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Plant function and evolutionary biology
RESEARCH ARTICLE

Shoot branching in response to nodal roots is mimicked by application of exogenous cytokinin in Trifolium repens

Roderick G. Thomas A and Michael J. M. Hay A B
+ Author Affiliations
- Author Affiliations

A Forage Improvement, AgResearch Grasslands, Private Bag 11 008, Palmerston North, New Zealand.

B Corresponding author. Email: mike.hay@agresearch.co.nz

Functional Plant Biology 42(2) 115-125 https://doi.org/10.1071/FP14158
Submitted: 11 June 2014  Accepted: 31 August 2014   Published: 8 October 2014

Abstract

In nodally-rooting prostrate herbs the outgrowth of shoot axillary buds is highly influenced by the supply of a branch-promoting signal exported from nodal roots to the shoot. The aim of this study was to establish whether cytokinin could be a candidate for the positive component within this net root stimulus (NRS). The approach taken was based on the notion that should cytokinin be the activating signal, then the effects on bud outgrowth induced by exogenous supply of cytokinin (6-benzylaminopurine (BAP)) to plants should largely mimic the responses observed when experimental manipulations alter intra-plant supply of NRS. In Trifolium repens experimental results consistently indicated that supply of BAP into the stem vasculature induced responses mimicking those induced by manipulation of NRS supply: it induced the outgrowth of a similar number of distal axillary buds, activated buds to a similar extent, had similar properties of transport along stems, induced a similar dose dependent response in distal buds and also had the ability to induce bud outgrowth in P-deficient plants. These findings indicate a requirement for further detailed hormonal analytical work to confirm this result and identify the nature of the cytokinin(s) involved in the NRS signalling pathway.

Additional keywords: axillary bud outgrowth, BAP, prostrate clonal herbs, white clover, 6-benzylaminopurine.


References

Aguilar-Martínez JA, Posa-Carrión C, Cubas P (2007) Arabidopsis BRANCHED1 acts as an integrator of branching signals within axillary buds. The Plant Cell 19, 458–472.
Arabidopsis BRANCHED1 acts as an integrator of branching signals within axillary buds.Crossref | GoogleScholarGoogle Scholar | 17307924PubMed |

Beveridge CA (2006) Axillary bud outgrowth: sending a message. Current Opinion in Plant Biology 9, 35–40.
Axillary bud outgrowth: sending a message.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XitFynsw%3D%3D&md5=b5fef06f5c2679f01e981884d4a3f9cbCAS | 16325456PubMed |

Birch CPD, Hutchings MJ (1992) Stolon growth and branching in Glechoma hederacea L.: an application of a plastochron index. New Phytologist 122, 545–551.
Stolon growth and branching in Glechoma hederacea L.: an application of a plastochron index.Crossref | GoogleScholarGoogle Scholar |

Brewer PB, Dun EA, Ferguson BJ, Rameau C, Beveridge CA (2009) Strigolactone acts downstream of auxin to regulate bud outgrowth in pea and Arabidopsis. Plant Physiology 150, 482–493.
Strigolactone acts downstream of auxin to regulate bud outgrowth in pea and Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlvFahsb8%3D&md5=c4040998b750a4d1792d86540feb3c63CAS | 19321710PubMed |

Brewer PB, Koltai H, Beveridge CA (2013) Diverse roles of strigolactones in plant development. Molecular Plant 6, 18–28.
Diverse roles of strigolactones in plant development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFCnurs%3D&md5=b753f11128f6f42ad6bc2b5204a281bbCAS | 23155045PubMed |

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 damping auxin transport. Development 137, 2905–2913.
Strigolactones enhance competition between shoot branches by damping auxin transport.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlaku7jF&md5=decfb6c13822933215e91acf90aff1fcCAS | 20667910PubMed |

Domagalska MA, Leyser O (2011) Signal integration in the control of shoot branching. Nature Reviews. Molecular Cell Biology 12, 211–221.
Signal integration in the control of shoot branching.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjs1Cqsb8%3D&md5=bb163962433defa3461a89f15c27c2e3CAS | 21427763PubMed |

Dun EA, Brewer PB, Beveridge CA (2009a) Strigolactones: discovery of the elusive shoot branching hormone. Trends in Plant Science 14, 364–372.
Strigolactones: discovery of the elusive shoot branching hormone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXosVajsrc%3D&md5=bbf18059cf179f5b349d2c85aae1d370CAS | 19540149PubMed |

Dun EA, Hanan J, Beveridge CA (2009b) Computational modelling and molecular physiology experiments reveal new insights into shoot branching in pea. The Plant Cell 21, 3459–3472.
Computational modelling and molecular physiology experiments reveal new insights into shoot branching in pea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXovVWrtA%3D%3D&md5=94c5f269b07c02ea836232593a5b195dCAS | 19948786PubMed |

Dun EA, Saint Germain A, Rameau C, Beveridge CA (2012) Antagonistic action of strigolactone and cytokinin in bud outgrowth control. Plant Physiology 158, 487–498.
Antagonistic action of strigolactone and cytokinin in bud outgrowth control.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XltFSnt7s%3D&md5=73947de2e27efeb7517b2fb409354b89CAS | 22042819PubMed |

Faiss M, Zalubilova J, Strnad M, Schmulling T (1997) Conditional transgenic expression of the ipt gene indicates a function for cytokinins in paracrine signalling in whole tobacco plants. The Plant Journal 12, 401–415.
Conditional transgenic expression of the ipt gene indicates a function for cytokinins in paracrine signalling in whole tobacco plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmsVams7k%3D&md5=10798a049cabd03b07e94657cff88761CAS | 9301091PubMed |

Ferguson BJ, Beveridge CA (2009) Roles for auxin, cytokinin and strigolactone in regulating shoot branching. Plant Physiology 149, 1929–1944.
Roles for auxin, cytokinin and strigolactone in regulating shoot branching.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXks1Wnsr4%3D&md5=485b9ad70dce6ed9267d2ce3e44d2237CAS | 19218361PubMed |

Forde BG (2002) The role of long-distance signalling in plant responses to nitrate and other nutrients. Journal of Experimental Botany 53, 39–43.
The role of long-distance signalling in plant responses to nitrate and other nutrients.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXptlKgtLg%3D&md5=2a49b6561b93f59a05bd57ce299832f7CAS | 11741039PubMed |

Franco-Zorrilla JM, Martín AC, Leyva A, Paz-Ares J (2005) Interaction between phosphate-starvation, sugar and cytokinin signalling in Arabidopsis and the roles of cytokinin receptors CRE1/AHK4 and AHK3. Plant Physiology 138, 847–857.
Interaction between phosphate-starvation, sugar and cytokinin signalling in Arabidopsis and the roles of cytokinin receptors CRE1/AHK4 and AHK3.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmtVejsrk%3D&md5=26ec0e4f1f2098ff08734de3b19c862bCAS | 15923327PubMed |

Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pagès 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, 189–194.
Strigolactone inhibition of shoot branching.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtV2qtLzK&md5=dd20c6346859f81eba6363fb7ca52496CAS | 18690209PubMed |

Hayward A, Stirnberg P, Beveridge C, Leyser O (2009) Interactions between auxin and strigolactone in shoot branching control. Plant Physiology 151, 400–412.
Interactions between auxin and strigolactone in shoot branching control.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFOjsbrO&md5=d4189505c825413166b21349337dc6a2CAS | 19641034PubMed |

Hu Z, Yamauchi T, Yang J, Jikumaru Y, Tsuchida-Mayama T, Ichikawa H, Takamure I, Nagamura Y, Tsutsumi N, Yamaguchi S, Kyozuka J, Nakazono M (2014) Strigolactone and cytokinin act antagonistically in regulating rice mesocotyle elongation in darkness. Plant & Cell Physiology 55, 30–41.
Strigolactone and cytokinin act antagonistically in regulating rice mesocotyle elongation in darkness.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXlvFGrtQ%3D%3D&md5=3c0b063f1cb2b31513feaeb198fa5e8fCAS |

Kohlen W, Charnikhova T, Liu Q, Bours R, Domagalska MA, Beguerie S, Verstappen F, Leyser O, Bouwmeester H, Ruyter-Spira C (2011) Strigolactones are transported through the xylem and play a key role in shoot architectural response to phosphorus deficiency in non-AM host Arabidopsis thaliana. Plant Physiology 155, 974–987.
Strigolactones are transported through the xylem and play a key role in shoot architectural response to phosphorus deficiency in non-AM host Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXksFymtbo%3D&md5=bade62bf3767268a7aa3f586d6d66fe6CAS | 21119045PubMed |

Leyser O (2009) The control of shoot branching: an example of plant information processing. Plant, Cell & Environment 32, 694–703.
The control of shoot branching: an example of plant information processing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmslemsLs%3D&md5=4d2bb603b67ae7ffb362d6cf5a269a33CAS |

Liang J, Zhao L, Challis R, Leyser O (2010) Strigolactone regulation of shoot branching in chrysanthemum (Dendranthema grandiflorum). Journal of Experimental Botany 61, 3069–3078.
Strigolactone regulation of shoot branching in chrysanthemum (Dendranthema grandiflorum).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXotVWktrg%3D&md5=8547e1d027ebd34290e0d43bee80ee69CAS | 20478970PubMed |

Lötscher M, Nösberger J (1996) Influence of position and number of nodal roots on outgrowth of axillary buds and development of branches in Trifolium repens L. Annals of Botany 78, 459–465.
Influence of position and number of nodal roots on outgrowth of axillary buds and development of branches in Trifolium repens L.Crossref | GoogleScholarGoogle Scholar |

Lovatt-Doust L, Lovatt-Doust J (1982) The battle strategies of plants. New Scientist 95, 81–84.

Mason MG, Ross JJ, Babst BA, Wienclaw BN, Beveridge CA (2014) Sugar demand, not auxin, is the initial regulator of apical dominance. Proceedings of the National Academy of Sciences of the United States of America 111, 6092–6097.
Sugar demand, not auxin, is the initial regulator of apical dominance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmtlWksbY%3D&md5=d0f6144439a5b2a600fc710d81c6b4cfCAS | 24711430PubMed |

Müller D, Leyser O (2011) Auxin, cytokinin and the control of shoot branching. Annals of Botany 107, 1203–1212.
Auxin, cytokinin and the control of shoot branching.Crossref | GoogleScholarGoogle Scholar | 21504914PubMed |

Nordström A, Tarkowski P, Tarkowska D, Norbaek R, Åstot C, Dolezal K, Sandberg G (2004) Auxin regulation of cytokinin biosynthesis in Arabidopsis thaliana: a factor of potential importance for auxin-cytokinin-regulated development. Proceedings of the National Academy of Sciences of the United States of America 101, 8039–8044.
Auxin regulation of cytokinin biosynthesis in Arabidopsis thaliana: a factor of potential importance for auxin-cytokinin-regulated development.Crossref | GoogleScholarGoogle Scholar | 15146070PubMed |

Ongaro V, Leyser O (2008) Hormonal control of shoot branching. Journal of Experimental Botany 59, 67–74.
Hormonal control of shoot branching.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1Sitbw%3D&md5=be9a341e9a07563a8913ade5df7634a1CAS | 17728300PubMed |

Ongaro V, Bainbridge K, Williamson L, Leyser O (2008) Interactions between axillary branches of Arabidopsis. Molecular Plant 1, 388–400.
Interactions between axillary branches of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXoslyksLs%3D&md5=c407b9eaf2e7f9d1b8e05049a39514deCAS | 19825548PubMed |

Rubio V, Bustos R, Irigoyen ML, Cardona-López X, Rojas-Triana M, Paz-Ares J (2009) Plant hormones and nutrient signalling. Plant Molecular Biology 69, 361–373.
Plant hormones and nutrient signalling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhvVOis7c%3D&md5=a8647330a1cd0d0f72423cb89cfb7760CAS | 18688730PubMed |

Sachs T, Thimann KV (1967) The role of auxins and cytokinins in the release of buds from dominance. American Journal of Botany 54, 136–144.
The role of auxins and cytokinins in the release of buds from dominance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF2sXnsFWgsw%3D%3D&md5=6f851bfff536798e14bf711d166b6190CAS |

Shimizu-Sato S, Tanaka M, Mori H (2009) Auxin-cytokinin interactions in the control of shoot branching. Plant Molecular Biology 69, 429–435.
Auxin-cytokinin interactions in the control of shoot branching.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhvVOis7Y%3D&md5=6922b482b70ec13988252be9eeecd14eCAS | 18974937PubMed |

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 Biology 11, e1001474
Strigolactone can promote or inhibit shoot branching by triggering rapid depletion of the auxin efflux protein PIN1 from the plasma membrane.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXivVeiuro%3D&md5=8c566f3eab3b1191bcaebebdee4d8345CAS | 23382651PubMed |

Simons JL, Napoli CA, Janssen BJ, Plummer KM, Snowden CA (2007) Analysis of the DECREASED APICAL DOMINANCE genes of petunia in the control of axillary branching. Plant Physiology 143, 697–706.
Analysis of the DECREASED APICAL DOMINANCE genes of petunia in the control of axillary branching.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhvFWnsbw%3D&md5=bcd8cdbb2b83de7c1254438443d1e32dCAS | 17158589PubMed |

Tanaka M, Takei K, Kojima M, Sakakibara H, Mori H (2006) Auxin controls local cytokinin biosynthesis in the nodal stem in apical dominance. The Plant Journal 45, 1028–1036.
Auxin controls local cytokinin biosynthesis in the nodal stem in apical dominance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjs1Smsb8%3D&md5=9e5525976cbb156af12282eddc584528CAS | 16507092PubMed |

Thomas RG (1987) Vegetative growth and development. In ‘White clover’. (Eds MJ Baker, WM Williams) pp. 31–62. (CABI International: Wallingford, UK)

Thomas RG, Hay MJM (2004) Evidence suggests plagiotropic clonal species have evolved a branching physiology emphasizing regulation by nodal roots. Evolutionary Ecology 18, 409–428.
Evidence suggests plagiotropic clonal species have evolved a branching physiology emphasizing regulation by nodal roots.Crossref | GoogleScholarGoogle Scholar |

Thomas RG, Hay MJM (2007) Cumulative activation of axillary buds by nodal roots in Trifolium repens L. Journal of Experimental Botany 58, 2069–2078.
Cumulative activation of axillary buds by nodal roots in Trifolium repens L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXosFeksbg%3D&md5=33cf7c06ffc9cae716459979d2a2a0c1CAS | 17470443PubMed |

Thomas RG, Hay MJM (2008a) Regulation of shoot branching patterns by the basal root system: towards a predictive model. Journal of Experimental Botany 59, 1163–1173.
Regulation of shoot branching patterns by the basal root system: towards a predictive model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlt1aitbg%3D&md5=846711d19a84e0100c08b8bdd3f4f7d4CAS | 18375931PubMed |

Thomas RG, Hay MJM (2008b) Adaptive variation in physiological traits underpinning stem elongation responses among nodally-rooting herbs. Evolutionary Ecology 22, 369–381.
Adaptive variation in physiological traits underpinning stem elongation responses among nodally-rooting herbs.Crossref | GoogleScholarGoogle Scholar |

Thomas RG, Hay MJM (2009) Axillary buds acquire an outgrowth potential from their parent apical bud. Journal of Experimental Botany 60, 4275–4285.
Axillary buds acquire an outgrowth potential from their parent apical bud.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlGitL%2FJ&md5=acbc2f281c66538f666a2a00b7ce62f4CAS | 19717528PubMed |

Thomas RG, Hay MJM (2010) The role of nodal roots in prostrate clonal herbs: ‘phalanx’ versus ‘guerrilla’. Evolutionary Ecology 24, 1489–1504.
The role of nodal roots in prostrate clonal herbs: ‘phalanx’ versus ‘guerrilla’.Crossref | GoogleScholarGoogle Scholar |

Thomas RG, Hay MJM (2011) Existing branches correlatively inhibit further branching in Trifolium repens: possible mechanisms. Journal of Experimental Botany 62, 1027–1036.
Existing branches correlatively inhibit further branching in Trifolium repens: possible mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVekurg%3D&md5=3eb149e1d80eda7768f26422cfaadc67CAS | 21071681PubMed |

Thomas RG, Hay MJM (2014) Shoot branching in nutrient-limited Trifolium repens is primarily restricted by shortage of root-supplied promoter signals. Functional Plant Biology 41, 401–410.
Shoot branching in nutrient-limited Trifolium repens is primarily restricted by shortage of root-supplied promoter signals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXktlCmsrw%3D&md5=90af41083d7591d2fc1d39417170ed46CAS |

Thomas RG, Hay MJM, Newton PCD (2002) A developmentally based categorisation of branching in Trifolium repens L.: influence of nodal roots. Annals of Botany 90, 379–389.
A developmentally based categorisation of branching in Trifolium repens L.: influence of nodal roots.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38vnt1Gmtg%3D%3D&md5=8cdba37581cab18e557cb9f107290a9cCAS | 12234150PubMed |

Thomas RG, Hay MJM, Newton PCD (2003) Relationships among shoot sinks for resources exported from nodal roots regulate branch development of distal non-rooted portions of Trifolium repens L. Journal of Experimental Botany 54, 2091–2104.
Relationships among shoot sinks for resources exported from nodal roots regulate branch development of distal non-rooted portions of Trifolium repens L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXns1Slu70%3D&md5=efb7bfe1bddfe6c7bc6af1d9182d58a1CAS | 12885859PubMed |

Thomas RG, Li FY, Hay MJM (2014) Differential bud activation by a net positive root signal explains branching phenotype in prostrate clonal herbs: a model. Journal of Experimental Botany 65, 673–682.
Differential bud activation by a net positive root signal explains branching phenotype in prostrate clonal herbs: a model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhs1Chsr0%3D&md5=5e45372a095f00d71509e69b39ccefddCAS | 24399176PubMed |

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, 195–201.
Inhibition of shoot branching by new terpenoid plant hormones.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtV2qtLnE&md5=4982d2e2ea6efb67e3bf13fe03ff1d4bCAS | 18690207PubMed |

Umehara M, Hanada A, Magome H, Takeda-Kamiya N, Yamaguchi S (2010) Contribution of strigolactone to the inhibition of tiller bud outgrowth under phosphate deficiency in rice. Plant & Cell Physiology 51, 1118–1126.
Contribution of strigolactone to the inhibition of tiller bud outgrowth under phosphate deficiency in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXptlalsLw%3D&md5=24ba7ea672e80fda8499ae809575a0b8CAS |

Xie XN, Yoneyama K, Yoneyama K (2010) The strigolactone story. Annual Review of Phytopathology 48, 93–117.
The strigolactone story.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1Wgt77K&md5=38c393e0035d52267c3855d7017730b8CAS |