Skip to main content
SpringerLink
Log in

Regulation of rice responses to submergence by WRKY transcription factors

  • Original paper
  • Published:
Biologia Plantarum

Abstract

Responses of rice to submergence have been extensively studied, but the molecular network behind the tolerance to this stress is still incomplete. Transcription factors (TFs) are important players in gene transcription regulation during stresses. Here, we analyzed expression of WRKY genes and morphological and anatomical changes in different rice cultivars under submergence. When they were submerged for 48 h, changes in root number, fresh and dry masses, and aerenchyma development were observed. Although accumulations of WRKY transcripts were observed in both shoots and roots, root tissues showed higher accumulation with a peak already after 6 h under submergence. Especially transcriptions of OsWRKY11 and OsWRKY56 were high, more than 100-fold in comparison with controls. The WRKY promoter analysis showed that some cis-regulatory elements could be characterized as stress-responsive elements and linked to oxygen depletion. In the promoter of OsWRKY62, two cis-regulatory elements were found: ARE and GC-motif. These elements are known to be involved in oxygen deficiency responses. In addition, the W-box cis-regulatory element, the target of WRKY transcription factors, was found in OsWRKY11, OsWRKY56, and OsWRKY62, suggesting a feedback control acting on the upregulation of WRKY transcription factors. Genes involved in the submergence stress and resulting aerenchyma development had a W-box in their promoter regions, which also suggested regulation by WRKYs. Overall, the results support the role of WRKY transcription factors in rice submergence tolerance and unveil their action in other tolerance mechanisms.

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

Similar content being viewed by others

Abbreviations

ABA:

abscisic acid

CL:

coleoptile length

CREs:

cis-regulatory elements

ERF:

ethylene response factor

LN:

leaf number

MeJA:

methyl jasmonate

QTL:

quantitative trait locus

RDM:

root dry mass

RFM:

root fresh mass

RL:

root length

RN:

root number

RT-qPCR:

reverse transcription quantitative polymerase chain reaction

SA:

salicylic acid

SAM:

S-adenosyl-L-methionine

SDM:

shoot dry mass

SFM:

shoot fresh mass

SL:

shoot length

TFs:

transcription factors

References

  • Bailey-Serres, J., Lee, S.C., Brinton, E.: Waterproofing crops: effective flooding survival strategies. - Plant Physiol. 160: 1698–1709, 2012.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bailey-Serres, J., Voesenek, L.A.C.J.: Flooding stress: acclimations and genetic diversity. - Annu. Rev. Plant. Biol. 59: 313–339, 2008.

    Article  PubMed  CAS  Google Scholar 

  • Bakshi, M., Oelmüller, R.: WRKY transcription factors: jack of many trades in plants. - Plant Signal Behav. 9: e27700, 2014.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Banerjee, A., Roy Choudhury, A.: WRKY Proteins: signaling and regulation of expression during abiotic stress responses. - Sci. World J. 807560: 17, 2015.

    Google Scholar 

  • Bazzini, A.A., Almasia, N.I., Manacorda, C.A., Mongelli, V.C., Conti, G., Maroniche, G.A., Rodriguez, M.C., Distéfano, A.J., Hopp, H.E., Del Vas, M., Asurmendi, S.: Virus infection elevates transcriptional activity of miR164a promoter in plants. - BMC Plant Biol. 9: 152, 2009.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bustin, S.A., Benes, V., Garson, J.A., Hellemans, J., Huggett, J., Kubista, M., Mueller, R., Nolan, T., Pfaffl, M.W., Shipley, G.L., Vandesompele, J., Wittwer, C.T.: The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. - Clin. Chem. 55: 611–622, 2009.

    Article  PubMed  CAS  Google Scholar 

  • Campbell, M.T., Proctor, C.A., Dou, Y., Schmitz, A.J., Phansak, P., Kruger, G.R., Zhang C., Walia, H.: Genetic and molecular characterization of submergence response identifies Subtol6 as a major submergence tolerance locus in maize. - PLoS ONE 10: e0120385, 2016.

    Article  CAS  Google Scholar 

  • Dawood, T., Rieu, I., Wolters-Arts, M., Derksen, E.B., Mariani, C., Visser, E.J.W.: Rapid flooding-induced adventitious root development from preformed primordia in Solanum dulcamara. - AoB Plants 6: plt058, 2014.

    Article  PubMed  CAS  Google Scholar 

  • Drew, M.C., He, C.J., Morgan, P.W.: Programmed cell death and aerenchyma formation in roots. - Trends Plant Sci. 5: 123–127, 2000.

    Article  PubMed  CAS  Google Scholar 

  • Fukao, T., Bailey-Serres, J.: Submergence tolerance conferred by Sub1A is mediated by SLR1 and SLRL1 restriction of gibberellin responses in rice. - PNAS 105: 16814–16819, 2008.

    Article  PubMed  Google Scholar 

  • Fukushima, S., Mori, M., Sugano, S., Takatsuji, H.: Transcription factor WRKY62 plays a role in pathogen defense and hypoxia-responsive gene expression in rice. - Plant Cell Physiol. 57: 2541–2551, 2016.

    Article  PubMed  CAS  Google Scholar 

  • Gonzaga, Z.J.C., Carandang, J., Singh, A., Collard, B.C.Y., Thomson, M.J., Septiningsih, E.M.: Mapping QTLs for submergence tolerance in rice using a population fixed for SUB1A tolerant allele. - Mol Breed. 37: 47, 2017.

    Article  CAS  Google Scholar 

  • Hattori, Y., Nagai, K., Furukawa, S., Song, X.J., Kawano, R., Sakakibara, H., Wu, J., Matsumoto, T., Yoshimura, A., Kitano, H., Matsuoka, M., Mori, H., Ashikari, M.: The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water. - Nature 460: 1026–1030, 2009.

    Article  PubMed  CAS  Google Scholar 

  • Hoeren, F.U., Dolferus, R., Wu, Y., Peacock, W.J., Dennis, E.S.: Evidence for a role for AtMYB2 in the induction of the Arabidopsis alcohol dehydrogenase gene (ADH1) by low oxygen. - Genetics 149: 479–490, 1998.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Hsu, F.C., Chou, M.Y., Peng, H.P., Chou, S.J., Shih, M.C.: Insights into hypoxic systemic responses based on analyses of transcriptional regulation in Arabidopsis. - PloS ONE 6: e28888, 2011.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jackson, M.B., Ismail, A.M.: Introduction to the special issue: electrons, water and rice fields: plant response and adaptation to flooding and submergence stress. - AoB Plants 7: plv078, 2015.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jain, M., Nijhawan, A., Tyagi, A.K., Khurana, J.P.: Validation of housekeeping genes as internal control for studying gene expression in rice by quantitative real-time PCR. - Biochem. biophys. Res. Commun. 345: 646–651, 2006.

    Article  PubMed  CAS  Google Scholar 

  • Karnovsky, M.J.: A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. - J. Cell Biol. 27: 137–138, 1965.

    Google Scholar 

  • Kato Y., Collard B.C.Y., Septiningsih E.M.S., Ismail A.M.: Physiological analyses of traits associated with tolerance of long-term partial submergence in rice. - AoB Plants 6: plu058, 2014.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Klok, E.J., Wilson, I.W., Wilson, D., Chapman, S.C., Ewing, R.M., Somerville, S.C., Peacock, W.J., Dolferus, R., Dennis, E.S.: Expression profile analysis of the low-oxygen response in Arabidopsis root cultures. - Plant Cell 14: 2481–2494, 2002.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kreuzwieser, J., Hauberg, J., Howell, K.A., Carroll, A., Rennenberg, H., Millar, A.H., Whelan, J.: Differential response of gray poplar leaves and roots underpins stress adaptation during hypoxia. - Plant Physiol. 149: 461–473, 2009.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Krzyzanowski, F.C., Vieira, R.D., Neto, J.B.F.: [Seed Vigour: Concepts and Tests]. - Associação Brasileira de Sementes, Lodrina - Paraná 1999. [In Port.]

    Google Scholar 

  • Lescot, M., Déhais, P., Moreau, Y., De Moor, B., Rouzé, P., Rombauts, S.: PlantCare: a database of plant cis- regulatory regulatory elements and a portal to tools for in silico analysis of promoter seuences.–Nucl. Acids Res. 30: 325–327, 2002.

    Article  PubMed  CAS  Google Scholar 

  • Liu, F., VanToai, T., Moy, L.P., Bock, G., Linford, L.D., Quackenbush, J.: Global transcription profiling reveals comprehensive insights into hypoxic response in Arabidopsis. - Plant Physiol. 137: 1115–1129, 2005.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu, L., Xu, W., Hu, X., Liu, H., Lin, Y.: W-box and G-box elements play important roles in early senescence of rice flag leaf. - Sci. Rep. 6: 20881, 2016.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Livak, K.J., Schmittgen, T.D.: Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT Method. - Methods 25: 402–408, 2001.

    Article  PubMed  CAS  Google Scholar 

  • Loreti, E., Van Veen, H., Perata, P.: Plant responses to flooding stress. - Curr. Opin. Plant Biol. 33: 64–71, 2016.

    Article  PubMed  CAS  Google Scholar 

  • Magneschi, L., Perata, P.: Rice germination and seedling growth in the absence of oxygen. - Ann. Bot. 103: 181–196, 2009.

    Article  PubMed  CAS  Google Scholar 

  • Mohanty, B., Takahashi, H., De Los Reyes, B.G., Wijaya, E., Nakazono, M., Lee, D.Y.: Transcriptional regulatory mechanism of alcohol dehydrogenase 1-deficient mutant of rice for cell survival under complete submergence. - Rice 9: 1–8, 2016.

    Article  Google Scholar 

  • Mustroph, A., Zanetti, M.E., Jang, C.J., Holtan, H.E., Repetti, P.P., Galbraith, D.W., Girke, T., Bailey-Serres, J.: Profiling translatomes of discrete cell populations resolves altered cellular priorities during hypoxia in Arabidopsis. - PNAS 106: 18843–18848, 2009.

    Article  PubMed  PubMed Central  Google Scholar 

  • Phukan, U.J., Jeena, G.S., Shukla, R.K.: WRKY transcription factors: molecular regulation and stress responses in plants. - Front. Plant Sci. 7: 760, 2016.

    Article  PubMed  PubMed Central  Google Scholar 

  • Raineri, J., Ribichich, K.F., Chan, R.L.: The sunflower transcription factor HaWRKY76 confers drought and flood tolerance to Arabidopsis thaliana plants without yield penalty. - Plant Cell Rep. 34: 2065–2080, 2015.

    Article  PubMed  CAS  Google Scholar 

  • Rivera-Contreras, I.K., Zamora-Hernández, T., Huerta-Heredia, A.A., Capataz-Tafur, J., Barrera-Figueroa, B.E., Juntawong, P., Peña-Castro, J.M.: Transcriptomic analysis of submergence-tolerant and sensitive Brachypodium distachyon ecotypes reveals oxidative stress as a major tolerance factor. - Nature 6: 27686, 2016.

    CAS  Google Scholar 

  • Rushton, P.J., Somssich, I.E., Ringler, P., Shen, Q.J.: WRKY transcription factors. - Trends Plant Sci. 15: 247–258, 2010.

    Article  PubMed  CAS  Google Scholar 

  • Sakai, W.S.: Simple method for differential staining of paraffin embedded plant material using toluidine blue. - Stain Technol. 48: 247–249, 1973.

    Article  PubMed  CAS  Google Scholar 

  • Schneider, A.C., Rasband, W.S., Eliceiri, K.W.: NIH Image to ImageJ: 25 years of image analysis. - Nat. Methods 9: 671–675, 2012.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Setter, T.L., Waters, I.: Review of prospects for germplasm improvement for waterlogging tolerance in wheat, barley and oats. - Plant Soil 253: 1–34, 2003.

    Article  CAS  Google Scholar 

  • Suralta, R.R., Yamauchi, A.: Root growth, aerenchyma development, and oxygen transport in rice genotypes subjected to drought and waterlogging. - Environ. exp. Bot. 64: 75–82, 2008.

    Article  CAS  Google Scholar 

  • Tamang, B.G., Fukao, T.: Plant adaptation to multiple stresses during submergence and following desubmergence. - Int. J. mol. Sci. 16: 30164–30180, 2015.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Van de Poel, B., Straeten, D.V.: 1-aminocyclopropane-1- carboxylic acid (ACC) in plants: more than just the precursor of ethylene!. - Front. Plant Sci. 5: 640, 2014.

    PubMed  PubMed Central  Google Scholar 

  • Wang, K.L.C., Li, H., Ecker, J.R.: Ethylene biosynthesis and signaling networks. - Plant Cell 14: 131–151, 2002.

    Article  CAS  Google Scholar 

  • Xu, K., Xu, X., Fukao, T., Canlas, P., Maghirang-Rodriguez, R., Heuer, S., Ismail, A.M., Bailey-Serres, J., Ronald, P.C., Mackill, D.J.: Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. - Nature 442: 705–708, 2006.

    Article  PubMed  CAS  Google Scholar 

  • Yoo, Y-H., Choi, H-K., Jung, K-H.: Genome-wide identification and analysis of genes associated with lysigenous aerenchyma formation in rice roots. - J. Plant Biol. 58: 117–127, 2015.

    Article  CAS  Google Scholar 

  • Yoshida, S., Forno, D.A., Cock, J.H., Gomez, K.A. (ed.): Laboratory Manual for Physiological Studies of Rice. - The International Rice Research Institute, Los Baños 1976.

    Google Scholar 

  • Yukiyoshi, K., Karahara, I.: Role of ethylene signalling in the formation of constitutive aerenchyma in primary roots of rice. - AoB Plants 6: plu043, 2014.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Graduate Program in Biotechnology, Center for Technological Development, Federal University of Pelotas, Pelotas, 96001970, RS, Brazil

    V. E. Viana & A. Costa de Oliveira

  2. Plant Genomics and Breeding Center, Eliseu Maciel School of Agronomy, Federal University of Pelotas, Pelotas, 96001970, RS, Brazil

    V. E. Viana, N. Marini, C. Busanello, C. Pegoraro, L. C. Da Maia & A. Costa de Oliveira

  3. Department of Botany, Institute of Biology, Federal University of Pelotas, Pelotas, 96001970, RS, Brazil

    J. A. Fernando

Authors
  1. V. E. Viana
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. N. Marini
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. C. Busanello
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. C. Pegoraro
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. J. A. Fernando
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. L. C. Da Maia
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. A. Costa de Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. Costa de Oliveira.

Additional information

Acknowledgments: The financial support of the Coordination for the Improvement of Higher Education Personnel (CAPES), the Research Support Foundation of Rio Grande do Sul (FAPERGS), and the Brazilian National Council for Scientific, Technological Development (CNPq) was appreciated, as well as the possibility of the use of facilities of the Plant Anatomy Laboratory of Escola Superior de Agricultura ‘Luiz de Queiroz’, Universidade São Paulo. We also thank Miss Victoria Oliveira (Lafayette, IN, USA) for the English revision of this manuscript.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Viana, V.E., Marini, N., Busanello, C. et al. Regulation of rice responses to submergence by WRKY transcription factors. Biol Plant 62, 551–560 (2018). https://doi.org/10.1007/s10535-018-0806-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10535-018-0806-3

Additional key words

Search

Navigation