Skip to main content

Advertisement

Springer Nature Link
Log in

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

  • Original Paper
  • Published:
Tree Genetics & Genomes Aims and scope Submit manuscript

Abstract

Buds are specialized structures that protect fragile meristematic regions during dormancy and are part of the mechanism that plants use to survive unfavorable environmental conditions such as low temperature or dessication stress. The evergrowing (evg) mutant of peach [Prunus persica (L.) Batsch] does not form terminal vegetative buds in response to dormancy-inducing conditions such as short days and low temperatures, and the terminal meristems maintain constant growth (leaf addition and internode elongation). We genetically mapped the evg trait and identified the corresponding genomic region in a wild-type genome. We sequenced and annotated the 132-kb region. Nineteen genes were predicted to be in the sequenced region. Ten of the predicted genes were demonstrated to be expressed in the wild-type germplasm but six of these were not expressed in mutant tissues. These six genes are a cluster of MIKC-type MADS-box transcription factors similar to genes from Ipomoea batatas and Solanum tuberosum MADS-box, which also regulate meristem growth in vegetative tissues. A 41,746-bp deletion is present in this region of the mutant genome which results in the loss of all or part of four of the six MADS-box genes. The six MADS-box genes that are not expressed in the mutant are candidates for the regulation of growth cessation and terminal bud formation in peach in response to dormancy-inducing conditions and have been named dormancy-associated MADS-box (DAM) genes.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    PubMed  CAS  Google Scholar 

  • Alvarez-Buylla ER, Liljegren SJ, Pelaz S, Gold SE, Burgeff C, Ditta GS, Vergara-Silva F, Yanofsky MF (2000) MADS-box gene evolution beyond flowers: expression in pollen, endosperm, guard cells, roots and trichomes. Plant J 24:457–466

    Article  PubMed  CAS  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 

  • Aranzana MJ, Garcia-Mas J, Carbo J, Arus P (2002) Development and variability analysis of microsatellite markers in peach. Plant Breed 121:87–92

    Article  CAS  Google Scholar 

  • Aswath CR, Mo SY, Kim SH, Kim DH (2004) IbMADS4 regulates the vegetative shoot development in transgenic chrysanthemum (Dendrathema grandiflora (Ramat.) Kitamura). Plant Sci 166:847–854

    Article  CAS  Google Scholar 

  • Barak S, Tobin EM, Andronis C, Sugano S, Green RM (2000) All in good time: the Arabidopsis circadian clock. Trends Plant Sci 5:517–522

    Article  PubMed  CAS  Google Scholar 

  • Besemer J, Borodovsky M (2005) GeneMark: web software for gene finding in prokaryotes, eukaryotes and viruses. Nucleic Acids Res 33:W451–W454

    Article  PubMed  CAS  Google Scholar 

  • 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 Heredity 95:436–444

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Brill EM, Watson JM (2004) Ectopic expression of a Eucalyptus grandis SVP orthologue alters the flowering time of Arabidopsis thaliana. Funct Plant Biol 3::217–224

    Article  Google Scholar 

  • Burge C, Karlin S (1997) Prediction of complete gene structures in human genomic DNA. J Mol Biol 268:78–94

    Article  PubMed  CAS  Google Scholar 

  • Cantini C, Iezzoni AF, Lamboy WF, Boritzki M, Struss D (2001) DNA fingerprinting of tetraploid cherry germplasm using simple sequence repeats. J Am Soc Hortic Sci 126:205–209

    CAS  Google Scholar 

  • Cipriani G, Lot G, Huang WG, Marrazzo MT, Peterlunger E, Testolin R (1999) AC/GT and AG/CT microsatellite repeats in peach [Prunus persica (L) Batsch]: isolation, characterisation and cross-species amplification in Prunus. Theor Appl Genet 99:65–72

    Article  CAS  Google Scholar 

  • Dennis FG (1996) A physiological compasion of seed and bud dormancy. In: Lang GA (ed) Plant Dormancy: Physiology, Biochemistry, and Molecular Biology. CAB, New York, pp 47–56

    Google Scholar 

  • Dirlewanger E, Cosson P, Tavaud M, Aranzana MJ, Poizat C, Zanetto A, Arus P, Laigret F (2002) Development of microsatellite markers in peach [Prunus persica (L.) Batsch] and their use in genetic diversity analysis in peach and sweet cherry (Prunus avium L.). Theor Appl Genet 105:127–138

    Article  PubMed  CAS  Google Scholar 

  • Dirlewanger E, Graziano E, Joobeur T, Garriga-Caldere F, Cosson P, Howad W, Arus P (2004) Comparative mapping and marker-assisted selection in Rosaceae fruit crops. Proc Nat Acad Sci USA 101:9891–9896

    Article  PubMed  CAS  Google Scholar 

  • Duarte JM, Cui LY, Wall PK, Zhang Q, Zhang XH, Leebens-Mack J, Ma H, Altman N, dePamphilis CW (2006) Expression pattern shifts following duplication indicative of subfunctionalization and neofunctionalization in regulatory genes of Arabidopsis. Mol Biol Evol 23:469–478

    Article  PubMed  CAS  Google Scholar 

  • Faust M, Erez A, Rowland LJ, Wang SY, Norman HA (1997) Bud dormancy in perennial fruit trees: physiological basis for dormancy induction, maintenance, and release. Hortscience 32:623–629

    Google Scholar 

  • Fuchigami LH, Wisniewski M (1997) Quantifying bud dormancy: physiological approaches. Hortscience 32:618–623

    Google Scholar 

  • Garcia-Maroto F, Carmona MJ, Garrido JA, Vilches-Ferron M, Rodriguez-Ruiz J, Alonso DL (2003) New roles for MADS-box genes in higher plants. Biologia Plantarum 46:321–330

    Article  CAS  Google Scholar 

  • Georgi LL, Wang Y, Yvergniaux D, Ormsbee T, Inigo M, Reighard G, Abbott AG (2002) Construction of a BAC library and its application to the identification of simple sequence repeats in peach Prunus persica (L.) Batsch. Theor Appl Genet 105:1151–1158

    Article  PubMed  CAS  Google Scholar 

  • Gevaudant F, Samson I, Guilliot A, Petel G (1999) An improved method for isolating polyphenol-free RNA from woody plant tissues. J Trace Microprobe Tech 17:445–450

    CAS  Google Scholar 

  • Gevaudant F, Petel G, Guilliot A (2001) Differential expression of four members of the H + -ATPase gene family during dormancy of vegetative buds of peach trees. Planta 212:619–626

    Article  PubMed  CAS  Google Scholar 

  • Gish W, States DJ (1993) Identification of protein coding regions by database similarity search. Nature Genet 3:266–272

    Article  PubMed  CAS  Google Scholar 

  • Horn R (2005) Candidate gene database and transcript map for peach, a model species for fruit trees. Theor Appl Genet 110:1419–1428

    Article  PubMed  Google Scholar 

  • Horvath DP, Anderson JV (2002) A molecular approach to understanding root bud dormancy in leafy spurge. Weed Sci 50:227–231

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Joobeur T, Viruel MA, de Vicente MC, Jauregui B, Ballester J, Dettori MT, Verde I, Truco MJ, Messeguer R, Batlle I, Quarta R, Dirlewanger E, Arus P (1998) Construction of a saturated linkage map for Prunus using an almond x peach F-2 progeny. Theor Appl Genet 97:1034–1041

    Article  CAS  Google Scholar 

  • Jung S, Jesudurai C, Staton M, Du ZD, Ficklin S, Cho IH, Abbott A, Tomkins J, Main D (2004) GDR (Genome Database for Rosaceae): integrated web resources for Rosaceae genomics and genetics research. BMC Bioinformatics 5: Art. No. 130

  • Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J (2005) Repbase update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 110::462–467

    Article  CAS  Google Scholar 

  • Klee H, Estelle M (1991) Molecular genetic approaches to plant hormone biology. Ann Rev Plant Physiol Plant Mol Biol 42:529–551

    Article  CAS  Google Scholar 

  • Koornneef M, Bentsink L, Hilhorst H (2002) Seed dormancy and germination. Curr Opin Plant Biol 5:33–36

    Article  PubMed  CAS  Google Scholar 

  • Kovarík A, Matzke MA, Matzke AJM, Koukalová B (2001) Transposition of IS10 from the host Escherichia coli genome to a plasmid may lead to cloning artefacts. Mol Genet Genom 266:216–222

    Article  Google Scholar 

  • Kozlowski TT, Pallardy SG (1997) In: Physiology of woody plants. 2nd edn. Academic, San Diego

    Google Scholar 

  • Kumar A, Bennetzen JL (1999) Plant retrotransposons. Ann Rev Genet 33:479–532

    Article  PubMed  CAS  Google Scholar 

  • Lawton-Rauh A (2003) Evolutionary dynamics of duplicated genes in plants. Mol Phylogenet Evol 29:396–409

    Article  PubMed  CAS  Google Scholar 

  • Majoros WH, Pertea M, Salzberg SL (2004) TigrScan and GlimmerHMM: two open source ab initio eukaryotic gene-finders. Bioinformatics 20:2878–2879

    Article  PubMed  CAS  Google Scholar 

  • Messina R, Lain O, Marrazzo MT, Cipriani G, Testolin R (2004) New set of microsatellite loci isolated in apricot. Mol Ecol Notes 4:432–434

    Article  CAS  Google Scholar 

  • Michaels SD, Amasino RM (2000) Memories of winter: vernalization and the competence to flower. Plant Cell Environ 23:1145–1153

    Article  Google Scholar 

  • Molmann JA, Berhanu AT, Stormo SK, Ernstsen A, Junttila O, Olsen JE (2003) Metabolism of gibberellin A(19) is under photoperiodic control in Populus, Salix and Betula, but not in daylength-insensitive Populus overexpressing phytochrome A. Physiologia Plantarum 119:278–286

    Article  CAS  Google Scholar 

  • Molmann JA, Asante DKA, Jensen JB, Krane MN, Ernstsen A, Junttila O, Olsen JE (2005) Low night temperature and inhibition of gibberellin biosynthesis override phytochrome action and induce bud set and cold acclimation, but not dormancy in PHYA overexpressors and wild-type of hybrid aspen. Plant Cell Environ 28:1579–1588

    Article  Google Scholar 

  • Moore RC, Purugganan MD (2005) The evolutionary dynamics of plant duplicate genes. Curr Opin Plant Biol 8:122–128

    Article  PubMed  CAS  Google Scholar 

  • Moore RC, Grant SR, Purugganan MD (2005) Molecular population genetics of redundant floral-regulatory genes in Arabidopsis thaliana. Mol Biol Evol 22:91–103

    Article  PubMed  CAS  Google Scholar 

  • Olsen JE (2003) Molecular and Physiological Mechanisms of Bud Dormancy Regulation. In: Tanino KK et al (ed) XXVI International Horticultural Congress-Environmental Stress, Vol 618. ISHS, Leuven, pp 437–453

    Google Scholar 

  • Parenicova L, de Folter S, Kieffer M, Horner DS, Favalli C, Busscher J, Cook HE, Ingram 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 openings to the MADS world. Plant Cell 15:1538–1551

    Article  PubMed  CAS  Google Scholar 

  • Peace CP, Crisosto CH, Gradziel TM (2005) Endopolygalacturonase: a candidate gene for freestone and melting flesh in peach. Mol Breed 16:21–31

    Article  CAS  Google Scholar 

  • Prakash AP, Kumar PP (2002) PkMADS1 is a novel MADS box gene regulating adventitious shoot induction and vegetative shoot development in Paulownia kawakamii. Plant J 29:141–151

    Article  PubMed  CAS  Google Scholar 

  • Rai M (2006) Refinement of the Citrus tristeza virus resistance gene (Ctv) positional map in Poncirus trifoliata and generation of transgenic grapefruit (Citrus paradisi) plant lines with candidate resistance genes in this region. Plant Mol Biol 61:399–414

    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 

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

    Article  PubMed  CAS  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, Vol 1. Kluwer, Dordrecht, pp 89–134

    Google Scholar 

  • Rowland LJ, Ogden EL, Arora R, Lim CC, Lehman JS, Levi A, Panta GR (1999) Use of blueberry to study genetic control of chilling requirement and cold hardiness in woody perennials. Hortscience 34:1185–1191

    Google Scholar 

  • Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics Methods and Protocols: Methods in Molecular Biology. Humana, Totowa, pp 365–386

    Google Scholar 

  • Ruonala R, Rinne PLH, Baghour M, Moritz T, Tuominen H, Kangasjarvi J (2006) Transitions in the functioning of the shoot apical meristem in birch (Betula pendula) involve ethylene. Plant J 46:628–640

    Article  PubMed  CAS  Google Scholar 

  • Salamov AA, Solovyev VV (2000) Ab initio gene finding in Drosophila genomic DNA. Genome Res 10:516–522

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Russell DW (2002) In: Molecular cloning: a laboratory manual Vol 2. 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Scorza R, Sherman WB (1996) Peaches. In: Janick J, Moore JN (eds) Fruit Breeding, Vol 1 Tree and tropical fruits. Wiley, New York, pp 325–440

    Google Scholar 

  • Theissen G, Strater T, Fischer A, Saedler H (1995) Structural characterization, chromosomal localization and phylogenetic evaluation of two pairs of agamous-like MADS-box genes from maize. Gene 156:155–166

    Article  PubMed  CAS  Google Scholar 

  • Thompson MM, Smith DC, Burgess JE (1985) Non-dormant mutants in a temperate tree species, Corylus avellana L. Theor Appl Genet 70:687–692

    Article  Google Scholar 

  • van der Linden CG, Vosman B, Smulders MJM (2002) Cloning and characterization of four apple MADS-box genes isolated from vegetative tissue. J Exp Bot 53:1025–1036

    Article  PubMed  Google Scholar 

  • Van Ooijen JW, Voorrips RE (2001) JoinMap® 3.0, Software for the calculation of genetic linkage maps. Plant Research, Wageningen

    Google Scholar 

  • Vrebalov J, Ruezinsky D, Padmanabhan V, White R, Medrano D, Drake R, Schuch W, Giovannoni J (2002) A MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (Rin) locus. Science 296:343–346

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Georgi LL, Reighard GL, Scorza R, Abbott AG (2002a) Genetic mapping of the evergrowing gene in peach Prunus persica (L.) Batsch. J Heredity 93:352–358

    Article  CAS  Google Scholar 

  • Wang Y, Georgi LL, Zhebentyayeva TN, Reighard GL, Scorza R, Abbott AG (2002b) High-throughput targeted SSR marker development in peach (Prunus persica). Genome 45:319–328

    Article  PubMed  CAS  Google Scholar 

  • Werner DJ, Okie WR (1998) A history and description of the Prunus persica plant introduction collection. Hortscience 33:787–793

    Google Scholar 

  • Yang ZN, Ye XR, Molina J, Roose ML, Mirkov TE (2003) Sequence analysis of a 282-kilobase region surrounding the Citrus tristeza virus resistance gene (Ctv) locus in Poncirus trifoliata L. Raf. Plant Physiology 131:482–492

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Dr. M. Staton for valuable assistance with the bioinformatics and Dr. W.V. Baird for valuable comments on the manuscript.

Author information

Authors and Affiliations

  1. Department of Horticulture, Clemson University, 152 Poole Agricultural Center, Clemson, SC, 29634-0319, USA

    Douglas Gary Bielenberg, Zhigang Li & Gregory Lynn Reighard

  2. Department of Genetics & Biochemistry, Clemson University, Clemson, SC, 29634-0318, USA

    Ying (Eileen) Wang, Tetyana Zhebentyayeva, Shenghua Fan & Albert Glenn Abbott

  3. Appalachian Fruit Research Station, USDA-ARS, Kearneysville, WV, 25430, USA

    Ralph Scorza

Authors
  1. Douglas Gary Bielenberg
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. Ying (Eileen) Wang
    View author publications

    You can also search for this author inPubMed Google Scholar

  3. Zhigang Li
    View author publications

    You can also search for this author inPubMed Google Scholar

  4. Tetyana Zhebentyayeva
    View author publications

    You can also search for this author inPubMed Google Scholar

  5. Shenghua Fan
    View author publications

    You can also search for this author inPubMed Google Scholar

  6. Gregory Lynn Reighard
    View author publications

    You can also search for this author inPubMed Google Scholar

  7. Ralph Scorza
    View author publications

    You can also search for this author inPubMed Google Scholar

  8. Albert Glenn Abbott
    View author publications

    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence to Douglas Gary Bielenberg.

Additional information

Communicated by J. Davis

Financial Source

This work was supported in part by United States Department of Agriculture (USDA) Cooperative State Research, Education, and Extension Service (CSREES) Special Research Grant AC 2004-06140 to GLR and USDA CSREES NRI Grant #2005-35300-15452 to AGA.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bielenberg, D.G., Wang, Y.(., Li, Z. et al. 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 Genetics & Genomes 4, 495–507 (2008). https://doi.org/10.1007/s11295-007-0126-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11295-007-0126-9

Keywords