Abstract
Plant MADS-box genes encode transcriptional regulators that are critical for a number of developmental processes, such as the establishment of floral organ identity, flowering time, and fruit development. It appears that the MADS-box gene family has undergone considerable gene duplication and divergence within various angiosperm lineages. SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1)/Tomato MADS-box gene 3 (TM3)-like genes are members of the MADS-box gene family and have undergone repeated duplication events. Here, we isolated and characterized the SOC1/TM3-like gene TrcMADS1 from Trillium camtschatcense (Trilliaceae) to infer the ancestral function of SOC1/TM3-like genes. The alignment of SOC1/TM3-like genes revealed the presence of a highly conserved region in the C-terminal of predicted protein sequences, designated the SOC1 motif. Phylogenetic analysis indicated that TrcMADS1 is at the basal position of the SOC1/TM3-like gene family. The TrcMADS1 mRNA was detected in both vegetative and reproductive organs by RT-PCR. Our results suggest that duplicated copies of SOC1/TM3-like gene evolved to become variously functionally specialized.
References
Borner R, Kampmann G, Chandler J, Gleissner R, Wisman E, Apel K, Melzer S (2000) A MADS domain gene involved in the transition to flowering in Arabidopsis. Plant J 24:591–599
Cseke LJ, Zheng J, Podila GK (2003) Characterization of PTM5 in aspen trees: a MADS-box gene expressed during woody vascular development. Gene 318:55–67
Decroocq V, Zhu X, Kauffman M, Kyozuka J, Peacock WJ, Dennis ES, Llewellyn DJ (1999) A TM3-like MADS-box gene from Eucalyptus expressed in both vegetative and reproductive tissues. Gene 228:155–160
Egea-Cortines M, Saedler H, Sommer H (1999) 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 18:5370–5379
Felsenstein J (2004) PHYLIP: phylogeny inference package, version 3.6. University of Washington, Seattle
Frohman MA, Dush MK, Martin GR (1988) Rapid production of full-length cDNA from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci USA 85:8998–9002
Galant R, Carroll SB (2002) Evolution of a transcriptional repression domain in an insect HOX protein. Nature 415:910–913
Hepworth SR, Valverde F, Ravenscroft D, Mouradov A, Coupland G (2002) Antagonistic regulation of flowering-time gene SOC1 by CONSTANS and FLC via separate promoter motif. EMBO J 20:4327–4337
Heuer S, Hansen S, Bantin J, Brettschneider R, Kranz E, Lorz H, Dresselhas T (2001) The maize MADS box gene ZmMADS3 affectes node number and spikelet development and is co-expressed with ZmMADS1 during flower development, in egg cells, and early embryogenesis. Plant Physiol 127:33–45
Lamb RS, Irish VF (2003) Functional divergence within the APETALA3/PISTILLATA floral homeotic gene lineages. Proc Natl Acad Sci USA 100:6558–6563
Lee H, Suh S, Park E, Cho E, Ahn JH, Kim S, Lee JS, Kwon YM, Lee I (2000) The AGAMOUS-LIKE20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes Dev 14:2366–2376
Levine M (2002) How insects lose their limbs. Nature 415:848–849
Mandel T, Lutziger I, Kuhlemeier C (1994) A ubiquitously expressed MADS-box gene from Nicotiana tabacum. Plant Mol Biol 25:319–321
Michaels SD, Ditta G, Gustafson-Brown C, Pelez S, Yanofsky M, Amasino RM (2003) AGL24 acts as a prompter of flowering in Arabidopsis and is positively regulated by vernalization. Plant J 33:867–874
Moon J, Suh SS, Lee H, Choi KR, Hong CB, Paek NC, Kim SG, Lee I (2003) The SOC1 MADS-box gene integrates vernalization and gibberellin signals for flowering in Arabidopsis. Plant J 35:613–623
Parenicova L, de Folter S, Kieffer M, Horner DS, Favalli C, Busscher J, Cook HE, Ingham RM, Kater MM, Davies B, Angenent GC, Colombo L (2003) Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis: new opening to the MADS world. Plant Cell 15:1538–1551
Ronshaugen M, McGinnis N, McGinnis W (2002) Hox protein mutation and macroevolution of the insect body plan. Nature 415:914–917
Samach A, Onouchi H, Gold SE, Ditta GS, Schwarz-Sommer Z, Yanofsky MF, Coupland G (2000) Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288:1613–1616
Schwart-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
Soltis PS, Soltis DE, Chase MW (1999) Angiosperm phylogeny inferred from multiple genes as a tool for comparative biology. Nature 402:402–404
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 Biotec J 1:361–369
Theissen G, Becker A, Di Rosa A, Kanno A, Kim JT, Münster T, Winter KU, Saedler H (2000) A short history of MADS-box genes in plants. Plant Mol Biol 42:115–149
Thompson JD, Higgins DG, Gibson TJ (1994) Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Vandenbussche M, Theissen G, Van de Peer Y, Gerats T (2003) Structural diversification and neo-functionalization during floral MADS-box gene evolution by C-terminal frameshift mutations. Nucleic Acids Res 31:4401–4409
Acknowledgements
We thank Prof. M. Ohara for kindly providing plant materials. In addition, we thank Mr. H. Tokairin for collaboration in culturing the plants. We are additionally grateful to Y. Ishikawa, P.-Y. Yun, T. Ito, Y. Mashiko, H. Ashizawa, M. Nakada, R. Shinohara, M. Komatsu, S-Y. Kim, and M. Hirai for providing help and advice. This work was supported, in part, by a Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology, Japan, and by the Sasakawa Scientific Research Grant from the Japan Science Society.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Nakamura, T., Song, IJ., Fukuda, T. et al. Characterization of TrcMADS1 gene of Trillium camtschatcense (Trilliaceae) reveals functional evolution of the SOC1/TM3-like gene family. J Plant Res 118, 229–234 (2005). https://doi.org/10.1007/s10265-005-0215-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10265-005-0215-5