Advertisement

Journal of Plant Growth Regulation

, Volume 38, Issue 1, pp 225–240 | Cite as

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

  • Xinyuan Hao
  • Hu Tang
  • Bo Wang
  • Lu Wang
  • Hongli Cao
  • Yuchun Wang
  • Jianming Zeng
  • Shuang Fang
  • Jinfang Chu
  • Yajun YangEmail author
  • Xinchao WangEmail author
Article
  • 177 Downloads

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.

Keywords

Auxin Bud dormancy Tea plant Expression profile IAA content 

Notes

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.

Compliance with Ethical Standards

Conflict of interest

The authors declare no conflict of interest.

Supplementary material

344_2018_9834_MOESM1_ESM.xlsx (52 kb)
Supplementary material 1 (XLSX 51 KB)
344_2018_9834_MOESM2_ESM.docx (20 kb)
Supplementary material 2 (DOCX 19 KB)
344_2018_9834_MOESM3_ESM.xlsx (28 kb)
Supplementary material 3 (XLSX 27 KB)
344_2018_9834_MOESM4_ESM.xlsx (19 kb)
Supplementary material 4 (XLSX 18 KB)
344_2018_9834_MOESM5_ESM.docx (17 kb)
Supplementary material 5 (DOCX 16 KB)

References

  1. 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 110:37–44CrossRefGoogle Scholar
  2. Anderson JV, Chao WS, Horvath DP (2001) Review: a current review on the regulation of dormancy in vegetative buds. Weed Sci 49:581–589CrossRefGoogle Scholar
  3. 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 108:3418–3423CrossRefGoogle Scholar
  4. Barua DN (1969) Seasonal dormancy in tea (Camellia sinensis L.). Nature 224:514CrossRefGoogle Scholar
  5. 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 Google Scholar
  6. 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 CrossRefGoogle Scholar
  7. 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 94:281–302CrossRefGoogle Scholar
  8. 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 56:133–150CrossRefGoogle Scholar
  9. Cooke JEK, Eriksson ME, Junttila O (2012) The dynamic nature of bud dormancy in trees: environmental control and molecular mechanisms. Plant Cell Environ 35:1707–1728CrossRefGoogle Scholar
  10. 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 71:860–870CrossRefGoogle Scholar
  11. 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 28:1081–1087CrossRefGoogle Scholar
  12. Grunewald W, Friml J (2010) The march of the PINs: developmental plasticity by dynamic polar targeting in plant cells. EMBO J 29:2700–2714CrossRefGoogle Scholar
  13. 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 12:118CrossRefGoogle Scholar
  14. 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 8:553Google Scholar
  15. 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 169:643–648CrossRefGoogle Scholar
  16. 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 6:989CrossRefGoogle Scholar
  17. 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 88:269–286CrossRefGoogle Scholar
  18. 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 6:47–59CrossRefGoogle Scholar
  19. 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 88:360–371CrossRefGoogle Scholar
  20. 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 151:691–701CrossRefGoogle Scholar
  21. 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 140:1109–1117CrossRefGoogle Scholar
  22. 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 160:308–318CrossRefGoogle Scholar
  23. Khan S, Stone JM (2007) Arabidopsis thaliana GH3.9 in auxin and jasmonate cross talk. Plant Signal Behav 2:483–485CrossRefGoogle Scholar
  24. 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 54:609–621CrossRefGoogle Scholar
  25. Lavy M, Estelle M (2016) Mechanisms of auxin signaling. Development 143:3226–3229CrossRefGoogle Scholar
  26. 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 Google Scholar
  27. McWatters HG, Devlin PF (2011) Timing in plants-A rhythmic arrangement. FEBS Lett 585:1474–1484CrossRefGoogle Scholar
  28. 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 459:1136–1140CrossRefGoogle Scholar
  29. Nagar PK (1996) Changes in endogenous abscisic acid and phenols during winter dormancy in tea (Camellia sinesis L.(O) Kunze). Acta Physiol Plant 18:33–38Google Scholar
  30. 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
  31. Nagar P, Sood S (2006) Changes in endogenous auxins during winter dormancy in tea (Camellia sinensis L.) O. Kuntze. Acta Physiol Plant 28:165–169CrossRefGoogle Scholar
  32. 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 20:843–855CrossRefGoogle Scholar
  33. Paul A, Kumar S (2011) Responses to winter dormancy, temperature, and plant hormones share gene networks. Funct Integr Genomics 11:659–664CrossRefGoogle Scholar
  34. 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 24:2874–2885CrossRefGoogle Scholar
  35. Ren H, Gray WM (2015) SAUR Proteins as effectors of hormonal and environmental signals in plant growth. Mol Plant 8:1153–1164CrossRefGoogle Scholar
  36. 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 66:6745–6760CrossRefGoogle Scholar
  37. 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 19:2370–2390CrossRefGoogle Scholar
  38. 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 213:511–524CrossRefGoogle Scholar
  39. Stafstrom JP, Ripley BD, Devitt ML, Drake B (1998) Dormancy-associated gene expression in pea axillary buds. Plants 205:547–552CrossRefGoogle Scholar
  40. 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 17:616–627CrossRefGoogle Scholar
  41. 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 113:6071–6076CrossRefGoogle Scholar
  42. 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 43:669–677CrossRefGoogle Scholar
  43. 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 371:279–290CrossRefGoogle Scholar
  44. 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 14:236CrossRefGoogle Scholar
  45. 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 10:1149–1159CrossRefGoogle Scholar
  46. Weijers D, Friml J (2009) SnapShot: auxin signaling and transport. Cell 136:1172CrossRefGoogle Scholar
  47. 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 94:97–107CrossRefGoogle Scholar
  48. 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 8:256Google Scholar
  49. 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 14:297CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Tea Research InstituteChinese Academy of Agricultural SciencesHangzhouChina
  2. 2.National Center for Tea Improvement, Key Laboratory of Tea Biology and Resources UtilizationMinistry of AgricultureHangzhouChina
  3. 3.College of HorticultureNorthwest A&F UniversityXianyangChina
  4. 4.National Centre for Plant Gene Research (Beijing), Institute of Genetics and Developmental BiologyChinese Academy of SciencesBeijingChina

Personalised recommendations