Advertisement

Plant Cell Reports

, Volume 37, Issue 3, pp 425–441 | Cite as

Differential expression of gibberellin- and abscisic acid-related genes implies their roles in the bud activity-dormancy transition of tea plants

  • Chuan Yue
  • Hongli Cao
  • Xinyuan Hao
  • Jianming Zeng
  • Wenjun Qian
  • Yuqiong Guo
  • Naixing Ye
  • Yajun Yang
  • Xinchao Wang
Original Article

Abstract

Key message

Thirty genes involved in GA and ABA metabolism and signalling were identified, and the expression profiles indicated that they play crucial roles in the bud activity-dormancy transition in tea plants.

Abstract

Gibberellin (GA) and abscisic acid (ABA) are fundamental phytohormones that extensively regulate plant growth and development, especially bud dormancy and sprouting transition in perennial plants. However, there is little information on GA- and ABA-related genes and their expression profiles during the activity-dormancy transition in tea plants. In the present study, 30 genes involved in the metabolism and signalling pathways of GA and ABA were first identified, and their expression patterns in different tissues were assessed. Further evaluation of the expression patterns of selected genes in response to GA3 and ABA application showed that CsGA3ox, CsGA20ox, CsGA2ox, CsZEP and CsNCED transcripts were differentially expressed after exogenous treatment. The expression profiles of the studied genes during winter dormancy and spring sprouting were investigated, and somewhat diverse expression patterns were found for GA- and ABA-related genes. This diversity was associated with the bud activity-dormancy cycle of tea plants. These results indicate that the genes involved in the metabolism and signalling of GA and ABA are important for regulating the bud activity-dormancy transition in tea plants.

Keywords

Abscisic acid (ABA) Bud dormancy Gene expression Gibberellins (GA) Tea plant 

Notes

Acknowledgements

This work was supported by the National Natural Science Foundation of China (31370690, 31600555), the Natural Science Foundation of Fujian Province (2017J01616), and the Earmarked Fund for China Agriculture Research System (CARS-19), and the Chinese Academy of Agricultural Sciences through an Innovation Project for Agricultural Sciences and Technology (CAAS-ASTIP-2017-TRICAAS).

Supplementary material

299_2017_2238_MOESM1_ESM.docx (1.6 mb)
Fig. A1 Daily temperatures at the sampling sites and morphological changes in lateral buds on the sampling dates. The average, maximum (Max) and minimum (Min) temperatures from 1 Oct. to 31 Mar. of 2013-14 (a) and 2014–15 (b) were recorded. In 2013–14, buds were collected on 2 Nov. 2013, 1 Dec. 2013, 2 Jan. 2014, 14 Feb. 2014, 3 Mar. 2014 and 27 Mar. 2014; in 2014–15, samples were collected on 4 Nov. 2014, 2 Dec. 2014, 5 Jan. 2015, 5 Feb. 2015, 3 Mar. 2015 and 26 Mar. 2015. The time points at which the samples were taken are indicated by arrows, and the morphological changes in the lateral buds on the sampling dates are shown. Fig. A2 Neighbour-joining phylogeny of tea plant genes encoding proteins involved in GA metabolism and signalling pathways and those of other plants. a, ent-kaurene synthase (KS); b, ent-kaurene oxidase (KO); c, ent-kaurene acid oxidase; d, gibberellin 20 oxidase (GA20ox); e, gibberellin 3-oxidase (GA3ox); f, gibberellin 2-oxidase (GA2ox); g, gibberellin receptor (GID1s); h, DELLA proteins (DELLAs). Fig. A3 Neighbour-joining phylogeny of tea plant genes encoding proteins involved in ABA metabolism and signalling pathways and those of other plants. a, zeaxanthin epoxidase (ZEP); b, 9-cis-epoxycarotenoid dioxygenase (NCED); c, short-chain dehydrogenase/reductase (SDR); d, abscisic aldehyde oxidase (AAO); e, ABA 8′-hydroxylase (CYP707A); f, pyrabactin resistance-like proteins (PYLs); g, protein phosphatase 2Cs (PP2Cs). Table A1 Primers used in qRT-PCR analysis (DOCX 1628 KB)

References

  1. Achard P, Vriezen WH, Van Der Straeten D, Harberd NP (2003) Ethylene regulates Arabidopsis development via the modulation of DELLA protein growth repressor function. Plant Cell 15:2816–2825CrossRefPubMedPubMedCentralGoogle Scholar
  2. Antoni R, Rodriguez L, Gonzalez-Guzman M, Pizzio GA, Rodriguez PL (2011) News on ABA transport, protein degradation, and ABFs/WRKYs in ABA signaling. Curr Opin Plant Biol 14:547–553CrossRefPubMedGoogle Scholar
  3. Barros PM, Goncalves N, Saibo NJ, Oliveira MM (2012) Cold acclimation and floral development in almond bud break: insights into the regulatory pathways. J Exp Bot 63:4585–4596CrossRefPubMedGoogle Scholar
  4. Barua DN (1969) Seasonal dormancy in tea (Camellia sinensis L.). Nature 224:514–514CrossRefGoogle Scholar
  5. Bomke C, Rojas MC, Gong F, Hedden P, Tudzynski B (2008) Isolation and characterization of the gibberellin biosynthetic gene cluster in Sphaceloma manihoticola. Appl Environ Microbiol 74:5325–5339CrossRefPubMedPubMedCentralGoogle Scholar
  6. Boursiac Y, Leran S, Corratge-Faillie C, Gojon A, Krouk G, Lacombe B (2013) ABA transport and transporters. Trends Plant Sci 18:325–333CrossRefPubMedGoogle Scholar
  7. Carles CC, Fletcher JC (2003) Shoot apical meristem maintenance: the art of a dynamic balance. Trends plant Sci 8:394–401CrossRefPubMedGoogle Scholar
  8. Carrera E, Jackson SD, Prat S (1999) Feedback control and diurnal regulation of gibberellin 20-oxidase transcript levels in potato. Plant Physiol 119:765–774CrossRefPubMedPubMedCentralGoogle Scholar
  9. Choubane et al (2012) Photocontrol of bud burst involves gibberellin biosynthesis in Rosa sp. J Plant Physiol 13:1271–1280CrossRefGoogle Scholar
  10. Cooke JE, Eriksson ME, Junttila O (2012) The dynamic nature of bud dormancy in trees: environmental control and molecular mechanisms. Plant Cell Environ 35:1707–1728CrossRefPubMedGoogle Scholar
  11. de Lucas M et al (2008) A molecular framework for light and gibberellin control of cell elongation. Nature 451:480–484CrossRefPubMedGoogle Scholar
  12. Druart N et al (2007) Environmental and hormonal regulation of the activity-dormancy cycle in the cambial meristem involves stage-specific modulation of transcriptional and metabolic networks. Plant J 50:557–573CrossRefPubMedGoogle Scholar
  13. Du Q, Li C, Li D, Lu S (2015) Genome-wide analysis, molecular cloning and expression profiling reveal tissue-specifically expressed, feedback-regulated, stress-responsive and alternatively spliced novel genes involved in gibberellin metabolism in Salvia miltiorrhiza. BMC Genom 16:1087CrossRefGoogle Scholar
  14. Finkelstein R (2013) Abscisic acid synthesis and response. Arabidopsis book 11:e0166CrossRefPubMedPubMedCentralGoogle Scholar
  15. Gallego-Giraldo C, Hu J, Urbez C, Gomez MD, Sun TP, Perez-Amador MA (2014) Role of the gibberellin receptors GID1 during fruit-set in Arabidopsis. Plant J 79:1020–1032CrossRefPubMedPubMedCentralGoogle Scholar
  16. Gao Y, Chen J, Zhao Y, Li T, Wang M (2012) Molecular cloning and expression analysis of a RGA-like gene responsive to plant hormones in Brassica napus. Mol Biol Rep 39:1957–1962CrossRefPubMedGoogle Scholar
  17. Golldack D, Li C, Mohan H, Probst N (2013) Gibberellins and abscisic acid signal crosstalk: living and developing under unfavorable conditions. Plant Cell Rep 32:1007–1016CrossRefPubMedGoogle Scholar
  18. Griffiths J et al (2006) Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis. Plant Cell 18:3399–3414CrossRefPubMedPubMedCentralGoogle Scholar
  19. Hansen E, Olsen JE, Junttila O (1999) Gibberellins and subapical cell divisions in relation to bud set and bud break in Salix pentandra. J Plant Growth Regul 18:167–170CrossRefPubMedGoogle Scholar
  20. Hao X, Horvath D, Chao W, Yang Y, Wang X, Xiao B (2014) Identification and evaluation of reliable reference genes for quantitative real-time PCR analysis in tea plant (Camellia sinensis (L.) O. Kuntze). Int J Mol Sci 15:22155–22172CrossRefPubMedPubMedCentralGoogle Scholar
  21. Hao X, Yang Y, Yue C, Wang L, Horvath DP, Wang X (2017) Comprehensive transcriptome analyses reveal differential gene expression profiles of Camellia sinensis axillary buds at para-, endo-, ecodormancy, and bud flush stages. Front Plant Sci 8:553PubMedPubMedCentralGoogle Scholar
  22. Horvath DP, Anderson JV, Chao WS, Foley ME (2003) Knowing when to grow: signals regulating bud dormancy. Trends Plant Sci 8:534–540CrossRefPubMedGoogle Scholar
  23. Huang Y, Yang W, Pei Z, Guo X, Liu D, Sun J, Zhang A (2012) The genes for gibberellin biosynthesis in wheat. Funct Integr Genom 12:199–206CrossRefGoogle Scholar
  24. Huerta L, Garcia-Lor A, Garcia-Martinez JL (2009) Characterization of gibberellin 20-oxidases in the citrus hybrid Carrizo citrange. Tree Physiol 29:569–577CrossRefPubMedGoogle Scholar
  25. Jeyaraj A, Chandran V, Gajjeraman P (2014) Differential expression of microRNAs in dormant bud of tea [Camellia sinensis (L.) O. Kuntze]. Plant Cell Rep 33:1053–1069CrossRefPubMedGoogle Scholar
  26. Jiang C, Fu X (2007) GA action: turning on de-DELLA repressing signaling. Curr Opin Plant Biol 10:461–465CrossRefPubMedGoogle Scholar
  27. Kakkar RK, Nagar PK (1997) Distribution and changes in endogenous polyamines during winter dormancy in tea [Camellia sinensis L. (O) Kuntze]. J Plant Physiol 151:63–67CrossRefGoogle Scholar
  28. Kaneko M, Itoh H, Inukai Y, Sakamoto T, Ueguchi-Tanaka M, Ashikari M, Matsuoka M (2003) Where do gibberellin biosynthesis and gibberellin signaling occur in rice plants? Plant J 35:104–115CrossRefPubMedGoogle Scholar
  29. Khalil-Ur-Rehman M, Sun L, Li CX, Faheem M, Wang W, Tao JM (2017) Comparative RNA-seq based transcriptomic analysis of bud dormancy in grape. BMC Plant Biol 17:18CrossRefPubMedPubMedCentralGoogle Scholar
  30. Krishnaraj T, Gajjeraman P, Palanisamy S, Subhas Chandrabose SR, Azad Mandal AK (2011) Identification of differentially expressed genes in dormant (banjhi) bud of tea (Camellia sinensis (L.) O. Kuntze) using subtractive hybridization approach. Plant Physiol Biochem 49:565–571CrossRefPubMedGoogle Scholar
  31. Lefebvre V et al (2006) Functional analysis of Arabidopsis NCED6 and NCED9 genes indicates that ABA synthesized in the endosperm is involved in the induction of seed dormancy. Plant J 45:309–319CrossRefPubMedGoogle Scholar
  32. Li C, Junttila O, Heino P, Palva ET (2003) Different responses of northern and southern ecotypes of Betula pendula to exogenous ABA application. Tree Physiol 23:481–487CrossRefPubMedGoogle Scholar
  33. Li A, Yang W, Li S, Liu D, Guo X, Sun J, Zhang A (2013) Molecular characterization of three GIBBERELLIN-INSENSITIVE DWARF1 homologous genes in hexaploid wheat. J Plant Physiol 170:432–443CrossRefPubMedGoogle Scholar
  34. Li L et al (2015) Transcriptomic insights into antagonistic effects of gibberellin and abscisic acid on petal growth in Gerbera hybrida. Front Plant Sci 6:168PubMedPubMedCentralGoogle Scholar
  35. Liu B et al (2016) Silencing of the gibberellin receptor homolog, CsGID1a, affects locule formation in cucumber (Cucumis sativus) fruit. New Phytol 210:551–563CrossRefPubMedGoogle Scholar
  36. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 – ∆∆CT method. Methods 25:402–408CrossRefPubMedGoogle Scholar
  37. Lou Y, Sun H, Li L, Zhao H, Gao Z (2017) Characterization and primary functional analysis of a Bamboo ZEP Gene from Phyllostachys edulis. DNA Cell Biol.  https://doi.org/10.1089/dna.2017.3705 PubMedGoogle Scholar
  38. Martinez-Andujar C, Ordiz MI, Huang Z, Nonogaki M, Beachy RN, Nonogaki H (2011) Induction of 9-cis-epoxycarotenoid dioxygenase in Arabidopsis thaliana seeds enhances seed dormancy. PNAS 108:17225–17229CrossRefPubMedPubMedCentralGoogle Scholar
  39. Meier AR, Saunders MR, Michler CH (2012) Epicormic buds in trees: a review of bud establishment, development and dormancy release. Tree Physiol 32:565–584CrossRefPubMedGoogle Scholar
  40. Merilo E, Jalakas P, Laanemets K, Mohammadi O, Horak H, Kollist H, Brosche M (2015) Abscisic acid transport and homeostasis in the context of stomatal regulation. Mol Plant 8:1321–1333CrossRefPubMedGoogle Scholar
  41. Mitchum MG et al (2006) Distinct and overlapping roles of two gibberellin 3-oxidases in Arabidopsis development. Plant J 45:804–818CrossRefPubMedGoogle Scholar
  42. Muniz Garcia MN, Stritzler M, Capiati DA (2014) Heterologous expression of Arabidopsis ABF4 gene in potato enhances tuberization through ABA-GA crosstalk regulation. Planta 239:615–631CrossRefPubMedGoogle Scholar
  43. Murase K, Hirano Y, Sun TP, Hakoshima T (2008) Gibberellin-induced DELLA recognition by the gibberellin receptor GID1. Nature 456:459–463CrossRefPubMedGoogle Scholar
  44. Nagar PK, Kumar A (2000) Changes in endogenous gibberellin activity during winter dormancy in tea (Camellia sinensis (L.) O. Kuntze). Acta Physiol Plant 22:439–443CrossRefGoogle Scholar
  45. Nagar PK, Sood S (2006) Changes in endogenous auxins during winter dormancy in tea (Camellia sinensis L.) O. Kuntze. Acta Physiol Plant 28:165–169CrossRefGoogle Scholar
  46. Nonogaki M, Nonogaki H (2017) Prevention of preharvest sprouting through hormone engineering and germination recovery by chemical biology. Front Plant Sci 8:90PubMedPubMedCentralGoogle Scholar
  47. Nonogaki M, Sall K, Nambara E, Nonogaki H (2014) Amplification of ABA biosynthesis and signaling through a positive feedback mechanism in seeds. Plant J 78:527–539CrossRefPubMedGoogle Scholar
  48. O’Neill DP et al (2010) Regulation of the gibberellin pathway by auxin and DELLA proteins. Planta 232:1141–1149CrossRefPubMedGoogle Scholar
  49. Olsen JE (2010) Light and temperature sensing and signaling in induction of bud dormancy in woody plants. Plant Mol Biol 73:37–47CrossRefPubMedGoogle Scholar
  50. Parada F, Noriega X, Dantas D, Bressan-Smith R, Perez FJ (2016) Differences in respiration between dormant and non-dormant buds suggest the involvement of ABA in the development of endodormancy in grapevines. J Plant Physiol 201:71–78CrossRefPubMedGoogle Scholar
  51. Paul A, Kumar S (2011) Responses to winter dormancy, temperature, and plant hormones share gene networks. Funct Integr Genom 11:659–664CrossRefGoogle Scholar
  52. Paul A, Jha A, Bhardwaj S, Singh S, Shankar R, Kumar S (2014) RNA-seq-mediated transcriptome analysis of actively growing and winter dormant shoots identifies non-deciduous habit of evergreen tree tea during winters. Sci Rep 4:5932CrossRefPubMedPubMedCentralGoogle Scholar
  53. Pearce S et al (2015) Heterologous expression and transcript analysis of gibberellin biosynthetic genes of grasses reveals novel functionality in the GA3ox family. BMC Plant Biol 15:130CrossRefPubMedPubMedCentralGoogle Scholar
  54. Ravindran P, Verma V, Stamm P, Kumar P (2017) A novel RGL2–DOF6 complex contributes to primary seed dormancy in Arabidopsis thaliana by regulating a GATA transcription factor. Mol Plant 10:1307–1320CrossRefPubMedGoogle Scholar
  55. Regnault T, Daviere JM, Heintz D, Lange T, Achard P (2014) The gibberellin biosynthetic genes AtKAO1 and AtKAO2 have overlapping roles throughout Arabidopsis development. Plant J 80:462–474CrossRefPubMedGoogle Scholar
  56. Rohde A, Bhalerao RP (2007) Plant dormancy in the perennial context. Trends Plant Sci 12:217–223CrossRefPubMedGoogle Scholar
  57. Roumeliotis E, Kloosterman B, Oortwijn M, Lange T, Visser RG, Bachem CW (2013) Down regulation of StGA3ox genes in potato results in altered GA content and affect plant and tuber growth characteristics. J Plant Physiol 170:1228–1234CrossRefPubMedGoogle Scholar
  58. Ruttink T et al (2007) A molecular timetable for apical bud formation and dormancy induction in poplar. Plant Cell 19:2370–2390CrossRefPubMedPubMedCentralGoogle Scholar
  59. Saito S, Hirai N, Matsumoto C, Ohigashi H, Ohta D, Sakata K, Mizutani M (2004) Arabidopsis CYP707As encode (+)-abscisic acid 8′-hydroxylase, a key enzyme in the oxidative catabolism of abscisic acid. Plant Physiol 134:1439–1449CrossRefPubMedPubMedCentralGoogle Scholar
  60. Schwarz N, Armbruster U, Iven T, Bruckle L, Melzer M, Feussner I, Jahns P (2015) Tissue-specific accumulation and regulation of zeaxanthin epoxidase in Arabidopsis reflect the multiple functions of the enzyme in plastids. Plant Cell Physiol 56:346–357CrossRefPubMedGoogle Scholar
  61. Seo M, Kanno Y, Frey A, North HM, Marion-Poll A (2016) Dissection of Arabidopsis NCED9 promoter regulatory regions reveals a role for ABA synthesized in embryos in the regulation of GA-dependent seed germination. Plant Sci 246:91–97CrossRefPubMedGoogle Scholar
  62. Shen Q, Cui J, Fu XQ, Yan TX, Tang KX (2015) Cloning and characterization of DELLA genes in Artemisia annua. Genet Mol Res 14:10037–10049CrossRefPubMedGoogle Scholar
  63. Shu K et al (2013) ABI4 regulates primary seed dormancy by regulating the biogenesis of abscisic acid and gibberellins in arabidopsis. PLoS Genet 9:e1003577CrossRefPubMedPubMedCentralGoogle Scholar
  64. Shu K et al (2016) ABI4 mediates antagonistic effects of abscisic acid and gibberellins at transcript and protein levels. Plant J 85:348–361CrossRefPubMedGoogle Scholar
  65. Tan BC, Joseph LM, Deng WT, Liu L, Li QB, Cline K, McCarty DR (2003) Molecular characterization of the Arabidopsis 9-cis epoxycarotenoid dioxygenase gene family. Plant J 35:44–56CrossRefPubMedGoogle Scholar
  66. Tanino KK (2004) Hormones and endodormancy induction in woody plants. J Crop Improv 10:157–199CrossRefGoogle Scholar
  67. Tanino KK, Kalcsits L, Silim S, Kendall E, Gray GR (2010) Temperature-driven plasticity in growth cessation and dormancy development in deciduous woody plants: a working hypothesis suggesting how molecular and cellular function is affected by temperature during dormancy induction. Plant Mol Biol 73:49–65CrossRefPubMedGoogle Scholar
  68. Thirugnanasambantham K, Prabu G, Palanisamy S, Chandrabose SR, Mandal AK (2013) Analysis of dormant bud (Banjhi) specific transcriptome of tea [Camellia sinensis (L.) O. Kuntze] from cDNA library revealed dormancy-related genes. App Bioch Biotech 169:1405–1417CrossRefGoogle Scholar
  69. Thomas SG, Phillips AL, Hedden P (1999) Molecular cloning and functional expression of gibberellin 2-oxidases, multifunctional enzymes involved in gibberellin deactivation. PNAS 96:4698–4703CrossRefPubMedPubMedCentralGoogle Scholar
  70. Tuan PA, Bai S, Saito T, Ito A, Moriguchi T (2017) Dormancy-associated MADS-box (DAM) and abscisic acid pathway regulate pear endodormancy through a feedback mechanism. Plant Cell Physiol.  https://doi.org/10.1093/pcp/pcx074 PubMedGoogle Scholar
  71. Ueguchi-Tanaka M et al (2005) GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature 437:693–698CrossRefPubMedGoogle Scholar
  72. Ueguchi-Tanaka M, Nakajima M, Motoyuki A, Matsuoka M (2007) Gibberellin receptor and its role in gibberellin signaling in plants. Annu Rev Plant Biol 58:183–198CrossRefPubMedGoogle Scholar
  73. Umezawa T, Nakashima K, Miyakawa T, Kuromori T, Tanokura M, Shinozaki K, Yamaguchi-Shinozaki K (2010) Molecular basis of the core regulatory network in ABA responses: sensing, signaling and transport. Plant Cell Physiol 51:1821–1839CrossRefPubMedPubMedCentralGoogle Scholar
  74. Vergara R, Noriega X, Aravena K, Prieto H, PÉREZ FC (2017) ABA represses the expression of cell cycle genes and may modulate the development of endodormancy in grapevine buds. Front Plant Sci, 8: 812CrossRefPubMedPubMedCentralGoogle Scholar
  75. Voegele A, Linkies A, Muller K, Leubner-Metzger G (2011) Members of the gibberellin receptor gene family GID1 (GIBBERELLIN INSENSITIVE DWARF1) play distinct roles during Lepidium sativum and Arabidopsis thaliana seed germination. J Exp Bot 62:5131–5147CrossRefPubMedPubMedCentralGoogle Scholar
  76. Vyas D, Kumar S, Ahuja PS (2007) Tea (Camellia sinensis) clones with shorter periods of winter dormancy exhibit lower accumulation of reactive oxygen species. Tree Physiol 27:1253–1259CrossRefPubMedGoogle Scholar
  77. Wang F, Deng X (2011) Plant ubiquitin-proteasome pathway and its role in gibberellin signaling. Cell Res 6:1286–1294CrossRefGoogle Scholar
  78. Wang X, Wang Z, Dong J, Wang M, Gao H (2009) Cloning of a 9-cis-epoxycarotenoid dioxygenase gene and the responses of Caragana korshinskii to a variety of abiotic stresses. Gene Genet Syst 84:397–405CrossRefGoogle Scholar
  79. Wang X et al (2014) Identification of differential gene expression profiles between winter dormant and sprouting axillary buds in tea plant (Camellia sinensis) by suppression subtractive hybridization. Tree Genet Genom 10:1149–1159CrossRefGoogle Scholar
  80. Wang D et al (2015) Expression of ABA metabolism-related genes suggests similarities and differences between seed dormancy and bud dormancy of peach (Prunus persica). Front Plant Sci 6:1248PubMedGoogle Scholar
  81. Xia EH et al (2017) The tea tree genome provides insights into tea flavor and independent evolution of caffeine biosynthesis. Mol Plant 10:866–877CrossRefPubMedGoogle Scholar
  82. Xiao YH et al (2010) Gibberellin 20-oxidase promotes initiation and elongation of cotton fibers by regulating gibberellin synthesis. J Plant Physiol 167:829–837CrossRefPubMedGoogle Scholar
  83. Xue T et al (2008) Genome-wide and expression analysis of protein phosphatase 2C in rice and Arabidopsis. BMC Genom 9:550CrossRefGoogle Scholar
  84. Yamaguchi S (2008) Gibberellin metabolism and its regulation. Annu Rev Plant Biol 59:225–251CrossRefPubMedGoogle Scholar
  85. Yamaguchi S, Kamiya Y, Sun T (2001) Distinct cell-specific expression patterns of early and late gibberellin biosynthetic genes during Arabidopsis seed germination. Plant J 28:443–453CrossRefPubMedGoogle Scholar
  86. Yang C, Liu J, Dong X, Cai Z, Tian W, Wang X (2014) Short-term and continuing stresses differentially interplay with multiple hormones to regulate plant survival and growth. Mol Plant 7:841–855CrossRefPubMedGoogle Scholar
  87. Yano K, Aya K, Hirano K, Ordonio RL, Ueguchi-Tanaka M, Matsuoka M (2015) Comprehensive gene expression analysis of rice aleurone cells: probing the existence of an alternative gibberellin receptor. Plant Physiol 167:531–544CrossRefPubMedGoogle Scholar
  88. Ye H et al (2015) Map-based cloning of seed dormancy1–2 identified a gibberellin synthesis gene regulating the development of endosperm-imposed dormancy in rice. Plant Physiol 169:2152–2165PubMedPubMedCentralGoogle Scholar
  89. Yue C et al (2014) Molecular cloning and expression analysis of tea plant aquaporin (AQP) gene family. Plant Physiol Biochem 83:65–76CrossRefPubMedGoogle Scholar
  90. Zentella R et al (2007) Global analysis of della direct targets in early gibberellin signaling in Arabidopsis. Plant Cell 19:3037–3057CrossRefPubMedPubMedCentralGoogle Scholar
  91. Zhang Z et al (2016) MsZEP, a novel zeaxanthin epoxidase gene from alfalfa (Medicago sativa), confers drought and salt tolerance in transgenic tobacco. Plant Cell Rep 35:439–453CrossRefPubMedGoogle Scholar
  92. Zheng C, Halaly T, Acheampong AK, Takebayashi Y, Jikumaru Y, Kamiya Y, Or E (2015) Abscisic acid (ABA) regulates grape bud dormancy, and dormancy release stimuli may act through modification of ABA metabolism. J Exp Bot 66:1527–1542CrossRefPubMedPubMedCentralGoogle Scholar
  93. Zhuang W, Gao Z, Wang L, Zhong W, Ni Z, Zhang Z (2013) Comparative proteomic and transcriptomic approaches to address the active role of GA4 in Japanese apricot flower bud dormancy release. J Exp Bot 64:4953–4966CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  1. 1.College of Horticulture, Key Laboratory of Tea Science in Universities of Fujian ProvinceFujian Agriculture and Forestry UniversityFuzhouChina
  2. 2.Tea Research Institute of the Chinese Academy of Agricultural Sciences, National Center for Tea Improvement, Key Laboratory of Tea Biology and Resources UtilizationMinistry of AgricultureHangzhouChina

Personalised recommendations