Evolutionary trends in the floral transcriptome: Insights from one of the basalmost angiosperms, the water lily Nuphar advena (Nymphaeaceae)

Plant Journal

Volumn 64, Issue 4, 2010, Pages 687-698

  Yoo, Mi Jeong ^a,d   Chanderbali, André S ^a,b   Altman, Naomi S ^c   Soltis, Pamela S ^b   Soltis, Douglas E ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c PENNSYLVANIA STATE UNIVERSITY   (United States)

^d IOWA STATE UNIVERSITY   (United States)

Author keywords

ABCE model; floral developmental genetics; floral evolution; Nuphar; transcriptome profiling

Indexed keywords

ABCE MODEL; DEVELOPMENTAL GENETICS; FLORAL EVOLUTION; NUPHAR; TRANSCRIPTOME PROFILING;

CHROMOSOMES; GENE EXPRESSION;

PLANTS (BOTANY);

ARABIDOPSIS; ARTICLE; AVOCADO; COMPARATIVE STUDY; EXPRESSED SEQUENCE TAG; FLOWER; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; MOLECULAR EVOLUTION; NUPHAR; PLANT GENE;

ARABIDOPSIS; EVOLUTION, MOLECULAR; EXPRESSED SEQUENCE TAGS; FLOWERS; GENE EXPRESSION PROFILING; GENES, PLANT; NUPHAR; PERSEA;

ARABIDOPSIS; ARABIDOPSIS THALIANA; LILIUM; MAGNOLIIDAE; MAGNOLIOPHYTA; NUPHAR; NUPHAR ADVENA; NYMPHAEA; NYMPHAEACEAE; PERSEA; PERSEA AMERICANA;

EID: 78449233840     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2010.04357.x     Document Type: Article

References (86)

1. Adam, H., Jouannic, S., Orieux, Y., Morcillo, F., Richaud, F., Duval, Y., and, Tregear, J.W., (2007) Functional characterization of MADS box genes involved in the determination of oil palm flower structure. J. Exp. Bot. 58, 1245-1259.
2. Albert, V.A., Soltis, D.E., Carlson, J.E., etal. (2005) Floral gene resources from basal angiosperms for comparative genomics research. BMC Plant Biol. 5, 5.
3. Altman, N.S., and, Hua, J., (2006) Extending the loop design for two-channel microarray experiments. Genet. Res. 88, 153-163.
4. Altman, N.S., Leebens-Mack, J., Zahn, L., Chanderbali, A.S., Tian, D., Werner, L., Ma, H., and, DePamphilis, C., (2006) Behind the scenes: planning a multi-species microarray experiment. Chance, 19, 27-38.
5. Alves-Ferreira, M., Wellmer, F., Banhara, A., Kumar, V., Riechmann, J.L., and, Meyerowitz, E.M., (2007) Global expression profiling applied to the analysis of Arabidopsis stamen development. Plant Physiol. 145, 747-762.
6. Ambrose, B.A., Lerner, D.R., Ciceri, P., Padilla, C.M., Yanofsky, M.F., and, 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.
7. Angenent, G.C., Franken, J., Busscher, M., Colombo, L., and, Van Tunen, A.J., (1993) Petal and stamen formation in petunia is regulated by the homeotic gene fbp1. Plant J. 4, 101-112.
8. Baum, D.A., and, Hileman, L.C., (2006) A developmental genetic model for the origin of the flower. In Flowering and Its Manipulation (, Ainsworth, C., ed.). Sheffield: Blackwell Publishing, pp. 3-27.
9. Borsch, T., Hilu, K.W., Wiersema, J.H., Löhne, C., Barthlott, W., and, Wilde, V., (2007) Phylogeny of Nymphaea (Nymphaeaceae): evidence from substitutions and microstructural changes in the chloroplast trnT-trnF region. Int. J. Plant Sci. 168, 639-671.
10. Borsch, T., Löhne, C., and, Wiersema, J.H., (2008) Phylogeny and evolutionary patterns in Nymphaeales: integrating genes, genomes and morphology. Taxon, 57, 1052-1081.
11. Buzgo, M., Soltis, P.S., and, Soltis, D.E., (2004) Floral developmental morphology of Amborella trichopoda (Amborellaceae). Int. J. Plant Sci. 165, 925-947.
12. Buzgo, M., Soltis, P.S., Kim, S., and, Soltis, D.E., (2005) The making of the flower. Biologists, 52, 149-154.
13. Chanderbali, A.S., Kim, S., Buzgo, M., Zheng, Z., Oppenheimer, D.G., Soltis, D.E., and, Soltis, P.S., (2006) Genetic footprints of stamen ancestors guide perianth evolution in Persea (Lauraceae). Int. J. Plant Sci. 167, 1075-1089.
14. Chanderbali, A.S., Albert, V.A., Leebens-Mack, J., Altman, N.S., Soltis, D.E., and, Soltis, P.S., (2009) Transcriptional signatures of ancient floral developmental genetics in avocado (Persea americana; Lauraceae). Proc. Natl. Acad. Sci. USA, 106, 8929-8934.
15. Chen, C., Wang, S., and, Huang, H., (2000) LEUNIG has multiple functions in gynoecium development in Arabidopsis. Genesis, 26, 42-54.
16. Coen, E.S., and, Meyerowitz, E.M., (1991) The war of the whorls: genetic interactions controlling flower development. Nature, 353, 31-37.
17. Conner, J., and, Liu, Z., (2000) LEUNIG, a putative transcriptional corepressor that regulates AGAMOUS expression during flower development. Proc. Natl. Acad. Sci. USA, 97, 12902-12907.
18. Davies, B., Cartolano, M., and, Schwarz-Sommer, Z., (2006) Flower development: the Antirrhinum perspective. Adv. Bot. Res. 44, 280-321.
19. Ditta, G., Pinyopich, A., Robles, P., Pelaz, S., and, Yanofsky, M.F., (2004) The SEP4 gene of Arabidopsis thaliana functions in floral organ and meristem identity. Curr. Biol. 14, 1935-1940.
20. Eisen, M.B., Spellman, P.T., Brown, P.O., and, Botstein, D., (1998) Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. USA, 95, 14863-14868.
21. Endress, P.K., (2001) The flowers in extant basal angiosperms and inferences on ancestral flowers. Int. J. Plant Sci. 162, 1111-1140.
22. Fan, J., Li, W., Dong, X., Guo, W., and, Shu, H., (2007) Ectopic expression of a hyacinth AGL6 homolog caused earlier flowering and homeotic conversion in Arabidopsis. Sci. China, C, Life Sci. 50, 676-689.
23. Fornara, F., Parenicová, L., Falasca, G., Pelucchi, N., Masiero, S., Ciannamea, S., Lopez-Dee, Z., Altamura, M.M., Colombo, L., and, Kater, M.M., (2004) Functional characterization of OsMADS18, a member of the AP1/SQUA subfamily of MADS box genes. Plant Physiol. 135, 2207-2219.
24. Frohlich, M.W., and, Parker, D.S., (2000) The mostly male theory of flower evolutionary origins: from genes to fossils. Syst. Bot. 25, 155-170.
25. Gomez-Mena, C., De Folter, S., Costa, M.M., Angenent, G.C., and, Sablowski, R., (2005) Transcriptional program controlled by the floral homeotic gene AGAMOUS during early organogenesis. Development, 132, 429-438.
26. Guo, Y., and, Gan, S., (2006) AtNAP, a NAC family transcription factor, has an important role in leaf senescence. Plant J. 46, 601-612.
27. Hardenack, S., Ye, D., Saedler, H., and, Grant, S., (1994) Comparison of MADS box gene expression in developing male and female flowers of the dioecious plant white campion. Plant Cell, 6, 1775-1787.
28. Hase, Y., Trung, K.H., Matsunaga, T., and, Tanaka, A., (2006) A mutation in the uvi4 gene promotes progression of endo-reduplication and confers increased tolerance towards ultraviolet B light. Plant J. 46, 317-326.
29. Hennig, L., Gruissem, W., Grossniklaus, U., and, Kohler, C., (2004) Transcriptional programs of early reproductive stages in Arabidopsis. Plant Physiol. 135, 1765-1775.
30. Hiepko, P., (1965) Vergleichend-morphologische und entwicklungsgeschichtliche Untersuchungen uber das Perianth bei den Polycarpicae. Bot. Jahrb. Syst. 84, 359-508.
31. Honma, T., and, Goto, K., (2001) Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature, 409, 525-529.
32. De Hoon, M.J., Imoto, S., and, Miyano, S., (2002) Statistical analysis of a small set of time-ordered gene expression data using linear splines. Bioinformatics, 18, 1477-1485.
33. Hsu, H.F., Huang, C.H., Chou, L.T., and, Yang, C.H., (2003) Ectopic expression of an orchid (Oncidium Gower Ramsey) AGL6-like gene promotes flowering by activating flowering time genes in Arabidopsis thaliana. Plant Cell Physiol. 44, 783-794.
34. Jakoby, M., Weisshaar, B., Droge-Laser, W., Vicente-Carbajosa, J., Tiedemann, J., Kroj, T., and, Parcy, F., (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci. 7, 106-111.
35. Jansen, R.K., Cai, Z., Raubeson, L.A., etal. (2007) Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns. Proc. Natl. Acad. Sci. USA, 104, 19369-19374.
36. Kang, H.G., Noh, Y.S., Chung, Y.Y., Costa, M.A., An, K., and, An, G., (1995) Phenotypic alterations of petal and sepal by ectopic expression of a rice MADS box gene in tobacco. Plant Mol. Biol. 29, 1-10.
37. Kang, H.G., Jeon, J.S., Lee, S., and, An, G., (1998) Identification of class B and class C floral organ identity genes from rice plants. Plant Mol. Biol. 38, 1021-1029.
38. Kerstetter, R.A., Bollman, K., Taylor, R.A., Bomblies, K., and, Poethig, R.S., (2001) KANADI regulates organ polarity in Arabidopsis. Nature, 411, 706-709.
39. Kim, G.T., Tsukaya, H., and, Uchimiya, H., (1998) The CURLY LEAF gene controls both division and elongation of cells during the expansion of the leaf blade in Arabidopsis thaliana. Planta, 206, 175-183.
40. Kim, G.T., Shoda, K., Tsuge, T., Cho, K.H., Uchimiya, H., Yokoyama, R., Nishitani, K., and, Tsukaya, H., (2002) The ANGUSTIFOLIA gene of Arabidopsis, a plant CtBP gene, regulates leaf-cell expansion, the arrangement of cortical microtubules in leaf cells and expression of a gene involved in cell-wall formation. EMBO J. 21, 1267-1279.
41. Kim, S., Koh, J., Yoo, M.J., Kong, H., Hu, Y., Ma, H., Soltis, P.S., and, Soltis, D.E., (2005) Expression of floral MADS-box genes in basal angiosperms: implications for the evolution of floral regulators. Plant J. 43, 724-744.
42. Kramer, E.M., and, Hall, J.C., (2005) Evolutionary dynamics of genes controlling floral development. Curr. Opin. Plant Biol. 8, 13-18.
43. Leebens-Mack, J., Raubeson, L.A., Cui, L., Kuehl, J.V., Fourcade, M.H., Chumley, T.W., Boore, J.L., Jansen, R.K., and, Depamphilis, C.W., (2005) Identifying the basal angiosperm node in chloroplast genome phylogenies: sampling one's way out of the Felsenstein zone. Mol. Biol. Evol. 22, 1948-1963.
44. Les, D.H., Schneider, E.L., Padgett, D.J., Soltis, P.S., Soltis, D.E., and, Zanis, M., (1999) Phylogeny, classification and floral evolution of water lilies (Nymphaeaceae; Nymphaeales): a synthesis of non-molecular, rbcL, matK, and 18S rDNA data. Syst. Bot. 24, 28-46.
45. Li, Y., Sorefan, K., Hemmann, G., and, Bevan, M.W., (2004) Arabidopsis NAP and PIR regulate actin-based cell morphogenesis and multiple developmental processes. Plant Physiol. 136, 3616-3627.
46. Löhne, C., Borsch, T., and, Wiersema, J.H., (2007) Phylogenetic analysis of Nymphaeales using fast-evolving and noncoding chloroplast markers. Bot. J. Linn. Soc. 154, 141-163.
47. Lü, S., Du, X., Lu, W., Chong, K., and, Meng, Z., (2007) Two AGAMOUS-like MADS-box genes from Taihangia rupestris (Rosaceae) reveal independent trajectories in the evolution of class C and class D floral homeotic functions. Evol. Dev. 9, 92-104.
48. Ma, H., Yanofsky, M.F., and, Meyerowitz, E.M., (1991) AGL1-AGL6, an Arabidopsis gene family with similarity to floral homeotic and transcription factor genes. Genes Dev. 5, 484-495.
49. Moore, M.J., Bell, C.D., Soltis, P.S., and, Soltis, D.E., (2007) Using plastid genome-scale data to resolve enigmatic relationships among basal angiosperms. Proc. Natl. Acad. Sci. USA, 104, 19363-19368.
50. Mouradov, A., Glassick, T.V., Hamdorf, B.A., Murphy, L.C., Marla, S.S., Yang, Y., and, Teasdale, R.D., (1998) Family of MADS-Box genes expressed early in male and female reproductive structures of monterey pine. Plant Physiol. 117, 55-62.
51. Nijhawan, A., Jain, M., Tyagi, A.K., and, Khurana, J.P., (2008) Genomic survey and gene expression analysis of the basic leucine zipper transcription factor family in rice. Plant Physiol. 146, 333-350.
52. Pelaz, S., Ditta, G.S., Baumann, E., Wisman, E., and, Yanofsky, M.F., (2000) B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature, 405, 200-203.
53. Poupin, M.J., Federici, F., Medina, C., Matus, J.T., Timmermann, T., and, Arce-Johnson, P., (2007) Isolation of the three grape sub-lineages of B-class MADS-box TM6, PISTILLATA and APETALA3 genes which are differentially expressed during flower and fruit development. Gene, 404, 10-24.
54. Qiu, Y.L., Dombrovska, O., Lee, J., etal. (2005) Phylogenetic analyses of basal angiosperms based on nine plastid, mitochondrial, and nuclear genes. Int. J. Plant Sci. 166, 815-842.
55. Reinheimer, R., and, Kellogg, E.A., (2009) Evolution of AGL6-like MADS box genes in grasses (Poaceae): ovule expression Is ancient and palea expression is new. Plant Cell, 21, 2591-2605.
56. Rijpkema, A.S., Zethof, J., Gerats, T., and, Vandenbussche, M., (2009) The petunia AGL6 gene has a SEPALLATA-like function in floral patterning. Plant J. 60, 1-9.
57. Rounsley, S.D., Ditta, G.S., and, Yanofsky, M.F., (1995) Diverse roles for MADS box genes in Arabidopsis development. Plant Cell, 7, 1259-1269.
58. Saarela, J.M., Rai, H.S., Doyle, J.A., Endress, P.K., Mathews, S., Marchant, A.D., Briggs, B.G., and, Graham, S.W., (2007) Hydatellaceae identified as a new branch near the base of the angiosperm phylogenetic tree. Nature, 446, 312-315.
59. Sablowski, R.W., and, Meyerowitz, E.M., (1998) A homolog of NO APICAL MERISTEM is an immediate target of the floral homeotic genes APETALA3/PISTILLATA. Cell, 92, 93-103.
60. Saldanha, A.J., (2004) Java Treeview - extensible visualization of microarray data. Bioinformatics, 20, 3246-3248.
61. Schauer, S.E., Schluter, P.M., Baskar, R., Gheyselinck, J., Bolanos, A., Curtis, M.D., and, Grossniklaus, U., (2009) Intronic regulatory elements determine the divergent expression patterns of AGAMOUS-LIKE6 subfamily members in Arabidopsis. Plant J. 59, 987-1000.
62. Schmid, M., Uhlenhaut, N.H., Godard, F., Demar, M., Bressan, R., Weigel, D., and, Lohmann, J.U., (2003) Dissection of floral induction pathways using global expression analysis. Development, 130, 6001-6012.
63. Schmid, M., Davison, T.S., Henz, S.R., Pape, U.J., Demar, M., Vingron, M., Scholkopf, B., Weigel, D., and, Lohmann, J.U., (2005) A gene expression map of Arabidopsis thaliana development. Nat. Genet. 37, 501-506.
64. Shan, H., Su, K., Lu, W., Kong, H., Chen, Z., and, Meng, Z., (2006) Conservation and divergence of candidate class B genes in Akebia trifoliata (Lardizabalaceae). Dev. Genes. Evol. 216, 785-795.
65. Shindo, S., Ito, M., Ueda, K., Kato, M., and, Hasebe, M., (1999) Characterization of MADS genes in the gymnosperm Gnetum parvifolium and its implication on the evolution of reproductive organs in seed plants. Evol. Dev. 1, 180-190.
66. Smyth, G.K., (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3, Article3.
67. Smyth, G.K., (2005) Limma: linear models for microarray data. In Bioinformatics and Computational Biology Solutions using R and Bioconductor (, Gentleman, R., Carey, V., Dudoit, S., Irizarry, R., and, Huber, W., eds). New York: Springer, pp. 397-420.
68. Smyth, G.K., Michaud, J., and, Scott, H.S., (2005) Use of within-array replicate spots for assessing differential expression in microarray experiments. Bioinformatics, 21, 2067-2075.
69. Soltis, P.S., Soltis, D.E., and, Chase, M.W., (1999) Angiosperm phylogeny inferred from multiple genes as a tool for comparative biology. Nature, 402, 402-404.
70. Soltis, D.E., Soltis, P.S., Chase, M.W., etal. (2000) Angiosperm phylogeny inferred from 18S rDNA, rbcL, and atpB sequences. Bot. J. Linn. Soc. 133, 381-461.
71. Soltis, D.E., Ma, H., Frohlich, M.W., Soltis, P.S., Albert, V.A., Oppenheimer, D.G., Altman, N.S., DePamphilis, C., and, Leebens-Mack, J., (2007) The floral genome: an evolutionary history of gene duplication and shifting patterns of gene expression. Trends Plant Sci. 12, 358-367.
72. Takhtajan, A., (1991) Evolutionary Trends in Flowering Plants. New York, NY, USA: Columbia University Press.
73. Taylor, S.A., Hofer, J.M., Murfet, I.C., Sollinger, J.D., Singer, S.R., Knox, M.R., and, Ellis, T.H., (2002) PROLIFERATING INFLORESCENCE MERISTEM, a MADS-box gene that regulates floral meristem identity in pea. Plant Physiol. 129, 1150-1159.
74. Theissen, G., and, Melzer, R., (2007) Molecular mechanisms underlying origin and diversification of the angiosperm flower. Ann. Bot. 100, 603-619.
75. Theissen, G., and, Saedler, H., (2001) Plant biology. Floral quartets. Nature, 409, 469-471.
76. Warner, K.A., Rudall, P.J., and, Frohlich, M.W., (2008) Differentiation of perianth organs in Nymphaeales. Taxon, 57, 1096-1109.
77. Warner, K.A., Rudall, P.J., and, Frohlich, M.W., (2009) Environmental control of sepalness and petalness in perianth organs of waterlilies: a new Mosaic theory for the evolutionary origin of a differentiated perianth. J. Exp. Bot. 60, 3559-3574.
78. Wellmer, F., and, Riechmann, J.L., (2005) Gene network analysis in plant development by genomic technologies. Int. J. Dev. Biol. 49, 745-759.
79. Wellmer, F., Riechmann, J.L., Alves-Ferreira, M., and, Meyerowitz, E.M., (2004) Genome-wide analysis of spatial gene expression in Arabidopsis flowers. Plant Cell, 16, 1314-1326.
80. Wellmer, F., Alves-Ferreira, M., Dubois, A., Riechmann, J.L., and, Meyerowitz, E.M., (2006) Genome-wide analysis of gene expression during early Arabidopsis flower development. PLoS Genet. 2, e117.
81. Winter, K.U., Becker, A., Munster, T., Kim, J.T., Saedler, H., and, Theissen, G., (1999) MADS-box genes reveal that gnetophytes are more closely related to conifers than to flowering plants. Proc. Natl. Acad. Sci. USA, 96, 7342-7347.
82. Yamaguchi, T., Lee, D.Y., Miyao, A., Hirochika, H., An, G., and, Hirano, H.Y., (2006) Functional diversification of the two C-class MADS box genes OsMADS3 and OsMADS58 in Oryza sativa. Plant Cell, 18, 15-28.
83. Yoo, M.J., Soltis, P.S., and, Soltis, D.E., (2010) Expression of floral MADS-box genes in two divergent "water lilies": Nymphaeales and Nelumbo. Int. J. Plant Sci. 171, 121-146.
84. Yu, D., Kotilainen, M., Pollanen, E., Mehto, M., Elomaa, P., Helariutta, Y., Albert, V.A., and, Teeri, T.H., (1999) Organ identity genes and modified patterns of flower development in Gerbera hybrida (Asteraceae). Plant J. 17, 51-62.
85. Zahn, L.M., Kong, H., Leebens-Mack, J.H., Kim, S., Soltis, P.S., Landherr, L.L., Soltis, D.E., Depamphilis, C.W., and, Ma, H., (2005) The evolution of the SEPALLATA subfamily of MADS-box genes: a preangiosperm origin with multiple duplications throughout angiosperm history. Genetics, 169, 2209-2223.
86. Zhang, X., Feng, B., Zhang, Q., Zhang, D., Altman, N., and, Ma, H., (2005) Genome-wide expression profiling and identification of gene activities during early flower development in Arabidopsis. Plant Mol. Biol. 58, 401-419.