MADS goes genomic in conifers: Towards determining the ancestral set of MADS-box genes in seed plants

Annals of Botany

Volumn 114, Issue 7, 2014, Pages 1407-1429

  Gramzow, Lydia ^a   Weilandt, Lisa ^a   Theißen, Günter ^a  

^a FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

ancestral gene set; conifer; flower development; gymnosperm; MADS box gene; most recent common ancestor; MRCA; Picea; pine; Pinus; seed plant; spruce

Indexed keywords

ANGIOSPERM; COMMON ANCESTRY; COMPLEXITY; CONIFEROUS TREE; FLOWER; GENOMICS; GREEN ALGA;

CONIFEROPHYTA; GYMNOSPERMAE; PICEA; SPERMATOPHYTA;

MADS DOMAIN PROTEIN; TRANSCRIPTOME; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; CHROMOSOME MAP; CLASSIFICATION; CONIFER; GENE EXPRESSION REGULATION; GENETICS; GENOMICS; GYMNOSPERM; LOBLOLLY PINE; MOLECULAR EVOLUTION; MOLECULAR GENETICS; PHYLOGENY; PLANT GENOME; PLANT SEED; SEQUENCE ALIGNMENT; SPRUCE;

AMINO ACID SEQUENCE; CHROMOSOME MAPPING; CONIFEROPHYTA; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, PLANT; GENOME, PLANT; GENOMICS; GYMNOSPERMS; MADS DOMAIN PROTEINS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PICEA; PINUS TAEDA; PLANT PROTEINS; SEEDS; SEQUENCE ALIGNMENT; TRANSCRIPTOME;

EID: 84913554643     PISSN: 03057364     EISSN: 10958290     Source Type: Journal    
DOI: 10.1093/aob/mcu066     Document Type: Review

References (129)

1. Adamczyk BJ, Lehti-Shiu MD, Fernandez DE. 2007. The MADS domain factors AGL15 and AGL18 act redundantly as repressors of the floral transition in Arabidopsis. The Plant Journal 50: 1007-1019.
2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. Journal of Molecular Biology 215: 403-10.
3. Alvarez-Buylla ER,Pelaz S, Liljegren SJ, et al. 2000. An ancestral MADS-box gene duplication occurred before the divergence of plants and animals. Proceedings of the National Academy of Sciences of the United States of America 97: 5328-5333.
4. Ando S, Sato Y, Kamachi S, Sakai S. 2001. Isolation of a MADS-box gene (ERAF17) and correlation of its expression with the induction of formation of female flowers by ethylene in cucumber plants (Cucumis sativus L.). Planta 213: 943-52.
5. Arora R, Agarwal P, Ray S, et al. 2007. MADS-box gene family in rice: genome-wide identification, organization and expression profiling during reproductive development and stress. BMC Genomics 8: 242.
6. Banks JA, Nishiyama T, Hasebe, et al. 2011. The Selaginella genome identifies genetic changes associated with the evolution of vascular plants. Science 332: 960-3.
7. Barker EI, AshtonNW. 2013.Aparsimonious model of lineage-specific expansion of MADS-box genes in Physcomitrella patens. Plant Cell Reports 32: 1161-1177.
8. Becker A, Theissen G. 2003. The major clades of MADS-box genes and their role in the development and evolution of flowering plants. Molecular Phylogenetics and Evolution 29: 464-489.
9. Becker A, Winter KU, Meyer B, Saedler H, Theissen G. 2000. MADS-Box gene diversity in seed plants 300 million years ago. Molecular Biology and Evolution 17: 1425-34.
10. Becker A, Kaufmann K, Freialdenhoven A, et al. 2002. A novel MADS-box gene subfamily with a sister-group relationship to class B floral homeotic genes. Molecular Genetics and Genomics 266: 942-50.
11. Bemer M,Wolters-Arts M, Grossniklaus U, Angenent GC. 2008. TheMADS domain protein DIANA acts together with AGAMOUS-LIKE80 to specify the central cell in Arabidopsis ovules. The Plant Cell 20: 2088-101.
12. Bemer M, Gordon J,Weterings K, Angenent GC. 2010. Divergence of recently duplicatedMg-typeMADS-box genes inPetunia. Molecular Biologyand Evolution 27: 481-495.
13. Bergsten J. 2005. A review of long-branch attraction. Cladistics 21: 163-193.
14. Birol I, Raymond A, Jackman SD, et al. 2013. Assembling the 20 Gb white spruce (Picea glauca) genome from whole-genome shotgun sequencing data. Bioinformatics 29: 1492-1497.
15. Borner R, Kampmann G, Chandler J, et al. 2000. A MADS domain gene involved in the transition to flowering in Arabidopsis. The Plant Journal 24: 591-599.
16. Bowe LM, Coat G. 2000. Phylogeny of seed plants based on all three genomic compartments: extant gymnosperms are monophyletic and Gnetales' closest relatives are conifers. Proceedings of the National Academy of Sciences of the United States of America 97: 4092-4097.
17. Carlsbecker A, Sundstrom J, Tandre K, et al. 2003. The DAL10 gene from Norway spruce (Picea abies) belongs to a potentially gymnosperm-specific subclass of MADS-box genes and is specifically active in seed cones and pollen cones. Evolution and Development 5: 551-61.
18. Carlsbecker A, Tandre K, Johanson U, EnglundM, Engstrom P. 2004. The MADS-box gene DAL1is a potential mediator of the juvenile-to-adult transition in Norway spruce (Picea abies). The Plant Journal 40: 546-57.
19. Carlsbecker A, Sundstrom JF, Englund M, et al. 2013. Molecular control of normal and acrocona mutant seed cone development in Norway spruce (Picea abies) and the evolution of conifer ovule-bearing organs. New Phytologist 200: 261-75.
20. Chaw S-M, Zharkikh A, Sung HM, Lau TC, Li WH. 1997. Molecular phylogeny of extant gymnosperms and seed plant evolution: analysis of nuclear 18S rRNAsequences. Molecular Biology and Evolution 14: 56-68.
21. Chaw S-M, Parkinson CL, Cheng Y, Vincent TM, Palmer JD. 2000. Seed plant phylogeny inferred from all three plant genomes: monophyly of extant gymnosperms and origin of Gnetales from conifers. Proceedings of the National Academy of Sciences of the United States of America 97: 4086-4091.
22. Chen MK, Hsu WH, Lee PF, Thiruvengadam M, Chen HI, Yang CH. 2011. The MADS box gene, FOREVER YOUNG FLOWER, acts as a repressor controlling floral organ senescence and abscission in Arabidopsis. The Plant Journal 68: 168-185.
23. Colombo M, Masiero S,Vanzulli S, LardelliP,KaterMM,Colombo L. 2008. AGL23, a type I MADS-box gene that controls female gametophyte and embryo development in Arabidopsis. The Plant Journal 54: 1037-48.
24. Cronk QCB. 2001. Plant evolution and development in a post-genomic context. Nature Reviews Genetics 2: 607-619.
25. De Bodt S, Raes J, Florquin K, et al. 2003. Genomewide structural annotation and evolutionary analysis of the type I MADS-box genes in plants. Journal of Molecular Evolution 56: 573-86.
26. Deng W, Ying H, Helliwell CA, Taylor JM, Peacock WJ, Dennis ES. 2011. FLOWERING LOCUS C (FLC) regulates development pathways throughout the life cycle of Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 108: 6680-6685.
27. Derelle E, Ferraz C, Rombauts S, et al. 2006. Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proceedings of the National Academy of Sciences of the United States of America 103: 11647-52.
28. Diaz-Riquelme J, Lijavetzky D, Martinez-Zapater JM, Carmona MJ. 2009. Genome-wide analysis of MIKCC-type MADS box genes in grapevine. Plant Physiology 149: 354-369.
29. Dorca-Fornell C, Gregis V, Grandi V, Coupland G, Colombo L, Kater MM. 2011. The Arabidopsis SOC1-like genes AGL42, AGL71 and AGL72 promote flowering in the shoot apical and axillary meristems. The Plant Journal 67: 1006-17.
30. Eddy SR. 1996. Hidden Markov models. Current Opinion in Structural Biology 6: 361-365.
31. Englund M, Carlsbecker A, Engstrom P, Vergara-Silva F. 2011. Morphological 'primary homology' and expression of AG-subfamily MADS-box genes in pines, podocarps, and yews. Evolution & Development 13: 171-181.
32. Ferrándiz C,GuQ, Martienssen R,YanofskyMF. 2000.Redundant regulation of meristem identity and plant architecture by FRUITFULL, APETALA1 and CAULIFLOWER. Development 127: 725-734.
33. Fornara F, Gregis V, Pelucchi N, Colombo L, Kater M. 2008. The rice StMADS11-like genesOsMADS22 andOsMADS47 cause floral reversions in Arabidopsis without complementing the svp and agl24 mutants. Journal of Experimental Botany 59: 2181-2190.
34. Fukui M, Futamura N, Mukai Y, Wang Y, Nagao A, Shinohara K. 2001. Ancestral MADS box genes in Sugi, Cryptomeria japonica D. Don (Taxodiaceae), homologous to the B function genes in angiosperms. Plant and Cell Physiology 42: 566-75.
35. Futamura N, Totoki Y, Toyoda A, et al. 2008. Characterization of expressed sequence tags from a full-length enriched cDNA library of Cryptomeria japonica male strobili. BMC Genomics 9: 383.
36. Garay-Arroyo A, Ortiz-Moreno E, de la Paz Sanchez M, et al. 2013. The MADS transcription factor XAL2/AGL14 modulates auxin transport during Arabidopsis root development by regulating PIN expression. EMBO Journal 32: 2884-95.
37. Garcia-Gil MR. 2008. Evolutionary aspects of functional and pseudogene members of the phytochrome gene family in Scots pine. Journal of Molecular Evolution 67: 222-232.
38. Goff SA, Ricke D, Lan TH, et al. 2002. A draft sequence of the rice genome (Oryza sativa L. ssp japonica). Science 296: 92-100.
39. Goto K, Meyerowitz EM. 1994. Function and regulation of the Arabidopsis floral homeotic gene PISTILLATA. Genes & Development 8: 1548-1560.
40. Gramzow L, Theissen G. 2010. A hitchhiker's guide to the MADS world of plants. Genome Biology 11: 214.
41. GramzowL, Theißen G. 2013. Phylogenomics of MADS-boxgenes in plants - two opposing life styles in one gene family. Biology 2: 1150-1164.
42. Gramzow L, Ritz MS, Theissen G. 2010. On the origin of MADS-domain transcription factors. Trends in Genetics 26: 149-153.
43. Gramzow L, Barker E, Schulz C, et al. 2012. Selaginella genome analysis- entering the 'homoplasy heaven' of the MADS world. Frontiers in Plant Science 3: 214.
44. Groth E,TandreK, EngstromP,Vergara-SilvaF. 2011.AGAMOUS subfamily MADS-box genes and the evolution of seed cone morphology in Cupressaceae and Taxodiaceae. Evolution and Development 13: 159-70.
45. Gugerli F, Sperisen C, Büchler U, Brunner I, Brodbeck S, Palmer JD, Qiu YL. 2001. The evolutionary split of Pinaceae from other conifers: evidence from an intron loss and a multigene phylogeny. Molecular Phylogenetics and Evolution 21: 167-175.
46. HanP, García-Ponce B, Fonseca-Salazar G, Alvarez-Buylla ER,YuH. 2008. AGAMOUS-LIKE17, a novelflowering promoter, acts in a FT-independent photoperiod pathway. The Plant Journal 55: 253-265.
47. Hartmann U, Höhmann S, Nettesheim K,Wisman E, Saedler H, Huijser P. 2000. Molecular cloning of SVP: a negative regulator of the floral transition in Arabidopsis. The Plant Journal 21: 351-360.
48. He C, Saedler H. 2005. Heterotopic expression of MPF2 is the key to the evolution of the Chinese lantern of Physalis, a morphological novelty in Solanaceae. Proceedings of the National Academy of Sciences of the United States of America 102: 5779-5784.
49. Hedman H, Zhu TQ, von Arnold S, Sohlberg JJ. 2013. Analysis of the WUSCHEL-RELATED HOMEOBOX gene family in the conifer picea abies reveals extensive conservation as well as dynamic patterns. BMC Plant Biology 13.
50. Henschel K, Kofuji R, Hasebe M, Saedler H, Munster T, Theissen G. 2002. Two ancient classes of MIKC-type MADS-box genes are present in the moss Physcomitrella patens. Molecular Biology and Evolution 19: 801-814.
51. JagerM,HassaninA,ManuelM,LeGuyaderH, Deutsch J. 2003.MADS-box genes in Ginkgo biloba and the evolution of the AGAMOUS family. Molecular Biology and Evolution 20: 842-54.
52. Jaillon O, Aury JM, Noel B, et al. 2007. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449: 463-467.
53. Kang IH, Steffen JG, PortereikoMF, Lloyd A, Drews GN. 2008. The AGL62 MADSdomain protein regulates cellularization during endosperm development in Arabidopsis. The Plant Cell 20: 635-647.
54. Khan MR, Ali GM. 2013. Functional evolution of cis-regulatory modules of STMADS11 superclade MADS-box genes. Plant Molecular Biology 83: 489-506.
55. Kim S, Soltis PS, Soltis DE. 2013. AGL6-like MADS-box genes are sister to AGL2-like MADS-box genes. Journal of Plant Biology 56: 315-325.
56. KinlawCS, Neale DB. 1997.Complex gene families in pine genomes. Trends in Plant Science 2: 356-359.
57. Koo SC, Bracko O, Park MS, et al. 2010. Control of lateral organ development and flowering time by the Arabidopsis thaliana MADS-box gene AGAMOUS-LIKE6. The Plant Journal 62: 807-816.
58. Kutter C, Schob H, Stadler M, Meins FJr, Si-Ammour A. 2007. MicroRNA-mediated regulation of stomatal development in Arabidopsis. The Plant Cell 19: 2417-2429.
59. Kvarnheden A, Albert VA, Engstrom P. 1998. Molecular evolution of cdc2 pseudogenes in spruce (Picea). Plant Molecular Biology 36: 767-774.
60. Kwantes M, Liebsch D, Verelst W. 2012. How MIKC∗ MADS-box genes originated and evidence for their conserved function throughout the evolution of vascular plant gametophytes. Molecular Biology and Evolution 29: 293-303.
61. Lee H, Suh SS, Park E, et al. 2000. The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes and Development 14: 2366-76.
62. Lee S, Choi SC,AnG. 2008. Rice SVP-group MADS-boxproteins, OsMADS22 and OsMADS55, are negative regulators of brassinosteroid responses. The Plant Journal 54: 93-105.
63. LesebergCH,Li A,KangH, DuvallM,MaoL. 2006. Genome-wide analysis of the MADS-box gene family in Populus trichocarpa. Gene 378: 84-94.
64. Liljegren SJ, DittaGS, EshedY, Savidge B,Bowman JL,Yanofsky MF. 2000. SHATTERPROOFMADS-boxgenes control seed dispersal in Arabidopsis. Nature 404: 766-770.
65. LiuY, Cui S,WuF, et al. 2013. Functional conservation of MIKC∗-TypeMADS box genes in Arabidopsis and rice pollen maturation. The Plant Cell 25: 1288-303.
66. LorenzWW, AyyampalayamS, Bordeaux JM, et al. 2012. Conifer DBMagic: a database housing multiple de novo transcriptome assemblies for 12 diverse conifer species. Tree Genetics & Genomes 8: 1477-1485.
67. Lovisetto A, Guzzo F, Tadiello A, Toffali K, Favretto A, Casadoro G. 2012. Molecular analyses of MADS-box genes trace back to Gymnosperms the invention of fleshy fruits. Molecular Biology and Evolution 29: 409-419.
68. Lovisetto A, Guzzo F, Busatto N, Casadoro G. 2013. Gymnosperm B-sister genes may be involved in ovule/seed development and, in some species, in the growth of fleshy fruit-like structures. Annals of Botany 112: 535-544.
69. Ma H, Yanofsky MF, Meyerowitz EM. 1991. AGL1-AGL6, an Arabidopsis gene family with similarity to floral homeotic and transcription factor genes. Genes and Development 5: 484-95.
70. Mandel MA, Gustafson-BrownC, Savidge B,YanofskyMF. 1992. Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 360: 273-277.
71. Melzer R,Wang YQ, Theissen G. 2010. The naked and the dead: the ABCs of gymnosperm reproduction and the origin of the angiosperm flower. Seminars in Cell and Developmental Biology 21: 118-128.
72. Merchant SS, Prochnik SE, Vallon O, et al. 2007. The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318: 245-251.
73. Michael TP, Jackson S. 2013. The first 50 plant genomes. Plant Genome, 6.
74. Michaels SD, Amasino RM. 2001. Loss of FLOWERING LOCUS C activity eliminates the late-flowering phenotype of FRIGIDA and autonomous pathway mutations but not responsiveness to vernalization. The Plant Cell Online 13: 935-941.
75. Michaels SD, Ditta G, Gustafson-Brown C, Pelaz S, Yanofsky M, Amasino RM. 2003. AGL24 acts as a promoter of flowering in Arabidopsis and is positively regulated by vernalization. The Plant Journal 33: 867-874.
76. Miller MA, Pfeiffer W, Schwartz T. 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In Gateway Computing Environments Workshop (GCE), 2010. Piscataway, NJ: IEEE.
77. Moreno-Risueno MA, Van Norman JM, Moreno A, Zhang J, Ahnert SE, Benfey PN. 2010. Oscillating gene expression determines competence for periodic Arabidopsis root branching. Science 329: 1306-1311.
78. Mouradov A, Hamdorf B, Teasdale RD, Kim JT, Winter KU, Theissen G. 1999. A DEF/GLO-like MADS-box gene from a gymnosperm: Pinus radiata contains an ortholog of angiosperm B class floral homeotic genes. Developmental Genetics 25: 245-252.
79. Münster T, Faigl W, Saedler H, Theißen G. 2002. Evolutionary aspects of MADS-box genes in the eusporangiate fern Ophioglossum. Plant Biology 4: 474-483.
80. NamJ, Kim J, Lee S, An G,MaH, Nei M. 2004. Type I MADS-box genes have experienced faster birth-and-death evolution than type II MADS-box genes in angiosperms. Proceedings of the National Academy of Sciences of the United States of America 101: 1910-5.
81. Nystedt B, Street NR,Wetterbom A, et al. 2013. The Norway spruce genome sequence and conifer genome evolution. Nature 497: 579-84.
82. Parenicova L, de Folter S, Kieffer M, et al. 2003. Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis: new openings to the MADS world. The Plant Cell 15: 1538-51.
83. Pelaz S, Ditta GS, Baumann E,Wisman E,YanofskyMF. 2000.BandC floral organ identity functions require SEPALLATA MADS-box genes. Nature 405: 200-203.
84. Pelaz S,Tapia-Lopez R, Alvarez-Buylla ER,YanofskyMF. 2001.Conversion of leaves into petals in Arabidopsis. Current Biology 11: 182-184.
85. PetersonKM,Rychel AL,Torii KU. 2010. Out of the mouths of plants: the molecular basis of the evolution and diversity of stomatal development. The Plant Cell 22: 296-306.
86. Pinyopich A, Ditta GS, Savidge B, et al. 2003. Assessing the redundancy of MADS-box genes during carpel and ovule development. Nature 424: 85-88.
87. Pnueli L, Abu-Abeid M, Zamir D, NackenW, Schwarz-Sommer Z, Lifschitz E. 1991. TheMADSbox gene family in tomato: temporal expression during floral development, conserved secondary structures and homology with homeotic genes from Antirrhinum and Arabidopsis. The Plant Journal 1: 255-266.
88. Portereiko MF, Lloyd A, Steffen JG, Punwani JA, Otsuga D, Drews GN. 2006. AGL80 is required for central cell and endosperm development in Arabidopsis. The Plant Cell 18: 1862-1872.
89. Rensing SA, Lang D, Zimmer AD, et al. 2008. The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319: 64-69.
90. Rijpkema AS, Zethof J, Gerats T, Vandenbussche M. 2009. The petunia AGL6 gene has a SEPALLATA-like function in floral patterning. The Plant Journal 60: 1-9.
91. Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
92. Roshan U, Livesay DR. 2006. Probalign: multiple sequence alignment using partition function posterior probabilities. Bioinformatics 22: 2715-2721.
93. Ruelens P, de Maagd RA, Proost S, Theißen G, Geuten K, Kaufmann K. 2013. FLOWERING LOCUS C in monocots and the tandem origin of angiosperm-specific MADS-box genes. Nature Communications 4: 2280.
94. Rutledge R,Regan S, Nicolas O, et al. 1998. Characterization of anAGAMOUS homologue from the conifer black spruce (Picea mariana) that produces floral homeotic conversions when expressed in Arabidopsis. The Plant Journal 15: 625-634.
95. Ryu CH, Lee S, Cho LH, et al. 2009. OsMADS50 and OsMADS56 function antagonistically in regulating long day (LD)-dependent flowering in rice. Plant, Cell & Environment 32: 1412-27.
96. Sang X, Li Y, Luo Z, et al. 2012. CHIMERIC FLORALORGANS1, encoding a monocot-specific MADSbox protein, regulates floral organ identity in rice. Plant Physiology 160: 788-807.
97. Sayers EW, Barrett T, Benson DA, et al. 2012. Database resources of the National Center for Biotechnology Information. Nucleic Acids Research 40: D13-25.
98. Schonrock N, Bouveret R, Leroy O, et al. 2006. Polycomb-group proteins repress the floral activator AGL19 in the FLC-independent vernalization pathway. Genes Development 20: 1667-78.
99. Schwarz-Sommer Z, Huijser P, Nacken W, Saedler H, Sommer H. 1990. Genetic control of flower development by homeotic genes in Antirrhinum majus. Science 250: 931-936.
100. Shindo S, ItoM,UedaK,KatoM,HasebeM. 1999. Characterization ofMADS genes in the gymnosperm Gnetum parvifolium and its implication on the evolution of reproductive organs in seed plants. Evolution and Development 1: 180-190.
101. SmaczniakC, ImminkRG,AngenentGC,KaufmannK. 2012. Developmental and evolutionary diversity of plant MADS-domain factors: insights from recent studies. Development 139: 3081-3098.
102. Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.
103. Steffen JG,KangIH,PortereikoMF, Lloyd A,DrewsGN.2008.AGL61interacts withAGL80and is required for central cell development in Arabidopsis. Plant Physiology 148: 259-268.
104. Sundstrom J, Engstrom P. 2002. Conifer reproductive development involves B-type MADS-box genes with distinct and different activities in male organ primordia. The Plant Journal 31: 161-169.
105. Tadege M, Sheldon CC, Helliwell CA, Upadhyaya NM, Dennis ES, Peacock WJ. 2003. Reciprocal control of flowering time by OsSOC1 in transgenic Arabidopsis and by FLC in transgenic rice. Plant Biotechnology Journal 1: 361-369.
106. TandreK, AlbertVA, Sundas A, EngstromP. 1995.Conifer homologsto genes that control floral development in angiosperms. Plant Molecular Biology 27: 69-78.
107. TandreK, Svenson M, Svensson ME, EngstromP. 1998.Conservation of gene structure and activity in the regulation of reproductive organ development of conifers and angiosperms. The Plant Journal 15: 615-623.
108. Tapia-Lápez R, García-Ponce B, Dubrovsky JG, et al. 2008. An AGAMOUS-related MADS-box gene, XAL1 (AGL12), regulates root meristem cell proliferation and flowering transition in Arabidopsis. Plant Physiology 146: 1182-1192.
109. The Amborella Genome Project. 2013. The Amborella genome and the evolution of flowering plants. Science 342: 1241089.
110. The Arabidopsis Genome Initiative. 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796-815.
111. Theissen G, Becker A, Di Rosa A, et al. 2000. A short history of MADS-box genes in plants. Plant Molecular Biology 42: 115-149.
112. ThompsonJD, Gibson TJ, PlewniakF, JeanmouginF, HigginsDG.1997. The CLUSTAL X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25: 4876-4882.
113. Trobner W, Ramirez L, Motte P, et al. 1992. GLOBOSA-a homeotic gene which interacts with DEFICIENS in the control of antirrhinum floral organogenesis. EMBO Journal 11: 4693-4704.
114. TuskanGA,Difazio S, Jansson S, et al. 2006. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313: 1596-1604.
115. Uddenberg D, Reimegard J, Clapham D, et al. 2013. Early cone setting in Picea abies acrocona is associated with increased transcriptional activity of a MADS box transcription factor. Plant Physiology 161: 813-823.
116. Walden AR,Walter C, Gardner RC. 1999. Genes expressed in Pinus radiata male cones include homologs to anther-specific and pathogenesis response genes. Plant Physiology 121: 1103-1116.
117. Walia H, Josefsson C, Dilkes B, Kirkbride R, Harada J, Comai L. 2009. Dosage-dependent deregulation of an AGAMOUS-LIKE gene cluster contributes to interspecific incompatibility. Current Biology 19: 1128-1132.
118. Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ. 2009. JalviewVersion 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 25: 1189-1191.
119. Wegrzyn JL, Lee JM, Tearse BR, Neale DB. 2008. TreeGenes: a forest tree genome database. International Journal of Plant Genomics 2008: 412875.
120. Whelan S, Goldman N. 2001. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Molecular Biology and Evolution 18: 691-699.
121. Wingen LU, Münster T, Faigl W, et al. 2012. Molecular genetic basis of pod corn (Tunicate maize). Proceedings of the National Academy of Sciences of the United States of America 109: 7115-7120.
122. Winter KU, Becker A, Munster T, Kim JT, Saedler H, Theissen G. 1999. MADS-box genes reveal that gnetophytes are more closely related to conifers than to flowering plants. Proceedings of the National Academy of Sciences of the United States of America 96: 7342-7347.
123. WuCS,Wang YN,HsuCY, LinCP,ChawSM.2011. Loss of different inverted repeat copies from the chloroplast genomes of Pinaceae and cupressophytes and influence of heterotachy on the evaluation of gymnosperm phylogeny. Genome Biology and Evolution 3: 1284-1295.
124. Xi Z, Rest JS, Davis CC. 2013. Phylogenomics and coalescent analyses resolve extant seed plant relationships. PLoS One 8: e80870.
125. Yang X, Wu F, Lin X, et al. 2012. Live and let die-the Bsister MADS-box gene OsMADS29 controls the degeneration of cells in maternal tissues during seed development of rice (Oryza sativa). PLoS One 7: e51435.
126. Yanofsky MF, Ma H, Bowman JL, Drews GN, Feldmann KA, Meyerowitz EM. 1990. The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature 346: 35-39.
127. Yoo SK, Lee JS, Ahn JH. 2006. Overexpression of AGAMOUS-LIKE 28 (AGL28)promotes flowering by upregulating expression of floral promoters within the autonomous pathway. Biochemistry and Biophysics Research Communications 348: 929-936.
128. Yoo SK,WuX, Lee JS, Ahn JH. 2011.AGAMOUS-LIKE 6 is a floral promoter that negatively regulates the FLC/MAF clade genes and positively regulates FT in Arabidopsis. The Plant Journal 65: 62-76.
129. Zhang H, Forde BG. 1998. An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279: 407-409.