Skip to main content
SpringerLink
Log in

Gene Characterization and Expression Analysis Reveal the Importance of Auxin Signaling in Bud Dormancy Regulation in Tea Plant

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

The tea plant is an economically important woody plant whose raw leaves are used for tea production. Winter bud dormancy is not only a useful biological strategy for tea plant survival but also a biological event that affects the economics of tea production. Based on our previous transcriptome analysis of axillary buds in different dormancy states, we reanalyzed a large number of differentially expressed auxin-related genes and determined the relative importance of the roles of auxin signaling in bud dormancy regulation in tea plant. Subsequently, we cloned the full-length cDNA sequence of several auxin-related genes in the AUX/LAX, PIN/PILS, AUX/IAA, GH3, and SAUR gene families, characterized these genes and performed a phylogenetic analysis, and conserved motif search using the sequences of their encoded proteins. Expression profile analyses, including tissue-specific expression and time-course expression during the active-dormant-active status transitions of overwinter buds, were carried out, combined with IAA content detection. Generally, the expression patterns of auxin-related genes were consistent with the IAA content changes in buds and their active-dormant status transition. In particular, we confirmed the crucial roles of the auxin transport gene CsLAX2 and the early auxin response genes CsGH3.6, CsGH3.9, CsGH3.10, CsIAA26, CsIAA33, CsSAUR50, and CsSAUR41 in bud dormancy regulation in tea plant. Our results validate the important role of auxin in tea plant dormancy regulation and provide useful information for further functional studies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Aloni R, Peterson CA (1997) Auxin promotes dormancy callose removal from the phloem of Magnolia kobus and callose accumulation and earlywood vessel differentiation in Quercus robur. J Plant Res 110:37–44

    Article  CAS  PubMed  Google Scholar 

  • Anderson JV, Chao WS, Horvath DP (2001) Review: a current review on the regulation of dormancy in vegetative buds. Weed Sci 49:581–589

    Article  CAS  Google Scholar 

  • Baba K, Karlberg A, Schmidt J, Schrader J, Hvidsten TR, Bako L, Bhalerao RP (2011) Activity-dormancy transition in the cambial meristem involves stage-specific modulation of auxin response in hybrid aspen. Proc Natl Acad Sci USA 108:3418–3423

    Article  PubMed  PubMed Central  Google Scholar 

  • Barua DN (1969) Seasonal dormancy in tea (Camellia sinensis L.). Nature 224:514

    Article  CAS  Google Scholar 

  • Bemer M, van Mourik H, Muino JM, Ferrandiz C, Kaufmann K, Angenent GC (2017) FRUITFULL controls SAUR10 expression and regulates Arabidopsis growth and architecture. J Exp Bot. https://doi.org/10.1093/jxb/erx184

    Article  PubMed  PubMed Central  Google Scholar 

  • Beziat C, Barbez E, Feraru MI, Lucyshyn D, Kleine-Vehn J (2017) Light triggers PILS-dependent reduction in nuclear auxin signalling for growth transition. Nat Plants 3:17105. https://doi.org/10.1038/nplants.2017.105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chao WS, Doğramac M, Horvath DP, Anderson JV, Foley ME (2017) Comparison of phytohormone levels and transcript profiles during seasonal dormancy transitions in underground adventitious buds of leafy spurge. Plant Mol Biol 94:281–302

    Article  CAS  PubMed  Google Scholar 

  • Chen Y, Hao X, Cao J (2014) Small auxin upregulated RNA (SAUR) gene family in maize: identification, evolution, and its phylogenetic comparison with Arabidopsis, rice, and sorghhum. J Integr Plant Biol 56:133–150

    Article  CAS  PubMed  Google Scholar 

  • Cooke JEK, Eriksson ME, Junttila O (2012) The dynamic nature of bud dormancy in trees: environmental control and molecular mechanisms. Plant Cell Environ 35:1707–1728

    Article  CAS  PubMed  Google Scholar 

  • Dal Bosco C, Dovzhenko A, Liu X, Woerner N, Rensch T, Eismann M, Eimer S, Hegermann J, Paponov IA, Ruperti B, Heberle-Bors E, Touraev A, Cohen JD, Palme K (2012) The endoplasmic reticulum localized PIN8 is a pollen-specific auxin carrier involved in intracellular auxin homeostasis. Plant J 71:860–870

    Article  CAS  PubMed  Google Scholar 

  • Fu J, Chu J, Sun X, Wang J, Yan C (2012) Simple, rapid, and simultaneous assay of multiple carboxyl containing phytohormones in wounded tomatoes by UPLC-MS/MS using single SPE purification and isotope dilution. Anal Sci 28:1081–1087

    Article  CAS  PubMed  Google Scholar 

  • Grunewald W, Friml J (2010) The march of the PINs: developmental plasticity by dynamic polar targeting in plant cells. EMBO J 29:2700–2714

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hao X, Li L, Hu Y, Zhou C, Wang X, Wang L, Zeng J, Yang Y (2016) Transcriptomic analysis of the effects of three different light treatments on the biosynthesis of characteristic compounds in the tea plant by RNA-SEq. Tree Genet Genomes 12:118

    Article  Google Scholar 

  • 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 8:553

    PubMed  PubMed Central  Google Scholar 

  • He D, Mathiason K, Fennell A (2012) Auxin and cytokinin related gene expression during active shoot growth and latent bud paradormancy in Vitis riparia grapevine. J Plant Physiol 169:643–648

    Article  CAS  PubMed  Google Scholar 

  • Howe GT, Horvath DP, Dharmawardhana P, Priest HD, Mockler TC, Strauss SH (2015) Extensive transcriptome changes during natural onset and release of vegetative bud dormancy in Populus. Front Plant Sci 6:989

    Article  PubMed  PubMed Central  Google Scholar 

  • Huang CK, Lo PC, Huang LF, Wu SJ, Yeh CH, Lu CA (2015) A single-repeat MYB transcription repressor, MYBH, participates in regulation of leaf senescence in Arabidopsis. Plant Mol Biol 88:269–286

    Article  CAS  PubMed  Google Scholar 

  • Jain M, Kaur N, Garg R, Thakur JK, Tyagi AK, Khurana JP (2006a) Structure and expression analysis of early auxin-responsive Aux/IAA gene family in rice (Oryza sativa). Funct Integr Genomics 6:47–59

    Article  CAS  PubMed  Google Scholar 

  • Jain M, Tyagi AK, Khurana JP (2006b) Genome-wide analysis, evolutionary expansion, and expression of early auxin-responsive SAUR gene family in rice (Oryza sativa). Genomics 88:360–371

    Article  CAS  PubMed  Google Scholar 

  • Kant S, Bi YM, Zhu T, Rothstein SJ (2009) SAUR39, a small auxin-up RNA gene, acts as a negative regulator of auxin synthesis and transport in Rice. Plant Physiol 151:691–701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kebrom TH, Burson BL, Finlayson SA (2006) Phytochrome B represses teosinte branched 1 expression and induces sorghum axillary bud outgrowth in response to light signals. Plant Physiol 140:1109–1117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kebrom TH, Chandler PM, Swain SM, King RW, Richards RA, Spielmeyer W (2012) Inhibition of tiller bud outgrowth in the tin mutant of wheat is associated with precocious intermode development. Plant Physiol 160:308–318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khan S, Stone JM (2007) Arabidopsis thaliana GH3.9 in auxin and jasmonate cross talk. Plant Signal Behav 2:483–485

    Article  PubMed  PubMed Central  Google Scholar 

  • Kong Y, Zhu Y, Gao C, She W, Lin W, Chen Y, Han N, Bian H, Zhu M, Wang J (2013) Tissue-specific expression of SMALL AUXIN UP RNA41 differentially regulates cell expansion and root meristem patterning in Arabidopsis. Plant Cell Physiol 54:609–621

    Article  CAS  PubMed  Google Scholar 

  • Lavy M, Estelle M (2016) Mechanisms of auxin signaling. Development 143:3226–3229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lavy M, Prigge MJ, Tao S, Shain S, Kuo A, Kirchsteiger K, Estelle M (2016) Constitutive auxin response in Physcomitrella reveals complex interactions between Aux/IAA and ARF proteins. Elife. https://doi.org/10.7554/eLife.13325

    Article  PubMed  PubMed Central  Google Scholar 

  • McWatters HG, Devlin PF (2011) Timing in plants-A rhythmic arrangement. FEBS Lett 585:1474–1484

    Article  CAS  PubMed  Google Scholar 

  • Mravec J, Skupa P, Bailly A, Hoyerova K, Krecek P, Bielach A, Petrasek J, Zhang J, Gaykova V, Stierhof YD, Dobrev PI, Schwarzerova K, Rolcik J, Seifertova D, Luschnig C, Benkova E, Zazimalova E, Geisler M, Friml J (2009) Subcellular homeostasis of phytohormone auxin is mediated by the ER-localized PIN5 transporter. Nature 459:1136–1140

    Article  CAS  PubMed  Google Scholar 

  • Nagar PK (1996) Changes in endogenous abscisic acid and phenols during winter dormancy in tea (Camellia sinesis L.(O) Kunze). Acta Physiol Plant 18:33–38

    CAS  Google Scholar 

  • Nagar PK, Kumar A (2000) Changes in endogenous gibberellin activity during winter dormancy in tea (Camellia sinensis (L.) O. Kuntze). Acta Physiol Plant 22:439–443

    Article  CAS  Google Scholar 

  • Nagar P, Sood S (2006) Changes in endogenous auxins during winter dormancy in tea (Camellia sinensis L.) O. Kuntze. Acta Physiol Plant 28:165–169

    Article  CAS  Google Scholar 

  • Nilsson J, Karlberg A, Antti H, Lopez-Vernaza M, Mellerowicz E, Perrot-Rechenmann C, Sandberg G, Bhalerao RP (2008) Dissecting the molecular basis of the regulation of wood formation by auxin in hybrid aspen. Plant Cell 20:843–855

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paul A, Kumar S (2011) Responses to winter dormancy, temperature, and plant hormones share gene networks. Funct Integr Genomics 11:659–664

    Article  CAS  PubMed  Google Scholar 

  • Peret B, Swarup K, Ferguson A, Seth M, Yang Y, Dhondt S, James N, Casimiro I, Perry P, Syed A, Yang H, Reemmer J, Venison E, Howells C, Perez-Amador MA, Yun J, Alonso J, Beemster GT, Laplaze L, Murphy A, Bennett MJ, Nielsen E, Swarup R (2012) AUX/LAX genes encode a family of auxin influx transporters that perform distinct functions during Arabidopsis development. Plant Cell 24:2874–2885

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ren H, Gray WM (2015) SAUR Proteins as effectors of hormonal and environmental signals in plant growth. Mol Plant 8:1153–1164

    Article  CAS  PubMed  Google Scholar 

  • Rinne PLH, Paul LK, Vahala J, Ruonala R, Kangasjärvi J, van der Schoot C (2015) Long and short photoperiod buds in hybrid aspen share structural development and expression patterns of marker genes. J Exp Bot 66:6745–6760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruttink T, Arend M, Morreel K, Storme V, Rombauts S, Fromm J, Bhalerao RP, Boerjan W, Rohde A (2007) A molecular timetable for apical bud formation and dormancy induction in poplar. Plant Cell 19:2370–2390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh RK, Svystun T, AlDahmash B, Jonsson AM, Bhalerao RP (2017) Photoperiod- and temperature-mediated control of phenology in trees—a molecular perspective. New Phytol 213:511–524

    Article  CAS  PubMed  Google Scholar 

  • Stafstrom JP, Ripley BD, Devitt ML, Drake B (1998) Dormancy-associated gene expression in pea axillary buds. Plants 205:547–552

    Article  CAS  Google Scholar 

  • Staswick PE, Serban B, Rowe M, Tiryaki I, Maldonado MT, Maldonado MC, Suza W (2005) Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell 17:616–627

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun N, Wang J, Gao Z, Dong J, He H, Terzaghi W, Wei N, Deng XW, Chen H (2016) Arabidopsis SAURs are critical for differential light regulation of the development of various organs. Proc Natl Acad Sci USA 113:6071–6076

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang H, Hao XY, Wang L, Xiao B, Wang XC, Yang YJ (2017) Molecular regulation and substance exchange dynamics at dormancy and budbreak stages in overwintering buds of tea plant. Acta Agron Sin 43:669–677

    Article  Google Scholar 

  • Terol J, Domingo C, Talon M (2006) The GH3 family in plants: genome wide analysis in rice and evolutionary history based on EST analysis. Gene 371:279–290

    Article  CAS  PubMed  Google Scholar 

  • Ueno S, Klopp C, Leple JC, Derory J, Noirot C, Leger V, Prince E, Kremer A, Plomion C, Provost GL (2013) Transcriptional profiling of bud dormancy induction and release in oak by next-generation sequencing. BMC Genomics 14:236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang X, Hao X, Ma C, Cao H, Yue C, Wang L, Zeng J, Yang Y (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 Genomes 10:1149–1159

    Article  Google Scholar 

  • Weijers D, Friml J (2009) SnapShot: auxin signaling and transport. Cell 136:1172

    Article  CAS  PubMed  Google Scholar 

  • Xu YX, Xiao MZ, Liu Y, Fu JL, He Y, Jiang DA (2017) The small auxin-up RNA OsSAUR45 affects auxin synthesis and transport in rice. Plant Mol Biol 94:97–107

    Article  CAS  PubMed  Google Scholar 

  • Yang J, Yuan Z, Meng Q, Huang G, Perin C, Bureau C, Meunier AC, Ingouff M, Bennett MJ, Liang W, Zhang D (2017) Dynamic regulation of auxin response during rice development revealed by newly established hormone biosensor markers. Front Plant Sci 8:256

    PubMed  PubMed Central  Google Scholar 

  • Yuan H, Zhao K, Lei H, Shen X, Liu Y, Liao X, Li T (2013) Genome-wide analysis of the GH3 family in apple (Malus x domestica). BMC Genomics 14:297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the Zhejiang Provincial Natural Science Foundation (LY16C160001), the National Natural Science Foundation of China (31370690, 31600563), the Earmarked Fund for China Agriculture Research System (CARS-19), the Chinese Academy of Agricultural Sciences through an Innovation Project for Agricultural Sciences and Technology (CAAS-ASTIP-2017-TRICAAS), and CAS Key Technology Talent Program.

Author information

Authors and Affiliations

  1. Tea Research Institute, Chinese Academy of Agricultural Sciences, Hangzhou, 310008, China

    Xinyuan Hao, Bo Wang, Lu Wang, Hongli Cao, Yuchun Wang, Jianming Zeng, Yajun Yang & Xinchao Wang

  2. National Center for Tea Improvement, Key Laboratory of Tea Biology and Resources Utilization, Ministry of Agriculture, Hangzhou, 310008, China

    Xinyuan Hao, Lu Wang, Jianming Zeng, Yajun Yang & Xinchao Wang

  3. College of Horticulture, Northwest A&F University, Yangling, Xianyang, 712100, China

    Hu Tang

  4. National Centre for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, 100101, China

    Shuang Fang & Jinfang Chu

Authors
  1. Xinyuan Hao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hu Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bo Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lu Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hongli Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yuchun Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jianming Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Shuang Fang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jinfang Chu
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Yajun Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Xinchao Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Yajun Yang or Xinchao Wang.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hao, X., Tang, H., Wang, B. et al. Gene Characterization and Expression Analysis Reveal the Importance of Auxin Signaling in Bud Dormancy Regulation in Tea Plant. J Plant Growth Regul 38, 225–240 (2019). https://doi.org/10.1007/s00344-018-9834-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-018-9834-7

Keywords

Search

Navigation