Skip to main content
SpringerLink
Log in

The maize ATP-binding cassette (ABC) transporter ZmMRPA6 confers cold and salt stress tolerance in plants

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

Abstract

Key message

ZmMRPA6 was cloned and characterized as the first ATP-binding cassette (ABC) transporter in maize to be proven to participate in cold and salt tolerance. Homologous genes AtABCC4 and AtABCC14 of ZmMRPA6 also responded to salt stress.

Abstract

ATP-binding cassette (ABC) proteins are major transmembrane transporters that play significant roles in plant development against various abiotic stresses. However, available information regarding stress-related ABC genes in maize is minimal. In this study, a maize ABC transporter gene, ZmMRPA6, was identified through genome-wide association analysis (GWAS) for cold tolerance in maize seeds germination and functionally characterized. During germination and seedling stages, the zmmrpa6 mutant exhibited enhanced resistance to cold or salt stress. Mutated of ZmMRPA6 did not affect the expression of downstream response genes related cold or salt response at the transcriptional level. Mass spectrometry analysis revealed that most of the differential proteins between zmmrpa6 and wild-type plants were involved in response to stress process including oxidative reduction, hydrolase activity, small molecule metabolism, and photosynthesis process. Meanwhile, the plants which lack the ZmMRPA6 homologous genes AtABCC4 or AtABCC14 were sensitive to salt stress in Arabidopsis. These results indicated that ZmMRPA6 and its homologous genes play a conserved role in cold and salt stress, and functional differentiation occurs in monocotyledonous and dicotyledonous plants. In summary, these findings dramatically improved our understanding of the function of ABC transporters resistance to abiotic stresses in plants.

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
Fig. 8

Similar content being viewed by others

Data availability

The authors confirm that all relevant data supporting the findings of this study are available within the article and its supplementary material. Raw data that supports the findings of this study are available from the corresponding author upon reasonable request.

References

  • An L, Ma Q, Du J, Yu M, Li F, Luan J, Jiang J, Li H (2019) Preliminary classification of the ABC transporter family in Betula halophila and expression patterns in response to exogenous phytohormones and abiotic stresses. Forests 10:722

    Article  Google Scholar 

  • Borghi L, Kang J, de Brito FR (2019) Filling the gap: functional clustering of ABC proteins for the investigation of hormonal transport in planta. Front Plant Sci 10:422

    Article  PubMed  PubMed Central  Google Scholar 

  • Cao Y, Liang X, Yin P, Zhang M, Jiang C (2019) A domestication-associated reduction in K+-preferring HKT transporter activity underlies maize shoot K+ accumulation and salt tolerance. New Phytol 222:301–317

    Article  CAS  PubMed  Google Scholar 

  • Cao Y, Zhang M, Liang X, Li F, Shi Y, Yang X, Jiang C (2020) Natural variation of an EF-hand Ca2+-binding-protein coding gene confers saline-alkaline tolerance in maize. Nat Commun 11:186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dahuja A, Kumar RR, Sakhare A, Watts A, Singh B, Goswami S, Sachdev A, Praveen S (2021) Role of ATP-binding cassette transporters in maintaining plant homeostasis under abiotic and biotic stresses. Physiol Plantarum 171:785–801

    Article  CAS  Google Scholar 

  • Dean JV, Willis M, Shaban L (2022) Transport of acylated anthocyanins by the Arabidopsis ATP-binding cassette transporters AtABCC1, AtABCC2, and AtABCC14. Physiol Plantarum 174:e13780

    Article  CAS  Google Scholar 

  • Do THT, Martinoia E, Lee Y (2018) Functions of ABC transporters in plant growth and development. Curr Opin Plant Biol 41:32–38

    Article  CAS  PubMed  Google Scholar 

  • Dou D, Han S, Cao L et al (2021) CLA4 regulates leaf angle through multiple hormone signaling pathways in maize. J Exp Bot 72:1782–1794

    Article  CAS  PubMed  Google Scholar 

  • Du H, Huang M, Hu J, Li J (2016) Modification of the fatty acid composition in Arabidopsis and maize seeds using a stearoyl-acyl carrier protein desaturase-1 (ZmSAD1) gene. BMC Plant Biol 16:1–10

    Article  Google Scholar 

  • Garcia O, Bouige P, Forestier C, Dassa E (2004) Inventory and comparative analysis of rice and Arabidopsis ATP-binding cassette (ABC) systems. J Mol Biol 343:249–265

    Article  CAS  PubMed  Google Scholar 

  • Gong J, Yao L, Jiao C, Guo Z, Li S, Zuo Y, Shen Y (2022) Ethyl Vinyl Ketone activates K+ Efflux to regulate stomatal closure by MRP4-Dependent eATP accumulation working upstream of H2O2 burst in Arabidopsis. Int J Mol Sci 23:9002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo Z, Yuan X, Li L, Zeng M, Yang J, Tang H, Duan C (2022) Genome-wide analysis of the ATP-binding cassette (ABC) transporter family in Zea mays L. and its response to heavy metal stresses. Int J Mol Sci 23:2109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Han Q, Qi J, Hao G, Zhang C, Wang C, Dirk LM, Downie AB, Zhao T (2020) ZmDREB1A regulates RAFFINOSE SYNTHASE controlling raffinose accumulation and plant chilling stress tolerance in maize. Plant Cell Physiol 61:331–341

    Article  CAS  PubMed  Google Scholar 

  • Jiang H, Shi Y, Liu J et al (2022) Natural polymorphism of ZmICE1 contributes to amino acid metabolism that impacts cold tolerance in maize. Nat Plants 8:1176–1190

    Article  CAS  PubMed  Google Scholar 

  • Kang J, Park J, Choi H, Burla B, Kretzschmar T, Lee Y, Martinoia, E (2011) Plant ABC transporters. Arabidopsis Book/American Society of Plant Biologists 9

  • Kim DY, Jin JY, Alejandro S, Martinoia E, Lee Y (2010) Overexpression of AtABCG36 improves drought and salt stress resistance in Arabidopsis. Physiol Plantarum 139:170–180

    Article  CAS  Google Scholar 

  • Klein M, Geisler M, Suh SJ et al (2004) Disruption of AtMRP4, a guard cell plasma membrane ABCC-type ABC transporter, leads to deregulation of stomatal opening and increased drought susceptibility. Plant J 39:219–236

    Article  CAS  PubMed  Google Scholar 

  • Lee EK, Kwon M, Ko JH et al (2004) Binding of sulfonylurea by AtMRP5, an Arabidopsis multidrug resistance-related protein that functions in salt tolerance. Plant Physiol 134:528–538

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li B, Li Y, Liu F et al (2019a) Overexpressed tomosyn binds syntaxins and blocks secretion during pollen development. Plant Physiol 181:1114–1126

    Article  PubMed  PubMed Central  Google Scholar 

  • Li M, Lin L, Zhang Y, Sui N (2019b) ZmMYB31, a R2R3-MYB transcription factor in maize, positively regulates the expression of CBF genes and enhances resistance to chilling and oxidative stress. Mol Biol Rep 46:3937–3944

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Fu D, Wang X et al (2022) The transcription factor bZIP68 negatively regulates cold tolerance in maize. Plant Cell 34:2833–2851

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu J, Guo X, Zhai T, Shu A, Zhao L, Liu Z, Zhang S (2020) Genome-wide identification and characterization of microRNAs responding to ABA and GA in maize embryos during seed germination. Plant Biol 22:949–957

    Article  CAS  PubMed  Google Scholar 

  • Lu X, Liu J, Ren W et al (2018) Gene-indexed mutations in maize. Mol Plant 11:496–504

    Article  CAS  PubMed  Google Scholar 

  • Luo T, Zou T, Yuan G et al (2020) Less and shrunken pollen 1 (LSP1) encodes a member of the ABC transporter family required for pollen wall development in rice (Oryza sativa L.). Crop J 8:492–504

    Article  Google Scholar 

  • Luo M, Zhang Y, Li J et al (2021) Molecular dissection of maize seedling salt tolerance using a genome-wide association analysis method. Plant Biotechnol J 19:1937–1951

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Makarevitch I, Waters AJ, West PT, Stitzer M, Hirsch CN, Ross-Ibarra J, Springer NM (2015) Transposable elements contribute to activation of maize genes in response to abiotic stress. PLoS Genet 11:e1004915

    Article  PubMed  PubMed Central  Google Scholar 

  • Meng C, Sui N (2019) Overexpression of maize MYB-IF35 increases chilling tolerance in Arabidopsis. Plant Physiol Bioch 135:167–173

    Article  CAS  Google Scholar 

  • Mishra SK, Khan MH, Misra S, Dixit VK, Gupta S, Tiwari S, Gupta SC, Chauhan PS (2020) Drought tolerant Ochrobactrum sp. inoculation performs multiple roles in maintaining the homeostasis in Zea mays L. subjected to deficit water stress. Plant Physiol Bioch 150:1–14

    Article  CAS  Google Scholar 

  • Moons A (2003) Ospdr9, which encodes a PDR-type ABC transporter, is induced by heavy metals, hypoxic stress and redox perturbations in rice roots. FEBS Lett 553:370–376

    Article  CAS  PubMed  Google Scholar 

  • Nguyen VNT, Moon S, Jung KH (2014) Genome-wide expression analysis of rice ABC transporter family across spatio-temporal samples and in response to abiotic stresses. J Plant Physiol 171:1276–1288

    Article  CAS  PubMed  Google Scholar 

  • Ofori PA, Mizuno A, Suzuki M, Martinoia E, Reuscher S, Aoki K, Shibata D, Otagaki S, Matsumoto S, Shiratake K (2018) Genome-wide analysis of ATP binding cassette (ABC) transporters in tomato. PLoS One 13:e0200854

    Article  PubMed  PubMed Central  Google Scholar 

  • Pang K, Li Y, Liu M, Meng Z, Yu Y (2013) Inventory and general analysis of the ATP-binding cassette (ABC) gene superfamily in maize (Zea mays L.). Gene 526:411–428

    Article  CAS  PubMed  Google Scholar 

  • Qin F, Sakuma Y, Li J, Liu Q, Li YQ, Shinozaki K, Yamaguchi-Shinozaki K (2004) Cloning and functional analysis of a novel DREB1/CBF transcription factor involved in cold-responsive gene expression in Zea mays L. Plant Cell Physiol 45:1042–1052

    Article  CAS  PubMed  Google Scholar 

  • Sánchez-Fernández R, Davies TE, Coleman JO, Rea PA (2001) The Arabidopsis thaliana ABC protein superfamily, a complete inventory. J Biol Chem 276:30231–30244

    Article  PubMed  Google Scholar 

  • Sollich M, Yoshinaga MY, Häusler S, Price RE, Hinrichs KU, Bühring SI (2017) Heat stress dictates microbial lipid composition along a thermal gradient in marine sediments. Front Microbiol 8:1550

    Article  PubMed  PubMed Central  Google Scholar 

  • Van Zelm E, Zhang Y, Testerink C (2020) Salt tolerance mechanisms of plants. Annu Rev Plant Biol 71:403–433

    Article  PubMed  Google Scholar 

  • Verrier PJ, Bird D, Burla B et al (2008) Plant ABC proteins-a unified nomenclature and updated inventory. Trends Plant Sci 13:151–159

    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 X, Wang H, Liu S, Ferjani A, Li J, Yan J, Yang X, Qin F (2016) Genetic variation in ZmVPP1 contributes to drought tolerance in maize seedlings. Nat Genet 48:1233–1241

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Cao Y, Liang X, Zhuang J, Wang X, Qin F, Jiang C (2022) A dirigent family protein confers variation of Casparian strip thickness and salt tolerance in maize. Nat Commun 13:2222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weckwerth P, Ehlert B, Romeis T (2015) ZmCPK1, a calcium-independent kinase member of the Zea mays CDPK gene family, functions as a negative regulator in cold stress signalling. Plant Cell Environ 38:544–558

    Article  CAS  PubMed  Google Scholar 

  • Wu J, Jiang Y, Liang Y, Chen L, Chen W, Cheng B (2019) Expression of the maize MYB transcription factor ZmMYB3R enhances drought and salt stress tolerance in transgenic plants. Plant Physiol Bioch 137:179–188

    Article  CAS  Google Scholar 

  • Xiang Y, Bian X, Wei T, Yan J, Sun X, Han T, Dong B, Zhang G, Li J, Zhang A (2021) ZmMPK5 phosphorylates ZmNAC49 to enhance oxidative stress tolerance in maize. New Phytol 232:2400–2417

    Article  CAS  PubMed  Google Scholar 

  • Yang W, Zhou Z, Chu Z (2023) Emerging roles of salicylic acid in plant saline stress tolerance. Int J Mol Sci 24:3388

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu Z, Duan X, Luo L, Dai S, Ding Z, Xia G (2020) How plant hormones mediate salt stress responses. Trends Plant Sci 25:1117–1130

    Article  CAS  PubMed  Google Scholar 

  • Zang Y, Liu J, Tang XX, Zhou B (2018) Description of a Zostera marina catalase gene involved in responses to temperature stress. PeerJ 6:e4532

    Article  PubMed  PubMed Central  Google Scholar 

  • Zeng R, Li Z, Shi Y, Fu D, Yin P, Cheng J, Jiang C, Yang S (2021) Natural variation in a type-A response regulator confers maize chilling tolerance. Nat Commun 12:4713

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang M, Cao Y, Wang Z, Wang ZQ, Shi J, Liang X, Song W, Chen Q, Lai J, Jiang C (2018a) A retrotransposon in an HKT1 family sodium transporter causes variation of leaf Na+ exclusion and salt tolerance in maize. New Phytol 217:1161–1176

    Article  CAS  PubMed  Google Scholar 

  • Zhang S, Dou Y, Li S, Ren G, Chevalier D, Zhang C, Yu B (2018b) DAWDLE interacts with DICER-LIKE proteins to mediate small RNA biogenesis. Plant Physiol 177:1142–1151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang M, Liang X, Wang L, Cao Y, Song W, Shi J, Lai J, Jiang C (2019) A HAK family Na+ transporter confers natural variation of salt tolerance in maize. Nat Plants 5:1297–1308

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Tong T, Fang Y, Zheng J, Zhang X, Niu C, Li J, Zhang X, Xue D (2020) Genome-wide identification of barley ABC genes and their expression in response to abiotic stress treatment. Plants 9:1281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Zhu J, Gong Z, Zhu JK (2022) Abiotic stress responses in plants. Nat Rev Genet 23:104–119

    Article  PubMed  Google Scholar 

  • Zhang M, Li Y, Liang X, Lu M, Lai J, Song W, Jiang C (2023) A teosinte-derived allele of an HKT1 family sodium transporter improves salt tolerance in maize. Plant Biotech J 21:97–108

    Article  Google Scholar 

Download references

Funding

This work was supported by Taishan Scholars (tsqn20161020), the National Natural Science Foundation (31871543), the Natural Science Foundation of Shandong Province (ZR2017MC065 and ZR2020QC029).

Author information

Author notes

  1. Wei Yang, Xiao Liu, and Shaowei Yu have equally contributed to this work.

Authors and Affiliations

  1. State Key Laboratory of Crop Biology, College of Life Sciences, Shandong Agricultural University, Tai’an, 271018, China

    Wei Yang, Xiao Liu, Shaowei Yu, Lijun Jiang, Yinggao Liu, Jiedao Zhang, Xiang Li & Shuxin Zhang

  2. Institute of Molecular Breeding for Maize, Qilu Normal University, Jinan, 250200, Shandong, China

    Jisheng Liu & Xiaoduo Lu

Authors
  1. Wei Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiao Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shaowei Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jisheng Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lijun Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xiaoduo Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yinggao Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jiedao Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Xiang Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Shuxin Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

SZ and WY designed research; XL, SY, YS, JL, LJ, and JZ performed research; JL, WY, YL, XL, and SZ analyzed data; XL, WY and SZ wrote the paper. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Xiang Li or Shuxin Zhang.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Communicated by Kinya Toriyama.

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

Yang, W., Liu, X., Yu, S. et al. The maize ATP-binding cassette (ABC) transporter ZmMRPA6 confers cold and salt stress tolerance in plants. Plant Cell Rep 43, 13 (2024). https://doi.org/10.1007/s00299-023-03094-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00299-023-03094-7

Keywords

Search

Navigation