Molecular evolution of the petal and stamen identity genes, APETALA3 and PISTILLATA, after petal loss in the Piperales

Molecular Phylogenetics and Evolution

Volumn 44, Issue 2, 2007, Pages 598-609

  Jaramillo, M Alejandra ^a   Kramer, Elena M ^a  

^a HARVARD UNIVERSITY   (United States)

Author keywords

APETALA3; B class genes; Petal loss; Piperales; PISTILLATA; Relaxed selection

Indexed keywords

MADS DOMAIN PROTEIN;

AMINO ACID SEQUENCE; ANGIOSPERM; ARABIDOPSIS; ARISTOLOCHIA; ARTICLE; CHEMISTRY; CLASSIFICATION; FLOWER; GENE; GENETICS; HISTOLOGY; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ANGIOSPERMS; ARABIDOPSIS; ARISTOLOCHIA; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; FLOWERS; GENES, PLANT; MADS DOMAIN PROTEINS; MOLECULAR SEQUENCE DATA; PHYLOGENY; SEQUENCE ALIGNMENT;

ARISTOLOCHIACEAE; MAGNOLIOPHYTA; PIPERACEAE; PIPERALES; SAURURACEAE;

EID: 34447277846     PISSN: 10557903     EISSN: 10959513     Source Type: Journal    
DOI: 10.1016/j.ympev.2007.03.015     Document Type: Article

References (85)

1. Aagaard J.E., Willis J.H., and Phillips P.C. Relaxed selection among duplicate floral regulatory genes in Lamiales. J. Mol. Evol. 63 (2006) 493-503
2. Alvarez-Buylla E.R., Pelaz S., Liljegren S.J., Gold S.E., Burgeff C., Ditta G.S., Ribas de Pouplana L., Martinez-Castilla L., and Yanofsky M.F. An ancestral MADS-box gene duplication occurred before the divergence of plants and animals. Proc. Natl. Acad. Sci. USA 97 (2000) 5328-5333
3. Ambrose B.A., Lerner D.R., Ciceri P., Padilla C.M., Yanofsky M.F., and 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
4. Aoki S., Uehara K., Imafuku M., Hasebe M., and Ito M. Phylogeny and divergence of basal angiosperms inferred from APETALA3- and PISTILLATA-like MADS-box genes. J. Plant Res. 117 (2004) 229-244
5. APG, 2003. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG II. Bot. J. Linn. Soc. 141, 399-436.
6. Baum D.A., Yoon H.S., and Oldham R.L. Molecular evolution of the transcription factor LEAFY in Brassicaceae. Mol. Phylogenet. Evol. 37 (2005) 1-14
7. Becker A., Kaufmann K., Freialdenhoven A., Vincent C., Li M.A., Saedler H., and Theissen G. A novel MADS-box gene subfamily with a sister-group relationship to class B floral homeotic genes. Mol. Genet. Genomics 266 (2002) 942-950
8. Bennett M.D., and Leitch I.J. Nuclear DNA amounts in angiosperms. Ann. Bot. 76 (1995) 113-176
9. Bennett M.D., Smith J.B., and Heslop-Harrison J.S. Nuclear-DNA amounts in angiosperms. Proc. Roy. Soc. Lon. Ser. B. Biol. Sci. 216 (1982) 179-199
10. Borsch T., Hilu K.W., Quandt D., Wilde V., Neinhuis C., and Barthlott W. Noncoding plastid trnT-trnF sequences reveal a well resolved phylogeny of basal angiosperms. J. Evol. Biol. 16 (2003) 558-576
11. Bowman J.L., Smyth D.R., and Meyerowitz E.M. Genes directing flower development in Arabidopsis. Plant Cell 1 (1989) 37-52
12. Causier B., Castillo R., Zhou J.L., Ingram R., Xue Y.B., Schwarz-Sommer Z., and Davies B. Evolution in action: following function in duplicated floral homeotic genes. Curr. Biol. 15 (2005) 1508-1512
13. Cho S., Jang S., Chae S., Chung K.M., Moon Y.-W., An G., and Jang S.K. Analysis of the C-terminal region of Arabidopsis thaliana APETALA1 as a transcription activation domain. Plant Mol. Biol. 40 (1999) 419-429
14. Coen E.S., and Meyerowitz E.M. The war of the whorls: genetic interactions controlling flower development. Nature 353 (1991) 31-37
15. Conant G.C., and Wagner A. Asymmetric sequence divergence of duplicate genes. Genome Res. 13 (2003) 2052-2058
16. Crandall K.A., and Hillis D.M. Rhodopsin evolution in the dark. Nature 387 (1997) 667-668
17. Cronquist A. An Integrated System of Classification of Flowering Plants (1981), Columbia University Press, New York
18. Darwin C. On the Origin of Species by Means of Natural Selection, or the Perservation of Favoured Races in the Struggle for Life (1859), John Murray, London
19. dePamphilis C.W., Young N.D., and Wolfe A.D. Evolution of plastid gene rps2 in a lineage of hemiparasitic and holoparasitic plants: Many losses of photosynthesis and complex patterns of rate variation. Proc. Natl. Acad. Sci. USA 94 (1997) 7367-7372
20. Doyle J.A., and Endress P.K. Morphological phylogenetic analysis of basal angiosperms: comparison and combination with molecular data. Int. J. Plant Sci. 161 (2000) S121-S153
21. Doyle J.J., and Doyle J.A. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem. Bull., Bot. Soc. Am. 19 (1987) 11-15
22. Egea-Cortines M., Saedler H., and 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
23. Force A., Lynch M., Pickett F.B., Amores A., Yan Y.-L., and Postlethwait J. Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151 (1999) 1531-1545
24. Goto K., and Meyerowitz E.M. Function and regulation of the Arabidopsis floral homeotic gene PISTILLATA. Genes Dev. 8 (1994) 1548-1560
25. Graham S.W., and Olmstead R.G. Utility of 17 chloroplast genes for inferring the phylogeny of the basal angiosperms. Am. J. Bot. 87 (2000) 1712-1730
26. Gregory M.P. A phyletic rearrangement in the Aristolochiaceae. Am. J. Bot. 43 (1956) 110-122
27. Hilu K.W., Borsch T., Muller K., Soltis D.E., Soltis P.S., Savolainen V., Chase M.W., Powell M.P., Alice L.A., Evans R., Sauquet H., Neinhuis C., Slotta T.A.B., Rohwer J.G., Campbell C.S., and Chatrou L.W. Angiosperm phylogeny based on matK sequence information. Am. J. Bot. 90 (2003) 1758-1776
28. Honma T., and Goto K. Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409 (2001) 525-529
29. Huelsenbeck J., and Ronquist F. MrBayes v3 (2002), Uppsala University, Uppsala, Switzerland
30. Hughes A.L. Adaptive Evolution of Genes and Genomes (1999), Oxford University Press
31. Jack T. Molecular and genetic mechanisms of floral control. Plant Cell 16 (2004) S1-S17
32. Jack T., Fox G.L., and Meyerowitz E.M. Arabidopsis homeotic gene APETALA3 ectopic expression: transcriptional and posttranscriptional regulation determine floral organ identity. Cell 76 (1994) 703-716
33. Jaramillo M.A., and Kramer E.M. APETALA3 and PISTILLATA homologs exhibit novel expression patterns in the unique perianth in Aristolochia (Aristolochiaceae). Evol. Dev. 6 (2004) 449-458
34. Jaramillo M.A., Manos P.S., and Zimmer E.A. Phylogenetic relationships of the perianthless Piperales: reconstructing the evolution of floral development. Int. J. Plant Sci. 165 (2004) 403-416
35. Jeffery W.R. Cavefish as a model system in evolutionary developmental biology. Dev. Biol. 231 (2001) 1-12
36. Jenik P.D., and Irish V.F. The Arabidopsis floral homeotic gene APETALA3 differentially regulates intercellular signaling required for petal and stamen development. Development 128 (2001) 13-23
37. Jordan I.K., Wolf Y.I., and Koonin E.V. Duplicated genes evolve slower than singletons despite the initial rate increase. BMC Evol. Biol. 4 (2004)
38. Kang H.-G., Jeon J.-S., Lee S., and An G. Identification of class B and class C floral organ identity genes from rice plants. Plant Mol. Biol. 38 (1998) 1021-1029
39. Kanno A., Saeki H., Kameya T., Saedler H., and Theissen G. Heterotopic expression of class B floral homeotic genes supports a modified ABC model for tulip (Tulipa gesneriana). Plant Mol. Biol. 52 (2003) 831-841
40. Kim S., Koh J., Yoo M.J., Kong H.Z., Hu Y., Ma H., Soltis P.S., and Soltis D.E. Expression of floral MADS-box genes in basal angiosperms: implications for the evolution of floral regulators. Plant J. 43 (2005) 724-744
41. Kim S., Yoo M., Albert V.A., Farris J.S., Soltis P.S., and Soltis D.E. Phylogeny and diversification of B-function genes in angiosperms: evolutionary and functional implications of a 260-million year old duplication. Am. J. Bot. 91 (2004) 2102-2118
42. Kimura M. The Neutral Theory of Molecular Evolution (1983), Cambridge University Press, Cambridge, UK
43. Kramer E.M., Di Stilio V.S., and Schluter P. Complex patterns of gene duplication in the APETALA3 and PISTILLATA lineages of the Ranunculaceae. Int. J. Plant Sci. 164 (2003) 1-11
44. Kramer E.M., Dorit R.L., and Irish V.F. Molecular evolution of genes controlling petal and stamen development: duplication and divergence within the APETALA3 and PISTILLATA MADS-box gene lineages. Genetics 149 (1998) 765-783
45. Kramer E.M., and Irish V.F. Evolution of genetic mechanisms controlling petal development. Nature 399 (1999) 144-148
46. Kramer E.M., and 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
47. Kramer E.M., and Jaramillo M.A. The genetic basis for innovations in floral organ identity. J. Exp. Zool. (Mol. Dev. Evol.) 304B (2005) 526-535
48. Kramer E.M., Su H.-J., Wu J.M., and Hu J.M. A simplified explanation for the frameshift mutation that created a novel C-terminal motif in the APETALA3 gene lineage. BMC Evol. Biol. 6 (2006) 30
49. Krizek B.A., and Meyerowitz E.M. Mapping the protein regions responsible for the functional specificities of the Arabidopsis MADS domain organ-identity proteins. Proc. Natl. Acad. Sci. USA 93 (1996) 4063-4070
50. Lamb R.S., and Irish V.F. Functional divergence within the APETALA3/PISTILLATA floral homeotic gene lineages. Proc. Natl. Acad. Sci. USA 100 (2003) 6558-6563
51. Lawton-Rauh A.L., Buckler E.S., and Purugganan M.D. Patterns of molecular evolution among paralogous floral homeotic genes. Mol. Biol. Evol. 16 (1999) 1037-1045
52. Leebens-Mack J., and dePamphilis C.W. Power analysis of tests for loss of selective constraint in cave crayfish and nonphotosynthetic plant lineages. Mol. Biol. Evol. 19 (2002) 1291-1302
53. Li G.S., Meng Z., Kong H.Z., Chen Z.D., Theissen G., and Lu A.M. Characterization of candidate class A, B and E floral homeotic genes from the perianthless basal angiosperm Chloranthus spicatus (Chloranthaceae). Dev. Genes Evol. 215 (2005) 437-449
54. Long M., Betrán E., Thornton K., and Wang W. The origin of new genes: glimpses from the young and old. Nat. Rev. Gen. 4 (2003) 865-875
55. Mathews S. Phytochrome evolution in green and nongreen plants. J. Heredity 96 (2005) 197-204
56. Mathews S., Burleigh J.G., and Donoghue M.J. Adaptive evolution in the photosensory domain of phytochrome A in early angiosperms. Mol. Biol. Evol. 20 (2003) 1087-1097
57. Mathews S., and Donoghue M.J. The root of the angiosperm phylogeny inferred from duplicate phytochrome genes. Science 286 (1999) 947-950
58. Moore R.C., Grant S.R., and Purugganan M. Molecular population genetics of redundant floral-regulatory genes in Arabidopsis thaliana. Mol. Biol. Evol. 22 (2005) 91-103
59. Nagasawa N., Miyoshi M., Sano Y., Satoh H., Hirano H., Sakai H., and Nagato Y. SUPERWOMAN1 and DROOPING LEAF genes control floral organ identity in rice. Development 130 (2003) 705-718
60. Nickrent D.L., Blarer A., Qiu Y.-L., Soltis D.E., Soltis P.S., and Zanis M. Molecular data place Hydnoraceae with Aristolochiaceae. Am. J. Bot. 89 (2002) 1809-1817
61. Posada D., and Crandall K.A. MODELTEST: testing the model of DNA substitution. Bioinformatics 14 (1998) 817-818
62. Qiu Y.-L., Lee J., Bernasconi-Quadroni F., Soltis D.E., Soltis P.A., Zanis M., Zimmer E.A., Chen Z., Savolainen V., and Chase M.W. The earliest angiosperms: evidence from mitochondrial, plastid and nuclear genomes. Nature 402 (1999) 404-407
63. Qiu Y.-L., Lee J., Bernasconi-Quadroni F., Soltis D.E., Soltis P.S., Zanis M., Zimmer E.A., Chen Z., Savolainen V., and Chase M.W. Phylogeny of basal angiosperms: analyses of five genes from three genomes. Int. J. Plant Sci. 161 (2000) S3-S27
64. Riechmann J.L., Krizek B.A., and 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
65. Riechmann J.L., Wang M., and Meyerowitz E.M. DNA-binding properties of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA and AGAMOUS. Nucleic Acids Res. 24 (1996) 3134-3141
66. Samuel R., Smith J.B., and Bennett M.D. Nuclear DNA variation in Piper (Piperaceae). Can. J. Gen. Cyt. 28 (1986) 1041-1043
67. Seoighe C., Johnston C.R., and Shields D.C. Significantly different patterns of amino acid replacement after gene duplication as compared to after speciation. Mol. Biol. Evol. 20 (2003) 484-490
68. Shimodaira H., and Hasegawa M. Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol. Biol. Evol. 16 (1999) 1114-1116
69. Soltis D.E., Soltis P.S., Chase M.W., Mort M.E., Albach D.C., Zanis M., Savolainen V., Hahn W.H., Hoot S.B., Fay M.F., Axtell M., Swensen S.M., Prince L.M., Kress W.J., Nixon K.C., and Farris J.S. Angiosperm phylogeny inferred from 18S rDNA, rbcL, and atpB sequences. Bot. J. Linn. Soc. 133 (2000) 381-461
70. Soltis P.S., Soltis D.E., and Chase M.W. Angiosperm phylogeny inferred from multiple genes as a tool for comparative biology. Nature 402 (1999) 402-403
71. Sommer H., Beltrán J.-P., Huijser P., Pape H., Lönnig W.-E., Saedler H., and Schwarz-Sommer Z. Deficiens, a homeotic gene involved in the control of flower morphogenesis in Antirrhinum majus: the protein shows homology to transcription factors. EMBO J. 9 (1990) 605-613
72. Stellari G.M., Jaramillo M.A., and Kramer E.M. Evolution of the APETALA3 and PISTILLATA lineages of MADS-box containing genes in basal angiosperms. Mol. Biol. Evol. 21 (2004) 506-519
73. Sun B.Y., Stuessy T.F., and Crawford D.J. Chromosome counts from the flora of the Juan Fernandez Islands, Chile. III. Pac. Sci. 44 (1990) 258-264
74. Swofford D.L. PAUP*: Phylogenetic Analysis Using Parasimony (* and other methods) (2002), Sinauer Associates, Sunderland, Massachusetts
75. Trobner W., Ramirez L., Motte P., Hue I., Huijser P., Lonnig W.E., Saedler H., Sommer H., and Schwarz-Sommer Z. Globosa-a homeotic gene which interacts with deficiens in the control of antirrhinum floral organogenesis. EMBO J. 11 (1992) 4693-4704
76. Tucker S.C., and Douglas A.W. Utility of ontogenetic and conventional characters in determining phylogenentic relationships of Saururaceae and Piperaceae (Piperales). Syst. Bot. 18 (1993) 614-641
77. Vandenbussche M., Theissen G., Van de Peer Y., and 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
78. Winter K.U., Weiser C., Kaufmann K., Bohne A., Kirchner C., Kanno A., Saedler H., and Theissen G. Evolution of class B floral homeotic proteins: obligate heterodimerization originated from homodimerization. Mol. Biol. Evol. 19 (2002) 587-596
79. Yalovsky S., Rodriguez-Concepcion M., Bracha K., Toledo-Ortiz G., and Gruissem W. Prenylation of the floral transcription factor APETALA1 modulates its function. Plant Cell 12 (2000) 1257-1266
80. Yang Y., Fanning L., and Jack T. The K domain mediates heterodimerization of the Arabidopsis floral organ identity proteins, APETALA3 and PISTILLATA. Plant J. 33 (2003) 47-59
81. Yang Z. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput. Appl. Biosci. 13 (1997) 555-556
82. Yokoyama S., and Blow N.S. Molecular evolution of the cone visual pigments in the pure rod-retina of the nocturnal gecko, Gekko gekko. Gene 276 (2001) 117-125
83. Zachgo S., de Andrade Silva E., Motte P., Trobner W., Saedler H., and Schwarz-Sommer Z. Functional analysis of the Antirrhinum floral homeotic Deficiens gene in vivo and in vitro by using a temperature-sensitive mutant. Development 121 (1995) 2861-2875
84. Zanis M., Soltis P.S., Qiu Y.-L., Zimmer E.A., and Soltis D.E. Phylogenetic analyses and perianth evolution in basal angiosperms. Ann. Mo. Bot. Gard. 90 (2003) 129-150
85. Zhang J.Z. Evolution by gene duplication: an update. Trends Ecol. Evol. 18 (2003) 292-298