Comparative Transcriptional Profiling Provides Insights into the Evolution and Development of the Zygomorphic Flower of Vicia sativa (Papilionoideae)

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Liu, Zhipeng ^a   Ma, Lichao ^a   Nan, Zhibiao ^a   Wang, Yanrong ^a  

^a LANZHOU UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; TRANSCRIPTOME;

ARABIDOPSIS; ARTICLE; BARREL MEDIC; COMMON VETCH; CONTROLLED STUDY; DOWN REGULATION; FLOWER DEVELOPMENT; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; MOLECULAR EVOLUTION; MOLECULAR MODEL; MOLECULAR PHYLOGENY; NUCLEOTIDE SEQUENCE; PLANT EVOLUTION; PLANT GENETICS; PLANT GENOME; PLANT LEAF; PLANT ROOT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; SEQUENCE ANALYSIS; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS;

ARABIDOPSIS; BIOLOGICAL EVOLUTION; FLOWERS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; PHYLOGENY; PLANT LEAVES; PLANT ROOTS; TRANSCRIPTOME; VICIA SATIVA;

EID: 84874338202     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0057338     Document Type: Article

References (73)

1. Coen ES, Meyerowitz EM, (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353: 31-37.
2. 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.
3. Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, et al. (2005) A gene expression map of Arabidopsis thaliana development. Nat Genet 37: 501-506.
4. Zahn LM, Ma XA, Altman NS, Zhang Q, Wall PK, et al. (2010) Comparative transcriptomics among floral organs of the basal eudicot Eschscholzia californica as reference for floral evolutionary developmental studies. Genome Biol 11: R101.
5. Voelckel C, Borevitz JO, Kramer EM, Hodges SA, (2010) Within and between whorls: comparative transcriptional profiling of Aquilegia and Arabidopsis. PLoS ONE 5: e9735.
6. Chanderbali AS, Albert VA, Leebens-Mack J, Altman NS, Soltis DE, et al. (2009) Transcriptional signatures of ancient floral developmental genetics in avocado (Persea americana; Lauraceae). PNAS 106: 8929-8934.
7. Yoo MJ, Chanderbali AS, Altman NS, Soltis PS, Soltis DE, (2010) Evolutionary trends in the floral transcriptome: insights from one of the basalmost angiosperms, the water lily Nuphar advena (Nymphaeaceae). Plant J 64: 687-698.
8. Doyle JJ, Luckow MA, (2003) The rest of the iceberg. Legume diversity and evolution in a phylogenetic context. Plant Physiol 131: 900-910.
9. Tucker SC, (2003) Floral development in legumes. Plant Physiol 131: 911-926.
10. Darwin CR, (1857) Bees and fertilisation of kidney beans. Gard Chron Agric Gaz 43: 725.
11. Hofer J, Turner L, Hellens R, Ambrose M, Matthews P, et al. (1997) UNIFOLIATA regulates leaf and flower morphogenesis in pea. Curr Biol 7: 581-587.
12. Ferrandiz C, Navarro C, Gomez MD, Canas LA, Beltran JP, (1999) Flower development in Pisum sativum: from the war of the whorls to the battle of the common primordia. Dev Genet 25: 280-290.
13. Benloch R, Navarro C, Beltran JP, Canas LA, (2003) Floral development of the model legume Medicago truncatula: ontogeny studies as a tool to better characterize homeotic mutations. Sex Plant Reprod 15: 231-241.
14. Benlloch R, d'Erfurth I, Ferrandiz C, Cosson V, Beltran JP, et al. (2006) Isolation of mtpim proves Tnt1 a useful reverse genetics tool in Medicago truncatula and uncovers new aspects of AP1-like functions in legumes. Plant Physiol 142: 972-983.
15. Foucher F, Morin J, Courtiade J, Cadioux S, Ellis N, et al. (2003) DETERMINATE and LATE FLOWERING are two TERMINAL FLOWER1/CENTRORADIALIS homologs that control two distinct phases of flowering initiation and development in pea. Plant Cell 15: 2742-2754.
16. Dong ZC, Zhao Z, Liu CW, Luo JH, Yang J, et al. (2005) Floral patterning in Lotus japonicus. Plant Physiol 137: 1272-1282.
17. Citerne HL, Pennington RT, Cronk QCB, (2006) An apparent reversal in floral symmetry in the legume Cadia is a homeotic transformation. PNAS 103: 12017-12020.
18. Domoney C, Duc G, Ellis THN, Ferrandiz C, Firnhaber C, et al. (2006) Genetic and genomic analysis of legume flowers and seeds. Curr Opin Plant Biol 9: 133-141.
19. Feng XZ, Zhao Z, Tian ZX, Xu SL, Luo YH, et al. (2006) Control of petal shape and floral zygomorphy in Lotus japonicus. PNAS 103: 4970-4975.
20. Wang HL, Chen JH, Wen JQ, Tadege M, Li GM, et al. (2008) Control of compound leaf development by FLORICAULA/LEAFY ortholog SINGLE LEAFLET1 in Medicago truncatula. Plant Physiol 146: 1759-1772.
21. Wang Z, Luo YH, Li X, Wang LP, Xu SL, et al. (2008) Genetic control of floral zygomorphy in pea (Pisum sativum L.). PNAS 105: 10414-10419.
22. Yan J, Cai XF, Luo JH, Sato S, Jiang QY, et al. (2010) The REDUCED LEAFLET genes encode key components of the trans-acting small interfering RNA pathway and regulate compound leaf and flower development in Lotus japonicus. Plant Physiol 152: 797-807.
23. Yang X, Pang HB, Liu BL, Qiu ZJ, Gao Q, et al. (2012) Evolution of double positive autoregulatory feedback loops in CYCLOIDEA2 clade genes is associated with the origin of floral zygomorphy. Plant Cell 24: 1834-1847.
24. Hogslund N, Radutoiu S, Krusell L, Voroshilova V, Hannah MA, et al. (2009) Dissection of symbiosis and organ development by integrated transcriptome analysis of Lotus japonicus mutant and wild-type plants. PLoS ONE 4: e6556.
25. Benedito VA, Torres-Jerez I, Murray JD, Andriankaja A, Allen S, et al. (2008) A gene expression atlas of the model legume Medicago truncatula. Plant J 55: 504-513.
26. Libault M, Farmer A, Joshi T, Takahashi K, Langley RJ, et al. (2010) An integrated transcriptome atlas of the crop model Glycine max, and its use in comparative analyses in plants. Plant J 63: 86-99.
27. Hoen PAC, Ariyurek Y, Thygesen HH, Vreugdenhil E, Vossen R, et al. (2008) Deep sequencing-based expression analysis shows major advances in robustness, resolution and inter-lab portability over five microarray platforms. Nucleic Acids Res 36: e141.
28. Marioni JC, Mason CE, Mane SM, Stephens M, Gilad Y, (2008) RNA-seq: An assessment of technical reproducibility and comparison with gene expression arrays. Genome Res 18: 1509-1517.
29. Asmann YW, Klee EW, Thompson EA, Perez EA, Middha S, et al. (2009) 3 ' tag digital gene expression profiling of human brain and universal reference RNA using Illumina Genome Analyzer. BMC Genomics 10: 531.
30. Sanders PM, Bui AQ, Weterings K, McIntire KN, Hsu YC, et al. (1999) Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sex Plant Reprod 11: 297-322.
31. Li RQ, Zhu HM, Ruan J, Qian WB, Fang XD, et al. (2010) De novo assembly of human genomes with massively parallel short read sequencing. Genome Res 20: 265-272.
32. Pertea G, Huang XQ, Liang F, Antonescu V, Sultana R, et al. (2003) TIGR Gene Indices clustering tools (TGICL): a software system for fast clustering of large EST datasets. Bioinformatics 19: 651-652.
33. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, et al. (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674-3676.
34. Wei LQ, Yan LF, Wang T, (2011) Deep sequencing on genome-wide scale reveals the unique composition and expression patterns of microRNAs in developing pollen of Oryza sativa. Genome Biol 12: R53.
35. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B, (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5: 621-628.
36. Wei LQ, Xu WY, Deng ZY, Su Z, Xue YB, et al. (2010) Genome-scale analysis and comparison of gene expression profiles in developing and germinated pollen in Oryza sativa. BMC Genomics 11: 338.
37. Li MN, Xu WY, Yang WQ, Kong ZS, Xue YB, (2007) Genome-wide gene expression profiling reveals conserved and novel molecular functions of the stigma in rice. Plant Physiol 144: 1797-1812.
38. Zhou D, Zhou X, Ling Y, Zhang ZH, Zhen S, (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38: 64-70.
39. Higo K, Ugawa Y, Iwamoto M, Korenaga T, (1999) Plant cis-acting regulatory DNA elements (PLACE) database:1999. Nucleic Acids Res 27: 297-300.
40. Chanderbali AS, Yoo MJ, Zahn LM, Brockington SF, Wall PK, et al. (2010) Conservation and canalization of gene expression during angiosperm diversification accompany the origin and evolution of the flower. PNAS 107: 22570-22575.
41. Martin-Trillo M, Cubas P, (2010) TCP genes: a family snapshot ten years later. Trends in Plant Science 15: 31-39.
42. Zik M, Irish VF, (2003) Global identification of target genes regulated by APETALA3 and PISTILLATA floral homeotic gene action. Plant Cell 15: 207-222.
43. Wellmer F, Riechmann JL, Alves-Ferreira M, Meyerowitz EM, (2004) Genome-wide analysis of spatial gene expression in Arabidopsis flowers. Plant Cell 16: 1314-1326.
44. Bowman JL, Smyth DR, Meyerowitz EM, (1991) Genetic interactions among floral homeotic genes of Arabidopsis. Development 112: 1-20.
45. Sommer H, Nacken W, Beltran P, Huijser P, Pape H, et al. (1991) Properties of deficiens, a homeotic gene involved in the control of flower morphogenesis in Antirrhinum majus. Development 9: 169-175.
46. Zachgo S, Silva ED, Motte P, Trobner W, Saedler H, et al. (1995) Functional-analysis of the Antirrhinum floral homeotic deficiens gene in-vivo and in-vitro by using a temperature-sensitive mutant. Development 121: 2861-2875.
47. Angenent GC, Franken J, Busscher M, Colombo L, Vantunen AJ, (1993) Petal and stamen formation in petunia is regulated by the homeotic gene fbp1. Plant J 4: 101-112.
48. Kang HG, Jeon JS, Lee S, An GH, (1998) Identification of class B and class C floral organ identity genes from rice plants. Plant Mol Biol 38: 1021-1029.
49. Fornara F, Parenicova L, Falasca G, Pelucchi N, Masiero S, et al. (2004) Functional characterization of OsMADS18, a member of the AP1/SQUA subfamily of MADS box genes. Plant Physiol 135: 2207-2219.
50. Yamaguchi T, Lee DY, Miyao A, Hirochika H, An GH, et al. (2006) Functional diversification of the two C-class MADS box genes OSMADS3 and OSMADS58 in Oryza sativa. Plant Cell 18: 15-28.
51. Yu DY, Kotilainen M, Pollanen E, Mehto M, Elomaa P, et al. (1999) Organ identity genes and modified patterns of flower development in Gerbera hybrida (Asteraceae). Plant J 17: 51-62.
52. Ambrose BA, Lerner DR, Ciceri P, Padilla CM, Yanofsky MF, et al. (2000) Molecular and genetic analyses of the silky1 gene reveal conservation in floral organ specification between eudicots and monocots. Mol Cell 5: 569-579.
53. Taylor SA, Hofer JMI, Murfet IC, Sollinger JD, Singer SR, et al. (2002) PROLIFERATING INFLORESCENCE MERISTEM, a MADS-box gene that regulates floral meristem identity in pea. Plant Physiol 129: 1150-1159.
54. Yu H, Ito T, Wellmer F, Meyerowitz EM, (2004) Repression of AGAMOUS-LIKE 24 is a crucial step in promoting flower development. Nat Genet 36: 157-161.
55. Kramer EM, Hall JC, (2005) Evolutionary dynamics of genes controlling floral development. Curr Opin Plant Biol 8: 13-18.
56. Causier B, Schwarz-Sommer Z, Davies B, (2010) Floral organ identity: 20 years of ABCs. Semin Cell Dev Biol 21: 73-79.
57. Becker A, Kaufmann K, Freialdenhoven A, Vincent C, Li MA, et al. (2002) A novel MADS-box gene subfamily with a sister-group relationship to class B floral homeotic genes. Mol Genet Genomics 266: 942-950.
58. Endress PK, (2001) The flowers in extant basal angiosperms and inferences on ancestral flowers. Int J Plant Sci 162: 1111-1140.
59. Ronse DCLP, (2007) Are petals sterile stamens or bracts? the origin and evolution of petals in the core eudicots. Ann Bot-London 100: 621-630.
60. Derstine KS, Tucker SC, (1991) Organ initiation and development of inflorescences and flowers of Acacia baileyana. Am J Bot 78: 816-832.
61. Liao BY, Zhang JZ, (2006) Evolutionary conservation of expression profiles between human and mouse orthologous genes. Mol Biol Evol 23: 530-540.
62. Singer GAC, Lloyd AT, Huminiecki LB, Wolfe KH, (2005) Clusters of co-expressed genes in mammalian genomes are conserved by natural selection. Mol Biol Evol 22: 767-775.
63. Zhang JZ, He XL, (2005) Significant impact of protein dispensability on the instantaneous rate of protein evolution. Mol Biol Evol 22: 1147-1155.
64. Yanai I, Hunter CP, (2009) Comparison of diverse developmental transcriptomes reveals that coexpression of gene neighbors is not evolutionarily conserved. Genome Res 19: 2214-2220.
65. Parikh A, Miranda ER, Katoh-Kurasawa M, Fuller D, Rot G, et al. (2010) Conserved developmental transcriptomes in evolutionarily divergent species. Genome Biol 11: R35.
66. Luo D, Carpenter R, Vincent C, Copsey L, Coen E, (1996) Origin of floral asymmetry in Antirrhinum. Nature 383: 794-799.
67. Luo D, Carpenter R, Copsey L, Vincent C, Clark J, et al. (1999) Control of organ asymmetry in flowers of Antirrhinum. Cell 99: 367-376.
68. Hileman LC, Kramer EM, Baum DA, (2003) Differential regulation of symmetry genes and the evolution of floral morphologies. PNAS 100: 12814-12819.
69. Song CF, Lin QB, Liang RH, Wang YZ, (2009) Expressions of ECE-CYC2 clade genes relating to abortion of both dorsal and ventral stamens in Opithandra (Gesneriaceae). BMC Evol Biol 9: 244.
70. Zhang WH, Kramer EM, Davis CC, (2010) Floral symmetry genes and the origin and maintenance of zygomorphy in a plant-pollinator mutualism. PNAS 107: 6388-6393.
71. Howarth DG, Martins T, Chimney E, Donoghue MJ, (2011) Diversification of CYCLOIDEA expression in the evolution of bilateral flower symmetry in Caprifoliaceae and Lonicera (Dipsacales). Ann Bot-London 107: 1521-1532.
72. Citerne HL, Luo D, Pennington RT, Coen E, Cronk QCB, (2003) A phylogenomic investigation of CYCLOIDEA-like TCP genes in the Leguminosae. Plant Physiol 131: 1042-1053.
73. Tamura K, Dudley J, Nei M, Kumar S, (2007) MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596-1599.