Skip to main content
SpringerLink
Log in

Gene expression of DAM5 and DAM6 is suppressed by chilling temperatures and inversely correlated with bud break rate

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

We previously identified a cluster of d ormancy-a ssociated M ADS-box transcription factors (DAM genes) in peach [Prunus persica (L.) Batsch] as potential candidates for control of the non-dormant phenotype observed in the evg mutant. Of these genes, DAM3, DAM5 and DAM6 were winter expressed, suggesting a role for these genes during endodormancy. We used peach cultivars with contrasting chilling requirements (CR) for bud break to observe the expression of DAM3, DAM5 and DAM6 in response to chilling accumulation in the field and controlled environments. Vegetative terminal and floral buds were sampled weekly from field grown ‘Contender’ (1050 h CR), ‘Rubyprince’ (850 h CR) and ‘Springprince’ (650 h CR) peach cultivars through winter 2008-2009. Flower and vegetative terminal bud break potential was evaluated at each sampling by forcing cuttings in a growth-permissive environment. We also measured vegetative terminal bud break and DAM gene expression in potted ‘Contender’ and ‘Peen-To’ (450 h CR) trees under controlled-environment cold exposure. DAM3, DAM5 and DAM6 are all suppressed by exposure to chilling temperatures in the field and in controlled conditions. Expression of DAM5 and DAM6 are higher in high chill cultivars prior to chilling accumulation and their expression level reaches a minimum in each cultivar coincident with acquisition of bud break competence. Expression levels of DAM5 and DAM6 in vegetative tips in controlled environment conditions were negatively correlated with the time required for bud break in forcing conditions. The expression patterns of DAM5 and DAM6 are consistent with a role as quantitative repressors of bud break.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Alonso JM, Anson JM, Espiau MT, Company RSI (2005) Determination of endodormancy break in almond flower buds by a correlation model using the average temperature of different day intervals and its application to the estimation of chill and heat requirements and blooming date. J Am Soc Hortic Sci 130:308–318

    Google Scholar 

  • Anderson JV, Chao WS, Horvath DP (2001) A current review on the regulation of dormancy in vegetative buds. Weed Sci 49:581–589

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Andres MV, Duran JM (1999) Cold and heat requirements of the apricot tree (Prunus armeniaca L.). J Hortic Science Biotechnol 74:757–761

    Google Scholar 

  • Arora R, Rowland LJ, Tanino K (2003) Induction and release of bud dormancy in woody perennials: a science comes of age. Hortscience 38:911–921

    Google Scholar 

  • Aukerman MJ, Sakai H (2003) Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell 15:2730–2741

    Article  CAS  PubMed  Google Scholar 

  • Baldocchi D, Wong S (2008) Accumulated winter chill is decreasing in the fruit growing regions of California. Clim Change 87:S153–S166

    Article  Google Scholar 

  • Bielenberg DG, Wang Y, Li Z, Zhebentyayeva T, Fan S, 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

    Article  Google Scholar 

  • Bonhomme M, Rageau R, Gendraud M (2000) Influence of temperature on the dynamics of ATP, ADP and non-adenylic triphosphate nucleotides in vegetative and floral peach buds during dormancy. Tree Physiol 20:615–621

    CAS  PubMed  Google Scholar 

  • Brunner A, Yakovlev I, Strauss S (2004) Validating internal controls for quantitative plant gene expression studies. BMC Plant Biol 4:1–14

    Article  Google Scholar 

  • Chen THH, Howe GT, Bradshaw HD (2002) Molecular genetic analysis of dormancy-related traits in poplars. Weed Sci 50:232–240

    Article  CAS  Google Scholar 

  • Dennis FG (2003) Problems in standardizing methods for evaluating the chilling requirements for the breaking of dormancy in buds of woody plants. Hortscience 38:347–350

    Google Scholar 

  • Druart N, Johansson A, Baba K, Schrader J, Sjodin A, Bhalerao RR, Resman L, Trygg J, Moritz T, Bhalerao RP (2007) Environmental and hormonal regulation of the activity-dormancy cycle in the cambial meristem involves stage-specific modulation of transcriptional and metabolic networks. Plant J 50:557–573

    Article  CAS  PubMed  Google Scholar 

  • Easterling WE (2007) Climate change and the adequacy of food and timber in the 21st century. Proc Natl Acad Sci USA 104:19679

    Article  PubMed  Google Scholar 

  • Egea J, Ortega E, Martinez-Gomez P, Dicenta F (2003) Chilling and heat requirements of almond cultivars for flowering. Environ Exp Bot 50:79–85

    Google Scholar 

  • Erez A, Fishman S (1998) The dynamic model for chilling evaluation in peach buds. Acta Hortic 465:507–510

    Google Scholar 

  • Erez A, Faust M, Line MJ (1998) Changes in water status in peach buds on induction, development and release from dormancy. Sci Hortic 73:111–123

    Article  Google Scholar 

  • Fan S, Bielenberg DG, Zhebentyayeva TN, Reighard GL, Okie WR, Holland D, Abbott AG (2009) Mapping quantitative trait loci associated with chilling requirement, heat requirement and bloom date in peach (Prunus persica). New Phytol. doi: 10.1111/j.1469-8137.2009.03119.x

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Gibson PG, Reighard GL (2002) Chilling requirement and postrest heat accumulation in peach trees inoculated with peach latent mosaic viroid. J Am Soc Hortic Sci 127:333–336

    Google Scholar 

  • Harrington CA, Gould PJ, St.Clair JB (2009) Modeling the effects of winter environment on dormancy release of Douglas-fir. For Ecol Manage. doi:10.1016/j.foreco.2009.06.018

  • Horvath DP, Anderson JV, Chao WS, Foley ME (2003) Knowing when to grow: signals regulating bud dormancy. Trends Plant Sci 8:534–540

    Article  CAS  PubMed  Google Scholar 

  • Horvath DP, Chao WS, Suttle JC, Thimmapuram J, Anderson JV (2008) Transcriptome analysis identifies novel responses and potential regulatory genes involved in seasonal dormancy transitions of leafy spurge (Euphorbia esula L.). BMC Genomics 9:17

    Article  Google Scholar 

  • Howden SM, Soussana J-F, Tubiello FN, Chhetri N, Dunlop M (2007) Adapting agriculture to climate change. Proc Natl Acad Sci USA 104:19691–19696

    Article  CAS  PubMed  Google Scholar 

  • Imaizumi T, Kay SA (2006) Photoperiodic control of flowering: not only by coincidence. Trends Plant Sci 11:550–558

    Article  CAS  PubMed  Google Scholar 

  • Jackson SD (2009) Plant responses to photoperiod. New Phytol 181:517–531

    Article  CAS  PubMed  Google Scholar 

  • Jiménez S, Lawton-Rauh AL, Reighard GL, Abbott AG, Bielenberg DG (2009) Phylogenetic analysis and molecular evolution of the dormancy associated MADS-box genes from peach. BMC Plant Biol 9: doi:10.1186/1471-2229-9-81

  • Kidner CA, Martienssen RA (2005) The developmental role of microRNA in plants. Curr Opin Plant Biol 8:38–44

    Article  CAS  PubMed  Google Scholar 

  • Kirilenko AP, Sedjo RA (2007) Climate change impacts on forestry. Proc Natl Acad Sci USA 104:10702–19697

    Article  Google Scholar 

  • Kozlowski TT, Pallardy SG (1997) Physiology of woody plants. Academic Press, San Diego

    Google Scholar 

  • Labuschagne IF, Louw JH, Schmidt K, Sadie A (2003) Selection for increased budbreak in apple. J Am Soc Hortic Sci 128:363–373

    Google Scholar 

  • Lang GA (1987) Dormancy—a new universal terminology. Hortscience 22:817–820

    Google Scholar 

  • 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 Exper Bot. doi:10.1093/jxb/erp195

  • Luedeling E, Gebauer J, Buerkert A (2009a) Climate change effects on winter chill for tree crops with chilling requirements on the Arabian Peninsula. Clim Change. doi:10.1007/s10584-009-9581-7

  • Luedeling E, Zhang M, Girvetz EH (2009b) Climatic changes lead to declining winter chill for fruit and nut trees in California during 1950–2099. PLoS One 4. doi:10.1371/journal.pone.0006166

  • Lyrene PM (2005) Breeding low-chill blueberries and peaches for subtropical areas. Hortscience 40:1947–1949

    Google Scholar 

  • Mathiason K, He D, Grimplet J, Venkateswari J, Galbraith D, Or E, Fennell A (2009) Transcript profiling in Vitis riparia during chilling requirement fulfillment reveals coordination of gene expression patterns with optimized bud break. Funct Integ Genomics 9:81–96

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • McClung CR (2001) Circadian rhythms in plants. Annu Rev Plant Physiol Plant Mol Biol 52:139

    Article  CAS  PubMed  Google Scholar 

  • Meisel L, Fonseca B, Gonzalez S, Baeza-Yates R, Cambiazo V, Campos R, Gonzalez M, Orellana A, Retamales J, Silva H (2005) A rapid and efficient method for purifying high quality total RNA from peaches (Prunus persica) for functional genomics analyses. Biol Res 38:83–88

    Article  CAS  PubMed  Google Scholar 

  • Metzger JD (1996) A physiological comparison of vernalization and dormancy chilling requirement. In: Lang GA (ed) Plant dormancy: physiology, biochemistry, and molecular biology. CAB International, New York, pp 147–155

    Google Scholar 

  • Ogundiwin EA, Martí C, Forment J, Pons C, Granell A, Gradziel TM, Peace CP, Crisosto CH (2008) Development of ChillPeach genomic tools and identification of cold-responsive genes in peach fruit. Plant Mol Biol 68:379–397

    Article  CAS  PubMed  Google Scholar 

  • Okie WR (1984) Rapid multiplication of peach seedlings by herbaceous stem cuttings. Hortscience 19(2):249–251

    CAS  Google Scholar 

  • Okie WR (1998) Handbook of peach and nectarine varieties: performance in the southeastern United States and index of names (SuDoc A 1.76:714). United States Department of Agriculture, Agricultural Research Service

  • Okie WR (1999) Register of new fruit and nut varieties: list 39. Hortscience 34:181–205

    Google Scholar 

  • Pawasut A, Fujishige N, Yamane K, Yamaki Y, Honjo H (2004) Relationships between chilling and heat requirement for flowering in ornamental peaches. J Japanese Soc Hortic Sci 73:519–523

    Article  Google Scholar 

  • Penfield S (2008) Temperature perception and signal transduction in plants. New Phytol 179:615–628

    Article  CAS  PubMed  Google Scholar 

  • Ramos A, Perez-Solis E, Ibanez C, Casado R, Collada C, Gomez L, Aragoncillo C, Allona I (2005) Winter disruption of the circadian clock in chestnut. Proc Natl Acad Sci USA 102:7037–7042

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez J, Sherman WB, Scorza R, Wisniewski M, Okie WR (1994) Evergreen peach, its inheritance and dormant behavior. J Am Soc Hortic Sci 119:789–792

    Google Scholar 

  • Rohde A, Howe GT, Olsen JE, Moritz T, Van Montagu M, Junttila O, Boerjan W (2000) Molecular aspects of bud dormancy in trees. In: Jain SM, Minocha SC (eds) Molecular biology of woody plants. Kluwer Academic Publishers, Dordrecht, pp 89–134

    Google Scholar 

  • Ruijter JM, Ramakers C, Hoogaars WMH, Karlen Y, Bakker O, van den Hoff MJB, Moorman AFM (2009) Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res 37:e45

    Article  CAS  PubMed  Google Scholar 

  • Santner A, Estelle M (2009) Recent advances and emerging trends in plant hormone signalling. Nature 459:1071–1078

    Article  CAS  PubMed  Google Scholar 

  • Schefe JH, Lehmann KE, Buschmann IR, Unger T, Funke-Kaiser H (2006) Quantitative real-time RT-PCR data analysis: current concepts and the novel “gene expression’s C-T difference” formula. J Mol Med 84:901–910

    Article  CAS  PubMed  Google Scholar 

  • Sunley RJ, Atkinson CJ, Jones HG (2006) Chill unit models and recent changes in the occurence of Winter chill and Spring frost in the United Kingdom. J Hortic Sci Biotechnol 81:949–958

    Google Scholar 

  • Topp BL, Sherman WB, Raseira MCB (2008) Low-chill cultivar development. In: Layne DR, Bassi D (eds) The peach: botany, production and uses. CAB International, Cambridge, pp 106–138

    Chapter  Google Scholar 

  • Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3: RESEARCH0034

  • Weinberger JH (1950) Chilling requirements of peach varieties. Proc Am Soc Hortic Sci 56:122–128

    Google Scholar 

  • 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 133:708–716

    Google Scholar 

  • Zaratiegui M, Irvine DV, Martienssen RA (2007) Noncoding RNAs and gene silencing. Cell 128:763–776

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This project was supported by the National Research Initiative of the USDA Cooperative State Research, Education and Extension Service grants number 2005-06137 and 2007-35304-17896. We gratefully acknowledge Dr. Halina Knap for access to the real-time PCR equipment and the Clemson University Musser Experimental Fruit Research Farm staff for plant material management. This is Technical Contribution no. 5763 of the Clemson University Experiment Station.

Author information

Authors and Affiliations

  1. Department of Environmental Horticulture, Clemson University, Clemson, SC, USA

    S. Jiménez, G. L. Reighard & D. G. Bielenberg

  2. Department of Biological Sciences, Clemson University, Clemson, SC, USA

    D. G. Bielenberg

Authors
  1. S. Jiménez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. G. L. Reighard
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. D. G. Bielenberg
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to D. G. Bielenberg.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jiménez, S., Reighard, G.L. & Bielenberg, D.G. Gene expression of DAM5 and DAM6 is suppressed by chilling temperatures and inversely correlated with bud break rate. Plant Mol Biol 73, 157–167 (2010). https://doi.org/10.1007/s11103-010-9608-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-010-9608-5

Keywords

Search

Navigation