SpringerLink
Log in

Transcriptional regulation of Arabidopsis copper amine oxidase ζ (CuAOζ) in indole-3-butyric acid-induced lateral root development

  • Original paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Spatiotemporal regulation of reactive oxygen species (ROS) is fine-tuned at multiple levels, including transcriptional regulation. Arabidopsis copper amine oxidase ζ (CuAOζ) is localized in peroxisomes, and the CuAOζ-derived ROS is required for indole-3-butyric acid (IBA)-induced lateral root (LR) development. Here, we showed that both GATA2 and NIGT1.2 transcription factors interacted with the 5′ untranslated region (5′ UTR) of CuAOζ, using enhanced yeast one-hybrid analysis. NIGT1.2 was highly expressed in root tips and was upregulated by IBA. Phenotypic analysis, localization, and genetic studies demonstrate that NIGT1.2 positively regulated IBA-induced CuAOζ expression, ROS generation, and LR development. Furthermore, another transcription factor, UPBEAT1 (UPB1), regulated the basal expression of CuAOζ in roots, suggesting a putative functional regulation of CuAOζ in cellular proliferation and differentiation in the root. Together, our findings indicate that transcriptional regulation of peroxisomal CuAOζ plays an important role in determining CuAOζ spatiotemporal activity and ROS homeostasis within a develo** root.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

References

  • Adamowski M, Friml J (2015) PIN-dependent auxin transport: action, regulation, and evolution. Plant Cell 27:20–32

    Article  CAS  Google Scholar 

  • Alekhina OM, Vassilenko KS (2012) Translation initiation in eukaryotes: versatility of the scanning model. Biochemistry 77:1465–1477

    CAS  PubMed  Google Scholar 

  • An Z, **g W, Liu Y, Zhang W (2008) Hydrogen peroxide generated by copper amine oxidase is involved in abscisic acid-induced stomatal closure in Vicia faba. J Exp Bot 59:815–825

    Article  CAS  Google Scholar 

  • Angelini R, Cona A, Federico R, Fincato P, Tavladoraki P, Tisi A (2010) Plant amine oxidases ‘on the move’: an update. Plant Physiol Biochem 48:560–564

    Article  CAS  Google Scholar 

  • Bashandy T, Guilleminot J, Vernoux T, Caparros-Ruiz D, Ljung K, Meyer Y, Reichheld JP (2010) Interplay between the NADP-linked thioredoxin and glutathione systems in Arabidopsis auxin signaling. Plant Cell 22:376–391

    Article  CAS  Google Scholar 

  • Blomster T, Salojarvi J, Sipari N, Brosche M, Ahlfors R, Keinanen M, Overmyer K, Kangasjarvi J (2011) Apoplastic reactive oxygen species transiently decrease auxin signaling and cause stress-induced morphogenic response in Arabidopsis. Plant Physiol 157:1866–1883

    Article  CAS  Google Scholar 

  • Cerny M, Habanova H, Berka M, Luklova M, Brzobohaty B (2018) Hydrogen peroxide: its role in plant biology and crosstalk with signalling networks. Int J Mol Sci 19:2812

    Article  Google Scholar 

  • Chen YH, Chao YY, Hsu YY, Kao CH (2013) Heme oxygenase is involved in H2O2-induced lateral root formation in apocynintreated rice. Plant Cell Rep 32:219–226

    Article  CAS  Google Scholar 

  • Chen Z, Gu Q, Yu X, Huang L, Xu S, Wang R, Shen W, Shen W (2018) Hydrogen peroxide acts downstream of melatonin to induce lateral root formation. Ann Bot 121:1127–1136

    Article  CAS  Google Scholar 

  • Ditengou FA, Teale WD, Kochersperger P, Flittner KA, Kneuper I, van der Graaff E, Nziengui H, Pinosa F, Li X, Nitschke R (2008) Mechanical induction of lateral root initiation in Arabidopsis thaliana. Proc Natl Acad Sci USA 105:18818–18823

    Article  CAS  Google Scholar 

  • Du Y, Scheres B (2018) Lateral root formation and the multiple roles of auxin. J Exp Bot 69:155–167

    Article  CAS  Google Scholar 

  • Dubrovsky JG, Forde BG (2012) Quantitative analysis of lateral root development: pitfalls and how to avoid them. Plant Cell 24:4–14

    Article  CAS  Google Scholar 

  • Galvan-Ampudia CS, Testerink C (2011) Salt stress signals shape the plant root. Curr Opin Plant Biol 14:296–302

    Article  CAS  Google Scholar 

  • Giehl RF, Lima JE, von Wirén N (2012) Localized iron supply triggers lateral root elongation in Arabidopsis by altering the AUX1-mediated auxin distribution. Plant Cell 24:33–49

    Article  CAS  Google Scholar 

  • Hinnebusch AG, Ivanov IP, Sonenberg N (2016) Translational control by 5′-untranslated regions of eukaryotic mRNAs. Science 352:1413–1416

    Article  CAS  Google Scholar 

  • Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907

    Article  CAS  Google Scholar 

  • Kazan K (2013) Auxin and the integration of environmental signals into plant root development. Ann Bot 112:1655–1665

    Article  Google Scholar 

  • Kiba T, Inaba J, Kudo T, Ueda N, Konishi M, Mitsuda N, Takiguchi Y, Kondou Y, Yoshizumi T, Ohme-Takagi M, Matsui M, Yano K, Yanagisawa S, Sakakibara H (2018) Repression of nitrogen starvation responses by members of the Arabidopsis GARP-type transcription factor NIGT1/HRS1 subfamily. Plant Cell 30:925–945

    Article  CAS  Google Scholar 

  • Krouk G, Lacombe B, Bielach A, Perrine-Walker F, Malinska K, Mounier E, Hoyerova K, Tillard P, Leon S, Ljung K, Zazimalova E, Benkova E, Nacry P, Gojon A (2010) Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Dev Cell 18:927–937

    Article  CAS  Google Scholar 

  • Lavenus J, Goh T, Roberts I, Guyomarc’h S, Lucas M, De Smet I, Fukaki H, Beeckman T, Bennett M, Laplaze L (2013) Lateral root development in Arabidopsis: fifty shades of auxin. Trends Plant Sci 18:450–458

    Article  CAS  Google Scholar 

  • Li N, Sun L, Zhang L, Song Y, Hu P, Li C, Hao FS (2015) AtrbohD and AtrbohF negatively regulate lateral root development by changing the localized accumulation of superoxide in primary roots of Arabidopsis. Planta 241:591–602

    Article  CAS  Google Scholar 

  • Li BJ, Cai Q, Ma S, Li S, Zhang X, Yu Y (2018) Regulation of NPA and ACC on H2O2-induced Pea primary horizontal bending root. J Plant Growth Regul 37:246–254

    Article  CAS  Google Scholar 

  • Maeda Y, Konishi M, Kiba T, Sakuraba Y, Sawaki N, Kurai T, Ueda Y, Sakakibara H, Yanagisawa S (2018) A NIGT1-centred transcriptional cascade regulates nitrate signalling and incorporates phosphorus starvation signals in Arabidopsis. Nat Commun 9(1):1376

    Article  Google Scholar 

  • Manzano C, Pallero-Baena M, Casimiro I, De Rybel B, Orman-Ligeza B, Van Isterdael G, Beeckman T, Draye X, Casero P, Del Pozo JC (2014) The emerging role of reactive oxygen species signaling during lateral root development. Plant Physiol 165:1105–1119

    Article  CAS  Google Scholar 

  • Orosa-Puente B, Leftley N, von Wangenheim D, Banda J, Srivastava AK, Hill K, Truskina J, Bhosale R, Morris E, Srivastava M, Kümpers B, Goh T, Fukaki H, Vermeer JEM, Vernoux T, Dinneny JR, French AP, Bishopp A, Sadanandom A, Bennett MJ (2018) Root branching toward water involves posttranslational modification of transcription factor ARF7. Science 362:1407–1410

    Article  CAS  Google Scholar 

  • Overvoord P, Fukaki H, Beeckman T (2010) Auxin control of root development. Cold Spring Harbor Perspect Biol 2:a001537

    Google Scholar 

  • Peret B, Larrieu A, Bennett MJ (2009) Lateral root emergence: a difficult birth. J Exp Bot 60:3637–3643

    Article  CAS  Google Scholar 

  • Pestova TV, Kolupaeva VG (2002) The roles of individual eukaryotic translation initiation factors in ribosomal scanning and initiation codon selection. Gene Dev 16:2906–2922

    Article  CAS  Google Scholar 

  • Petricka JJ, Winter CM, Benfey PN (2012) Control of Arabidopsis root development. Ann Rev Plant Biol 63:563–590

    Article  CAS  Google Scholar 

  • Planas-Portell J, Gallart M, Tiburcio AF, Altabella T (2013) Coppercontaining amine oxidases contribute to terminal polyamine oxidation in peroxisomes and apoplast of Arabidopsis thaliana. BMC Plant Biol 13:109

    Article  Google Scholar 

  • Qu Y, An Z, Zhuang B, **g W, Zhang Q, Zhang W (2014) Copper amine oxidase and phospholipase D act independently in abscisic acid (ABA)-induced stomatal closure in Vicia faba and Arabidopsis. J Plant Res 127:533–544

    Article  CAS  Google Scholar 

  • Qu Y, Wang Q, Guo J, Wang P, Song P, Jia Q, Zhang X, Kudla J, Zhang W, Zhang Q (2017) Peroxisomal CuAOζ and its product H2O2 regulate the distribution of auxin and IBA-dependent lateral root development in Arabidopsis. J Exp Bot 68:4851–4867

    Article  CAS  Google Scholar 

  • Reyes JC, Muro-Pastor MI, Florencio FJ (2004) The GATA family of transcription factors in Arabidopsis and rice. Plant Physiol 134:1718–1732

    Article  CAS  Google Scholar 

  • Su GX, Zhang WH, Liu YL (2006) Involvement of hydrogen peroxide generated by polyamine oxidative degradation in the development of lateral roots in soybean. J Integr Plant Biol 48:426–432

    Article  CAS  Google Scholar 

  • Tian Y, Fan M, Qin Z, Lv H, Wang M, Zhang Z, Zhou W, Zhao N, Li X, Han C (2018) Hydrogen peroxide positively regulates brassinosteroid signaling through oxidation of the BRASSINAZOLE-RESISTANT1 transcription factor. Nat Commun 9:1063

    Article  Google Scholar 

  • Tognetti VB, Muhlenbock P, Van Breusegem F (2012) Stress homeostasis-the redox and auxin perspective. Plant Cell Environ 35:321–333

    Article  CAS  Google Scholar 

  • Tsukagoshi H, Busch W, Benfey PN (2010) Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 143:606–616

    Article  CAS  Google Scholar 

  • Wang P, Du Y, Li Y, Ren D, Song CP (2010) Hydrogen peroxide-mediated activation of MAP kinase 6 modulates nitric oxide biosynthesis and signal transduction in Arabidopsis. Plant Cell 22:2981–2998

    Article  CAS  Google Scholar 

  • Wu C, Feng J, Wang R, Liu H, Yang H, Rodriguez PL, Qin H, Liu X, Wang D (2012) HRS1 acts as a negative regulator of abscisic acid signaling to promote timely germination of Arabidopsis seeds. PLoS ONE 7:e35764

    Article  CAS  Google Scholar 

  • Xuan W, Audenaert D, Parizot B, Moller BK, Njo MF, De Rybel B, De Rop G, Van Isterdael G, Mahonen AP, Vanneste S, Beeckman T (2015) Root cap-derived auxin pre-patterns the longitudinal axis of the Arabidopsis root. Curr Biol 25:1381–1388

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Philip N. Benfey (Duke University) for kindly providing upb1 and P35S:UPB1-3YFP seeds. The work was supported by grants from the Natural Science Foundation of Jiangsu Province (BK20160720) and the National Natural Science Foundation of China (31700237) and the Fundamental Research Funds for the Central Universities (Y0201700648) to Y.Q. and the National Natural Science Foundation of China (31970300) and the Fundamental Research Funds for the Central Universities (KYZ201858) to Q.Z.

Author information

Authors and Affiliations

  1. College of Life Sciences, State Key Laboratory of Crop Genetics and Germplasm Enhancement, Nan**g Agricultural University, Nan**g, 210095, People’s Republic of China

    Yana Qu, **ao Liu, Xuedong Zhang, Yiwen Tang, Yanwei Hu, Shiyao Chen, Lixu **ang & Qun Zhang

Authors
  1. Yana Qu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. **ao Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xuedong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yiwen Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yanwei Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Shiyao Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Lixu **ang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Qun Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

YQ and QZ designed the research; XL, XZ, YT, YH, SC, LX, and QZ performed research; and YQ and QZ analyzed data and wrote the paper.

Corresponding author

Correspondence to Qun Zhang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Qu, Y., Liu, X., Zhang, X. et al. Transcriptional regulation of Arabidopsis copper amine oxidase ζ (CuAOζ) in indole-3-butyric acid-induced lateral root development. Plant Growth Regul 89, 287–297 (2019). https://doi.org/10.1007/s10725-019-00535-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-019-00535-w

Keywords

Search

Navigation