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Plant Cell Reports

, Volume 37, Issue 12, pp 1693–1705 | Cite as

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

  • MinJi Li
  • Qinping Wei
  • Yuansong Xiao
  • FuTian Peng
Original Article

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.

Keywords

Apical dominance Cytokinin Auxin Strigolactone Isopentenyltransferase Peach 

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

Notes

Funding

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

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

299_2018_2343_MOESM1_ESM.docx (631 kb)
Supplementary material 1 (DOCX 631 KB)

References

  1. Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827CrossRefGoogle Scholar
  2. Arús P, Verde I, Sosinski B, Zhebentyayeva T, Abbott AG (2012) The peach genome. Tree Genet Genom 8:531–547CrossRefGoogle Scholar
  3. 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):545–556CrossRefGoogle Scholar
  4. 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 194:439–442CrossRefGoogle Scholar
  5. Bangerth F, Li CJ, Gruber J (2000) Mutual interaction of auxin and CKs in regulating correlative dominance. Plant Growth Regul 32:205–217CrossRefGoogle Scholar
  6. Bennett T, Leyser O (2014) Strigolactone signalling: standing on the shoulders of DWARFs. Curr Opin Plant Biol 22:7–13CrossRefGoogle Scholar
  7. 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 16:553–563CrossRefGoogle Scholar
  8. Beveridge CA (2000) Long-distance signaling and a mutational analysis of branching in pea. Plant Growth Regul 32:193–203CrossRefGoogle Scholar
  9. Beveridge CA (2006) Axillary bud outgrowth: sending a message. Curr Opin Plant Biol 9:35–40CrossRefGoogle Scholar
  10. 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 115:1251–1258CrossRefGoogle Scholar
  11. Blackwell JR, Horgan R (1994) Cytokinin biosynthesis by extracts of zea mays. Phytochemistry 35(2):339–342CrossRefGoogle Scholar
  12. 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 14:1232–1238CrossRefGoogle Scholar
  13. Brewer PB, Beveridge CA (2009) Strigolactone acts downstream of auxin to regulate bud outgrowth in pea and Arabidopsis. Plant Physiol 150:482–493CrossRefGoogle Scholar
  14. Cline MG (1991) Apical dominance. Bot Rev 57:318–358CrossRefGoogle Scholar
  15. 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 950:21–29CrossRefGoogle Scholar
  16. 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 49:555–562Google Scholar
  17. 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 426:147–153CrossRefGoogle Scholar
  18. Golovko A, Sitbon F, Tillberg E, Nicander B (2002) Identification of a tRNA isopentenyl-transferase gene from Arabidopsis thaliana. Plant Mol Biol 49:161–169CrossRefGoogle Scholar
  19. Harrison MA, Kaufman PB (1982) Does ethylene play a role in the release of lateral buds (tillers) from apical dominance in oats. Plant Physiol 70:811–814CrossRefGoogle Scholar
  20. Hayward A, Stirnber GP, Beveridge CA et al (2009) Interactions between auxin and strigolactone in shoot branching control. Plant Physiol 151:400–412CrossRefGoogle Scholar
  21. 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):885–885CrossRefGoogle Scholar
  22. Kakimoto T (2001) Identification of plant cytokinin biosynthetic enzymes as dimethylallyl diphosphate: ATP/ADP isopentenyltransferases. Plant Cell Physiol 42:677–685CrossRefGoogle Scholar
  23. Langer RHM, Prasad PC, Laude HM (1973) Effects of kinetin in tiller bud elongation in wheat (Triticum aestivum L). Ann Bot 37:565–571CrossRefGoogle Scholar
  24. 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 426:29–32CrossRefGoogle Scholar
  25. Leyser O (2003) Regulation of shoot branching by auxin. Trends Plant Sci 8:541–545CrossRefGoogle Scholar
  26. Leyser O (2008) Strigolactones and shoot branching: a new trick for a young dog. Dev Cell 15(3):337–338CrossRefGoogle Scholar
  27. 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):169–174Google Scholar
  28. 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):402–408CrossRefGoogle Scholar
  29. 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 1:403–413CrossRefGoogle Scholar
  30. 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):547–553Google Scholar
  31. Mouchel CF, Leyser O (2007) Novel phytohormones involved in longrange signaling. Curr Opin Plant Biol 10:473–476CrossRefGoogle Scholar
  32. Muller D, Leyser O (2011) Auxin, cytokinin and the control of shoot branching. Ann Bot 107:1203–1212CrossRefGoogle Scholar
  33. 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 3:677–684CrossRefGoogle Scholar
  34. Ongaro V, Leyser O (2008) Hormonal control of shoots branching. J Exp Bot 59:67–74CrossRefGoogle Scholar
  35. Panigrahi BM, Audus LJ (1966) Apical dominance in Vicia faba. Ann Bot 30:457–473CrossRefGoogle Scholar
  36. Paponov IA, Teale WD, Trebar M, Blilou I, Palme K (2005) The PIN auxin efflux facilitarors: evolutionary and functional perspectives. Trends Plant Sci 10:170–177CrossRefGoogle Scholar
  37. 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):57–68CrossRefGoogle Scholar
  38. 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 5:438–446CrossRefGoogle Scholar
  39. Sachs T, Thimann KV (1964) Release of lateral buds from apical dominance. Nature 201:939–940CrossRefGoogle Scholar
  40. Sachs T, Thimann V (1967) The role of auxins and cytokinins in the release of buds from dominance. Am J Bot 54:136–144CrossRefGoogle Scholar
  41. 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 65:2439–2446CrossRefGoogle Scholar
  42. Shimizu-Sato S, Mori H (2001) Control of outgrowth and dormancy in axillary buds. Plant Physiol 127:1405–1413CrossRefGoogle Scholar
  43. 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):e1001474CrossRefGoogle Scholar
  44. 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 17:746–759CrossRefGoogle Scholar
  45. 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):78CrossRefGoogle Scholar
  46. Takei K, Sakakibara H, Sugiyama T (2001) Identification of genes encoding adenylate isopentenyltransferase, a cytokinin biosynthesis enzyme, in Arabidopsis thaliana. J Biol Chem 276:26405–26410CrossRefGoogle Scholar
  47. 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 53:971–977CrossRefGoogle Scholar
  48. 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 45:1028–1036CrossRefGoogle Scholar
  49. 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 19:714–716CrossRefGoogle Scholar
  50. 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 202:271–276CrossRefGoogle Scholar
  51. 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 455:195–200CrossRefGoogle Scholar
  52. 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 45:487–494CrossRefGoogle Scholar
  53. 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 163:591–600CrossRefGoogle Scholar
  54. Ward SP, Leyser O (2004) Shoot branching. Curr Opin Plant Biol 7:73–78CrossRefGoogle Scholar
  55. 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:e201643806Google Scholar
  56. 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 29:797–808CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • MinJi Li
    • 1
  • Qinping Wei
    • 1
  • Yuansong Xiao
    • 2
  • FuTian Peng
    • 2
  1. 1.Beijing Academy of Forestry and Pomology SciencesBeijing Academy of Agriculture and Forestry Sciences/Key Laboratory of Urban Agriculture (North China), Ministry of AgricultureBeijingPeople’s Republic of China
  2. 2.College of Horticulture Science and EngineeringShandong Agricultural UniversityTai’anPeople’s Republic of China

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