Abstract
DORMANCY ASSOCIATED MADS-BOX (DAM) genes are related to AGAMOUS-LIKE 24 and SHORT VEGETATIVE PHASE genes of arabidopsis and are differentially regulated coordinately with endodormancy induction and release in buds of several perennial plant species. DAM genes were first shown to directly impact endodormancy in peach where a deletion of a series of DAM resulted in loss of endodormancy induction. We have cloned and characterized several MADS box genes from the model perennial weed leafy spurge. Leafy spurge DAM genes are preferentially expressed in shoot tips and buds in response to cold temperatures and day length in a manner that is relative to the level of endodormancy induced by various environmental conditions. Over-expression of one DAM gene in arabidopsis delays flowering. Additionally, we show that at least one DAM gene is differentially regulated by chromatin remodeling. Comparisons of the DAM gene promoters between poplar and leafy spurge have identified several conserved sequences that may be important for their expression patterns in response to dormancy-inducing stimuli.
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Alabadi D, Oyama T, Yanovsky MJ, Harmon FG, Mas P, Kay SA (2001) Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science 293:880–883
Anderson JV, Gesch RW, Jia Y, Chao WS, Horvath DP (2005) Seasonal shifts in dormancy status, carbohydrate metabolism, and related gene expression in crown buds of leafy spurge. Plant Cell Environ 28:1567–1578
Anderson JV, Horvath DP, Chao WS, Foley ME, Hernandez AG, Thimmapuram J, Liu L, Gong GL, Band M, Kim R, Mikel MA (2007) Characterization of an EST database for the perennial weed leafy spurge: an important resource for weed biology research. Weed Sci 55:193–203
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
Bielenberg DG, Wang Y, Fan S, Reighard GL, Scorza R, Abbott AG (2004) A deletion affecting several gene candidates is present in the evergrowing peach mutant. J Hered 95:436–444
Bielenberg DG, Wang Y, Li ZG, Zhebentyayeva T, Fan SH, Reighard GL, Scorza R, Abbott AG (2008) Sequencing and annotation of the evergrowing locus in peach [Prunus persica (L.) Batsch] reveals a cluster of six MADS-box transcription factors as candidate genes for regulation of terminal bud formation. Tree Genet Genomes 4:495–507
Bohlenius H, Huang T, Charbonnel-Campaa L, Brunner AM, Jansson S, Strauss SH, Nilsson O (2006) CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312:1040–1043
Chao W, Anderson JV (2004) Euphorbia esula crop protection compendium. CAB International, Wallingford
Chao WS, Horvath DP, Anderson JV, Foley ME (2005) Potential model weeds to study genomics, ecology, and physiology in the 21st century. Weed Sci 53:929–937
Chao WS, Serpe MD, Anderson JV, Gesch RW, Horvath DP (2006) Sugars, hormones, and environment affect the dormancy status in underground adventitious buds of leafy spurge (Euphorbia esula). Weed Sci 54:59–68
Chen K-Y (2008) Type II MADS-box genes associated with poplar apical bud development and dormancy. Thesis Dissertation Department of Plant Sciences and Landscape Architecture, University of Maryland
Chouard P (1960) Vernalization and its relations to dormancy. Annu Rev Plant Physiol Plant Mol Biol 11:191–238
Diaz MD (1974) Vegetative and reproductive growth habits of evergreen peach trees in Mexico. In: Proceedings from the XIX International Horticulture Congress vol 18, p 525
Foley ME, Anderson JV, Horvath DP (2009) The effects of temperature, photoperiod, and vernalization on regrowth and flowering competence in Euphorbia esula (Euphorbiaceae) crown buds. Botany 87:986–992
Fujiwara S, Oda A, Yoshida R, Niinuma K, Miyata K, Tomozoe Y, Tajima T, Nakagawa M, Hayashi K, Coupland G, Mizoguchi T (2008) Circadian clock proteins LHY and CCA1 regulate SVP protein accumulation to control flowering in Arabidopsis. Plant Cell 20:2960–2971
Gumucio DL, Heilstedtwilliamson H, Gray TA, Tarle SA, Shelton D, Tagle DA, Slightom JL, Goodman M, Collins FS (1992) Phylogenetic footprinting reveals a nuclear-protein which binds to silencer sequences in the human-gamma and human-epsilon globin genes. Mol Cell Biol 12:4919–4929
Hartmann U, Hohmann S, Nettesheim K, Wisman E, Saedler H, Huijser P (2000) Molecular cloning of SVP: a negative regulator of the floral transition in Arabidopsis. Plant J 21:351–360
Horvath DP (1998) The role of specific plant organs and polar auxin transport in correlative inhibition of leafy spurge (Euphorbia esula) root buds. Can J Bot 76:1227–1231
Horvath DP (1999) Role of mature leaves in inhibition of root bud growth in Euphorbia esula L. Weed Sci 47:544–550
Horvath DP, Chao WS, Anderson JV (2002) Molecular analysis of signals controlling dormancy and growth in underground adventitious buds of leafy spurge. Plant Physiol 128:1439–1446
Horvath DP, Anderson JV, Chao WS, Foley ME (2003) Knowing when to grow: signals regulating bud dormancy. Trends Plant Sci 8:534–540
Horvath DP, Chao WS, Suttle JC, Thimmapuram J, Anderson JA (2008) Transcriptome analysis identifies novel responses and potential regulatory genes involved in seasonal dormancy transitions of leafy spurge (Euphorbia esula L.). BMC Genomics 9:536
Kotake T, Takada S, Nakahigashi K, Ohto M, Goto K (2003) Arabidopsis TERMINAL FLOWER 2 gene encodes a heterochromatin protein 1 homolog and represses both FLOWERING LOCUS T to regulate flowering time and several floral homeotic genes. Plant Cell Physiol 44:555–564
Lang GA (1987) Dormancy—a new universal terminology. Hortscience 22:817–820
Lee JH, Yoo SJ, Park SH, Hwang I, Lee JS, Ahn JH (2007) Role of SVP in the control of flowering time by ambient temperature in Arabidopsis. Genes Dev 21:397–402
Lee J, Oh M, Park H, Lee I (2008) SOC1 translocated to the nucleus by interaction with AGL24 directly regulates LEAFY. Plant J 55:832–843
Leseberg CH, Li AL, Kang H, Duvall M, Mao L (2006) Genome-wide analysis of the MADS-box gene family in Populus trichocarpa. Gene 378:84–94
Li Z, Reighard GL, Abbott AG, Bielenberg DG (2009) Dormancy-associated MADS genes from the EVG locus of peach [Prunus persica (L.) Batsch] have distinct seasonal and photoperiodic expression patterns. J Exp Bot 60:3521–3530
Mazzitelli L, Hancock RD, Haupt S, Walker PG, Pont SDA, McNicol J, Cardle L, Morris J, Viola R, Brennan R, Hedley PE, Taylor MA (2007) Co-ordinated gene expression during phases of dormancy release in raspberry (Rubus idaeus L.) buds. J Exp Bot 58:1035–1045
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. Plant J 33:867–874
Ruonala R, Rinne PLH, Kangasjarvi J, van der Schoot C (2008) CENL1 expression in the rib meristem affects stem elongation and the transition to dormancy in Populus. Plant Cell 20:59–74
Ruttink T, Arend M, Morreel K, Storme V, Rombauts S, Fromm J, Bhalerao RP, Boerjan W, Rohde A (2007) A molecular timetable for apical bud formation and dormancy induction in poplar. Plant Cell 19:2370–2390
Schulzschaeffer J, Gerhardt S (1989) Cytotaxonomic Analysis of the Euphorbia Spp (leafy spurge) complex. 2. Comparative-study of the chromosome morphology. Biologisches Zentralblatt 108:69–76
Shinozaki K, Yamaguchi-Shinozaki K (2000) Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol 3:217–223
Sung S, Amasino RM (2005) Remembering winter: toward a molecular understanding of vernalization. Annu Rev Plant Biol 56:491–508
Yamane H, Kashiwa Y, Ooka T, Tao R, Yonemori K (2008) Suppression subtractive hybridization and differential screening reveals endodormancy-associated expression of an SVP/AGL24-type MADS-box gene in lateral vegetative buds of Japanese apricot. J Am Soc Hortic Sci 33:708–716
Zhang X, Germann S, Blus BJ, Khorasanizadeh S, Gaudin V, Jacobsen SE (2007) The Arabidopsis LHP1 protein colocalizes with histone H3 Lys27 trimethylation. Nat Struct Mol Biol 14:869–871
Zhang JZ, Li ZM, Mei L, Yao JL, Hu CG (2009) PtFLC homolog from trifoliate orange (Poncirus trifoliata) is regulated by alternative splicing and experiences seasonal fluctuation in expression level. Planta 229:847–859
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I would like to thank Laura Kelly for significant technical assistance with these experiments and Dr. Marion Wood for her helpful commentary on this manuscript.
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Horvath, D.P., Sung, S., Kim, D. et al. Characterization, expression and function of DORMANCY ASSOCIATED MADS-BOX genes from leafy spurge. Plant Mol Biol 73, 169–179 (2010). https://doi.org/10.1007/s11103-009-9596-5
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DOI: https://doi.org/10.1007/s11103-009-9596-5