Skip to main content
Log in

Induction of endodormancy in crown buds of leafy spurge (Euphorbia esula L.) implicates a role for ethylene and cross-talk between photoperiod and temperature

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Leafy spurge is a model for studying well-defined phases of dormancy in underground adventitious buds (UABs) of herbaceous perennial weeds, which is a primary factor facilitating their escape from conventional control measures. A 12-week ramp down in both temperature (27 → 10 °C) and photoperiod (16 → 8 h light) is required to induce a transition from para- to endo-dormancy in UABs of leafy spurge. To evaluate the effects of photoperiod and temperature on molecular networks of UABs during this transition, we compared global transcriptome data-sets obtained from leafy spurge exposed to a ramp down in both temperature and photoperiod (RDtp) versus a ramp down in temperature (RDt) alone. Analysis of data-sets indicated that transcript abundance for genes associated with circadian clock, photoperiodism, flowering, and hormone responses (CCA1, COP1, HY5, MAF3, MAX2) preferentially increased in endodormant UABs. Gene-set enrichment analyses also highlighted metabolic pathways involved in endodormancy induction that were associated with ethylene, auxin, flavonoids, and carbohydrate metabolism; whereas, sub-network enrichment analyses identified hubs (CCA1, CO, FRI, miR172A, EINs, DREBs) of molecular networks associated with carbohydrate metabolism, circadian clock, flowering, and stress and hormone responses. These results helped refine existing models for the transition to endodormancy in UABs of leafy spurge, which strengthened the roles of circadian clock associated genes, DREBs, COP1-HY5, carbohydrate metabolism, and involvement of hormones (ABA, ethylene, and strigolactones). We further examined the effects of ethylene by application of 1-aminocyclopropane-1-carboxylate (ACC) to paradormant plants without a ramp down treatment. New vegetative growth from UABs of ACC-treated plants resulted in a dwarfed phenotype that mimicked the growth response in RDtp-induced endodormant UABs. The results of this study provide new insights into dormancy regulation suggesting a short-photoperiod treatment provides an additive cross-talk effect with temperature signals that may impact ethylene’s effect on AP2/ERF family members.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Adams DO, Yang SF (1979) Ethylene biosynthesis: identification of 1-aminocyclopropane-1-carboxylic acid as an intermediate in the conversion of methionine to ethylene. Proc Natl Acad Sci USA 76:170–174

    Article  PubMed  CAS  Google Scholar 

  • Alabadí D, Blázquez MA (2009) Molecular interactions between light and hormone signaling to control plant growth. Plant Mol Biol 69:409–417

    Article  PubMed  Google Scholar 

  • Anderson JV, Davis DG (2004) Abiotic stress alters transcript profiles and activity of glutathione S-transferase, glutathione peroxidase, and glutathione reductase in Euphorbia esula. Physiol Plant 120:421–433

    Article  PubMed  CAS  Google Scholar 

  • Anderson JV, Horvath DP (2000) Isolation of a cDNA clone (accession # AF220527) encoding a light-harvesting chlorophyll a/b-binding protein (Lhcb1) in underground adventitious buds of leafy spurge (Euphorbia esula L.). PGR00-052. Plant Physiol 122:1457

    Article  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 

  • Anderson JV, Horvath DP, Chao WS, Foley ME, Hernandez A, 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

    Article  CAS  Google Scholar 

  • Anderson JV, Horvath DP, Chao WS, Foley ME (2010) Bud dormancy in perennial plants: a mechanism for survival. In: Lubzens E, Cerda J, Clark M (eds) Dormancy and resistance in harsh environments. Topics in current genetics 21, Chapter 5, Hohmann S (series ed). Springer, Berlin, pp 69–90

    Chapter  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

    Article  PubMed  Google Scholar 

  • Chao WS (2008) Real-time PCR as a tool to study weed biology. Weed Sci 56:290–296

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Chao WS, Doğramacı M, Foley ME, Horvath DP, Anderson JV (2012) Selection and validation of endogenous reference genes for qRT-PCR analysis in leafy spurge (Euphorbia esula). PLoS ONE 7:e42839

    Article  PubMed  CAS  Google Scholar 

  • Christians MJ, Gingerich DJ, Hansen M, Binder BM, Kieber JJ, Vierstra RD (2009) The BTB ubiquitin ligases ETO1, EOL1 and EOL2 act collectively to regulate ethylene biosynthesis in Arabidopsis by controlling type-2 ACC synthase levels. Plant J 57:332–345

    Article  PubMed  CAS  Google Scholar 

  • Destefano-Beltrán L, Knauber D, Huckle L, Suttle JC (2006) Effects of postharvest storage and dormancy status on ABA content, metabolism, and expression of genes involved in ABA biosynthesis and metabolism in potato tuber tissues. Plant Mol Biol 61:607–687

    Article  Google Scholar 

  • Doğramacı M, Horvath DP, Chao WS, Foley ME, Christoffers MJ, Anderson JV (2010) Low temperatures impact dormancy status, flowering competence, and transcript profiles in crown buds of leafy spurge. Plant Mol Biol 73:207–226

    Article  PubMed  Google Scholar 

  • Doğramacı M, Horvath DP, Christoffers MJ, Anderson JV (2011) Dehydration and vernalization treatments identify overlapping molecular networks impacting endodormancy maintenance in leafy spurge crown buds. Funct Integr Genomics 11:611–626

    Article  PubMed  Google Scholar 

  • Dugardeyn J, Vandenbussche F, Van Der Straeten D (2008) To grow or not to grow: what can we learn on ethylene-gibberellins cross-talk by in silico gene expression analysis? J Exp Bot 59:1–16

    Article  PubMed  CAS  Google Scholar 

  • Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95:14863–14868

    Article  PubMed  CAS  Google Scholar 

  • El Kayal W, Navarro M, Marque G, Keller G, Marque C, Teulieres C (2006) Expression profile of CBF-like transcriptional factor genes from Eucalyptus in response to cold. J Exp Bot 57:2455–2469

    Article  PubMed  Google Scholar 

  • Eriksson ME (2000) The role of phytochrome A and gibberellins in growth under long and short day conditions. Studies in hybrid aspen. Swedish University of Agricultural Sciences, Umea (ISSN 1401-6230)

  • Fennell A, Hoover E (1991) Photoperiod influences growth, bud dormancy, and cold-acclimation in Vitis-Labruscana and V-Riparia. J Am Soc Hortic Sci 116:270–273

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Fowler SG, Cook D, Thomashow MF (2005) Low temperature induction of Arabidopsis CBF1, 2, and 3 is gated by the circadian clock. Plant Physiol 137:961–968

    Article  PubMed  CAS  Google Scholar 

  • Gagne JM, Smalle J, Gingerich DJ, Walker JM, Yoo SD, Yanagisawa S, Vierstra RD (2004) Arabidopsis EIN3-binding F-box 1 and 2 form ubiquitin-protein ligases that repress ethylene action and promote growth by directing EIN3 degradation. Proc Natl Acad Sci USA 101:6803–6808

    Article  PubMed  CAS  Google Scholar 

  • Gomez-Roldan V, Fermas S, Brewer PB, Puech-Page’s V, Dun EA, Pillot JP, Letisse F, Matusova R, Danoun S, Portais JC (2008) Strigolactone inhibition of shoot branching. Nature 455:189–194

    Article  PubMed  CAS  Google Scholar 

  • Graham IA (2008) Seed storage oil mobilization. Annu Rev Plant Biol 59:115–142

    Article  PubMed  CAS  Google Scholar 

  • Grossmann K, Hansen H (2001) Ethylene-triggered abscisic acid: a principle in plant growth regulation? Physiol Plant 113:9–14

    Article  CAS  Google Scholar 

  • Hayward A, Stirnberg P, Beveridge CA, Leyser O (2009) Interactions between auxin and strigolactone in shoot branching control. Plant Physiol 151:400–412

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Henriques R, Jang IC, Chua NH (2009) Regulated proteolysis in light-related signaling pathways. Curr Opin Plant Biol 12:49–56

    Article  PubMed  CAS  Google Scholar 

  • Horvath DP (2009) Common mechanisms regulate flowering and dormancy. Plant Sci 177:523–531

    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 

  • 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 9:536

    Article  PubMed  Google Scholar 

  • Hsu CY, Adams JP, Kim H, No K, Ma C, Strauss SH, Drnevich J, Vandervelde L, Ellis JD, Rice BM, Wickett N, Gunter LE, Tuskan GA, Brunner AM, Page GP, Barakat A, Carlson JE, dePamphilis CW, Luthe DS, Yuceer C (2011) FLOWERING LOCUS T duplication coordinates reproductive and vegetative growth in perennial poplar. Proc Natl Acad Sci USA 108:10756–10761

    Article  PubMed  CAS  Google Scholar 

  • Kende H (1993) Ethylene biosynthesis. Annu Rev Plant Physiol Plant Mol Biol 44:283–307

    Article  CAS  Google Scholar 

  • Khan MS (2011) The role of DREB transcription factors in abiotic stress tolerance of plants. Biotechnol Biotechnol Eq 25:2433–2442

    Article  CAS  Google Scholar 

  • Krishnaswamy S, Verma S, Rahman MH, Kav NNV (2011) Functional characterization of four APETALA2-family genes (RAP2.6, RAP2.6L, DREB19 and DREB26) in Arabidopsis. Plant Mol Biol 75:107–127

    Article  PubMed  CAS  Google Scholar 

  • Lang GA, Early JD, Martin GC, Darnell RL (1987) Endo-, para-, and eco-dormancy: physiological terminology and classification for dormancy research. Hort Sci 22:371–377

    Google Scholar 

  • Lazar G, Goodman HM (2006) MAX1, a regulator of the flavonoid pathway, controls vegetative axillary bud outgrowth in Arabidopsis. Proc Natl Acad Sci USA 103:472–476

    Article  PubMed  CAS  Google Scholar 

  • Li C, Junttila O, Ernstsen A, Heino P, Palva ET (2003) Photoperiodic control of growth, cold acclimation and dormancy development in silver birch (Betulapendula) ecotypes. Physiol Plant 117:206–212

    Article  CAS  Google Scholar 

  • Maruyama K, Takeda M, Kidokoro S, Yamada K, Sakuma Y, Urano K, Fujita M, Yoshiwara K, Matsukura S, Morishita Y, Sasaki R, Suzuki H, Saito K, Shibata D, Shinozaki K, Yamaguchi-Shinozaki K (2009) Metabolic pathways involved in cold acclimation identified by integrated analysis of metabolites and transcripts regulated by DREB1A and DREB2A. Plant Physiol 150:1972–1980

    Article  PubMed  CAS  Google Scholar 

  • Mathiason K, He D, Grimplet J, Venkateswari J, Galbraith DW, Or E, Fennell A (2008) Transcript profiling in Vitis riparia during chilling requirement fulfillment reveals coordination of gene expression patterns with optimized bud break. Funct Integr Genomics 9:81–96

    Article  PubMed  Google Scholar 

  • Moon J, Parry G, Estelle M (2004) The ubiquitin-proteasome pathway and plant development. Plant Cell 16:3181–3195

    Article  PubMed  CAS  Google Scholar 

  • Murphy AS, Peer WA, Taiz L (2000) Regulation of auxin transport by aminopeptidases and endogenous flavonoids. Planta 211:315–324

    Article  PubMed  CAS  Google Scholar 

  • Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140:411–432

    Article  PubMed  CAS  Google Scholar 

  • Nakashima K, Ito Y, Yamaguchi-Shinozaki K (2009) Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiol 149:88–95

    Article  PubMed  CAS  Google Scholar 

  • Pandey GK, Grant JJ, Cheong YH, Kim BG, Li L, Luan S (2005) ABR1, and APETALA2-Domain transcription factor that functions as a repressor of ABA response in Arabidopsis. Plant Physiol 139:1185–1193

    Article  PubMed  CAS  Google Scholar 

  • Peer WA, Murphy AS (2007) Flavonoids and auxin transport: modulators or regulators? Trends Plant Sci 12:556–563

    Article  PubMed  CAS  Google Scholar 

  • Peer WA, Blakeslee JJ, Yang H, Murphy AS (2011) Seven things we think we know about auxin transport. Mol Plant 4:487–504

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Puhakainen T, Chunyang L, Boije-Malm M, Kangasjärvi J, Heino P, Plava ET (2004) Short-day potentiation of low temperature-induced gene expression of a C-repeat-binding factor-controlled gene during cold acclimation in silver birch. Plant Physiol 136:4299–4307

    Article  PubMed  CAS  Google Scholar 

  • Qin Q, Kaas Q, Zhang C, Zhou L, Luo X, Zhou M, Sun X, Zhang L, Paek K-Y, Cui Y (2012) The cold awakening of Doritaenopsis ‘Tinny Tender’ orchid flowers: the role of leaves in cold-induced bud dormancy release. J Plant Growth Regul 31:139–155

    Article  CAS  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  PubMed  CAS  Google Scholar 

  • Ratcliffe OJ, Kuminoto 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 FLOWERING LOCUS C-mediated vernalization response: evidence from sugar beet (Beta vulgaris). Genetics 176:295–307

    Article  PubMed  CAS  Google Scholar 

  • Rodrigo MJ, Alquezar B, Zacarias L (2006) Cloning and characterization of two 9-cis-epoxycarotenoid dioxygenase genes, differentially regulated during fruit maturation and under stress conditions, from orange (Citrus sinensis L.Osbeck). J Exp Bot 57:633–643

    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 

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

    Article  PubMed  CAS  Google Scholar 

  • Ruonala R, Rinne PLH, Kangasjärvi 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • SAS Institute Inc (2008) SAS® 9.2, Cary, NC, USA

  • Shockey J, Browse J (2011) Genome-level and biochemical diversity of the acyl-activating enzyme superfamily in plants. Plant J 66:143–160

    Article  PubMed  CAS  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 27:371–377

    Article  CAS  Google Scholar 

  • Stirnberg P, Furner IJ, Leyser HMO (2007) MAX2 participates in an SCF complex which acts locally at the node to suppress shoot branching. Plant J 50:80–94

    Article  PubMed  CAS  Google Scholar 

  • Stougaard RN, Masters RA, Nissen SJ (1994) Leafy spurge (Euphorbia esula) control with imidazolinone and sulfonylurea herbicides. Weed Tech 8:494–498

    CAS  Google Scholar 

  • Suttle JC (1998) Involvement of ethylene in potato microtuber dormancy. Plant Physiol 118:843–848

    Article  PubMed  CAS  Google Scholar 

  • Sweetlove LJ, Beard KFM, Nunes-Nesi A, Fernie AR, Ratcliffe RG (2010) Not just a circle: flux modes in the plant TCA cycle. Trends Plant Sci 15:462–470

    Article  PubMed  CAS  Google Scholar 

  • Tarrant MK, Cole PA (2009) The chemical biology of protein phosphorylation. Annu Rev Biochem 78:797–825

    Article  PubMed  CAS  Google Scholar 

  • Tillet RL, Wheatley MD, Tattersall EAR, Schlauch KA, Cramer GR, Cushman JC (2012) The Vitis vinifera C-repeat binding protein 4 (VvCBF4) transcriptional factor enhances freezing tolerance in wine grape. Plant Biotechnol J 10:105–124

    Article  Google Scholar 

  • Tsuchiya Y, Vidaurre D, Toh S, Hanada A, Nambara E, Kamiya Y, Yamaguchi S, McCourt P (2010) A small-molecule screen identifies new functions for the plant hormone strigolactone. Nat Chem Biol 6:741–749

    Article  PubMed  CAS  Google Scholar 

  • Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T, Takeda-Kamiya N, Magome H, Kamiya Y, Shirasu K, Yoneyama K, Kyozuka J, Yamaguchi S (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455:195–200

    Article  PubMed  CAS  Google Scholar 

  • Wake CMF, Fennell A (2000) Morphological, physiological and dormancy responses of three Vitis genotypes to short photoperiod. Physiol Plant 109:203–210

    Article  CAS  Google Scholar 

  • Wisniewski M, Norelli J, Bassett C, Artlip T, Macarisin D (2011) Ectopic expression of a novel peach (Prunus persica) CBF transcription factor in apple (Malus × domestica) results in short-day induced dormancy and increased cold hardiness. Planta 233:971–983

    Article  PubMed  CAS  Google Scholar 

  • Xu Z-S, Chen M, Li L-C, Ma Y-Z (2011) Functions and Application of the AP2/ERF transcription factor family in crop improvement. J Integr Plant Biol 53:570–585

    Article  PubMed  CAS  Google Scholar 

  • Yang SF, Hoffman NE (1984) Ethylene biosynthesis and its regulation in higher plants. Ann Rev Plant Physiol 35:155–189

    Article  CAS  Google Scholar 

  • Zhang HS, Gavin M, Dahiya A, Postigo AA, Ma D, Luo RX, Harbour JW, Dean DC (2000) Exit from G1 and S phase of the cell cycle is regulated by repressor complexes containing HDAC-Rb-hSWI/SNF and Rb-hSWI/SNF. Cell 101:79–89

    Article  PubMed  CAS  Google Scholar 

  • Zhong S, Shi H, Xue C, Wang L, Xi Y, Li J, Quail PH, Deng XW, Guo H (2012) A molecular framework of light-controlled phytohormone action in Arabidopsis. Curr Biol 22:1–6

    Article  Google Scholar 

Download references

Acknowledgments

The authors wish to thank Brant B. Bigger, Cheryl A. Huckle and Wayne A. Sargent for their technical assistance during this study. The authors also thank Mark West for his help in analyzing data.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to James V. Anderson.

Additional information

Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US Department of Agriculture. USDA is an equal opportunity provider and employer.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Doğramacı, M., Foley, M.E., Chao, W.S. et al. Induction of endodormancy in crown buds of leafy spurge (Euphorbia esula L.) implicates a role for ethylene and cross-talk between photoperiod and temperature. Plant Mol Biol 81, 577–593 (2013). https://doi.org/10.1007/s11103-013-0026-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-013-0026-3

Keywords

Navigation