Skip to main content
SpringerLink
Log in

ipa1 improves rice drought tolerance at seedling stage mainly through activating abscisic acid pathway

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

Abstract

Key message

ipa1 enhances rice drought tolerance mainly through activating the ABA pathway. It endows rice seedlings with a more developed root system, smaller leaf stomata aperture, and enhanced carbon metabolism.

Abstract

Drought is a major abiotic stress to crop production. IPA1 (IDEAL PLANT ARCHITECTURE 1)/OsSPL14 encodes a transcription factor and has been reported to function in both rice ideal plant architecture and biotic resistance. Here, with a pair of IPA1 and ipa1-NILs (Near Iso-genic Lines), we found that ipa1 could significantly improve rice drought tolerance at seedling stage. The ipa1 plants had a better-developed root system and smaller leaf stomatal aperture. Analysis of carbon–nitrogen metabolism-associated enzyme activity, gene expression, and metabolic profile indicated that ipa1 could tip the carbon–nitrogen metabolism balance towards an increased carbon metabolism pattern. In both the control and PEG-treated conditions, ABA content in the ipa1 seedlings was significantly higher than that in the IPA1 seedlings. Expression of the ABA biosynthesis genes was detected to be up-regulated, whereas the expression of ABA catabolism genes was down-regulated in the ipa1 seedlings. In addition, based on yeast one-hybrid assay and dual-luciferase assay, IPA1 was found to directly activate the promoter activity of OsHOX12, a transcription factor promoting ABA biosynthesis, and OsNAC52, a positive regulator of the ABA pathway. The expression of OsHOX12 and OsNAC52 was significantly up-regulated in the ipa1 plants. Combined with the previous studies, our results suggested that ipa1 could improve rice seedling drought tolerance mainly through activating the ABA pathway and that regulation of the ipa1-mediated ABA pathway will be an important strategy for improving drought resistance of rice.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Aragon EL, De Datta SK (1982) Drought response of rice at different nitrogen levels using line source sprinkler system. Irrig Sci 3:63–73

    Article  Google Scholar 

  • Baillo EH, Kimotho RN, Zhang Z, Xu P (2019) Transcription factors associated with abiotic and biotic stress tolerance and their potential for crops improvement. Genes (basel) 10:771–793

    Article  CAS  Google Scholar 

  • Barnaby JY, Rohila JS, Henry CG, Sicher RC, Reddy VR, McClung AM (2019) Physiological and metabolic responses of rice to reduced soil moisture: relationship of water stress tolerance and grain production. Int J Mol Sci 20:1846

    Article  CAS  PubMed Central  Google Scholar 

  • Blanke MM, Ebert G (1992) Phosphoenolpyruvate carboxylase and carbon economy of apple seedlings. J Exp Bot 43:965–968

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    CAS  PubMed  Google Scholar 

  • Cai S, Jiang G, Ye N, Chu Z, Xu X, Zhang J, Zhu G (2015) A key ABA catabolic gene, OsABA8ox3, is involved in drought stress resistance in rice. PLoS ONE 10:e0116646

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen W, Gao Y, Xie W, Gong L, Lu K, Wang W, Li Y, Liu X, Zhang H, Dong H, Zhang W, Zhang L, Yu S, Wang G, Lian X, Luo J (2014) Genome-wide association analyses provide genetic and biochemical insights into natural variation in rice metabolism. Nat Genet 46:714–721

    Article  CAS  PubMed  Google Scholar 

  • Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61:651–679

    Article  CAS  PubMed  Google Scholar 

  • Doane TA, Horwáth WR (2003) Spectrophotometric determination of nitrate with a single reagent. Anal Lett 36:2713–2722

    Article  CAS  Google Scholar 

  • Droux M (2004) Sulfur assimilation and the role of sulfur in plant metabolism: a survey. Photosynth Res 79:331–348

    Article  CAS  PubMed  Google Scholar 

  • Fujii H, Chinnusamy V, Rodrigues A, Rubio S, Antoni R, Park SY, Cutler SR, Sheen J, Rodriguez PL, Zhu JK (2009) In vitro reconstitution of an abscisic acid signalling pathway. Nature 462:660–664

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao F, Xiong A, Peng R, Jin X, Xu J, Zhu B, Chen J, Yao Q (2010) OsNAC52, a rice NAC transcription factor, potentially responds to ABA and confers drought tolerance in transgenic plants. Plant Cell Tiss Organ Cult 100:255–262

    Article  CAS  Google Scholar 

  • Garg AK, Kim JK, Owens TG, Ranwala AP, Choi YD, Kochian LV, Wu RJ (2002) Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc Natl Acad Sci USA 99:15898–15903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gonzalez-Grandio E, Pajoro A, Franco-Zorrilla JM, Tarancon C, Immink RG, Cubas P (2017) Abscisic acid signaling is controlled by a BRANCHED1/HD-ZIP I cascade in Arabidopsis axillary buds. Proc Natl Acad Sci USA 114(2):E245–E254

    Article  CAS  PubMed  Google Scholar 

  • Han H, Tian Z, Fan Y, Cui Y, Cai J, Jiang D, Cao W, Dai T (2015) Water-deficit treatment followed by re-watering stimulates seminal root growth associated with hormone balance and photosynthesis in wheat (Triticum aestivum L.) seedlings. Plant Growth Regul 77:201–210

    Article  CAS  Google Scholar 

  • He F, Zhang F, Sun W, Ning Y, Wang GL (2018) A versatile vector toolkit for functional analysis of rice genes. Rice (NY) 11:27

    Article  Google Scholar 

  • Hu H, Xiong L (2014) Genetic engineering and breeding of drought-resistant crops. Annu Rev Plant Biol 65:715–741

    Article  CAS  PubMed  Google Scholar 

  • Hu H, Dai M, Yao J, Xiao B, Li X, Zhang Q, Xiong L (2006) Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc Natl Acad Sci USA 103:12987–12992

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang XY, Chao DY, Gao JP, Zhu MZ, Shi M, Lin HX (2009) A previously unknown zinc finger protein, DST, regulates drought and salt tolerance in rice via stomatal aperture control. Genes Dev 23:1805–1817

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang A, Sang Y, Sun W, Fu Y, Yang Z (2016) Transcriptomic analysis of responses to imbalanced carbon: nitrogen availabilities in rice seedlings. PLoS ONE 11:e0165732

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Huang Y, Guo Y, Liu Y, Zhang F, Wang Z, Wang H, Wang F, Li D, Mao D, Luan S, Liang M, Chen L (2018) 9-cis-epoxycarotenoid dioxygenase 3 regulates plant growth and enhances multi-abiotic stress tolerance in rice. Front Plant Sci 9:162

    Article  PubMed  PubMed Central  Google Scholar 

  • Hwang SG, Chen HC, Huang WY, Chu YC, Shii CT, Cheng WH (2010) Ectopic expression of rice OsNCED3 in Arabidopsis increases ABA level and alters leaf morphology. Plant Sci 178:12–22

    Article  CAS  Google Scholar 

  • Jiao Y, Wang Y, Xue D, Wang J, Yan M, Liu G, Dong G, Zeng D, Lu Z, Zhu X, Qian Q, Li J (2010) Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat Genet 42:541–544

    Article  CAS  PubMed  Google Scholar 

  • Li H, Liang Z, Ding G, Shi L, Xu F, Cai H (2016) A natural light/dark cycle regulation of carbon-nitrogen metabolism and gene expression in rice shoots. Front Plant Sci 7:1318

    PubMed  PubMed Central  Google Scholar 

  • Liang J, Cao X, Zhu Q (1996) Abscisic acid may involve in the regulation of grain filling in water stressed rice (Oryza sativa L.). Chin J Rice Sci 10:29–36

    Google Scholar 

  • Lin Q, Zhang Z, Wu F, Feng M, Sun Y, Chen W, Cheng Z, Zhang X, Ren Y, Lei C, Zhu S, Wang J, Zhao Z, Guo X, Wang H, Wan J (2020) The APC/C(TE) E3 ubiquitin ligase complex mediates the antagonistic regulation of root growth and tillering by ABA and GA. Plant Cell 32:1973–1987

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu M, Shi Z, Zhang X, Wang M, Zhang L, Zheng K, Liu J, Hu X, Di C, Qian Q, He Z, Yang DL (2019) Inducible overexpression of Ideal Plant Architecture1 improves both yield and disease resistance in rice. Nat Plants 5:389–400

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Hu Q, Yan J, Sun K, Liang Y, Jia M, Meng X, Fang S, Wang Y, Jing Y, Liu G, Wu D, Chu C, Smith SM, Chu J, Wang Y, Li J, Wang B (2020) ζ-carotene isomerase suppresses tillering in rice through the coordinated biosynthesis of strigolactone and abscisic acid. Mol Plant 13:1784–1801

    Article  CAS  PubMed  Google Scholar 

  • Lu Z, Yu H, Xiong G, Wang J, Jiao Y, Liu G, Jing Y, Meng X, Hu X, Qian Q, Fu X, Wang Y, Li J (2013) Genome-wide binding analysis of the transcription activator IDEAL PLANT ARCHITECTURE1 reveals a complex network regulating rice plant architecture. Plant Cell 25:3743–3759

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma X, Xia H, Liu Y, Wei H, Zheng X, Song C, Chen L, Liu H, Luo L (2016) Transcriptomic and metabolomic studies disclose key metabolism pathways contributing to well-maintained photosynthesis under the drought and the consequent drought-tolerance in rice. Front Plant Sci 7:1886

    PubMed  PubMed Central  Google Scholar 

  • McAdam SA, Brodribb TJ, Ross JJ (2016) Shoot-derived abscisic acid promotes root growth. Plant Cell Environ 39:652–659

    Article  CAS  PubMed  Google Scholar 

  • Miura K, Ikeda M, Matsubara A, Song XJ, Ito M, Asano K, Matsuoka M, Kitano H, Ashikari M (2010) OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat Genet 42:545–549

    Article  CAS  PubMed  Google Scholar 

  • Nakashima K, Fujita Y, Kanamori N, Katagiri T, Umezawa T, Kidokoro S, Maruyama K, Yoshida T, Ishiyama K, Kobayashi M, Shinozaki K, Yamaguchi-Shinozaki K (2009) Three Arabidopsis SnRK2 protein kinases, SRK2D/SnRK2.2, SRK2E/SnRK2.6/OST1 and SRK2I/SnRK2.3, involved in ABA signaling are essential for the control of seed development and dormancy. Plant Cell Physiol 50:1345–1363

    Article  CAS  PubMed  Google Scholar 

  • Osuna D, Prieto P, Aguilar M (2015) Control of seed germination and plant development by carbon and nitrogen availability. Front Plant Sci 6:1023

    Article  PubMed  PubMed Central  Google Scholar 

  • Schroeder JI, Kwak JM, Allen GJ (2001) Guard cell abscisic acid signalling and engineering drought hardiness in plants. Nature 410:327–330

    Article  CAS  PubMed  Google Scholar 

  • Shi H, Wang B, Yang P, Li Y, Miao F (2016) Differences in sugar accumulation and mobilization between sequential and non-sequential senescence wheat cultivars under natural and drought conditions. PLoS ONE 11:e0166155

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shields R, Burnett W (1960) Determination of protein-bound carbohydrate in serum by modified anthrone method. Anal Chem 32:885–886

    Article  CAS  Google Scholar 

  • Su H, Wang T, Ju C, Deng J, Zhang T, Li M, Tian H, Wang C (2021) Abscisic acid signaling negatively regulates nitrate uptake via phosphorylation of NRT1.1 by SnRK2s in Arabidopsis. J Integr Plant Biol 63:597–610

    Article  CAS  PubMed  Google Scholar 

  • Sun S-W, Lin Y-C, Weng Y-M, Chen M-J (2006) Efficiency improvements on ninhydrin method for amino acid quantification. J Food Compos Anal 19:112–117

    Article  CAS  Google Scholar 

  • Takasaki H, Maruyama K, Kidokoro S, Ito Y, Fujita Y, Shinozaki K, Yamaguchi-Shinozaki K, Nakashima K (2010) The abiotic stress-responsive NAC-type transcription factor OsNAC5 regulates stress-inducible genes and stress tolerance in rice. Mol Genet Genom 284:173–183

    Article  CAS  Google Scholar 

  • Tang T, Xie H, Wang Y, Lu B, Liang J (2009) The effect of sucrose and abscisic acid interaction on sucrose synthase and its relationship to grain filling of rice (Oryza sativa L.). J Exp Bot 60:2641–2652

    Article  CAS  PubMed  Google Scholar 

  • Vishal B, Kumar PP (2018) Regulation of seed germination and abiotic stresses by gibberellins and abscisic acid. Front Plant Sci 9:838

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang H, Wang H (2015) The miR156/SPL module, a regulatory hub and versatile toolbox, gears up crops for enhanced agronomic traits. Mol Plant 8:677–688

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Yu C, Xu S, Zhu Y, Huang W (2016) OsDi19-4 acts downstream of OsCDPK14 to positively regulate ABA response in rice. Plant Cell Environ 39:2740–2753

    Article  CAS  PubMed  Google Scholar 

  • Wang B, Smith SM, Li J (2018a) Genetic regulation of shoot architecture. Annu Rev Plant Biol 69:437–468

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Zhou L, Shi H, Chern M, Yu H, Yi H, He M, Yin J, Zhu X, Li Y, Li W, Liu J, Wang J, Chen X, Qing H, Wang Y, Liu G, Wang W, Li P, Wu X, Zhu L, Zhou J-M, Ronald PC, Li S, Li J, Chen X (2018b) A single transcription factor promotes both yield and immunity in rice. Science 361:1026–1028

    Article  CAS  PubMed  Google Scholar 

  • Wang Q, Nian J, Xie X, Yu H, Zhang J, Bai J, Dong G, Hu J, Bai B, Chen L, Xie Q, Feng J, Yang X, Peng J, Chen F, Qian Q, Li J, Zuo J (2018c) Genetic variations in ARE1 mediate grain yield by modulating nitrogen utilization in rice. Nat Commun 9:735

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yu S, Ali J, Zhang C, Li Z, Zhang Q (2020) Genomic breeding of green super rice varieties and their deployment in Asia and Africa. Theor Appl Genet 133:1427–1442

    Article  PubMed  PubMed Central  Google Scholar 

  • Zakari SA, Asad M-A-U, Han Z, Zhao Q, Cheng F (2020) Relationship of nitrogen deficiency-induced leaf senescence with ROS generation and ABA concentration in rice flag leaves. J Plant Growth Regul 39:1503–1517

    Article  CAS  Google Scholar 

  • Zhang DP, Zhou Y, Yin JF, Yan XJ, Lin S, Xu WF, Baluska F, Wang YP, Xia YJ, Liang GH, Liang JS (2015) Rice G-protein subunits qPE9-1 and RGB1 play distinct roles in abscisic acid responses and drought adaptation. J Exp Bot 66:6371–6384

    Article  CAS  PubMed  Google Scholar 

  • Zheng Z, Xu X, Crosley RA, Greenwalt SA, Sun Y, Blakeslee B, Wang L, Ni W, Sopko MS, Yao C, Yau K, Burton S, Zhuang M, McCaskill DG, Gachotte D, Thompson M, Greene TW (2010) The protein kinase SnRK2.6 mediates the regulation of sucrose metabolism and plant growth in Arabidopsis. Plant Physiol 153:99–113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors thank Dr. Q.Qian of the China National Rice Research Institute for providing the ipa1 donor rice cv. Shaoniejing used in this particular research. This work was financed by the Special Transgenic Program of the Ministry of Agriculture in China (No. 2016ZX08001004-002), the National Natural Science Foundation of China (No.31901522), and the Collaborative Innovation Center of Hubei Province for Hybrid Rice.

Author information

Authors and Affiliations

  1. State Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan University, Wuhan, 430072, China

    Menghao Zhu, Yonggang He, Mingqiang Zhu, Ayaz Ahmad, Shuang Xu, Zijun He, Shan Jiang, Jinqiu Huang, Zhihui Li, Shaojia Liu, Xin Hou & Zhihong Zhang

  2. Ezhou Seed Technology Research Institute of Hubei Province, Ezhou, 436043, China

    Menghao Zhu, Yonggang He, Shaojia Liu & Zhihong Zhang

Authors
  1. Menghao Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yonggang He
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mingqiang Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ayaz Ahmad
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shuang Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zijun He
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Shan Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jinqiu Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Zhihui Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Shaojia Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Xin Hou
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Zhihong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MZ and ZZ designed the experiments. MZ performed most experiments. MZ, YH and ZZ analyzed the data. MZ, AA, SX, ZH, SJ, JH, ZL and SL assisted in the materials and data collection. MZ, XH and ZZ drafted the manuscript.

Corresponding author

Correspondence to Zhihong Zhang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Emmanuel Guiderdoni.

Publisher's Note

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

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhu, M., He, Y., Zhu, M. et al. ipa1 improves rice drought tolerance at seedling stage mainly through activating abscisic acid pathway. Plant Cell Rep 41, 221–232 (2022). https://doi.org/10.1007/s00299-021-02804-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-021-02804-3

Keywords

Search

Navigation