Abstract
The Auxin/Indole acetic acid (Aux/IAA) genes are auxin primary response genes that play a pivotal role in apical dominance, phototropism, and embryonic development. In this study, we cloned the promoter of BpIAA10 and constructed a BpProIAA::Luc vector for transformation into Arabidopsis thaliana. The results indicated that BpIAA10 is expressed in the apical meristem, embryonic leaves, and young stem. The tissue-specific expression pattern was same in A. thaliana and Betula platyphylla. Additionally, IAA, IBA, GA, SA, and ABA could induce the expression of BpIAA10 while MeJA inhibited the expression of BpIAA10, suggesting that plant hormones influence the expression of BpIAA10. Strong light conditions also markedly induced the expression of BpIAA10, indicating that BpIAA10 is sensitive to light intensity and that light may be sufficient but not necessary for the normal expression of BpIAA10. Conversely, IBA-induced expression of BpIAA10 was suppressed with strong light, suggesting that IBA-induced BpIAA10 expression is partly light dependent. We predicted the presence of cis-acting elements in the BpIAA10 promoter and found many different types cis-acting elements. Furthermore, promoter analysis and yeast one-hybrid assay revealed that the bait2 (TGA-element) can specifically bind to transcription factors 14-3-3 and Ribosomal_L2, and the bait3 (ntBBF1ARROLB) can specifically bind to FAR1, 14-3-3 Like and kinesin-like protein. Therefore, our study characterized the expression of BpIAA10 and found five transcription factors that regulate expression of BpIAA10. This provides a basis for determining the function of BpIAA10.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11240-017-1336-y/MediaObjects/11240_2017_1336_Fig1_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11240-017-1336-y/MediaObjects/11240_2017_1336_Fig2_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11240-017-1336-y/MediaObjects/11240_2017_1336_Fig3_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11240-017-1336-y/MediaObjects/11240_2017_1336_Fig4_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11240-017-1336-y/MediaObjects/11240_2017_1336_Fig5_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11240-017-1336-y/MediaObjects/11240_2017_1336_Fig6_HTML.gif)
Similar content being viewed by others
Abbreviations
- Luc :
-
Luciferase reporter gene
- IBA:
-
Indole-3-butytric acid
- IAA:
-
Indole-3-acetic acid
- GA:
-
Gibberellin
- ABA:
-
Abscisic acid
- SA:
-
Salicylic acid
- MeJA:
-
Methyl jasmonate
- ETH:
-
Ethylene
- JA:
-
Jasmonate
- BR:
-
Brassinolide
- KN:
-
Kinetin
- PCR:
-
Polymerase chain reaction
- ORF:
-
Open reading frame
- ARF :
-
Auxin response factor
- Aux/IAA :
-
Auxin/indole acetic acid
- ABI3 :
-
ABSCISIC ACID-INSENSITIVE3
- ETR1 :
-
ETHYLENE TRIPLE RESPONSE 1
- SE:
-
Standard error
- SD media:
-
Synthetic defined yeast media
- Ura:
-
Uracil
- Leu:
-
Leucine
- Trp:
-
Tryptophan
- AbA:
-
Aureobasidin A
- HSP:
-
Heat shock protein
- RL2:
-
Ribosomal_L2
- FAR1:
-
Far-red impaired response 1
- KIN:
-
Kinesin-like protein
- GUS :
-
β-Glucuronidase
- TF:
-
Transcriptional factors
References
Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11(2):113–116
Chen JG, Pandey S, Huang J, Alonso JM, Ecker JR, Assmann SM, Jones AM (2004) GCR1 can act independently of heterotrimeric G-protein in response to brassinosteroids and gibberellins in Arabidopsis seed germination. Plant Physiol 135(2):907–915. https://doi.org/10.1104/pp.104.038992
Cheng Y-J, Guo W-W, Yi H-L, Pang X-M, Deng X (2003) An efficient protocol for genomic DNA extraction from Citrus species. Plant Mol Biol Rep 21(2):177–178. https://doi.org/10.1007/BF02774246
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6):735–743
del Viso F, Casaretto JA, Quatrano RS (2007) 14-3-3 Proteins are components of the transcription complex of the ATEM1 promoter in Arabidopsis. Planta 227(1):167–175. https://doi.org/10.1007/s00425-007-0604-1
Diedrich G, Spahn CM, Stelzl U, Schafer MA, Wooten T, Bochkariov DE, Cooperman BS, Traut RR, Nierhaus KH (2000) Ribosomal protein L2 is involved in the association of the ribosomal subunits, tRNA binding to A and P sites and peptidyl transfer. EMBO J 19(19):5241–5250. https://doi.org/10.1093/emboj/19.19.5241
Faivre-Rampant O, Cardle L, Marshall D, Viola R, Taylor MA (2004) Changes in gene expression during meristem activation processes in Solanum tuberosum with a focus on the regulation of an auxin response factor gene. J Exp Bot 55(397):613–622. https://doi.org/10.1093/jxb/erh075
Faust M, Erez A, Rowland LJ, Wang SY, Norman HA (1997) Bud dormancy in perennial fruit trees: physiological basis for dormancy induction, maintenance, and release. HortScience 32(4):623–629
Frewen BE, Chen TH, Howe GT, Davis J, Rohde A, Boerjan W, Bradshaw HD Jr (2000) Quantitative trait loci and candidate gene map** of bud set and bud flush in populus. Genetics 154(2):837–845
Galli M, Liu Q, Moss BL, Malcomber S, Li W, Gaines C, Federici S, Roshkovan J, Meeley R, Nemhauser JL, Gallavotti A (2015) Auxin signaling modules regulate maize inflorescence architecture. Proc Natl Acad Sci USA 112(43):13372–13377 https://doi.org/10.1073/pnas.1516473112
Gray WM, Kepinski S, Rouse D, Leyser O, Estelle M (2001) Auxin regulates SCF(TIR1)-dependent degradation of AUX/IAA proteins. Nature 414(6861):271–276. https://doi.org/10.1038/35104500
Horvath David P, Anderson JV, Chao Wun S, Foley Michael E (2003) Knowing when to grow: signals regulating bud dormancy. Trends Plant Sci 8(11):534–540. https://doi.org/10.1016/j.tplants.2003.09.013
Ishida S, Fukazawa J, Yuasa T, Takahashi Y (2004) Involvement of 14-3-3 signaling protein binding in the functional regulation of the transcriptional activator REPRESSION OF SHOOT GROWTH by gibberellins. Plant Cell 16(10):2641–2651. https://doi.org/10.1105/tpc.104.024604
Jain M, Kaur N, Garg R, Thakur JK, Tyagi AK, Khurana JP (2006) Structure and expression analysis of early auxin-responsive Aux/IAA gene family in rice (Oryza sativa). Funct Integr Genom 6(1):47–59. https://doi.org/10.1007/s10142-005-0005-0
Kalluri UC, Difazio SP, Brunner AM, Tuskan GA (2007) Genome-wide analysis of Aux/IAA and ARF gene families in Populus trichocarpa. BMC Plant Biol 7:59. https://doi.org/10.1186/1471-2229-7-59
Kim BC, Soh MC, Kang BJ, Furuya M, Nam HG (1996) Two dominant photomorphogenic mutations of Arabidopsis thaliana identified as suppressor mutations of hy2. Plant J 9(4):441–456
Kim BC, Soh MS, Hong SH, Furuya M, Nam HG (1998) Photomorphogenic development of the Arabidopsis shy2-1D mutation and its interaction with phytochromes in darkness. Plant J 15(1):61–68
Kim EH, Kim YS, Park SH, Koo YJ, Choi YD, Chung YY, Lee IJ, Kim JK (2009) Methyl jasmonate reduces grain yield by mediating stress signals to alter spikelet development in rice. Plant Physiol 149(4):1751–1760. https://doi.org/10.1104/pp.108.134684
Lachaud S, Bonnemain JL (1984) Seasonal variations in the polar-transport pathways and retention sites of [3 H] indole-3-acetic acid in young branches of Fagus sylvatica L. Planta 161(3):207–215
Leyser O (2001) Auxin signalling: the beginning, the middle and the end. Curr Opin Plant Biol 4(5):382–386
Liu L, Li B, Liu X (2016) FAR-RED ELONGATED HYPOCOTYL3 promotes floral meristem determinacy in Arabidopsis. Plant Signal Behav 11(10):e1238545. https://doi.org/10.1080/15592324.2016.1238545
Morris CF, Anderberg RJ, Goldmark PJ, Walker-Simmons MK (1991) Molecular cloning and expression of abscisic acid-responsive genes in embryos of dormant wheat seeds. Plant Physiol 95(3):814 – 21
Nemhauser JL, Hong F, Chory J (2006) Different plant hormones regulate similar processes through largely nonoverlap** transcriptional responses. Cell 126(3):467–475. https://doi.org/10.1016/j.cell.2006.05.050
Nitsch JP (1957) Growth responses of woody plants to photoperiodic stimuli. Proc Am Soc Hort Sci 70:512–525
Ouellet F, Overvoorde PJ, Theologis A (2001) IAA17/AXR3: biochemical insight into an auxin mutant phenotype. Plant Cell 13(4):829–841
Ouyang X, Li J, Li G, Li B, Chen B, Shen H, Huang X, Mo X, Wan X, Lin R, Li S, Wang H, Deng XW (2011) Genome-wide binding site analysis of FAR-RED ELONGATED HYPOCOTYL3 reveals Its novel function in arabidopsis development. Plant Cell 23(7):2514–2535. https://doi.org/10.1105/tpc.111.085126
Overvoorde PJ, Okushima Y, Alonso JM, Chan A, Chang C, Ecker JR, Hughes B, Liu A, Onodera C, Quach H, Smith A, Yu G, Theologis A (2005) Functional genomic analysis of the AUXIN/INDOLE-3-ACETIC ACID gene family members in Arabidopsis thaliana. Plant Cell 17(12):3282–3300. https://doi.org/10.1105/tpc.105.036723
Rohde A, Bhalerao RP (2007) Plant dormancy in the perennial context. Trends Plant Sci 12(5):217–223. https://doi.org/10.1016/j.tplants.2007.03.012
Rohde A, Prinsen E, De Rycke R, Engler G, Van Montagu M, Boerjan W (2002) PtABI3 im**es on the growth and differentiation of embryonic leaves during bud set in poplar. Plant Cell 14(8):1885–1901
Rohde A, Ruttink T, Hostyn V, Sterck L, Van Driessche K, Boerjan W (2007) Gene expression during the induction, maintenance, and release of dormancy in apical buds of poplar. J Exp Bot 58(15–16):4047–4060. https://doi.org/10.1093/jxb/erm261
Ruonala R, Rinne PL, Baghour M, Moritz T, Tuominen H, Kangasjarvi J (2006) Transitions in the functioning of the shoot apical meristem in birch (Betula pendula) involve ethylene. Plant J 46(4):628–640. https://doi.org/10.1111/j.1365-313X.2006.02722.x
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(8):2370–2390. https://doi.org/10.1105/tpc.107.052811
Santamaria ME, Rodriguez R, Canal MJ, Toorop PE (2011) Transcriptome analysis of chestnut (Castanea sativa) tree buds suggests a putative role for epigenetic control of bud dormancy. Ann Bot 108(3):485–498. https://doi.org/10.1093/aob/mcr185
Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3(6):1101–1108
Schoonheim PJ, Sinnige MP, Casaretto JA, Veiga H, Bunney TD, Quatrano RS, de Boer AH (2007) 14-3-3 adaptor proteins are intermediates in ABA signal transduction during barley seed germination. Plant J 49(2):289–301. https://doi.org/10.1111/j.1365-313X.2006.02955.x
Schrader J, Baba K, May ST, Palme K, Bennett M, Bhalerao RP, Sandberg G (2003) Polar auxin transport in the wood-forming tissues of hybrid aspen is under simultaneous control of developmental and environmental signals. Proc Natl Acad Sci USA 100(17):10096–10101 https://doi.org/10.1073/pnas.1633693100
Schrader J, Moyle R, Bhalerao R, Hertzberg M, Lundeberg J, Nilsson P, Bhalerao RP (2004) Cambial meristem dormancy in trees involves extensive remodelling of the transcriptome. Plant J 40(2):173–187. https://doi.org/10.1111/j.1365-313X.2004.02199.x
Shen Z, Liu YC, Bibeau JP, Lemoi KP, Tuzel E, Vidali L (2015) The kinesin-like proteins, KAC1/2, regulate actin dynamics underlying chloroplast light-avoidance in Physcomitrella patens. J Integr Plant Biol 57(1):106–119. https://doi.org/10.1111/jipb.12303
Shimizu-Sato S, Mori H (2001) Control of outgrowth and dormancy in axillary buds. Plant Physiol 127(4):1405–1413
Song Y, You J, **ong L (2009) Characterization of OsIAA1 gene, a member of rice Aux/IAA family involved in auxin and brassinosteroid hormone responses and plant morphogenesis. Plant Mol Biol 70(3):297–309. https://doi.org/10.1007/s11103-009-9474-1
Ulmasov T, Hagen G, Guilfoyle TJ (1999a) Activation and repression of transcription by auxin-response factors. Proc Natl Acad Sci USA 96(10):5844–5849
Ulmasov T, Hagen G, Guilfoyle TJ (1999b) Dimerization and DNA binding of auxin response factors. Plant J 19(3):309–319
Weiser CJ (1970) Cold resistance and injury in woody plants: knowledge of hardy plant adaptations to freezing stress may help us to reduce winter damage. Science 169(3952):1269–1278. https://doi.org/10.1126/science.169.3952.1269
Yang G, Chen S, Wang S, Liu G, Li H, Huang H, Jiang J (2015) BpGH3.5, an early auxin-response gene, regulates root elongation in Betula platyphylla × Betula pendula. Plant Cell Tissue Organ Cult 120(1):239–250. https://doi.org/10.1007/s11240-014-0599-9
Yang G, Wang C, Wang Y, Guo Y, Zhao Y, Yang C, Gao C (2016) Overexpression of ThVHAc1 and its potential upstream regulator, ThWRKY7, improved plant tolerance of Cadmium stress. Sci Rep 6:18752. https://doi.org/10.1038/srep18752
Zhang D, Ren L, Yue JH, Wang L, Zhuo LH, Shen XH (2014) GA4 and IAA were involved in the morphogenesis and development of flowers in Agapanthus praecox ssp. orientalis. J Plant Physiol 171(11):966–976. https://doi.org/10.1016/j.jplph.2014.01.012
Acknowledgements
This work was supported by the National Natural Science Foundation of China (Grant No. 31370660).
Author information
Authors and Affiliations
Contributions
GL and JJ designed the experiments. WX and RH performed the molecular experiments. WX and SX analyzed the data. WX drafted the manuscript. GL and JJ revised the manuscript. All authors have read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
All authors declare no financial or commercial conflicts of interest.
Additional information
Communicated by Sergio J. Ochatt.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Xu, W., Han, R., Xu, S. et al. Expression of BpIAA10 from Betula platyphylla (birch) is differentially regulated by different hormones and light intensities. Plant Cell Tiss Organ Cult 132, 371–381 (2018). https://doi.org/10.1007/s11240-017-1336-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11240-017-1336-y