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TrMADS3, a new MADS-box gene, from a perennial species Taihangia rupestris (Rosaceae) is upregulated by cold and experiences seasonal fluctuation in expression level

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Abstract

In many temperate perennial plants, floral transition is initiated in the first growth season but the development of flower is arrested during the winter to ensure production of mature flowers in the next spring. The molecular mechanisms of the process remain poorly understood with few well-characterized regulatory genes. Here, a MADS-box gene, named as TrMADS3, was isolated from the overwintering inflorescences of Taihangia rupestris, a temperate perennial in the rose family. Phylogenetic analysis reveals that TrMADS3 is more closely related to the homologs of the FLOWERING LOCUS C lineage than to any of the other MIKC-type MADS-box lineages known from Arabidopsis. The TrMADS3 transcripts are extensively distributed in inflorescences, roots, and leaves during the winter. In controlled conditions, the TrMADS3 expression level is upregulated by a chilling exposure for 1 to 2 weeks and remains high for a longer period of time in warm conditions after cold treatment. In situ hybridization reveals that TrMADS3 is predominately expressed in the vegetative and reproductive meristems. Ectopic expression of TrMADS3 in Arabidopsis promotes seed germination on the media containing relatively high NaCl or mannitol concentrations. These data indicate that TrMADS3 in a perennial species might have its role in both vegetative and reproductive meristems in response to cold.

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References

  • Amasino R (2004) Vernalization, competence, and the epigenetic memory of winter. Plant Cell 16:2553–2559

    Article  PubMed  CAS  Google Scholar 

  • Ausín I, Alonso-Blanco C, Martínez-Zapater J-M (2005) Environmental regulation of flowering Int. J. Dev Biol 49:689–705

    Article  CAS  Google Scholar 

  • Battey NH (2000) Aspects of seasonality. J Exp Bot 51:1769–1780

    Article  PubMed  CAS  Google Scholar 

  • Becker A, Theissen G (2003) The major clades of MADS-box genes and their role in the development and evolution of flowering plants. Mol Phylogenet Evol 29:464–489

    Article  PubMed  CAS  Google Scholar 

  • Brunel N, Leduc N, Poupard P, Simoneau P, Mauget J-C, Viemont J-D (2002) KNAP2, a class I KN1-like gene is a negative marker of bud growth potential in apple trees (Malus domestica [L.] Borkh.). J Exp Bot 53:2143–2149

    Article  PubMed  CAS  Google Scholar 

  • Chen K, Coleman G (2006) TypeII MADS-box genes associated with poplar apical bud development and dormancy. Abstract presented at the American society of Plant Biologists Meeting, Boston MA, USA 5–9 August 2006 (http://abstracts.aspb.org/pb2006/public/P03/P03015.html)

  • Chouard P (1960) Vernalization and its relations to dormancy. Annu Rev Plant Physiol 11:191–238

    Article  CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  PubMed  CAS  Google Scholar 

  • Depledge DP, Dalby AR (2005) COPASAAR—a database for proteomic analysis of single amino acid repeats. BMC Bioinformatics 6:196

    Article  PubMed  CAS  Google Scholar 

  • Faivre-Rampant O, Cardle L, Marshall D, Viola R, Taylor MA (2004) Changes in gene expression during meristem activation processes in Solanum tuberosum with a focus on the regulation of an auxin response factor gene. J Exp Bot 55:613–622

    Article  PubMed  CAS  Google Scholar 

  • Frohman MA, Dush MK, Martin GR (1988) Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci U S A 85:8998–9002

    Article  PubMed  CAS  Google Scholar 

  • Golding GB (1999) Simple sequence is abundant in eukaryotic proteins. Protein Sci 8:1358–1361

    PubMed  CAS  Google Scholar 

  • Griffith M, Yaish MW (2004) Antifreeze proteins in overwintering plants: a tale of two activities. Trends Plant Sci 9:399–405

    Article  PubMed  CAS  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Heggie L, Halliday KJ (2005) The highs and lows of plant life: temperature and light interactions in development. Int J Dev Biol 49:675–687

    Article  PubMed  CAS  Google Scholar 

  • Heide OM (1974) Growth and dormancy in Norway spruce ecotypes. I. Interaction of photoperiod and temperature. Physiol Plant 30:1–12

    Article  Google Scholar 

  • Irish VF, Litt A (2005) Flower development and evolution: gene duplication, diversification and redeployment. Curr Opin Genet Dev 15:454–460

    Article  PubMed  CAS  Google Scholar 

  • Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282

    PubMed  CAS  Google Scholar 

  • Karlin S, Brocchieri L, Bergman A, Mrazek J, Gentles AJ (2002) Amino acid runs in eukaryotic proteomes and disease associations. Proc Natl Acad Sci U S A 99:333–338

    Article  PubMed  CAS  Google Scholar 

  • Katti MV, Sami-Subbu R, Ranjekar PK, Gupta VS (2000) Amino acid repeat patterns in protein sequences: their diversity and structural–functional implications. Protein Sci 9:1203–1209

    Article  PubMed  CAS  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  PubMed  CAS  Google Scholar 

  • Leseberg CH, Li A, Kang H, Duvall M, Mao L (2006) Genome-wide analysis of the MADS-box gene family in Populus trichocarpa. Gene 378:84–94

    Article  PubMed  CAS  Google Scholar 

  • Li GS, Meng Z, Kong HZ, Chen ZD, Theissen G, Lu AM (2005) Characterization of candidate class A, B and E floral homeotic genes from the perianthless basal angiosperm Chloranthus spicatus (Chloranthaceae). Dev Genes Evol 215:437–449

    Article  PubMed  CAS  Google Scholar 

  • Lin SI, Wang JG, Poon SY, Su CL, Wang SS, Chiou TJ (2005) Differential regulation of FLOWERING LOCUS C expression by vernalization in cabbage and Arabidopsis. Plant Physiol 137:1037–1048

    Article  PubMed  CAS  Google Scholar 

  • Liu J, Zhu JK (1997) An arabidopsis mutant that requires increased calcium for potassium nutrition and salt tolerance. Proc Natl Acad Sci U S A 94:14960–14964

    Article  PubMed  CAS  Google Scholar 

  • Lona F (1968) Intra-reproductive vernalization in Soldanella minima. Planta 82:145–152

    Article  Google Scholar 

  • Lü S, Du X, Lu W, Chong K, 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

    PubMed  Google Scholar 

  • Martinez-Castilla L, Alvarez-Buylla E (2003) Adaptive evolution in the Arabidopsis MADS-box gene family inferred from its complete resolved phylogeny. Proc Natl Acad Sci U S A 100:13407–13412

    Article  PubMed  CAS  Google Scholar 

  • Mazzitelli L, Hancock RD, Haupt S, Walker PG, Pont SD, McNicol J, Cardle L, Morris J, Viola R, Brennan R, Hedley PE, Taylor MA (2007) Coordinated gene expression during phases of dormancy release in raspberry (Rubus idaeus L.) buds. J Exp Bot 58:1035–1045

    Article  PubMed  CAS  Google Scholar 

  • McKay JK, Richards JH, Mitchell-Olds T (2003) Genetics of drought adaptation in Arabidopsis thaliana: I. Pleiotropy contributes to genetic correlations among ecological traits. Mol Ecol 12:1137–1151

    Article  PubMed  CAS  Google Scholar 

  • Mendoza I, Rubio F, Rodriguez-Navarro A, Pardo JM (1994) The protein phosphatase calcineurin is essential for NaCl tolerance of Saccharomyces cerevisiae. J Biol Chem 269:8792–8796

    PubMed  CAS  Google Scholar 

  • Michaels SD, Amasino RM (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11:949–956

    Article  PubMed  CAS  Google Scholar 

  • Mouradov A, Cremer F, Coupland G (2002) Control of flowering time: interacting pathways as a basis for diversity. Plant Cell 14(Suppl):S111–130

    PubMed  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio-assays with tobacco tissue culture. Plant Physiol 15:473–497

    Article  CAS  Google Scholar 

  • Perry T (1971) Dormancy of trees in winter. Science 171:29–36

    Article  PubMed  CAS  Google Scholar 

  • Ratcliffe OJ, Nadzan GC, Reuber TL, Riechmann JL (2001) Regulation of flowering in Arabidopsis by an FLC homologue. Plant Physiol 126:122–132

    Article  PubMed  CAS  Google Scholar 

  • Ratcliffe OJ, Kumimoto RW, Wong BJ, Riechmann JL (2003) Analysis of the Arabidopsis MADS AFFECTING FLOWERING gene family: MAF2 prevents vernalization by short periods of cold. Plant Cell 15:1159–1169

    Article  PubMed  CAS  Google Scholar 

  • Reeves PA, He Y, Schmitz RJ, Amasino RM, Panella LW, Richards CM (2007) Evolutionary conservation of the FLC mediated vernalization response: evidence from the sugar beet (Beta vulgaris). Genetics 176:295–307

    Article  PubMed  CAS  Google Scholar 

  • Rohde A, Bhalerao RP (2007) Plant dormancy in the perennial context. Trends Plant Sci 12:217–223

    Article  PubMed  CAS  Google Scholar 

  • Rorat T (2006) Plant dehydrins—tissue location, structure and function. Cell Mol Biol Lett 11:536–556

    Article  PubMed  CAS  Google Scholar 

  • Schmitz RJ, Amasino RM (2007) Vernalization: a model for investigating epigenetics and eukaryotic gene regulation in plants. Biochim Biophys Acta 1769:269–275

    PubMed  CAS  Google Scholar 

  • Schrader J, Moyle R, Bhalerao R, Hertzberg M, Lundeberg J, Nilsson P, Bhalerao RP (2004) Cambial meristem dormancy in trees involves extensive remodelling of the transcriptome. Plant J 40:173–187

    Article  PubMed  CAS  Google Scholar 

  • Schranz ME, Quijada P, Sung SB, Lukens L, Amasino R, Osborn TC (2002) Characterization and effects of the replicated flowering time gene FLC in Brassica rapa. Genetics 162:1457–1468

    PubMed  CAS  Google Scholar 

  • Scortecci KC, Michaels SD, Amasino RM (2001) Identification of a MADS-box gene, FLOWERING LOCUS M, that represses flowering. Plant J 26:229–236

    Article  PubMed  CAS  Google Scholar 

  • Sheldon CC, Burn JE, Perez PP, Metzger J, Edwards JA, Peacock WJ, Dennis ES (1999) The FLF MADS box gene: a repressor of flowering in Arabidopsis regulated by vernalization and methylation. Plant Cell 11:445–458

    Article  PubMed  CAS  Google Scholar 

  • Sheldon CC, Rouse DT, Finnegan EJ, Peacock WJ, Dennis ES (2000) The molecular basis of vernalization: the central role of FLOWERING LOCUS C (FLC). Proc Natl Acad Sci U S A 97:3753–3758

    Article  PubMed  CAS  Google Scholar 

  • Shen SH, Lu WL, Wang FH (1994) Studies on the reproductive biology of Taihangia rapestris: I analysis on the habitat of T. repestris. Biodivers Sci 2:210–212

    Google Scholar 

  • Tadege M, Sheldon CC, Helliwell CA, Stoutjesdijk P, Dennis ES, Peacock WJ (2001) Control of flowering time by FLC orthologues in Brassica napus. Plant J 28:545–553

    Article  PubMed  CAS  Google Scholar 

  • Thomashow M (1998) Role of cold-responsive genes in plant freezing tolerance. Plant Physiol 118:1–8

    Article  PubMed  CAS  Google Scholar 

  • Thompson J, Gibson T, Plewniak F, Jeanmougin F, Higgins D (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  PubMed  CAS  Google Scholar 

  • Vandenbussche M, Zethof J, Souer E, Koes R, Tornielli GB, Pezzotti M, Ferrario S, Angenent GC, Gerats T (2003) Toward the analysis of the petunia MADS box gene family by reverse and forward transposon insertion mutagenesis approaches: B, C, and D floral organ identity functions require SEPALLATA-like MADS box genes in petunia. Plant Cell 15:2680–2693

    Article  PubMed  CAS  Google Scholar 

  • Welling A, Moritz T, Palva E, Junttila O (2002) Independent activation of cold acclimation by low temperature and short photoperiod in hybrid aspen. Plant Physiol 129:1633–1641

    Article  PubMed  CAS  Google Scholar 

  • Wu SJ, Ding L, Zhu JK (1996) SOS1, a genetic locus essential for salt tolerance and potassium acquisition. Plant Cell 8:617–627

    Article  PubMed  CAS  Google Scholar 

  • Yü T, Li C (1980) Taihangia—a new genus of Rosaceae from China. Acta Phytotax Sin 18:469–472

    Google Scholar 

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Acknowledgements

We thank Suzhen Zhao, Hongyan Shan, and Kunmei Su for lab assistance. We are grateful to Prof. Dr. Günter Theissen for critical reading of the manuscript. We thank Dr. Hongzhi Kong for his helpful suggestions on phylogenetic analysis. We also thank all anonymous reviewers for helpful comments on the manuscript. This work was supported by National Nature Science Foundation of China (30121003, 30770212, and 30530090).

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Authors and Affiliations

  1. Laboratory of Photosynthesis and Environmental Molecular Physiology, Institute of Botany, Chinese Academy of Sciences, Xiangshan, Beijing, 100093, China

    Xiaoqiu Du, Qiying Xiao, Ran Zhao, Feng Wu, Qijiang Xu, Kang Chong & Zheng Meng

  2. Graduate School, Chinese Academy of Sciences, Beijing, 100039, China

    Xiaoqiu Du, Qiying Xiao & Ran Zhao

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  1. Xiaoqiu Du
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Correspondence to Zheng Meng.

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Fig. S1 The trees were constructed employing the neighbor-joining (a), maximum-likelihood (b), and maximum-parsimony (c) methods, respectively. The numbers next to some nodes give bootstrap percentages of 1,000 replicates. The trees show that TrMADS3 belongs to the clade that includes Arabidopsis FLC-like genes (highlighted by arrows). The accession numbers of the genes for phylogeny are as follows: U78782 (OsMADS6); NM_001054284 (Os02g0682200); L46397 (ZAG3); L46398 (ZAG5); DQ512353; BAA94287 (PMADS4); NM_130127 (AGL6); NM_115976 (AGL13); CAB44457 (GGM11); CAA56864(DAL1); CAA64741 (DEFH49); NM_126418 (AGL3); U78892 (OsMADS8); AAK21254 (FBP23); NM_180622 (AGL9); DQ344499; NM_111098 (AGL4); NM_121585 (AGL2); Q6Z4G0 (OsMADS28); AAF04972 (OsMADS18); NM_125484 (FUL); Q40170 (TM4); NM_105581 (AP1); NM_102395 (CAL); DQ248944; AAK21258 (FBP29); X63701 (SQUA); AAQ72500 (PMADS15); AW219962; DQ189210 (BvFL1_v1); DQ189211 (BvFL1_v2); EF520739; PTMADS5 (Leseberg et al. 2006); PTMADS55 (Leseberg et al. 2006); NM_125904 (MAF2); NM_125905 (MAF3); NM_180649 (MAF1); NM_125906 (MAF4); NM_125907 (MAF5); AY306125 (BoFLC3–2); AY273164; AY273160; NM_121052 (FLC); AY957537 (ThFLC); AY306124 (BoFLC4–1); EF460819 (BrFLC); EF542803; ABP96967; NM_127828 (AGL17); NM_119955 (AGL21); NM_115583 (AGL16); AF112149 (ZMMADS2); NM_126990 (ANR1); NM_115599 (AGL18); NM_121382 (AGL15); NM_122232 (TT16); AJ307056 (DEFH21); NM_105825 (AGL12); AB050647 (MPMADS5); NM_127820 (SVP); DQ402055; AF008652 (STMADS11); NM_118587 (AGL24); AJ132208 (GGM2); DQ512361 (TaAGL15); NM_115294 (AP3); X62810 (DEFICIENS); L37526 (OsMADS2); NM_122031 (PI); X68831 (GLOBOSA); NM_125610 (AGL42); NM_130128 (AGL20); NM_118424 (AGL19); NM_117258 (AGL14); AJ132207 (GGM1); X60760 (TDR8); AB046596 (ERAF17); AJ132209 (GGM3); NM_118013 (AG); L37528 (OsMADS3); NM_179020 (AGL11); NM_180046 (SHP2); NM_001084842 (SHP1).

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Du, X., Xiao, Q., Zhao, R. et al. TrMADS3, a new MADS-box gene, from a perennial species Taihangia rupestris (Rosaceae) is upregulated by cold and experiences seasonal fluctuation in expression level. Dev Genes Evol 218, 281–292 (2008). https://doi.org/10.1007/s00427-008-0218-z

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