Skip to main content

Advertisement

Log in

A comprehensive investigation of the regulatory roles of OsERF096, an AP2/ERF transcription factor, in rice cold stress response

  • Original Article
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

OsERF096 negatively regulates rice cold tolerance and mediates IAA biosynthesis and signaling under cold stress.

Abstract

The APETALA2/ethylene-responsive factor (AP2/ERF) transcription factors play important roles in regulating plant tolerance to abiotic stress. OsERF096 was previously identified as a direct target of miR1320, and was suggested to negatively regulate rice cold tolerance. In this study, we performed RNA-sequencing and targeted metabolomics assays to reveal the regulatory roles of OsERF096 in cold stress response. GO and KEGG analysis of differentially expressed genes showed that the starch and sucrose metabolism, plant–pathogen interaction, and plant hormone signal transduction pathways were significantly enriched. Quantification analysis confirmed a significant difference in sugar contents among WT and OsERF096 transgenic lines under cold treatment. Targeted metabolomics analysis uncovered that IAA accumulation and signaling were modified by OsERF096 in response to cold stress. Expectedly, qRT-PCR assays confirmed significant OsIAAs and OsARFs expression changes in OsERF096 transgenic lines. Finally, we identified three targets of OsERF096 based on RNA-seq, qRT-PCR, and dual-LUC assays. In summary, these results revealed the multiple regulatory roles of OsERF096 in cold stress response.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

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

Similar content being viewed by others

Data availability

The data generated or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Aslam M, Sugita K, Qin Y, Rahman A (2020) Aux/IAA14 regulates microrna-mediated cold stress response in Arabidopsis roots. Int J Mol Sci 21:8441

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ba L, Kuang J, Chen J, Lu W (2016) MaJAZ1 attenuates the MaLBD5-mediated transcriptional activation of jasmonate biosynthesis gene MaAOC2 in regulating cold tolerance of banana fruit. J Agric Food Chem 64:738–745

    Article  CAS  PubMed  Google Scholar 

  • Challam C, Ghosh T, Rai M, Tyagi W (2015) Allele mining across DREB1A and DREB1B in diverse rice genotypes suggest a highly conserved pathway inducible by low temperature. J Genet 94:231–238

    Article  CAS  PubMed  Google Scholar 

  • Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020a) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13:1194–1202

    Article  CAS  PubMed  Google Scholar 

  • Chen L, Huang X, Zhao S, Xiao D, Xiao L, Tong J, Wang W, Li Y, Ding Z, Hou B (2020b) IPyA glucosylation mediates light and temperature signaling to regulate auxin-dependent hypocotyl elongation in Arabidopsis. Proc Natl Acad Sci USA 117:6910–6917

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen H, Chien T, Chen T, Chiang M, Lai M, Chang M (2021) Overexpression of a novel ERF-X-Type transcription factor, OsERF106MZ, reduces shoot growth and tolerance to salinity stress in rice. Rice 14:82

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ding Y, Sun T, Ao K, Peng Y, Zhang Y, Li X, Zhang Y (2018) Opposite roles of salicylic acid receptors NPR1 and NPR3/NPR4 in transcriptional regulation of plant immunity. Cell 173:1454-1467.e1415

    Article  CAS  PubMed  Google Scholar 

  • Dombrecht B, Xue GP, Sprague SJ, Kirkegaard JA, Ross JJ, Reid JB, Fitt GP, Sewelam N, Schenk PM, Manners JM, Kazan K (2007) MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis. Plant Cell 19:2225–2245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Du H, Wu N, Fu J, Wang S, Li X, Xiao J, Xiong L (2012) A GH3 family member, OsGH3-2, modulates auxin and abscisic acid levels and differentially affects drought and cold tolerance in rice. J Exp Bot 63:6467–6480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Du H, Wu N, Chang Y, Li X, Xiao J, Xiong L (2013) Carotenoid deficiency impairs ABA and IAA biosynthesis and differentially affects drought and cold tolerance in rice. Plant Mol Biol 83:475–488

    Article  CAS  PubMed  Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Rebers PA (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    Article  CAS  Google Scholar 

  • Fonseca S, Fernández-Calvo P, Fernández GM, Díez-Díaz M, Gimenez-Ibanez S, López-Vidriero I, Godoy M, Fernández-Barbero G, Van Leene J, De Jaeger G, Franco-Zorrilla JM, Solano R (2014) bHLH003, bHLH013 and bHLH017 are new targets of jaz repressors negatively regulating JA responses. PLoS ONE 9:e86182

    Article  PubMed  PubMed Central  Google Scholar 

  • Fu J, Yu Q, Zhang C, Xian B, Fan J, Huang X, Yang W, Zou X, Chen S, Su L, He Y, Li Q (2023) CsAP2-09 confers resistance against citrus bacterial canker by regulating CsGH3.1L-mediated phytohormone biosynthesis. Int J Biol Macromol 229:964–973

    Article  CAS  PubMed  Google Scholar 

  • Hong Y, Wang H, Gao Y, Bi Y, Xiong X, Yan Y, Wang J, Li D, Song F (2022) ERF transcription factor OsBIERF3 positively contributes to immunity against fungal and bacterial diseases but negatively regulates cold tolerance in rice. Int J Mol Sci 23:606

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu Y, Jiang L, Wang F, Yu D (2013) Jasmonate regulates the inducer of cbf expression–c-repeat binding factor/DRE binding factor1 cascade and freezing tolerance in Arabidopsis. Plant Cell 25:2907–2924

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jackson RG, Lim E-K, 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  CAS  PubMed  Google Scholar 

  • Jisha V, Dampanaboina L, Vadassery J, Mithöfer A, Kappara S, Ramanan R (2015) Overexpression of an AP2/ERF type transcription factor OsEREBP1 confers biotic and abiotic stress tolerance in rice. PLoS ONE 10:e0127831

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jung H, Chung PJ, Park S, Redillas MCFR, Kim YS, Suh J, Kim J (2017) Overexpression of OsERF48 causes regulation of OsCML16, a calmodulin-like protein gene that enhances root growth and drought tolerance. Plant Biotechnol J 15:1295–1308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ke Y, Yang Z, Yu S, Li T, Wu J, Gao H, Fu Y, Luo L (2014) Characterization of OsDREB6 responsive to osmotic and cold stresses in rice. J Plant Biol 57:150–161

    Article  CAS  Google Scholar 

  • Kumar M, Kesawat MS, Ali A, Lee SC, Gill SS, Kim AHU (2019) Integration of abscisic acid signaling with other signaling pathways in plant stress responses and development. Plants 8:592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leisner CP, Potnis N, Sanz-Saez A (2022) Crosstalk and trade-offs: plant responses to climate change-associated abiotic and biotic stresses. Plant Cell Environ 46(10):2946–2963

    Article  Google Scholar 

  • Li W, Zhang M, Qiao L, Chen Y, Zhang D, Jing X, Gan P, Huang Y, Gao J, Liu W, Shi C, Cui H, Li H, Chen K (2022) Characterization of wavy root 1, an agravitropism allele, reveals the functions of OsPIN2 in fine regulation of auxin transport and distribution and in ABA biosynthesis and response in rice (Oryza sativa L.). Crop J 10:980–992

    Article  Google Scholar 

  • Liu D, Chen X, Liu J, Ye J, Guo Z (2012) The rice ERF transcription factor OsERF922 negatively regulates resistance to Magnaporthe oryzae and salt tolerance. J Exp Bot 63:3899–3911

    Article  CAS  PubMed Central  Google Scholar 

  • Liu CT, Wang W, Mao BG, Chu CC (2018) Cold stress tolerance in rice: physiological changes, molecular mechanism, and future prospects. Hereditas 40:171–185

    PubMed  Google Scholar 

  • Liu C, Li C, Bing H, Zhao J, Li L, Sun P, Li T, Du D, Zhao J, Wang X, Xiang W (2023) Integrated physiological, transcriptomic, and metabolomic analysis reveals the mechanism of guvermectin promoting seed germination in direct-seeded rice under chilling stress. J Agric Food Chem 71:7348–7358

    Article  CAS  PubMed  Google Scholar 

  • Luo J, Zhou J, Zhang J (2018) Aux/IAA gene family in plants: Molecular structure, regulation, and function. Int J Mol Sci 19:259

    Article  PubMed  PubMed Central  Google Scholar 

  • Madore MA (1990) Carbohydrate metabolism in photosynthetic and nonphotosynthetic tissues of variegated leaves of coleus blumei benth. Plant Physiol 93:617–622

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mao D, Chen C (2012) Colinearity and similar expression pattern of rice DREB1s reveal their functional conservation in the cold-responsive pathway. PLoS ONE 7:e47275

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mao X, Cai T, Olyarchuk JG, Wei L (2005) Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics 21:3787–3793

    Article  CAS  PubMed  Google Scholar 

  • Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) AP2/ERF family transcription factors in plant abiotic stress responses. Biochim Biophys Acta 1819:86–96

    Article  CAS  PubMed  Google Scholar 

  • Moon S-J, Min MK, Kim J-A, Kim DY, Yoon IS, Kwon TR, Byun MO, Kim B-G (2019) Ectopic expression of OsDREB1G, a member of the OsDREB1 subfamily, confers cold stress tolerance in rice. Front Plant Sci 10:297

    Article  Google Scholar 

  • Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140:411–432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nayyar H, Bains T, Kumar S (2005) Low temperature induced floral abortion in chickpea: relationship to abscisic acid and cryoprotectants in reproductive organs. Environ Exp Bot 53:39–47

    Article  CAS  Google Scholar 

  • Niu Y, Fan S, Cheng B, Li H, Wu J, Zhao H, Huang Z, Yan F, Qi B, Zhang L, Zhang G (2023) Comparative transcriptomics and co-expression networks reveal cultivar-specific molecular signatures associated with reproductive-stage cold stress in rice. Plant Cell Rep 42:707–722

    Article  CAS  PubMed  Google Scholar 

  • Olate E, Jiménez-Gómez JM, Holuigue L, Salinas J (2018) NPR1 mediates a novel regulatory pathway in cold acclimation by interacting with HSFA1 factors. Nat Plants 4:811–823

    Article  CAS  PubMed  Google Scholar 

  • Pillai SE, Kumar C, Dasgupta M, Kumar BK, Vungarala S, Patel HK, Sonti RV (2020) Ectopic expression of a cell-wall-degrading enzyme-induced OsAP2/ERF152 leads to resistance against bacterial and fungal infection in Arabidopsis. Phytopathology 110:726–733

    Article  CAS  PubMed  Google Scholar 

  • Rahman A (2013) Auxin: a regulator of cold stress response. Physiol Plant 147:28–35

    Article  CAS  PubMed  Google Scholar 

  • Rashid M, Guangyuan H, Guangxiao Y, Hussain J, Xu Y (2012) AP2/ERF transcription factor in rice: genome-wide canvas and syntenic relationships between monocots and eudicots. Evol Bioinform Online 8:321–355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ritonga FN, Ngatia JN, Wang Y, Khoso MA, Farooq U, Chen S (2021) AP2/ERF, an important cold stress-related transcription factor family in plants: a review. Physiol Mol Biol Plants 27:1953–1968

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruan J, Zhou Y, Zhou M, Yan J, Khurshid M, Weng W, Cheng J, Zhang K (2019) Jasmonic acid signaling pathway in plants. Int J Mol Sci 20:2479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi-Shinozaki K (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochem Biophys Res Commun 290:998–1009

    Article  CAS  PubMed  Google Scholar 

  • Schmidt R, Mieulet D, Hubberten HM, Obata T, Hoefgen R, Fernie AR, Fisahn J, San Segundo B, Guiderdoni E, Schippers JHM, Mueller-Roeber B (2013) Salt-responsive ERF1 regulates reactive oxygen species–dependent signaling during the initial response to salt stress in rice. Plant Cell 25:2115–2131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Serra TS, Figueiredo DD, Cordeiro AM, Almeida DM, Lourenço T, Abreu IA, Sebastián A, Fernandes L, Contreras-Moreira B, Oliveira MM, Saibo NJM (2013) OsRMC, a negative regulator of salt stress response in rice, is regulated by two AP2/ERF transcription factors. Plant Mol Biol 82:439–455

    Article  CAS  PubMed  Google Scholar 

  • Sheng Y (2015) Function analysis of stress tolerance gene OsSTAP1 in rice. Master, University of Chinese Academy of Agricultural Sciences

  • Shi Y, Yang S (2015) COLD1: a cold sensor in rice. Sci China Life Sci 58:409–410

    Article  PubMed  Google Scholar 

  • Sun M, Shen Y, Chen Y, Wang Y, Cai X, Yang J, Jia B, Dong W, Chen X, Sun X (2022) Osa-miR1320 targets the ERF transcription factor OsERF096 to regulate cold tolerance via JA-mediated signaling. Plant Physiol 189:2500–2516

    Article  PubMed  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  CAS  PubMed  Google Scholar 

  • Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 448:661–665

    Article  CAS  PubMed  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, Inzé 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  CAS  PubMed  PubMed Central  Google Scholar 

  • Tunsagool P, Jutidamrongphan W, Phaonakrop N, Jaresitthikunchai J, Roytrakul S, Leelasuphakul W (2019) Insights into stress responses in mandarins triggered by Bacillus subtilis cyclic lipopeptides and exogenous plant hormones upon Penicillium digitatum infection. Plant Cell Rep 38:559–575

    Article  CAS  PubMed  Google Scholar 

  • Wan L, Zhang J, Zhang H, Zhang Z, Quan R, Zhou S, Huang R (2011) Transcriptional activation of OsDERF1 in OsERF3 and OsAP2-39 negatively modulates ethylene synthesis and drought tolerance in rice. PLoS ONE 6:e25216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Q, Guan Y, Wu Y, Chen H, Chen F, Chu C (2008) Overexpression of a rice OsDREB1F gene increases salt, drought, and low temperature tolerance in both Arabidopsis and rice. Plant Mol Biol 67:589–602

    Article  CAS  PubMed  Google Scholar 

  • Wang F, Wang C, Liu P, Lei C, Hao W, Gao Y, Liu Y, Zhao K (2016) Enhanced rice blast resistance by CRISPR/Cas9-targeted mutagenesis of the ERF transcription factor gene OsERF922. PLoS ONE 11:e0154027

    Article  PubMed Central  Google Scholar 

  • Wang H, Li Y, Chern M, Zhu Y, Zhang L, Lu J, Li X, Dang W, Ma X, Yang Z, Yao S, Zhao Z, Fan J, Huang Y, Zhang J, Pu M, Wang J, He M, Li W, Chen X, Wu X, Li S, Li P, Li Y, Ronald PC, Wang W (2021a) Suppression of rice miR168 improves yield, flowering time and immunity. Nat Plants 7:129–136

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Pan L, Wang Y, Meng J, Deng L, Niu L, Liu H, Ding Y, Yao J-L, Nieuwenhuizen NJ, Ampomah-Dwamena C, Lu Z, Cui G, Wang Z, Zeng W (2021b) PpIAA1 and PpERF4 form a positive feedback loop to regulate peach fruit ripening by integrating auxin and ethylene signals. Plant Sci 313:111084

    Article  CAS  PubMed  Google Scholar 

  • Wang Y (2013) Cloning and functional identification of four stress-induced genes in rice. Master, University of Huazhong Agricultural Unversity

  • Xiong H, Yu J, Miao J, Li J, Zhang H, Wang X, Liu P, Zhao Y, Jiang C, Yin Z, Li Y, Guo Y, Fu B, Wang W, Li Z, Ali J, Li Z (2018) Natural variation in OsLG3 increases drought tolerance in rice by inducing ROS scavenging. Plant Physiol 178:451–467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yao Y, He RJ, Xie QL, Zhao Xh, Xm D, Jb He, Song L, He J, Marchant A, Chen X, Wu A (2017) ETHYLENE RESPONSE FACTOR 74 (ERF74) plays an essential role in controlling a respiratory burst oxidase homolog D (RbohD)-dependent mechanism in response to different stresses in Arabidopsis. New Phytol 213:1667–1681

    Article  CAS  PubMed  Google Scholar 

  • Young MD, Wakefield MJ, Smyth GK, Oshlack A (2010) Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 11:R14

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Chen C, Jin XF, Xiong AS, Peng RH, Hong YH, Yao QH, Chen JM (2009) Expression of a rice DREB1 gene, OsDREB1D, enhances cold and high-salt tolerance in transgenic Arabidopsis. BMB Rep 42:486–492

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Zhang J, Quan R, Pan X, Wan L, Huang R (2013) EAR motif mutation of rice OsERF3 alters the regulation of ethylene biosynthesis and drought tolerance. Planta 237:1443–1451

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Li J, Chen S, Ma X, Wei H, Chen C, Gao N, Zou Y, Kong D, Li T, Liu Z, Yu S, Luo L (2020) An APETALA2/ethylene responsive factor, OsEBP89 knockout enhances adaptation to direct-seeding on wet land and tolerance to drought stress in rice. Mol Genet Genom 295:941–956

    Article  CAS  Google Scholar 

Download references

Funding

This work was supported by the National Natural Science Foundation of China (32101672, U20A2025), and Key Research and Development Plan of Heilongjiang Province (GZ2022ZX02B05-2).

Author information

Authors and Affiliations

Authors

Contributions

XS and MS conceived and designed the experiment. XC and YC completed most of the experiments and wrote the main manuscript. YW prepared the materials for the experiment. YS and JY analyzed experimental data. BJ plotted the resulting images, Figs. 1, 2, 3, 4, 5, 6. All authors have read and approved the final manuscript.

Corresponding authors

Correspondence to Xiaoli Sun or Mingzhe Sun.

Ethics declarations

Conflict of interests

The authors declare that they have no conflicts of interests.

Additional information

Communicated by Leandro Peña.

Publisher's Note

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

Supplementary Information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cai, X., Chen, Y., Wang, Y. et al. A comprehensive investigation of the regulatory roles of OsERF096, an AP2/ERF transcription factor, in rice cold stress response. Plant Cell Rep 42, 2011–2022 (2023). https://doi.org/10.1007/s00299-023-03079-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-023-03079-6

Keywords

Navigation