Molecular Genetics and Genomics

, Volume 293, Issue 6, pp 1547–1563 | Cite as

Exogenous application of GA3 inactively regulates axillary bud outgrowth by influencing of branching-inhibitors and bud-regulating hormones in apple (Malus domestica Borkh.)

  • Ming Tan
  • Guofang Li
  • Xiaojie Liu
  • Fang Cheng
  • Juanjuan Ma
  • Caiping Zhao
  • Dong Zhang
  • Mingyu HanEmail author
Original Article


Although gibberellin (GA) has been reported to control branching, little is known about how GA mediates signals regulating the outgrowth of axillary buds (ABs). In the current study, the effect of the exogenous application of 5.0 mM GA3 on ABs outgrowth on 1-year-old ‘Nagafu No. 2’/T337/M. robusta Rehd. apple trees was investigated and compared to the bud-activating treatments, 5 mM BA or decapitation. Additionally, the expression of genes related to bud-regulating signals and sucrose levels in ABs was examined. Results indicated that GA3 did not promote ABs’ outgrowth, nor down-regulate the expression of branching repressors [MdTCP40, MdTCP33, and MdTCP16 (homologs of BRANCHED1 and BRC2)], which were significantly inhibited by the BA and decapitation treatments. MdSBP12 and MdSBP18, the putative transcriptional activators of these genes, which are expressed at lower levels in BA-treated and decapitated buds, were up-regulated in the GA3 treatment in comparison to the BA treatment. Additionally, GA3 did not up-regulate the expression of CK response- and auxin transport-related genes, which were immediately induced by the BA treatment. In addition, GA3 also up-regulated the expression of several Tre6P biosynthesis genes and reduced sucrose levels in ABs. Sucrose levels, however, were still higher than what was observed in BA-treated buds, indicating that sucrose may not be limiting in GA3-controlled AB outgrowth. Although GA3 promoted cell division, it was not sufficient to induce AB outgrowth. Conclusively, some branching-inhibiting genes and bud-regulating hormones are associated with the inability of GA3 to activate AB outgrowth.


Gibberellin Axillary bud outgrowth Branching Branching-inhibitor 



This work was supported by the National Apple Industry Technology System of Agriculture Ministry of China (CARS-28); Yangling Subsidiary Center Project of National Apple Improvement Center and Collaborative Innovation of Center Shaanxi Fruit Industry Development (C000088); Chinese postdoctoral project (2015M582713); Innovation project of science and technology plan projects of Shaanxi province (2016TZC-N-11-6).

Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflict of interest. Ming Tan declares that she has no conflict of interest. Guofang Li declares that he has no conflict of interest. Xiaojie Liu declares that he has no conflict of interest. Fang Cheng declares that she has no conflict of interest. Juanjuan Ma declares that she has no conflict of interest. Caiping Zhao declares that she has no conflict of interest. Dong Zhang declares that he has no conflict of interest. Mingyu Han declares that he has no conflict of interest.

Supplementary material

438_2018_1481_MOESM1_ESM.doc (1.3 mb)
Supplementary material 1 (DOC 1323 KB)


  1. Agharkar M, Lomba P, Altpeter F, Zhang H, Kenworthy K, Lange T (2007) Stable expression of AtGA2ox1 in a low-input turfgrass (Paspalum notatum Flugge) reduces bioactive gibberellin levels and improves turf quality under field conditions. Plant Biotechnol J 5:791–801PubMedGoogle Scholar
  2. Aguilarmartínez JA, Pozacarrión C, Cubas P (2007) Arabidopsis BRANCHED1 Acts as an integrator of branching signals within axillary buds. Plant Cell 19:458Google Scholar
  3. Agusti J, Herold S, Schwarz M, Sanchez P, Ljung K, Dun EA, Brewer PB, Beveridge CA, Sieberer T, Sehr EM (2011) Strigolactone signaling is required for auxin-dependent stimulation of secondary growth in plants. Proc Natl Acad Sci USA 108:20242–20247PubMedGoogle Scholar
  4. Argyros RD, Mathews DE, Chiang YH, Palmer CM, Thibault DM, Etheridge N, Argyros DA, Mason MG, Kieber JJ, Schaller GE (2008) Type B response regulators of Arabidopsis play key roles in cytokinin signaling and plant development. Plant Cell 20:2102–2116PubMedPubMedCentralGoogle Scholar
  5. Arite T, Iwata H, Ohshima K, Maekawa M, Nakajima M, Kojima M, Sakakibara H, Kyozuka J (2007) DWARF10, an RMS1/MAX4/DAD1 ortholog, controls lateral bud outgrowth in rice. Plant J 51:1019–1029PubMedGoogle Scholar
  6. Atay E, Koyuncu F (2013) A new approach for augmenting branching of nursery trees and its comparison with other methods. Sci Hortic 160:345–350Google Scholar
  7. Balla J, Kalousek P, Reinöhl V, Friml J, Procházka S (2011) Competitive canalization of PIN-dependent auxin flow from axillary buds controls pea bud outgrowth. Plant J Cell Mol Biol 65:571–577Google Scholar
  8. 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 16:553–563PubMedGoogle Scholar
  9. Bennett T, Hines G, Leyser O (2014) Canalization: what the flux? Trends Genet 30:41–48PubMedGoogle Scholar
  10. Bergmann C, Wegmann K, Frischmuth K, Samson E, Kranz A, Weigelt D, Koll P, Welzel P (1993) Stimulation of Orobanche crenata seed germination by (+)-strigol and structural analogues dependence on constitution and configuration of the germinatio stimulants. J Plant Physiol 142:338–342Google Scholar
  11. Bostan M (2010) Influence of crown formation method on development of the apple trees in the nursery. J Am Soc Hortic Sci 7:1193–1198Google Scholar
  12. Boucheron E, Healy JC, Sauvanet A, Rembur J, Noin M, Sekine M, Riou KC, Murray JA, Van OH, Chriqui D (2005) Ectopic expression of Arabidopsis CYCD2 and CYCD3 in tobacco has distinct effects on the structural organization of the shoot apical meristem. J Exp Bot 56:123–134PubMedGoogle Scholar
  13. Braun N, Germain ADS, Pillot JP, Boutet-Mercey S, Dalmais M, Antoniadi I, Xin L, Maia-Grondard A, Signor CL, Bouteiller N (2012) The pea TCP transcription factor PsBRC1 acts downstream of strigolactones to control shoot branching. Plant Physiol 158:225–238PubMedGoogle Scholar
  14. Brewer PB, Beveridge CA (2009) Strigolactone acts downstream of auxin to regulate bud outgrowth in pea and Arabidopsis. Plant Physiol 150:482–493PubMedPubMedCentralGoogle Scholar
  15. Cheng H, Qin L, Lee S, Fu X, Richards DE, Cao D, Luo D, Harberd NP, Peng J (2004) Gibberellin regulates Arabidopsis floral development via suppression of DELLA protein function. Development 131:1055PubMedGoogle Scholar
  16. Choubane D, Rabot A, Mortreau E, Legourrierec J, Péron T, Foucher F, Ahcène Y, Pelleschi-Travier S, Leduc N, Hamama L (2012) Photocontrol of bud burst involves gibberellin biosynthesis in Rosa sp. J Plant Physiol 169:1271–1280PubMedGoogle Scholar
  17. Crawford S, Shinohara NT, Williamson L, George G, Hepworth J, Muller D, Domagalska MA, Leyser O (2010) Strigolactones enhance competition between shoot branches by dampening auxin transport. Development 137:2905PubMedGoogle Scholar
  18. Daviere JM, Wild M, Regnault T, Baumberger N, Eisler H, Genschik P, Achard P (2014) Class I TCP-DELLA interactions in inflorescence shoot apex determine plant height. Curr Biol 24:1923–1928PubMedGoogle Scholar
  19. Davière JM, Achard P (2013) Gibberellin signaling in plants. Development 140:1147–1151PubMedGoogle Scholar
  20. De SGA, Ligerot Y, Dun EA, Pillot JP, Ross JJ, Beveridge CA, Rameau C (2013) Strigolactones stimulate internode elongation independently of gibberellins. Plant Physiol 163:1012–1025Google Scholar
  21. Domagalska MA, Leyser O (2011) Signal integration in the control of shoot branching. Nat Rev Mol Cell Biol 12:211PubMedGoogle Scholar
  22. Du L, Qi S, Ma J, Xing L, Fan S, Zhang S, Li Y, Shen Y, Zhang D, Han M (2017) Identification of TPS family members in apple (Malus × domestica Borkh.) and the effect of sucrose sprays on TPS expression and floral induction. Plant Physiol Biochem 120:10–23PubMedGoogle Scholar
  23. Dun EA, Germain ADS, Rameau C, Beveridge CA (2012) Antagonistic action of strigolactone and cytokinin in bud outgrowth control. Plant Physiol 158:487PubMedGoogle Scholar
  24. Dun EA, Germain ADS, Rameau C, Beveridge CA (2013) Dynamics of strigolactone function and shoot branching responses in Pisum sativum. Mol Plant 6:128PubMedGoogle Scholar
  25. Elfving DC (2010) Plant bioregulators in the deciduous fruit tree nursery. XI Int Symp Plant Bioregul Fruit Prod 884:159–166Google Scholar
  26. Elfving D, Visser D, Henry J (2011) Gibberellins stimulate lateral branch development in young sweet cherry trees in the orchard. Int J Fruit Sci 11:41–54Google Scholar
  27. Fan S, Zhang D, Gao C, Zhao M, Wu H, Li Y, Shen Y, Han M (2017) Identification, classification, and expression analysis of GRAS gene family in Malus domestica. Front Physiol 8:253PubMedPubMedCentralGoogle Scholar
  28. Fichtner F, Barbier FF, Feil R, Watanabe M, Annunziata MG, Chabikwa TG, Hofgen R, Stitt M, Beveridge CA, Lunn JE (2017) Trehalose 6-phosphate is involved in triggering axillary bud outgrowth in garden pea (Pisum sativum L.). Plant J 92:611–623PubMedGoogle Scholar
  29. Finlayson SA (2007) Arabidopsis teosinte Branched1-like 1 regulates axillary bud outgrowth and is homologous to monocot teosinte Branched1. Plant Cell Physiol 48:667PubMedGoogle Scholar
  30. Foster T, Kirk C, Jones WT, Allan AC, Espley R, Karunairetnam S, Rakonjac J (2006) Characterisation of the DELLA subfamily in apple (Malus × domestica Borkh.). Tree Genet Genomes 3:187–197Google Scholar
  31. François B, Thomas P, Marion L, Maria-Dolores PG, Quentin B, Jakub R, Stéphanie BM, Sylvie C, Remi L, Benoît P (2015) Sucrose is an early modulator of the key hormonal mechanisms controlling bud outgrowth in Rosa hybrida. J Exp Bot 66:2569Google Scholar
  32. Gambino G, Perrone I, Gribaudo I (2008) A rapid and effective method for RNA extraction from different tissues of grapevine and other woody plants. Phytochem Anal 19:520–525PubMedGoogle Scholar
  33. Ghosh A, Chikara J, Chaudhary DR (2011) Diminution of economic yield as affected by pruning and chemical manipulation of Jatropha curcas L. Biomass Bioenergy 35:1021–1029Google Scholar
  34. Greenboim-Wainberg Y, Weiss D (2005) Cross talk between gibberellin and cytokinin: the Arabidopsis GA response inhibitor SPINDLY plays a positive role in cytokinin signaling. Plant Cell 17:92PubMedPubMedCentralGoogle Scholar
  35. Hao L, Wang RX, Qian Q, Yan MX, Meng XB, Fu ZM, Yan CY, Jiang B, Zhen S, Li JY (2009) DWARF27, an iron-containing protein required for the biosynthesis of strigolactones, regulates rice tiller bud outgrowth. Plant Cell 21:1512Google Scholar
  36. Henry C, Rabot A, Laloi M, Mortreau E, Sigogne M, Leduc N, Lemoine R, Sakr S, Vian A, Pelleschitravier S (2011) Regulation of RhSUC2, a sucrose transporter, is correlated with the light control of bud burst in Rosa sp. Plant Cell Environ 34:1776–1789PubMedGoogle Scholar
  37. Ho KM, English S, Bell J (1981) The control of the patterned differentiation of vascular tissues. Adv Bot Res 9:151–262Google Scholar
  38. Holalu SV, Finlayson SA (2017) The ratio of red light to far red light alters Arabidopsis axillary bud growth and abscisic acid signalling before stem auxin changes. J Exp Bot 68:943–952PubMedPubMedCentralGoogle Scholar
  39. Itoh H, Ueguchitanaka M, Sato Y, Ashikari M, Matsuoka M (2002) The gibberellin signaling pathway is regulated by the appearance and disappearance of SLENDER RICE1 in nuclei. Plant Cell 14:57PubMedPubMedCentralGoogle Scholar
  40. Kebrom TH, Finlayson SA (2006) Phytochrome B represses Teosinte Branched1 expression and induces sorghum axillary bud outgrowth in response to light signals. Plant Physiol 140:1109PubMedPubMedCentralGoogle Scholar
  41. Kebrom TH, Mullet JE (2016) Transcriptome profiling of tiller buds provides new insights into PhyB regulation of tillering and indeterminate growth in Sorghum. Plant Physiol 170:2232–2250PubMedPubMedCentralGoogle Scholar
  42. Kebrom TH, Spielmeyer W, Finnegan EJ (2013) Grasses provide new insights into regulation of shoot branching. Trends Plant Sci 18:41–48PubMedGoogle Scholar
  43. Kosugi S, Ohashi Y (1997) PCF1 and PCF2 specifically bind to cis elements in the rice proliferating cell nuclear antigen gene. Plant Cell 9:1607PubMedPubMedCentralGoogle Scholar
  44. Kviklys D (2006) Induction of feathering of apple planting material. Agron Vestis 9:58–63Google Scholar
  45. Labuschagné IF, Louw JH, Schmidt K, Sadie A (2003) Selection for increased budbreak in apple. J Am Soc Hortic Sci 128:363–373Google Scholar
  46. Leyser O (2009) The control of shoot branching: an example of plant information processing. Plant Cell Environ 32:694–703PubMedGoogle Scholar
  47. Li C-J, Bangerth F (1999) Autoinhibition of indoleacetic acid transport in the shoots of two-branched pea (Pisum sativum) plants and its relationship to correlative dominance. Physiol Plant 106:415–420Google Scholar
  48. 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 160:1059–1063PubMedGoogle Scholar
  49. Li J, Hou H, Li X, Jiang X, Yin X, Gao H, Zheng Y, Bassett CL, Wang X (2013) Genome-wide identification and analysis of the SBP-box family genes in apple (Malus × domestica Borkh.). Plant Physiol Biochem 70:100PubMedGoogle Scholar
  50. Li Y, Zhang D, Zhang L, Zuo X, Fan S, Zhang X, Shalmani A, Han M (2017) Identification and expression analysis of cytokinin response-regulator genes during floral induction in apple (Malus domestica Borkh). Plant Growth Regul:1–10Google Scholar
  51. Liu J, Cheng X, Liu P, Sun J (2017) miR156-targeted SBP-box transcription factors interact with DWARF53 to regulate TEOSINTE BRANCHED1 and BARREN STALK1 expression in bread wheat. Plant Physiol 174:1931PubMedPubMedCentralGoogle Scholar
  52. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 25:402–408PubMedPubMedCentralGoogle Scholar
  53. Lo SF, Yang SY, Chen KT, Hsing YL, Zeevaart JAD, Chen LJ, Yu SM (2008) A novel class of gibberellin 2-oxidases control semidwarfism, tillering, and root development in rice. Plant Cell 20:2603–2618PubMedPubMedCentralGoogle Scholar
  54. Lu Z, Yu H, Xiong G, Wang J, Jiao Y, Liu G, Jing Y, Meng X, Hu X, Qian Q, Fu X, Wang Y, Li J (2013) Genome-wide binding analysis of the transcription activator ideal plant architecture1 reveals a complex network regulating rice plant architecture. Plant Cell 25:3743–3759PubMedPubMedCentralGoogle Scholar
  55. Lunn EJ, Feil R, Hendriks Janneke HM, Gibon Y, Morcuende R, Osuna D, Scheible W, Carillo P, Hajirezaei MR, Stitt M (2006) Sugar-induced increases in trehalose 6-phosphate are correlated with redox activation of ADP glucose pyrophosphorylase and higher rates of starch synthesis in Arabidopsis thaliana. Biochem J 397:139PubMedPubMedCentralGoogle Scholar
  56. Marínde lRN, Pfeiffer A, Hill K, Locascio A, Bhalerao RP, Miskolczi P, Grønlund AL, Wanchookohli A, Thomas SG, Bennett MJ (2015) Genome wide binding site analysis reveals transcriptional coactivation of cytokinin-responsive genes by DELLA proteins. Plos Genet 11:e1005337Google Scholar
  57. Martin K, Vera M, Richard W, Brendan D (2011) TCP14 and TCP15 affect internode length and leaf shape in Arabidopsis. Plant J Cell Mol Biol 68:147–158Google Scholar
  58. Martín-Trillo M, Grandío EG, Serra F, Marcel F, Rodríguez-Buey ML, Schmitz G, Theres K, Bendahmane A, Dopazo H, Cubas P (2011) Role of tomato BRANCHED1-like genes in the control of shoot branching. Plant J Cell Mol Biol 67:701Google Scholar
  59. Mason MG, Ross JJ, Babst BA, Wienclaw BN, Beveridge CA (2014) Sugar demand, not auxin, is the initial regulator of apical dominance. Proc Natl Acad Sci USA 111:6092–6097PubMedGoogle Scholar
  60. Mauriat M, Sandberg LG, Moritz T (2011) Proper gibberellin localization in vascular tissue is required to control auxin-dependent leaf development and bud outgrowth in hybrid aspen. Plant J Cell Mol Biol 67:805Google Scholar
  61. Maymon I, Greenboim-Wainberg Y, Sagiv S, Kieber JJ, Moshelion M, Olszewski N, Weiss D (2009) Cytosolic activity of SPINDLY implies the existence of a DELLA-independent gibberellin-response pathway. Plant J Cell Mol Biol 58:979Google Scholar
  62. Minakuchi K, Kameoka H, Yasuno N, Umehara M, Luo L, Kobayashi K, Hanada A, Ueno K, Asami T, Yamaguchi S (2010) FINE CULM1 (FC1) works downstream of strigolactones to inhibit the outgrowth of axillary buds in rice. Plant Cell Physiol 51:1127PubMedPubMedCentralGoogle Scholar
  63. Moubayidin L, Perilli S, Ioio RD, Mambro RD, Costantino P, Sabatini S (2010) The rate of cell differentiation controls the Arabidopsis root meristem growth phase. Curr Biol Cb 20:1138PubMedGoogle Scholar
  64. Muhr M, Prüfer N, Paulat M, Teichmann T (2016) Knockdown of strigolactone biosynthesis genes in Populus affects BRANCHED1 expression and shoot architecture. New Phytol 212:613–626PubMedGoogle Scholar
  65. Muller D, Leyser O (2011) Auxin, cytokinin and the control of shoot branching. Ann Bot 107:1203–1212PubMedPubMedCentralGoogle Scholar
  66. Muller 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 82:874–886PubMedPubMedCentralGoogle Scholar
  67. Murfet IC, Reid JB, Casey R, Davies DR (1993) Developmentalmutants. In: Casey R, Davies DR (eds) Peas genetics molecular biology and biotechnology Developmental mutants. Peas genetics molecular biology and biotechnology, (Wallingford: CAB), pp 165–216Google Scholar
  68. Nakamura H, Xue YL, Miyakawa T, Hou F, Qin HM, Fukui K, Shi X, Ito E, Ito S, Park SH (2013) Molecular mechanism of strigolactone perception by DWARF14. Nat Commun 4:2613PubMedGoogle Scholar
  69. Naor A, Flaishman M, Stern R, Moshe A, Erez A (2003) Temperature effects on dormancy completion of vegetative buds in apple. J Am Soc Hortic Sci Am Soc Hortic Sci 128:636–641Google Scholar
  70. Ni J, Gao CC, Chen MS, Pan BZ, Ye KQ, Xu ZF (2015) Gibberellin promotes shoot branching in the perennial woody plant Jatropha curcas. Plant Cell Physiol 56:1655–1666PubMedPubMedCentralGoogle Scholar
  71. Nicolas M, Rodríguez-Buey María L, Franco-Zorrilla José M, Cubas P (2015) A recently evolved alternative splice site in the BRANCHED1a gene controls potato plant architecture. Curr Biol 25:1799–1809PubMedGoogle Scholar
  72. Niwa M, Daimon Y, Kurotani K, Higo A, Pruneda-Paz JL, Breton G, Mitsuda N, Kay SA, Ohme-Takagi M, Endo M (2013) BRANCHED1 interacts with FLOWERING LOCUS T to repress the floral transition of the axillary meristems in Arabidopsis. Plant Cell 25:1228–1242PubMedPubMedCentralGoogle Scholar
  73. Nunes C, O’Hara LE, Primavesi LF, Delatte TL, Schluepmann H, Somsen GW, Silva AB, Fevereiro PS, Wingler A, Paul MJ (2013) The trehalose 6-phosphate/SnRK1 signaling pathway primes growth recovery following relief of sink limitation. Plant Physiol 162:1720–1732PubMedPubMedCentralGoogle Scholar
  74. Otori K, Tamoi M, Tanabe N, Shigeoka S (2017) Enhancements in sucrose biosynthesis capacity affect shoot branching in Arabidopsis. Biosci Biotechnol Biochem 81:1Google Scholar
  75. Patrick JW, Colyvas K (2014) Crop yield components—photoassimilate supply- or utilisation limited-organ development? Funct Plant Biol 41:893Google Scholar
  76. Peng J, Carol P, Richards DE, King KE, Cowling RJ, Murphy GP, Harberd NP (1997) The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Genes Dev 11:3194PubMedPubMedCentralGoogle Scholar
  77. Rabot A, Henry C, Ben BK, Mortreau E, Azri W, Lothier J, Hamama L, Boummaza R, Leduc N, Pelleschi-Travier S (2012) Insight into the role of sugars in bud burst under light in the rose. Plant Cell Physiol 53:1068PubMedGoogle Scholar
  78. Rameau C, Bertheloot J, Leduc N, Andrieu B, Foucher F, Sakr S (2015) Multiple pathways regulate shoot branching. Front Plant Sci 5:741PubMedPubMedCentralGoogle Scholar
  79. Richter R, Behringer C, Muller IK, Schwechheimer C (2010) The GATA-type transcription factors GNC and GNL/CGA1 repress gibberellin signaling downstream from DELLA proteins and phytochrome-interacting factors. Genes Dev 24:2093–2104PubMedPubMedCentralGoogle Scholar
  80. Rinne PL, Paul LK, Vahala J, Kangasjarvi J, van der Schoot C (2016) Axillary buds are dwarfed shoots that tightly regulate GA pathway and GA-inducible 1,3-beta-glucanase genes during branching in hybrid aspen. J Exp Bot 67:5975–5991PubMedPubMedCentralGoogle Scholar
  81. Roef L, Onckelen HV (2010) Cytokinin Regulation of the Cell Division Cycle. In: Davies PJ (ed) Plant Hormones. Springer, DordrechtGoogle Scholar
  82. Rosa M, Hilal M, González JA, Prado FE (2009) Low-temperature effect on enzyme activities involved in sucrose-starch partitioning in salt-stressed and salt-acclimated cotyledons of quinoa (Chenopodium quinoa Willd.) seedlings. Plant Physiol Biochem 47:300–307PubMedGoogle Scholar
  83. Sakai H, Honma T, Aoyama T, Sato S, Kato T, Tabata S, Oka A (2001) ARR1, a transcription factor for genes immediately responsive to cytokinins. Science 294:1519–1521PubMedGoogle Scholar
  84. Shimizu S, Mori H (1998) Analysis of cycles of dormancy and growth in pea axillary buds based on mRNA accumulation patterns of cell cycle-related genes. Plant Cell Physiol 39:255–262PubMedGoogle Scholar
  85. Silverstone AL, Ciampaglio CN, Sun T (1998) The Arabidopsis RGA gene encodes a transcriptional regulator repressing the gibberellin signal transduction pathway. Plant Cell 10:155PubMedPubMedCentralGoogle Scholar
  86. Simons JL, Napoli CA, Janssen BJ, Plummer KM, Snowden KC (2007) Analysis of the decreased apical dominance genes of petunia in the control of axillary branching. Plant Physiol 143:697PubMedPubMedCentralGoogle Scholar
  87. Sorefan K, Booker J, Haurogné K, Goussot M, Bainbridge K, Foo E, Chatfield S, Ward S, Beveridge C, Rameau C (2003) MAX4 and RMS1 are orthologous dioxygenase-like genes that regulate shoot branching in Arabidopsis and pea. Genes Dev 17:1469PubMedPubMedCentralGoogle Scholar
  88. Steiner E, Weiss D (2012) The Arabidopsis O-linked N-acetylglucosamine transferase SPINDLY interacts with class I TCPs to facilitate cytokinin responses in leaves and flowers. Plant Cell 24:96–108PubMedPubMedCentralGoogle Scholar
  89. Taniguchi M, Sasaki N, Tsuge T, Aoyama T, Oka A (2007) ARR1 directly activates cytokinin response genes that encode proteins with diverse regulatory functions. Plant Cell Physiol 48:263–277PubMedGoogle Scholar
  90. Thimann KV, Skoog F (1934) On the inhibition of bud development and other functions of growth substance in Vicia faba. In: Proceedings of the Royal Society of London series B-containing papers of a biological character, vol 114, pp 317–339Google Scholar
  91. Volz RK, Gibbs HM, Popenoe J (1994) Branch induction on apple nursery trees: effects of growth regulators and defoliation. New Zealand J Crop Hortic Sci 22:277–283Google Scholar
  92. Willige BC, Isono E, Richter R, Zourelidou M, Schwechheimer C (2011) Gibberellin regulates pin-formed abundance and is required for auxin transport-dependent growth and development in Arabidopsis thaliana. Plant Cell 23:2184–2195PubMedPubMedCentralGoogle Scholar
  93. Xu R, Sun P, Jia F, Lu L, Li Y, Zhang S, Huang J (2014) Genomewide analysis of TCP transcription factor gene family in Malus domestica. J Genet 93:733–746PubMedGoogle Scholar
  94. Yanai O, Shani E, Dolezal K, Tarkowski P, Sablowski R, Sandberg G, Samach A, Ori N (2005) Arabidopsis KNOXI Proteins Activate Cytokinin Biosynthesis. Current Biology 15(17):1566–1571PubMedGoogle Scholar
  95. Yadav UP, Ivakov A, Feil R, Duan GY, Walther D, Giavalisco P, Piques M, Carillo P, Hubberten HM, Stitt M (2014) The sucrose-trehalose 6-phosphate (Tre6P) nexus: specificity and mechanisms of sucrose signalling by Tre6P. J Exp Bot 65:1051PubMedPubMedCentralGoogle Scholar
  96. Yoneyama K, Xie X, Dai K, Sekimoto H, Sugimoto Y, Takeuchi Y, Yoneyama K (2007) Nitrogen deficiency as well as phosphorus deficiency in sorghum promotes the production and exudation of 5-deoxystrigol, the host recognition signal for arbuscular mycorrhizal fungi and root parasites. Planta 227:125–132PubMedGoogle Scholar
  97. Zawaski C, Busov VB (2014) Roles of gibberellin catabolism and signaling in growth and physiological response to drought and short-day photoperiods in Populus trees. Plos One 9:e86217–e86217PubMedPubMedCentralGoogle Scholar
  98. Zeng XF, Zhao DG (2016) Expression of IPT in Asakura-sanshoo (Zanthoxylum piperitum (L.) DC. f. inerme Makino) alters tree architecture, delays leaf senescence, and changes leaf essential oil composition. Plant Mol Biol Report 34:649–658PubMedGoogle Scholar
  99. Zhang S, Zhang D, Fan S, Du L, Shen Y, Xing L, Li Y, Ma J, Han M (2016) Effect of exogenous GA3 and its inhibitor paclobutrazol on floral formation, endogenous hormones, and flowering-associated genes in ‘Fuji’ apple (Malus domestica Borkh.). Plant Physiol Biochem 107:178–186PubMedGoogle Scholar

Copyright information

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

Authors and Affiliations

  • Ming Tan
    • 1
  • Guofang Li
    • 1
  • Xiaojie Liu
    • 1
  • Fang Cheng
    • 1
  • Juanjuan Ma
    • 1
  • Caiping Zhao
    • 1
  • Dong Zhang
    • 1
  • Mingyu Han
    • 1
    Email author
  1. 1.College of HorticultureNorthwest A & F UniversityYanglingChina

Personalised recommendations