Skip to main content

Advertisement

Log in

The effect of auxin and strigolactone on ATP/ADP isopentenyltransferase expression and the regulation of apical dominance in peach

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

Abstract

Key message

We confirmed the roles of auxin, CK, and strigolactones in apical dominance in peach and established a model of plant hormonal control of apical dominance in peach.

Abstract

Auxin, cytokinin, and strigolactone play important roles in apical dominance. In this study, we analyzed the effect of auxin and strigolactone on the expression of ATP/ADP isopentenyltransferase (IPT) genes (key cytokinin biosynthesis genes) and the regulation of apical dominance in peach. After decapitation, the expression levels of PpIPT1, PpIPT3, and PpIPT5a in nodal stems sharply increased. This observation is consistent with the changes in tZ-type and iP-type cytokinin levels in nodal stems and axillary buds observed after treatment; these changes are required to promote the outgrowth of axillary buds in peach. These results suggest that ATP/ADP PpIPT genes in nodal stems are key genes for cytokinin biosynthesis, as they promote the outgrowth of axillary buds. We also found that auxin and strigolactone inhibited the outgrowth of axillary buds. After decapitation, IAA treatment inhibited the expression of ATP/ADP PpIPTs in nodal stems to impede the increase in cytokinin levels. By contrast, after GR24 (GR24 strigolactone) treatment, the expression of ATP/ADP IPT genes and cytokinin levels still increased markedly, but the rate of increase in gene expression was markedly lower than that observed after decapitation in the absence of IAA (indole-3-acetic acid) treatment. In addition, GR24 inhibited basipetal auxin transport at the nodes (by limiting the expression of PpPIN1a in nodal stems), thereby inhibiting ATP/ADP PpIPT expression in nodal stems. Therefore, strigolactone inhibits the outgrowth of axillary buds in peach only when terminal buds are present.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

GR24:

(3aR*,8bS*,E)-3-(((R*)-4-methyl-5-oxo-2,5-dihydrofuran-2-yloxy)methylene)-3,3a,4,8b-tetrahydro-2H-indeno[1,2-b]furan-2-one, a synthetic strigolactone

iP:

Isopentenyladenine

iPR:

iP riboside

IAA:

Indole-3-acetic acid

SL:

Strigolactone

PpIPT:

Peach gene adenosine phosphate isopentenyltransferase

tZ:

Trans-zeatin

tZR:

Trans-zeatin riboside

References

  • Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827

    Article  CAS  Google Scholar 

  • Arús P, Verde I, Sosinski B, Zhebentyayeva T, Abbott AG (2012) The peach genome. Tree Genet Genom 8:531–547

    Article  Google Scholar 

  • Bacaicoa E, Mora V, Ángel María Z (2011) Auxin: a major player in the shoot-to-root regulation of root Fe-stress physiological responses to Fe deficiency in cucumber plants. Plant Physiol Biochem Ppb 49(5):545–556

    Article  CAS  Google Scholar 

  • Bangerth F (1994) Response of cytokinin concentration in the xylem exudate of bean (Phaseolus vulgaris L.) plants to decapitation and auxin treatment, and relationship to apical dominance. Planta 194:439–442

    Article  CAS  Google Scholar 

  • Bangerth F, Li CJ, Gruber J (2000) Mutual interaction of auxin and CKs in regulating correlative dominance. Plant Growth Regul 32:205–217

    Article  CAS  Google Scholar 

  • Bennett T, Leyser O (2014) Strigolactone signalling: standing on the shoulders of DWARFs. Curr Opin Plant Biol 22:7–13

    Article  CAS  Google Scholar 

  • Bennett T, Sieberer T, Willett B, Booker J, Luschnig C, Leyser O (2006) The Arabidopsis MAX pathway controls shoot branching by regulating auxin transport. Curr Biol 16:553–563

    Article  CAS  Google Scholar 

  • Beveridge CA (2000) Long-distance signaling and a mutational analysis of branching in pea. Plant Growth Regul 32:193–203

    Article  CAS  Google Scholar 

  • Beveridge CA (2006) Axillary bud outgrowth: sending a message. Curr Opin Plant Biol 9:35–40

    Article  CAS  Google Scholar 

  • Beveridge CA, Symons GM, Murfet IC, Ross JJ, Rameau C (1997) The rms1 mutant of pea has elevated indole-3-acetic acid levels and reduced root-sap zeatin riboside content but increased branching controlled by graft-transmissible signal(s). Plant Physiol 115:1251–1258

    Article  CAS  Google Scholar 

  • Blackwell JR, Horgan R (1994) Cytokinin biosynthesis by extracts of zea mays. Phytochemistry 35(2):339–342

    Article  CAS  Google Scholar 

  • Booker J, Auldridge M, Wills S, McCarty D, Klee H, Leyser O (2004) MAX3/CCD7 is a carotenoid cleavage dioxygenase required for the synthesis of a novel plant signaling molecule. Curr Biol 14:1232–1238

    Article  CAS  Google Scholar 

  • Brewer PB, Beveridge CA (2009) Strigolactone acts downstream of auxin to regulate bud outgrowth in pea and Arabidopsis. Plant Physiol 150:482–493

    Article  CAS  Google Scholar 

  • Cline MG (1991) Apical dominance. Bot Rev 57:318–358

    Article  Google Scholar 

  • Dobrev PI, Kaminek M (2002) Fast and efficient separation of cytokinins from auxin and abscisic acid and their purification using mixed-mode solid-phase extraction. J Chromatogr A 950:21–29

    Article  Google Scholar 

  • Emery RJN, Longnecker NE, Atkins CA (1998) Branch development in Lupinus angustifolius L. II. Relationship with endogenous ABA, IAA and cytokinins in axillary and main stem buds. J Exp Bot 49:555–562

    CAS  Google Scholar 

  • Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offerings R, Jurgens G (2003) Efflux-dependent auxin gradients establish the apicalbasal axis of Arabidopsis. Nature 426:147–153

    Article  CAS  Google Scholar 

  • Golovko A, Sitbon F, Tillberg E, Nicander B (2002) Identification of a tRNA isopentenyl-transferase gene from Arabidopsis thaliana. Plant Mol Biol 49:161–169

    Article  CAS  Google Scholar 

  • Harrison MA, Kaufman PB (1982) Does ethylene play a role in the release of lateral buds (tillers) from apical dominance in oats. Plant Physiol 70:811–814

    Article  CAS  Google Scholar 

  • Hayward A, Stirnber GP, Beveridge CA et al (2009) Interactions between auxin and strigolactone in shoot branching control. Plant Physiol 151:400–412

    Article  CAS  Google Scholar 

  • Immanen J, Nieminen K, Silva HD et al (2013) Characterization of cytokinin signaling and homeostasis gene families in two hardwood tree species: Populus trichocarpa, and Prunus persica. BMC Genom 14(1):885–885

    Article  Google Scholar 

  • Kakimoto T (2001) Identification of plant cytokinin biosynthetic enzymes as dimethylallyl diphosphate: ATP/ADP isopentenyltransferases. Plant Cell Physiol 42:677–685

    Article  CAS  Google Scholar 

  • Langer RHM, Prasad PC, Laude HM (1973) Effects of kinetin in tiller bud elongation in wheat (Triticum aestivum L). Ann Bot 37:565–571

    Article  CAS  Google Scholar 

  • Laureys F, Dewitte W, Witters E, Van Montagu M, Inze D, Van Onckelen H (1998) Zeatin is indispensable for the G2-M transition in tobacco BY-2 cells. FEBS Lett 426:29–32

    Article  CAS  Google Scholar 

  • Leyser O (2003) Regulation of shoot branching by auxin. Trends Plant Sci 8:541–545

    Article  CAS  Google Scholar 

  • Leyser O (2008) Strigolactones and shoot branching: a new trick for a young dog. Dev Cell 15(3):337–338

    Article  CAS  Google Scholar 

  • Liu Y, Xu JX, Ding YF, Wang QS, Li GH, Wang SH (2011) Auxin inhibits the outgrowth of tiller buds in rice (Oryza sativa L.) by downregulating OsIPT expression and cytokinin biosynthesis in nodes. Aust J Crop Sci 5(2):169–174

    CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the \(2^{- \Delta \Delta \text{C}_\text{T}}\) method. Methods 25(4):402–408

    Article  CAS  Google Scholar 

  • Medford JI, Horgan R, EI-Sawi Z, Klee HJ (1989) Alterations of endogenous cytokinins in transgenic plants using a chimeric isopentenyl transferase gene. Plant Cell 1:403–413

    Article  CAS  Google Scholar 

  • Miguel LC, Longnecker NE, Ma Q, Osborne L, Atkins CA (1998) Branch development in Lupinus angustifolius L. I. Not all branches have the same potential growth rate. J Exp Bot 49(320):547–553

    CAS  Google Scholar 

  • Mouchel CF, Leyser O (2007) Novel phytohormones involved in longrange signaling. Curr Opin Plant Biol 10:473–476

    Article  CAS  Google Scholar 

  • Muller D, Leyser O (2011) Auxin, cytokinin and the control of shoot branching. Ann Bot 107:1203–1212

    Article  Google Scholar 

  • Okada K, Ueda J, Komaki MK, Bell CJ, Shimura Y (1991) Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation. Plant Cell 3:677–684

    Article  CAS  Google Scholar 

  • Ongaro V, Leyser O (2008) Hormonal control of shoots branching. J Exp Bot 59:67–74

    Article  CAS  Google Scholar 

  • Panigrahi BM, Audus LJ (1966) Apical dominance in Vicia faba. Ann Bot 30:457–473

    Article  Google Scholar 

  • Paponov IA, Teale WD, Trebar M, Blilou I, Palme K (2005) The PIN auxin efflux facilitarors: evolutionary and functional perspectives. Trends Plant Sci 10:170–177

    Article  CAS  Google Scholar 

  • Pilkington SM, Montefiori M, Galer AL, Neil Emery RJ, Allan AC, Jameson PE (2013) Endogenous cytokinin in developing kiwifruit is implicated in maintaining fruit flesh chlorophyll levels. Ann Bot 112(1):57–68

    Article  CAS  Google Scholar 

  • Romano CP, Hein MB, Klee HJ (1991) Inactivation of auxin in tobacco transformed with the indoleacetic-acid lysine synthetase gene of Pseudomonas savastanoi. Genes Dev 5:438–446

    Article  CAS  Google Scholar 

  • Sachs T, Thimann KV (1964) Release of lateral buds from apical dominance. Nature 201:939–940

    Article  Google Scholar 

  • Sachs T, Thimann V (1967) The role of auxins and cytokinins in the release of buds from dominance. Am J Bot 54:136–144

    Article  CAS  Google Scholar 

  • Sakano Y, Okada Y, Matsunaga A, Suwama T, Kaneko T, Ito K, Noguchi H, Abe I (2004) Molecular cloning, expression, and characterization of adenylate isopentyltransferase from hop (Humulus lupulus L.). Phytochemistry 65:2439–2446

    Article  CAS  Google Scholar 

  • Shimizu-Sato S, Mori H (2001) Control of outgrowth and dormancy in axillary buds. Plant Physiol 127:1405–1413

    Article  CAS  Google Scholar 

  • Shinohara N, Taylor C, Leyser O (2013) Strigolactone can promote or inhibit shoot branching by triggering rapid depletion of the auxin efflux protein PIN1 from the plasma membrane. PLoS Biol 11(1):e1001474

    Article  CAS  Google Scholar 

  • Snowden KC, Simkin AJ, Janssen BJ, Templeton KR, Loucas HM, Simons JL, Karunairetnam S, Gleave AP, Clark DG, Klee HJ (2005) The decreased apical dominance 1/petunia hybrida carotenoid cleavage dioxygenase8 gene affects branch production and plays a role in leaf senescence, root growth, and flower development. Plant Cell 17:746–759

    Article  CAS  Google Scholar 

  • Song J, Jiang L, Paula J (2012) Co-ordinate regulation of cytokinin gene family members during flag leaf and reproductive development in wheat. BMC Plant Biol 12(1):78

    Article  CAS  Google Scholar 

  • Takei K, Sakakibara H, Sugiyama T (2001) Identification of genes encoding adenylate isopentenyltransferase, a cytokinin biosynthesis enzyme, in Arabidopsis thaliana. J Biol Chem 276:26405–26410

    Article  CAS  Google Scholar 

  • Takei K, Takahashi T, Sugiyama T, Yamaya T, Sakakibara H (2002) Multiple routes communicating nitrogen availability from roots to shoots: a signal transduction pathway mediated by cytokinin. J Exp Bot 53:971–977

    Article  CAS  Google Scholar 

  • Tanaka M, Takei K, Kojima MH, Sakakibara H, Mori H (2006) Auxin controls local cytokinin biosynthesis in the nodal stem in apical dominance. Plant J 45:1028–1036

    Article  CAS  Google Scholar 

  • Thimann KV, Skoog F (1933) Studies on the growth hormone of plants. III. The inhibiting action of the growth substance on bud development. Proc Natl Acad Sci USA 19:714–716

    Article  CAS  Google Scholar 

  • Turnbull CGN, Myriam AA, Raymond ICD, Morris DSE (1997) Rapid increases in cytokinin concentration in lateral buds of chickpea (Cicer arietinum L.) during release of apical dominance. Planta 202:271–276

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Verde I, Abbott AG, Scalabrin S, Jung S, Shu S, Marroni F, Zhebentyayeva T, Dettori MT, Grimwood J, Cattonaro F, Zuccolo A, Rossini L, Jenkins J, Vendramin E, Meisel LA, Decroocq V, Sosinski B, Prochnik S, Mitros T, Policriti A, Cipriani G, Dondini L, Ficklin S, Goodstein DM, Xuan P, Fabbro CD, Aramini V, Copetti D, Gonzalez S, Horner DS et al (2013) The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nat Genet 45:487–494

    Article  CAS  Google Scholar 

  • Wang GY, Romheld V, Li CJ, Bangerth F (2006) Involvement of auxin and CKs in boron deficiency induced changes in apical dominance of pea plants (Pisum sativum L.). J Plant Physiol 163:591–600

    Article  CAS  Google Scholar 

  • Ward SP, Leyser O (2004) Shoot branching. Curr Opin Plant Biol 7:73–78

    Article  CAS  Google Scholar 

  • Yang ZB, Liu G, Liu J, Zhang B, Meng W, Müller B, Hayashi KI, Zhang X, Zhao Z, De Smet I, Ding Z (2017) Synergistic action of auxin and cytokinin mediates aluminum-induced root growth inhibition in Arabidopsis. EMBO Rep 18:e201643806

    Google Scholar 

  • Zubko E, Adams CJ, Macha´e´kova´ I, Malbeck J, Scollan C, Meyer P (2002) Activation tagging identifies a gene from Petunia hybrida responsible for the production of active cytokinins in plants. Plant J 29:797–808

    Article  CAS  Google Scholar 

Download references

Funding

This work was supported by the China Agriculture Research System [CARS-31-3-03].

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to FuTian Peng.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Hiroyasu Ebinuma.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 631 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, M., Wei, Q., Xiao, Y. et al. The effect of auxin and strigolactone on ATP/ADP isopentenyltransferase expression and the regulation of apical dominance in peach. Plant Cell Rep 37, 1693–1705 (2018). https://doi.org/10.1007/s00299-018-2343-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-018-2343-0

Keywords

Navigation