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Ectopic expression of UGT75D1, a glycosyltransferase preferring indole-3-butyric acid, modulates cotyledon development and stress tolerance in seed germination of Arabidopsis thaliana

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Abstract

The formation of auxin glucose conjugate is proposed to be one of the molecular modifications controlling auxin homeostasis. However, the involved mechanisms and relevant physiological significances are largely unknown or poorly understood. In this study, Arabidopsis UGT75D1 was at the first time identified to be an indole-3-butyric acid (IBA) preferring glycosyltransferase. Assessment of enzyme activity and IBA conjugates in transgenic plants ectopically expressing UGT75D1 indicated that the UGT75D1 catalytic specificity was maintained in planta. It was found that the expression pattern of UGT75D1 was specific in germinating seeds. Consistently, we found that transgenic seedlings with over-produced UGT75D1 exhibited smaller cotyledons and cotyledon epidermal cells than the wild type. In addition, UGT75D1 was found to be up-regulated under mannitol, salt and ABA treatments and the over-expression lines were tolerant to osmotic and salt stresses during germination, resulting in an increased germination rate. Quantitative RT-PCR analysis revealed that the mRNA levels of ABA INSENSITIVE 3 (ABI3) and ABI5 gene in ABA signaling were substantially down-regulated in the transgenic lines under stress treatments. Interestingly, AUXIN RESPONSE FACTOR 16 (ARF16) gene of transgenic lines was also dramatically down-regulated under the same stress conditions. Since ARF16 functions as an activator of ABI3 transcription, we supposed that UGT75D1 might play a role in stress tolerance during germination through modulating ARF16–ABI3 signaling. Taken together, our work indicated that, serving as the IBA preferring glycosyltransferase but distinct from other auxin glycosyltransferases identified so far, UGT75D1 might be a very important player mediating a crosstalk between cotyledon development and stress tolerance of germination at the early stage of plant growth.

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References

  • Bensmihen S, Rippa S, Lambert G, Jublot D, Pautot V, Granier F, Giraudat J, Parcy F (2002) The homologous ABI5 and EEL transcription factors function antagonistically to fine-tune gene expression during late embryogenesis. Plant Cell 14:1391–1403

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bentsink L, Koornneef M (2008) Seed dormancy and germination. In: Somerville CR, Meyerowitz EM (eds) The arabidopsis book. American Society of Plant Biologists, Rockville, MD

  • Bowles D, Isayenkova J, Lim EK, Poppenberger B (2005) Glycosyltransferases: managers of small molecules. Curr Opin Plant Biol 8:254–263

    Article  PubMed  CAS  Google Scholar 

  • Bowles D, Lim EK, Poppenberger B, Vaistij FE (2006) Glycosyltransferases of lipophilic small molecules. Annu Rev Plant Biol 57:567–597

    Article  PubMed  CAS  Google Scholar 

  • Brady SM, Sarkar SF, Bonetta D, McCourt P (2003) The ABSCISIC ACID INSENSITIVE 3 (ABI3) gene is modulated by farnesylation and is involved in auxin signaling and lateral root development in Arabidopsis. Plant J 34:67–75

    Article  PubMed  CAS  Google Scholar 

  • Campbell JA, Davies GJ, Bulone V, Henrissat B (1997) A classification of nucleotide-diphospho-sugar glycosyltransferases based on amino acid sequence similarities. Biochem J 326(Pt 3):929–939

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Chen C, Letnik I, Hacham Y, Dobrev P, Ben-Daniel BH, Vanková R, Amir R, Miller G (2014) Ascorbate peroxidase 6 protects Arabidopsis thaliana desiccating and germinating seeds from stress and mediates crosstalk between ROS, ABA and auxin. Plant Physiol 166:370–383

    Article  PubMed  PubMed Central  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  PubMed  CAS  Google Scholar 

  • Epstein E, Ludwig-Müller J (1993) Indole-3-butyric acid in plants: occurrence, synthesis, metabolism and transport. Physiol Plant 88:382–389

    Article  CAS  Google Scholar 

  • Finkelstein RR, Lynch TJ (2000) The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12:599–609

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Finkelstein R, Somerville C (1989) Abscisic acid and high osmoticum promote accumulation of long-chain fatty acids in developing embryos of Brassica napus. Plant Sci 61:213–217

    Article  CAS  Google Scholar 

  • Gachon CM, Langlois-Meurinne M, Saindrenan P (2005) Plant secondary metabolism glycosyltransferases: the emerging functional analysis. Trends Plant Sci 10:542–549

    Article  PubMed  CAS  Google Scholar 

  • Giraudat J, Hauge BM, Valon C, Smalle J, Parcy F, Goodman HM (1992) Isolation of the Arabidopsis ABI3 gene by positional cloning. Plant Cell 4:1251–1261

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Hou B, Lim EK, Higgins GS, Bowles DJ (2004) N-glucosylation of cytokinins by glycosyltransferases of Arabidopsis thaliana. J Biol Chem 279:47822–47832

    Article  PubMed  CAS  Google Scholar 

  • Jackson RG, Lim EK, Li Y, Kowalczyk M, Sandberg G, Hoggett J, Ashford DA, Bowles DJ (2001) Identification and biochemical characterization of an Arabidopsis indole-3-acetic acid glucosyltransferase. J Biol Chem 276:4350–4356

    Article  PubMed  CAS  Google Scholar 

  • Jackson RG, Kowalczyk M, Li Y, Higgins G, Ross J, Sandberg G, Bowles DJ (2002) Overexpression of an Arabidopsis gene encoding a glucosyltransferase of indole-3-acetic acid: phenotypic characterization of transgenic lines. Plant J 32:573–583

    Article  PubMed  CAS  Google Scholar 

  • Jin SH, Ma XM, Han P, Wang B, Sun YG, Zhang GZ, Li YJ, Hou BK (2013) UGT74D1 is a novel auxin glycosyltransferase from Arabidopsis thaliana. PLoS ONE 8:e61705

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Jones P, Vogt T (2001) Glycosyltransferases in secondary plant metabolism: tranquilizers and stimulant controllers. Planta 213:164–174

    Article  PubMed  CAS  Google Scholar 

  • Korasick DA, Enders TA, Strader LC (2013) Auxin biosynthesis and storage forms. J Exp Bot 64:2541–2555

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Lairson LL, Henrissat B, Davies GJ, Withers SG (2008) Glycosyltransferases: structures, functions, and mechanisms. Annu Rev Biochem 77:521–555

    Article  PubMed  CAS  Google Scholar 

  • Lim EK, Bowles DJ (2004) A class of plant glycosyltransferases involved in cellular homeostasis. EMBO J 23:2915–2922

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Lim EK, Li Y, Parr A, Jackson R, Ashford DA, Bowles DJ (2001) Identification of glucosyltransferase genes involved in sinapate metabolism and lignin synthesis in Arabidopsis. J Biol Chem 276:4344–4349

    Article  PubMed  CAS  Google Scholar 

  • Liu PP, Montgomery TA, Fahlgren N, Kasschau KD, Nonogaki H, Carrington JC (2007) Repression of AUXIN RESPONSE FACTOR10 by microRNA160 is critical for seed germination and post-germination stages. Plant J 52:133–146

    Article  PubMed  CAS  Google Scholar 

  • Liu X, Barkawi L, Gardner G, Cohen JD (2012) Transport of indole-3-butyric acid and indole-3-acetic acid in Arabidopsis thaliana hypocotyls using stable isotope labeling. Plant Physiol 158:1988–2000

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Liu XD, Zhang H, Zhao Y, Feng ZY, Li Q, Yang HQ, Lu S, Lie JM, He ZH (2013) Auxin controls seed dormancy through stimulation of abscisic acid signaling by inducing ARF-mediated ABI3 activation in Arabidopsis. PNAS 110:15485–15490

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Lopez-Molina L, Mongrand S, McLachlin DT, Chait BT, Chua NH (2002) ABI5 acts downstream of ABI3 to execute an ABA-dependent growth arrest during germination. Plant J 32:317–328

    Article  PubMed  CAS  Google Scholar 

  • Ludwig-Müller J (2000) Indole-3-butyric acid in plant growth and development. Plant Growth Regul 32:219–230

    Article  Google Scholar 

  • Ludwig-Muller J, Epstein E (1991) Occurrence and in vivo biosynthesis of indole-3-butyric acid in corn (Zea mays L.). Plant Physiol 97:765–770

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Ludwig-Müller J, Sass S, Sutter EG, Wodner M, Epstein E (1993) Indole-3-butyric acid in Arabidopsis thaliana I. Identification and quantification. Plant Growth Regul 13:179–187

    Article  Google Scholar 

  • Ludwig-Müller J, Walz A, Slovin JP, Epstein E, Cohen JD, Dong WQ, Town CD (2005) Overexpression of Maize IAGLU in Arabidopsis thaliana alters plant growth and sensitivity to IAA but not IBA and 2,4-D. J Plant Growth Regul 24:127–141

    Article  Google Scholar 

  • Manfre AJ, Lanni LM, Marcotte WR Jr (2006) The Arabidopsis group 1 LATE EMBRYOGENESIS ABUNDANT protein ATEM6 is required for normal seed development. Plant Physiol 140:140–149

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Mansfield SG, Briarty LG (1996) The dynamics of seedling and cotyledon cell development in Arabidopsis thaliana during reserve mobilization. Int J Plant Sci 157:280–295

    Article  Google Scholar 

  • Messner B, Thulke O, Schäffner AR (2003) Arabidopsis glucosyltransferases with activities toward both endogenous and xenobiotic substrates. Planta 217:138–146

    PubMed  CAS  Google Scholar 

  • Monroe-Augustus M, Zolman BK, Bartel B (2003) IBR5, a dual-specificity phosphatase-like protein modulating auxin and abscisic acid responsiveness in Arabidopsis. Plant Cell 15:2979–2991

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Nag R, Maity MK, Dasgupta M (2005) Dual DNA binding property of ABA insensitive 3 like factors targeted to promoters responsive to ABA and auxin. Plant Mol Biol 59:821–838

    Article  PubMed  CAS  Google Scholar 

  • Paquette S, Moller BL, Bak S (2003) On the origin of family 1 plant glycosyltransferases. Phytochemistry 62:399–413

    Article  PubMed  CAS  Google Scholar 

  • Rinaldi MA, Liu J, Enders TA, Bartel B, Strader LC (2012) A gain-of-function mutation in IAA16 confers reduced responses to auxin and abscisic acid and impedes plant growth and fertility. Plant Mol Biol 79:359–373

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Ross J, Li Y, Lim E, Bowles DJ (2001) Higher plant glycosyltransferases. Genome Biol 2:REVIEWS3004

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Scarpella E, Barkoulas M, Tsiantis M (2010) Control of leaf and vein development by auxin. Cold Spring Harb Perspect Biol 2:a001511

    Article  PubMed  PubMed Central  Google Scholar 

  • Spiess GM, Hausman A, Yu P, Cohen JD, Rampey RA, Zolman BK (2014) Auxin input pathway disruptions are mitigated by changes in auxin biosynthetic gene expression in Arabidopsis. Plant Physiol 165:1092–1104

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Strader LC, Bartel B (2009) The Arabidopsis PLEIOTROPIC DRUG RESISTANCE8/ABCG36 ATP binding cassette transporter modulates sensitivity to the auxin precursor indole-3-butyric acid. Plant Cell 21:1992–2007

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Strader LC, Bartel B (2011) Transport and metabolism of the endogenous auxin precursor indole-3-butyric acid. Mol Plant 4:477–486

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Strader LC, Culler AH, Cohen JD, Bartel B (2010) Conversion of endogenous indole-3-butyric acid to indole-3-acetic acid drives cell expansion in Arabidopsis seedlings. Plant Physiol 153:1577–1586

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Strader LC, Wheeler DL, Christensen SE, Berens JC, Cohen JD, Rampey RA, Bartel B (2011) Multiple facets of Arabidopsis seedling development require indole-3-butyric acid-derived auxin. Plant Cell 23:984–999

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Szerszen JB, Szczyglowski K, Bandurski RS (1994) iaglu, a gene from Zea mays involved in conjugation of growth hormone indole-3-acetic acid. Science 265:1699–1701

    Article  PubMed  CAS  Google Scholar 

  • Thole JM, Beisner ER, Liu J, Venkova SV, Strader LC (2014) Abscisic acid regulates root elongation through the activities of auxin and ethylene in Arabidopsis thaliana. G3 (Genes/Genomics/Genet) 4:1259–1274

    Article  CAS  Google Scholar 

  • Tognetti VB, Van Aken O, Morreel K, Vandenbroucke K, van de Cotte B, De Clercq I, Chiwocha S, Fenske R, Prinsen E, Boerjan W, Genty B, Stubbs KA, Inze D, Van Breusegem F (2010) Perturbation of indole-3-butyric acid homeostasis by the UDP-glucosyltransferase UGT74E2 modulates Arabidopsis architecture and water stress tolerance. Plant Cell 22:2660–2679

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Vanneste S, Friml J (2009) Auxin: a trigger for change in plant development. Cell 136:1005–1016

    Article  PubMed  CAS  Google Scholar 

  • Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot 95:707–735

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Zhang Z, Li Q, Li Z, Staswick PE, Wang M, Zhu Y, He Z (2007) Dual regulation role of GH3.5 in salicylic acid and auxin signaling during Arabidopsis-Pseudomonas syringae interaction. Plant Physiol 145:450–464

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Zhang H, Ohyama K, Boudet J, Chen Z, Yang J, Zhang M, Muranaka T, Maurel C, Zhu JK, Gong Z (2008) Dolichol biosynthesis and its effects on the unfolded protein response and abiotic stress resistance in Arabidopsis. Plant Cell 20:1879–1898

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Zhao Y (2010) Auxin biosynthesis and its role in plant development. Annu Rev Plant Biol 61:49–64

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Zolman B, Yoder A, Bartel B (2000) Genetic analysis of indole-3-butyric acid response in Arabidopsis thaliana reveals four mutant classes. Genetics 156:1323–1327

    PubMed  CAS  PubMed Central  Google Scholar 

  • Zolman BK, Martinez N, Millius A, Adham AR, Bartel B (2008) Identification and characterization of Arabidopsis indole-3-butyric acid response mutants defective in novel peroxisomal enzymes. Genetics 180:237–251

    Article  PubMed  CAS  PubMed Central  Google Scholar 

Download references

Acknowledgments

This research was supported by the National Natural Science Foundation of China (No. 91217301 and No. 31570299).

Author contributions

B.K. Hou and G.Z. Zhang conceived and designed the experiments; G.Z. Zhang, S.H. Jin, X.Y. Jiang, R.R. Dong performed the experiments; G.Z. Zhang, R.R. Dong, P. Li analyzed the data; B.K. Hou, G.Z. Zhang and Y.J. Li wrote the paper.

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Authors and Affiliations

  1. Key Lab of Plant Cell Engineering and Germplasm Innovation, Chinese Ministry of Education; School of Life Sciences, Shandong University, Jinan, 250100, China

    Gui-Zhi Zhang, Xiao-Yi Jiang, Rui-Rui Dong, Pan Li, Yan-Jie Li & Bing-Kai Hou

  2. School of Life Science, Qingdao Agricultural University, Qingdao, 266109, China

    Shang-Hui Jin

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  1. Gui-Zhi Zhang
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Correspondence to Bing-Kai Hou.

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Zhang, GZ., Jin, SH., Jiang, XY. et al. Ectopic expression of UGT75D1, a glycosyltransferase preferring indole-3-butyric acid, modulates cotyledon development and stress tolerance in seed germination of Arabidopsis thaliana . Plant Mol Biol 90, 77–93 (2016). https://doi.org/10.1007/s11103-015-0395-x

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