsequent DNA binding, whereas the B-class proteins from lily can bind DNA as heterodimers (LRDEF-LRGLOA/LRGLOB) or as homodimers (e.g. LRGLOB-LRGLOB). The authors suggest that the obligate heterodimerization of DEF-like and GLO-like proteins from higher eudicots evolved in two steps, after a duplication event that originated the DEF and GLO lineages. Obligate heterodimerization implies the evolutionarily stable expression of the B genes, a condition that might have evolved in parallel with the standardisation of the floral structure at the base of the higher eudicot lineage.
28. Davies B., Motte P., Keck E., Saedler H., Sommer H., Schwarz-Sommer Z. PLENA and FARINELLI: redundancy and regulatory interactions between two Antirrhinum MADS-box factors controlling flower development. EMBO J. 18:1999;4023-4034.
29. Tsuchimoto S., van der Krol A.R., Chua N.-H. Ectopic expression of pMADS3 in transgenic petunia phenocopies the petunia blind mutant. Plant. Cell. 5:1993;843-853.
30. Kapoor M., Tsuda S., Tanaka Y., Mayama T., Okuyama Y., Tsuchimoto S., Takatsuji H. Role of petunia pMADS3 in determination of floral organ and meristem identity, as revealed by its loss of function. Plant J. 32:2002;115-127.
31. Kater M.M., Colombo L., Franken J., Busscher M., Masiero S., Campagne M.M.V., Angenent G.C. Multiple AGAMOUS homologs from cucumber and petunia differ in their ability to induce reproductive organ fate. Plant. Cell. 10:1998;171-182.
32. Yu D.Y., Kotilainen M., Pollanen E., Mehto M., Elomaa P., Helariutta Y., Albert V.A., Teeri T.H. Organ identity genes and modified patterns of flower development in Gerbera hybrida (Asteraceae). Plant J. 17:1999;51-62.
33. Mena M., Ambrose B.A., Meeley R.B., Briggs S.P., Yanofsky M.F., Schmidt R.J. Diversification of C-function activity in maize flower development. Science. 274:1996;1537-1540.
34. Pinyopich A., Ditta G.S., Savidge B., Liljegren S.J., Baumann E., Wisman E., Yanofsky M.F. Assessing the redundancy of MADS-box genes during carpel and ovule development. Nature. 424:2003;85-88 An extensive analysis of the AG clade in Arabidopsis, including studies of the phenotypes of double, triple and quadruple mutants, reveals partial redundancy between AG, SHP1 and SHP2 in controlling carpel development, and between AG, SHP1, SHP2 and STK in promoting ovule identity.
35. Angenent G.C., Franken J., Busscher M., van Dijken A., van Went J.L., Dons H.J.M., Van Tunen A.J. A novel class of MADS-box genes is involved in ovule development in petunia. Plant. Cell. 7:1995;1569-1582.
36. Favaro R., Pinyopich A., Battaglia R., Kooiker M., Borghi L., Ditta G., Yanofsky M.F., Kater M., Colombo L. MADS-box protein complexes control carpel and ovule development in Arabidopsis. Plant. Cell. 15:2003;2603-2611.
37. Immink R.G.H., Ferrario S., Busscher-Lange J., Kooiker M., Busscher M., Angenent G.C. Analysis of the petunia MADS-box transcription factor family. Mol. Genet. Genomics. 268:2003;598-606.
38. Immink R.G.H., Angenent G.C. Transcription factors do it together: the hows and whys of studying protein-protein interactions. Trends Plant. Sci. 7:2002;531-534.
39. Immink R.G.H., Gadella T.W.J., Ferrario S., Busscher M., Angenent G.C. Analysis of MADS-box protein-protein interactions in living plant cells. Proc. Natl. Acad. Sci. USA. 99:2002;2416-2421.
40. Yang Y., Fanning L., Jack T. The K domain mediates heterodimerization of the Arabidopsis floral organ identity proteins, APETALA3 and PISTILLATA. Plant. J. 33:2003;47-59.
41. Yang Y., Xiang H., Jack T. Pistillata-5, an Arabidopsis B class mutant with strong defects in petal but not in stamen development. Plant J. 33:2003;177-188.
42. Favaro R., Immink R.G.H., Ferioli V., Bernasconi B., Byzova M., Angenent G.C., Kater M., Colombo L. Ovule-specific MADS-box proteins have conserved protein-protein interactions in monocot and dicot plants. Mol. Genet. Genomics. 268:2002;152-159.
43. Egea-Cortines M., Davies B. Beyond the ABCs: ternary complex formation in the control of floral organ identity. Trends Plant. Sci. 5:2000;471-476.
44. Angenent G.C., Franken J., Busscher M., Weiss D., Van Tunen A.J. Co-suppression of the petunia homeotic gene fbp2 affects the identity of the generative meristem. Plant J. 5:1994;33-44.
45. Pnueli L., Hareven D., Broday L., Hurwitz C., Lifschitz E. The TM5 MADS-box gene mediates organ differentiation in the three inner whorls of tomato flowers. Plant. Cell. 6:1994;175-186.
46. Honma T., Goto K. Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature. 409:2001;525-529.
47. 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. 18:1999;5370-5379.
48. Lamb R.S., Irish V.F. Functional divergence within the APETALA3/PISTILLATA floral homeotic gene lineages. Proc. Natl. Acad. Sci. USA. 100:2003;6558-6563 A detailed analysis of the carboxyl termini of the AP3 and PI genes reveals the essential role of conserved short motifs in specifying the function of the corresponding proteins. Domain-swap experiments show that the carboxyl terminus of AP3, which contains the conserved motifs, is sufficient to confer AP3 function to the PI protein, however, the converse is not true. Furthermore, a correlation was found between the divergence of the AP3 carboxyl terminus in core eudicots and the acquisition of a role for this protein in specifying perianth structures.
49. Vandenbussche M., Theissen G., Van de Peer Y., Gerats T. Structural diversification and neo-functionalization during floral MADS-box gene evolution by C-terminal frameshift mutations. Nucleic Acids Res. 31:2003;4401-4409 The authors present the interesting hypothesis that different motifs in the carboxy-terminal domains of MADS-box sequences from lower angiosperms and higher eudicots may have evolved after a frameshift mutation in an ancestral MADS-box gene. They hypothesise that this led to newly formed carboxy-terminal motifs in A- and B-class genes that are only present in higher eudicots. The authors speculate that these motifs may have contributed to the functional diversification of primitive and higher angiosperms and to the highly standardised floral structure found in higher dicots.
50. Soltis D.E., Soltis P.S., Albert V.A., Oppenheimer D.G., dePamphilis C.W., Ma H., Frohlich M.W., Theissen G. Missing links: the genetic architecture of flower and floral diversification. Trends Plant. Sci. 7:2002;22-31 This review presents and discusses a genomics approach to understanding flower evolution and development. It is focussed on the identification and expression patterns of floral genes in species that differ principally in the arrangement, number and organisation of floral parts. The authors respond to criticism raised by colleagues who are in favour of a genetic and more functional approach to studying comparative flower development.
51. Goff S.A., Ricke D., Lan T.-H., Presting G., Wang R., Dunn M., Glazebrook J., Sessions A., Oeller P., Varma H.et al. A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science. 296:2002;92-100 This report reveals the draft genome sequence of rice, and compares Arabidopsis and rice sequences. Putative orthologues of known Arabidopsis flowering and flower-development genes were identified in rice, suggesting that part of the genetic network that regulates flower development exists in this monocot model. More interestingly, no clear rice homologue of several Arabidopsis genes, including SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1 (SOC1), FLOWERING LOCUS C (FLC), FRIGIDA (FRI) and UNUSUAL FLORAL ORGANS (UFO), could be identified, which may contribute to the differences in flowering between the two model species.
52. Izawa T., Takahashi Y., Yano M. Comparative biology comes into bloom: genomic and genetic comparison of flowering pathways in rice and Arabidopsis. Curr. Opin. Plant. Biol. 6:2003;113-120.
53. The Arabidopsis Genome Initiative: Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 2000, 408:796-815.
54. Yu J., Hu S., Wang J., Wong G.K.-S., Li S., Liu B., Deng Y., Dai L., Zhou Y., Zhang X.et al. A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science. 296:2002;79-92.
55. De Bodt S., Raes J., Florquin K., Rombauts S., Rouzé P., Theissen G., Van de Peer Y. Genomewide structural annotation and evolutionary analysis of the type I MADS-box genes in plants. J. Mol. Evol. 56:2003;573-586.
56. Pařenicová L., De Folter S., Kieffer M., Horner D.S., Favalli C., Busscher J., Cook H.E., Ingram R.M., Kater M.M., Davies B.et al. Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis: new openings to the MADS world. Plant. Cell. 15:2003;1538-1551.
57. Taylor G. Populus: Arabidopsis for forestry. Do we need a model tree? Ann. Bot. 90:2002;681-689.
58. Van den Bosch K.A., Stacey G. Summaries of legume genomics projects from around the globe. Community resources for crops and models. Plant. Physiol. 131:2003;840-865.
59. Young N.D., Mudge J., Ellis T.H.N. Legume genomes: more than peas in a pod. Curr. Opin. Plant. Biol. 6:2003;199-204.
60. Tucker S.C. Floral development in legumes. Plant. Physiol. 131:2003;911-926.
61. Benlloch R., Navarro C., Beltrán J.P., Cañas L.A. Floral development of the model legume Medicago truncatula: ontogeny studies as a tool to better characterize homeotic mutations. Sex Plant. Reprod. 15:2003;231-241.
62. Causier B., Davies B. Analysing protein-protein interactions with the yeast two-hybrid system. Plant. Mol. Biol. 50:2002;855-870.
63. Page D.R., Grossniklaus U. The art and design of genetic screens: Arabidopsis thaliana. Nat. Rev. Genet. 3:2002;124-136 An informative overview of well-designed forward genetic screens to identify Arabidopsis mutants and affected genes that are involved in many aspects of the plant life cycle. The authors describe systems for insertional mutagenesis, modifier and gametophytic screens and the use of reporter and recombinant inbred lines (RILs) to discover gene function.
64. Alonso J.M., Stepanova A.N., Leisse T.J., Kim C.J., Chen H., Shinn P., Stevenson D.K., Zimmerman J., Barajas P., Cheuk R.et al. Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science. 301:2003;653-657.
65. Riechmann J.L., Heard J., Martin G., Reuber L., Jiang C.-Z., Keddie J., Adam L., Pineda O., Ratcliffe O.J., Samaha R.R.et al. Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science. 290:2000;2105-2110.
66. Jofuku D., den Boer B.G.W., Van Montagu M., Okamuro J.K. Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant. Cell. 6:1994;1211-1235.
67. Vandenbussche M., Zethof J., Souer E., Koes R., Tornielli G.B., Pezzotti M., Ferrario S., Angenent G.C., Gerats T. Toward the analysis of the petunia MADS box gene family by reverse and forward transposon insertion mutagenesis approaches: B, C, and D floral organ identity functions require SEPALLATA-like MADS box genes in petunia. Plant. Cell. 15:2003;2680-2693.