Journal of Plant Growth Regulation

, Volume 38, Issue 1, pp 132–145 | Cite as

Correlative Inhibition Between Branches in Two-Branched Pea Seedlings is Cultivar-Dependent

  • Andrey A. KotovEmail author
  • Liudmila M. Kotova


The contributions of strigolactones (SLs), cytokinins (CKs), and indole-3-acetic acid (IAA) to the regulation of correlative inhibition (CI) in two-branched 10-day-old (2-B) pea seedlings were studied in different cultivars in comparison with single-shoot seedlings (1-B). The first group of cultivars (Adagumsky and Torsdag) was characterized by a tall phenotype, strong apical dominance, and CI between branches, with IAA export activity (IEA) being almost 1.5–2 times lower in the shoots of 2-B plants than in 1-B plants. Branching IAA-response (rms2-1) and SL response/deficient (rms4-1/rms1) mutants of Torsdag also displayed CI at the level of the shoot IEA. In Torsdag, vascular supply of 6-benzylaminopurine in the hypocotyl, which led to an increase in IEA, equalized IEA differences between the 2-B and 1-B shoots, thus overcoming CI. In 1-B plants of these cultivars, the levels of xylem-CK were three-fold higher than that of 2-B plants, suggesting a key role for xylem-CK in establishing CI. The previously proposed dynamic model, where IAA and CK interact in interlocking feedback loops, can account for the regulation of CI in these cultivars. By contrast, both the growth and IEA of shoots in the second group of cultivars (Térèse and Porta), which displayed a dwarf phenotype and weakened apical dominance, were similar between 2-B and 1-B plants. Porta had an increased shoot IEA, but low xylem-CK levels as compared to Adagumsky, with both cultivars showing a similar response to CK. Therefore, we assume that in the second cultivar group, the shoot IAA synthesis/export is probably independent from xylem-CK, and further studies are needed to find a factor responsible for loss of CI in these cultivars.


Pisum sativum Correlative inhibition Cytokinins Indole-3-acetic acid Strigolactones Xylem sap 



We thank Dr. Catherine Rameau (INRA Centre de Versailles-Grignon, France) very much for providing the seeds of pea wild-type cultivars and the rms mutants, Prof. Dr. B. Zwanenburg (Radboud University Nijmegen, The Netherlands) for the kind gift of the synthetic strigolactone GR24.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Arumingtyas EL, Floyd FS, Gregory MJ, Murfet IC (1992) Branching in Pisum: inheritance and allelism tests with 17 ramosus mutants. Pisum Genet 24:7–31Google Scholar
  2. 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
  3. Bangerth F, Li C-J, Gruber J (2000) Mutual interaction of auxin and cytokinins in regulating correlative dominance. Plant Growth Regul 32:205–217CrossRefGoogle Scholar
  4. Bayer E, Smith R, Mandel T, Nakayama N, Sauer M, Prusinkiewicz P, Kuhlemeier C (2009) Integration of transport-based models for phyllotaxis and midvein formation. Genes Dev 23:373–384CrossRefGoogle Scholar
  5. 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
  6. Bennett T, Hines G, Leyser O (2014) Canalization: what the flux? Trends Genet 30:41–48CrossRefGoogle Scholar
  7. Beveridge CA (2006) Axillary bud outgrowth: sending a message. Curr Opin Plant Biol 9:35–40CrossRefGoogle Scholar
  8. Beveridge CA, Ross JJ, Murfet IC (1994) Branching mutant rms-2 in Pisum sativum. Grafting studies and endogenous indole-3-acetic acid levels. Plant Physiol 104:953–959CrossRefGoogle Scholar
  9. Beveridge CA, Ross JJ, Murfet IC (1996) Branching in pea. Action of genes Rms3 and Rms4. Plant Physiol 110:859–865CrossRefGoogle Scholar
  10. Beveridge CA, Murfet IC, Kerhoas L, Sotta B, Miginiac E, Rameau C (1997) The shoot controls zeatin riboside export from pea roots: evidence from the branching mutant rms4. Plant J 11:339–345CrossRefGoogle Scholar
  11. Brenner WG, Schmülling T (2012) Transcript profiling of cytokinin action in Arabidopsis roots and shoots discovers largely similar but also organspecific responses. BMC Plant Biol 12:112CrossRefGoogle Scholar
  12. Brugiere N, Jiao SP, Hantke S, Zinselmeier C, Roessler JA, Niu XM, Jones RJ, Habben JE (2003) Cytokinin oxidase gene expression in maize is localized to the vasculature, and is induced by cytokinins, abscisic acid, and abiotic stress. Plant Physiol 132:1228–1240CrossRefGoogle Scholar
  13. Cline MG (1991) Apical dominance. Bot Rev 57:318–358CrossRefGoogle Scholar
  14. Crawford S, Shinohara N, Sieberer T, Williamson L, George G, Hepworth J, Müller D, Domagalska MA, Leyser O (2010) Strigolactones enhance competition between shoot branches by dampening auxin transport. Development 137:2905–2913CrossRefGoogle Scholar
  15. Dodd IC, Ngo C, Turnbull CGH, Beveridge C (2004) Effect of nitrogen supply on xylem delivery, transpiration and leaf expansion of pea genotypes differing in xylem-cytokinin concentration. Funct Plant Biol 31:903–911CrossRefGoogle Scholar
  16. Dun EA, de Saint Germain A, Rameau C, Beveridge CA (2012) Antagonistic action of strigolactone and cytokinin in bud outgrowth control. Plant Physiol 158:487–498CrossRefGoogle Scholar
  17. Dun EA, de Saint Germain A, Rameau C, Beveridge CA (2013) Dynamics of strigolactone function and shoot branching responses in Pisum sativum. Mol Plant 6:128–140CrossRefGoogle Scholar
  18. Foo E, Bullier E, Goussot M, Foucher F, Rameau C, Beveridge CA (2005) The branching gene RAMOSUS1 mediates interactions among two novel signals and auxin in pea. Plant Cell 17:464–474CrossRefGoogle Scholar
  19. Foo E, Morris SE, Parmenter K, Young N, Wang H, Jones A, Rameau C, Turnbull CG, Beveridge CA (2007) Feedback regulation of xylem cytokinin content is conserved in pea and Arabidopsis. Plant Physiol 143:1418–1428CrossRefGoogle Scholar
  20. Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pagés V, Dun EA, Pillot J-P, Letisse F, Matusova R, Danoun S, Portais J-C, Bouwmeester H, Bécard G, Beveridge CA, Rameau C, Rochange SF (2008) Strigolactone inhibition of shoot branching. Nature 455:189–194CrossRefGoogle Scholar
  21. Hayakawa Y, Tachikawa M, Mochizuki A (2014) Mathematical study for the mechanism of vascular and spot patterns by auxin and pin dynamics in plant development. J Theor Biol 365:12–22CrossRefGoogle Scholar
  22. Hayward A, Stirnberg P, Beveridge C, Leyser O (2009) Interactions between auxin and strigolactone in shoot branching control. Plant Physiol 151:1–13CrossRefGoogle Scholar
  23. Johnson X, Brcich T, Dun EA, Goussot M, Haurogne K, Beveridge CA, Rameau C (2006) Branching genes are conserved across species. Genes controlling a novel signal in pea are coregulated by other long-distance signals. Plant Physiol 142:1014–1026CrossRefGoogle Scholar
  24. Jones B, Gunneras SA, Petersson SV, Tarkowski P, Graham N, May S, Dolezal K, Sandberg G, Ljung K (2010) Cytokinin regulation of auxin synthesis in Arabidopsis involves a homeostatic feedback loop regulated via auxin and cytokinin signal transduction. Plant Cell 22:2956–2969CrossRefGoogle Scholar
  25. Kalousek P, Buchtová D, Balla J, Reinoehl V, Prochazka S (2010) Cytokinin and polar transport of auxin in axillary pea buds. Acta Univ Agric et Silviculturae Mendelianae Brunensis 58:79–88CrossRefGoogle Scholar
  26. Kieber JJ, Schaller GE (2014) Cytokinins. Arabidopsis Book 12:e0168. CrossRefGoogle Scholar
  27. Kolachevskaya OO, Sergeeva LI, Floková K, Getman IA, Lomin SN, Alekseeva VV, Rukavtsova EB, Buryanov YI, Romanov GA (2017) Auxin synthesis gene tms1 driven by tuber-specific promoter alters hormonal status of transgenic potato plants and their responses to exogenous phytohormones. Plant Cell Rep 36:419–435CrossRefGoogle Scholar
  28. Kotov AA, Kotova LM (2000) The contents of auxins and cytokinins in pea internodes as related to the growth of lateral buds. J Plant Physiol 156:438–448CrossRefGoogle Scholar
  29. Kotov AA, Kotova LM (2015) Role of acropetal water transport in regulation of cytokinin levels in stems of pea seedlings. Russ J Plant Physiol 62:390–400CrossRefGoogle Scholar
  30. Kotov AA, Kotova LM (2018) Auxin–cytokinin interactions in the regulation of correlative inhibition in two-branched pea seedlings. J Exp Bot 69:2967–2978CrossRefGoogle Scholar
  31. Kotova LM, Kotov AA, Kara AN (2004) Changes in phytohormone status in stems and roots after decapitation of pea seedlings. Russ J Plant Physiol 51:107–111CrossRefGoogle Scholar
  32. Kramer EM (2009) Auxin-regulated cell polarity: an inside job? Trends Plant Sci 14:242–247CrossRefGoogle Scholar
  33. Li C-H, Bangerth F (1992) The possible role of cytokinines, ethylene and indoleacetic acid in apical dominance. In: Karssen CM, van Loon LC, Vreugdenhil D (eds) Progress in plant growth regulation. Kluwer Academic Publishers, Dordrecht, pp 431–436CrossRefGoogle Scholar
  34. Li C-J, Bangerth F (1999) Autoinhibition of indoleacetic acid transport in the shoot of two-branched pea (Pisum sativum) plants and its relationship to correlative dominance. Physiol Plant 106:415–420CrossRefGoogle Scholar
  35. Li C, Bangerth F (2003) Stimulatory effect of cytokinins and interaction with IAA on the release of lateral buds of pea plants from apical dominance. J Plant Physiol 160:1059–1063CrossRefGoogle Scholar
  36. Li C-J, Guevara E, Herrera J, Bangerth F (1995) Effect of apex excision and replacement by 1-naphthylacetic acid on cytokinin concentration and apical dominance in pea plants. Physiol Plant 94:465–469CrossRefGoogle Scholar
  37. Ligerot Y, de Saint Germain A, Waldie T, Troadec C, Citerne S, Kadakia N, Pillot JP, Prigge M, Aubert G, Bendahmane A, Leyser O, Estelle M, Debellé F, Rameau C (2017) The pea branching RMS2 gene encodes the PsAFB4/5 auxin receptor and is involved in an auxin-strigolactone regulation loop. PLoS Genet 13:e1007089. CrossRefGoogle Scholar
  38. Müller D, Waldie T, Miyawaki K, To JP, Melnyk CW, Kieber JJ, Kakimoto T, Leyser O (2015) Cytokinin is required for escape but not release from auxin mediated apical dominance. Plant J 82:874–886CrossRefGoogle Scholar
  39. Neuman DS, Smit BA (1990) Interference from xylem sap in an enzyme-linked immunosorbent assay for zeatin riboside. Physiol Plant 78:548–553CrossRefGoogle Scholar
  40. Ni J, Gao C, Chen M-S, Pan B-Z, Ye K, Xu Z-F (2015) Gibberellin promotes shoot branching in the perennial woody plant Jatropha curcas. Plant Cell Physiol 56:1655–1666CrossRefGoogle Scholar
  41. Nordstrom A, Tarkowski P, Tarkowska D, Norbaek R, Astot C, Dolezal K, Sandberg G (2004) Auxin regulation of cytokinin biosynthesis in Arabidopsis thaliana: a factor of potential importance for auxin-cytokinin-regulated development. Proc Natl Acad Sci USA 101:8039–8044CrossRefGoogle Scholar
  42. Prusinkiewicz P, Crawford S, Smith RS, Ljung K, Bennett T, Ongaro V, Leyser O (2009) Control of bud activation by an auxin transport switch. Proc Natl Acad Sci USA 106:17431–17436CrossRefGoogle Scholar
  43. Rameau C, Bodelin C, Cadier D, Grandjean O, Miard F, Murfet IC (1997) New ramosus mutants at loci Rms1, Rms3 and Rms4 resulting from the mutation breeding program at Versailles. Pisum Genet 29:7–12Google Scholar
  44. Sachs T (1969) Polarity and the induction of organized vascular tissues. Ann Bot 33:263–275CrossRefGoogle Scholar
  45. Seale M, Bennett T, Leyser O (2017) BRC1 expression regulates bud activation potential but is not necessary or sufficient for bud growth inhibition in Arabidopsis. Development 144:1661–1673CrossRefGoogle Scholar
  46. 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:e1001474. CrossRefGoogle Scholar
  47. Tanaka M, Takei K, Kojima M, Sakakibara H, Mori H (2006) Auxin controls local cytokinin biosynthesis in the nodal stem in apical dominance. Plant J 45:1028–1036CrossRefGoogle Scholar
  48. Tanaka H, Kitakura S, Rakusová H, Uemura T, Feraru MI, De Rycke R, Robert S, Kakimoto T, Friml J (2013) Cell polarity and patterning by PIN trafficking through early endosomal compartments in Arabidopsis thaliana. PLoS Genet 9:e1003540. CrossRefGoogle Scholar
  49. 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 455:195–200CrossRefGoogle Scholar
  50. Waldie T, Leyser O (2018) Cytokinin targets auxin transport to promote shoot branching. Plant Physiol. Google Scholar
  51. Waldie T, McCulloch H, Leyser O (2014) Strigolactones and the control of plant development: lessons from shoot branching. Plant J 79:607–622CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018
Corrected publication July/2018

Authors and Affiliations

  1. 1.Institute of Plant PhysiologyRussian Academy of SciencesMoscowRussia

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