Skip to main content
SpringerLink
Log in

Dynamics of phytohormone and DNA methylation patterns changes during dormancy induction in strawberry (Fragaria × ananassa Duch.)

  • Original Paper
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Changes in endogenous phytohormone levels, DNA methylation patterns, and expression levels of related genes during induction of dormancy in two strawberry cultivars, Darselect and All Star, were studied under controlled environmental conditions. At 12°C, regardless of day length, potted, runner-derived plants of both cultivars gradually exhibited morphological traits typical of dormancy after treatment for 8 weeks. These morphological changes were accompanied by a synchronous significant decline in indole-3-acetic acid (IAA) level and increases in abscisic acid (ABA) content and global genomic DNA methylation in young leaves. Exposed at 15°C and a short-day photoperiod, the changes in morphology, phytohormone levels and DNA methylation of both cultivars were similar to those observed at 12°C. Slight but non-significant changes in IAA and ABA levels and genomic DNA methylation occurred in young leaves at both 15°C with long days and 18°C with short days. These results indicated that temperature alone was sufficient to induce strawberry to enter the typical dormant phase, and day length had no impact at 12°C. The higher temperature permissible for dormancy induction in strawberry was 15°C, but at this temperature dormancy induction was modified by day length. The expression patterns of FaPIN1, FaNCED1, FaDRM and FaROS1 were coincident with the changes in phytohormone levels and DNA methylation. Although the two tested cultivars have different temporal responses with the different degree of cold tolerance and depth of dormancy, both the endogenous phytohormone and DNA methylation were changed when induced by external environmental factors.

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
Fig. 8
Fig. 9

Similar content being viewed by others

Abbreviations

ABA:

Abscisic acid

IAA:

Indole-3-acetic acid

SD:

Short day

LD:

Long day

DRM:

Domain-rearranged methyltransferase

NCED:

9-cis-Epoxycarotenoid dioxygenase

ROS1:

Repressor of silencing 1

HPLC:

High-performance liquid chromatograph

QRT-PCR:

Quantitative real-time PCR

GAPDH:

Glyceraldehyde-3-phosphate dehydrogenase

References

  • Blakeslee JJ, Peer WA, Murphy AS (2005) Auxin transport. Curr Opin Plant Biol 8:494–500

    Article  PubMed  CAS  Google Scholar 

  • Böhlenius 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. doi:10.1126/science.1126038

    Article  PubMed  Google Scholar 

  • Burn JE, Bagnall DJ, Metzger JD, Dennis ES, Peacock WJ (1993) DNA methylation, vernalization, and the initiation of flowering. Proc Nat Acad Sci USA 90(1):287–291

    Article  PubMed  CAS  Google Scholar 

  • Chan SW, Henderson I, Jacobsen SE (2005) Gardening the genome: DNA methylation in Arabidopsis thaliana. Nat Rev Genet 6:351–360. doi:10.1038/nrg1601

    Article  PubMed  CAS  Google Scholar 

  • Chang LL, Zhang ZH, Han BM, Li H, Dai HY, He P, Tian HZ (2009) Isolation of DNA-methyltransferase genes from strawberry (Fragaria × ananassa Duch.) and their expression in relation to micropropagation. Plant Cell Rep 28:1373–1384. doi:10.1007/s00299-009-0737-8

    Article  PubMed  CAS  Google Scholar 

  • Chinnusamy V, Gong ZZ, Zhu JK (2008) Abscisic acid-mediated epigenetic processes in plant development and stress responses. J Integr Plant Biol l50(10):1187–1195. doi:10.1111/j.1744-7909.2008.00727.x

    Article  Google Scholar 

  • Demeulemeester MAC, Van Stallen N, De Proft MP (1999) Degree of DNA methylation in chicory (Cichorium intybus L.): influence of plant age and vernalization. Plant Sci 142:101–108. doi:10.1016/S0168-9452(99)00010-2

    Article  CAS  Google Scholar 

  • Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15

    Google Scholar 

  • Garner WW, Allard HA (1923) Further studies in photoperiodism, the response of the plant to relative length of day and night. J Agric Res 23:871–920

    Google Scholar 

  • Gocal GFW, Pharis RP, Yeung EC, Pearce D (1991) Changes after decapitation of indole-3-acetic acid and abscisic acid in the larger axillary bud of Phaseolus vulgaris L. cv Tender Green . Plant Physiol 95:344–350. doi:10.1104/pp.95.2.344

    Article  PubMed  CAS  Google Scholar 

  • Gong ZZ, Morales-Ruiz T, Ariza RR, Roldán-Arjona T, David L, Zhu JK (2002) ROS1, a repressor of transcriptional gene silencing in Arabidopsis, encodes a DNA glycosylase/lyase. Cell 3:803–814. doi:10.1016/S0092-8674(02)01133-9

    Google Scholar 

  • Håbjørg A (1978) Photoperiodic ecotypes in Scandinavian trees and shrubs. Meld Nor Landbrukshøgsk 57(33):1–20

    Google Scholar 

  • Halliday KJ, Salter MG, Thingnaes E, Whitelam CG (2003) Phytochrome control of flowering is temperature sensitive and correlates with expression of the floral integrator FT. Plant J 33:875–885. doi:10.1046/j.1365-313X.2003.01674.x

    Article  PubMed  CAS  Google Scholar 

  • Heide OM (2008) Interaction of photoperiod and temperature in the control of growth and dormancy of Prunus species. Sci Hortic 115:309–314. doi:10.1016/j.scienta.2007.10.005

    Article  Google Scholar 

  • Heide OM, Prestrud AK (2005) Low temperature, but not photoperiod, controls growth cessation and dormancy induction and release in apple and pear. Tree Physiol 25:109–114. doi:10.1093/treephys/25.1.109

    PubMed  CAS  Google Scholar 

  • Horvath DP, Chao WS, Suttle JC, Thimmapuram J, Anderson1 JV (2008) Transcriptome analysis identifies novel responses and potential regulatory genes involved in seasonal dormancy transitions of leafy spurge (Euphorbia esula L.). BMC Genomics 9:536. doi:10.1186/1471-2164-9-536

  • Iuchi S, Kobayashi M, Taji T, Naramoto M, Seki M, Kato T, Tabata S, Kakubari Y, Yamaguchi-Shinozaki K, Shinozaki K (2001) Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. Plant J 27:325–333. doi:10.1046/j.1365-313x.2001.01096.x

    Article  PubMed  CAS  Google Scholar 

  • Junttila O (2007) Regulation of annual shoot growth cycle in northern tree species. In: Taulavuori E, Taulavuori K (eds) Physiology of northern plants under changing environment. Res Signpost, Kerala, pp 177–210

    Google Scholar 

  • Lang GA, Early JD, Martin GC, Darnell RL (1987) Endodormancy, paradormancy and ecodormancy: physiological terminology and classification for dormancy research. Hortscience 22:371–377

    Google Scholar 

  • Law RD, Suttle JC (2002) Transient decreases in methylation at 5′-CCGG-3′ sequences in potato (Solanum tuberosum L.) meristem DNA during progression of tubers through dormancy precede the resumption of sprout growth. Plant Mol Biol 51:437–447. doi:10.1023/A:1022002304479

    Article  Google Scholar 

  • Nagar PK (1995) Change in absicisic-acid, phenols and indoleacetic-acid in bulbs of tuberose (polianthes-tuberosa L) during dormancy and spring. Sci Hortic 63(1–2):77–82

    Article  CAS  Google Scholar 

  • Nitsch JP (1957) Photoperiodism in woody plants. Proc Am Soc Hortic Sci 70:526–544. doi:10.1146/annurev.pp.07.060156.001203

  • Olsen JE (2010) Light and temperature sensing and signaling in induction of bud dormancy in woody plants. Plant Mol Biol 73:37–47. doi:10.1007/s11103-010-9620-9

    Article  PubMed  CAS  Google Scholar 

  • Pearce DW, Taylor JS, Robertson JM, Harker KN, Daly EJ (1995) Changes in abscisic acid and indole-3-acetic acid in axillary buds of Elytrigia repens released from apical dominance. Physiol Plant 94:110–116

    Article  CAS  Google Scholar 

  • Robert F, Risser G, PeÂtel G (1999) Photoperiod and temperature effect on growth of strawberry plant (Fragaria × ananassa Duch.): development of a morphological test to assess the dormancy induction. Sci Hortic 82:217–226. doi:10.1016/S0304-4238(99)00054-0

    Article  Google Scholar 

  • Rohde A, Bhalerao R (2007) Dormancy in the perennial context. Trends in Plant Sci 12:217–223. doi:10.1105/tpc.003186

    Article  CAS  Google Scholar 

  • Rohde A, Prinsen E, De Rycke R, Engler G, van Montagu M, Boerjan W (2002) PtABI3 impinges on the growth and differentiation of embryonic leaves during bud set in Poplar. Plant Cell 14:1885–1901. doi:10.1105/tpc.003186

    Google Scholar 

  • Ruttink T, Arend M (2007) A molecular timetable for apical bud formation and dormancy induction in poplar. Plant Cell 19:2370–2390. doi:10.1105/tpc.107.052811

    Article  PubMed  CAS  Google Scholar 

  • Salvatierra A, Pimentel P, Moya-Leon MA, Caligari PDS, Herrera R (2010) Comparison of transcriptional profiles of flavonoid genes and anthocyanin contents during fruit development of two botanical forms of Fragaria chiloensis ssp. chiloensis. Phytochemistry 71:1839–1847. doi:10.1016/j.phytochem.2010.08.005

    Article  PubMed  CAS  Google Scholar 

  • Santamaría ME, Hasbún R, Valera MJ, Meijón M, Valledor L, Rodríguez JL, Toorop PE, Cañal MJ, Rodríguez R (2009) Acetylated H4 histone and genomic DNA methylation patterns during bud set and bud burst in Castanea sativa. J Plant Physiol 166:1360–1369. doi:10.1016/j.jplph.2009.02.014

    Article  PubMed  Google Scholar 

  • Santos F, Teale W, Fleck C, Volpers M, Ruperti B, Palme K (2010) Modelling polar auxin transport in developmental patterning. Plant Biol. 12:s1 3–14. doi:10.1111/j.1438-8677.2010.00388.x

  • Sønsteby A, Heide OM (2006) Dormancy relations and flowering of the strawberry cultivars Korona and Elsanta as influenced by photoperiod and temperature. Sci Hortic 110:57–67. doi:10.1016/j.scienta.2006.06.012

    Article  Google Scholar 

  • Sorce C, Lorenzi R, Ceccarelli N, Ranalli P (2000) Changes in free and conjugated IAA during dormancy and sprouting of potato tubers. Aust J Plant Physiol 27(4):371–377. doi:10.1071/PP99150

    Article  CAS  Google Scholar 

  • Stafstrom JP (1993) Axillary bud development in pea: apical dominance, growth cycles, hormonal regulation and plant architecture. In: Amasino RM (ed) Cellular communication in plants. Plenum Press, New York, pp 75–86

    Google Scholar 

  • Swain SM, Singh DP (2005) Tall tales from sly dwarfs: novel functions of gibberellins in plant development. Trends Plant Sci 10:1360–1385. doi:10.1016/j.tplants.2005.01.007#

    Article  Google Scholar 

  • Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot 95:707–735. doi:10.1093/aob/mci083

    Article  PubMed  CAS  Google Scholar 

  • Yang FX, Jin F, Yan X (2010) Comprehensive evaluation of different strawberry varieties’ tolerance to coldness. J. Fruit Sci 27(3):368–372. doi:1009-9980(2010)03-368-05

    CAS  Google Scholar 

  • Yin KL (1999) The new French strawberry variety “Darselect”. South China Fruits 28(5):41–42

    Google Scholar 

  • Zhang YG, Cheng JH, Han ZH, Xu XF, Li TZ (2005) Comparison of methods for total RNA isolation from Malus xiaojinensis and cDNA amplified using LD-PCR. China Biotechnol Bull 4:50–53 (ISSN:1002-5464.0.2005-04-015)

    Google Scholar 

  • Zhang XZ, Zhao YB, Wang GP, Chang RF, Li CM, Shu HR (2008) Dynamics of endogenous cytokinins during phase trogen change in Malus domestica Borkh. Acta Hort 774:29–33

    CAS  Google Scholar 

Download references

Acknowledgments

This project was supported by the National Key Technologies R&D Program of China (grant nos. 2011BAD12B02 and 2006BAD07B06-04), and the Key Laboratory of the Beijing Municipality of Stress Physiology and Molecular Biology for Fruit Trees.

Author information

Authors and Affiliations

  1. Institute for Horticultural Plants, China Agricultural University, No. 2 Yuanmingyuan West Road, Haidian District, Beijing, 100193, People’s Republic of China

    Li Zhang, Yi Wang, Xinzhong Zhang, Deguo Han, Changpeng Qiu & Zhenhai Han

  2. College of Bioengineering, Henan University of Technology, Zhengzhou, 450001, Henan, People’s Republic of China

    Li Zhang

  3. Department of Entomology, University of Arizona, Tucson, AZ, 85721, USA

    Min Zhang

Authors
  1. Li Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yi Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xinzhong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Min Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Deguo Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Changpeng Qiu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Zhenhai Han
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhenhai Han.

Additional information

Communicated by Q. Zhao.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 114 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, L., Wang, Y., Zhang, X. et al. Dynamics of phytohormone and DNA methylation patterns changes during dormancy induction in strawberry (Fragaria × ananassa Duch.). Plant Cell Rep 31, 155–165 (2012). https://doi.org/10.1007/s00299-011-1149-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-011-1149-0

Keywords

Search

Navigation