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Identification of Germplasm and Sugar Transporter Gene ZmSWEET1b Associated with Salt Tolerance in Maize

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Abstract

Soil salinity influences various aspects of crop growth and development. Identification of novel germplasm and genetic regulators of salt tolerance will help to alleviate the threat of land salinization. Here, we identified salt-tolerant SHEN5003 and -sensitive YZ26 maize germplasm from different heterotic groups. Salt-grown SHEN5003 (PA group) lines exhibited decreased reduction in fresh weight and dry weight, high SPAD value, total sugar and K+ contents, as well as low Na+ content relative to salt-treated YZ26 (BSSS group) plants. Salt-tolerant SHEN5003 and -sensitive YZ26 lines were followingly used for the discovery of genetic regulators of salt tolerance. Transcriptome outcome showed the expression of genes relevant to Na+/K+ homeostasis, such as H+-ATPase, HKT1, and HAKs together with CAT2 for ROS detoxification was altered in salt-treated SHEN5003 line. Moreover, GO enrichment analysis indicated differentially expressed genes of SHEN5003 upon salt treatment was significantly enriched in the stress response pathway (GO:0006950). By integrated transcriptome analyses of SHEN5003 and YZ26 lines grown in normal and salinity conditions, positive regulator of salt tolerance ZmSWEET1b was revealed, which exhibited the opposite expression pattern between salt-treated SHEN5003 and YZ26 lines. ZmSWEET1b interacted with multiple partners, such as Sucrose synthase 2 to shape a functional association network in the modulation of sugar metabolism upon salinity stress.

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References

  • Bazihizina N, Colmer TD, Cuin TA, Mancuso S, Shabala S (2019) Friend or foe? Chloride patterning in halophytes. Trends Plant Sci 24:142–151

    Article  CAS  PubMed  Google Scholar 

  • Borsani O, Zhu J, Verslues PE, Sunkar R, Zhu JK (2005) Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell 123:1279–1291

    Article  CAS  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 

  • Cheng X, Zhang S, Tao W, Zhang X, Liu J, Sun J, Zhang H, Pu L, Huang R, Chen T (2018) INDETERMINATE SPIKELET1 recruits histone deacetylase and a transcriptional repression complex to regulate rice salt tolerance. Plant Physiol 178:824–837

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chow PS, Landhäusser SM (2004) A method for routine measurements of total sugar and starch content in woody plant tissues. Tree Physiol 24:1129–1136

    Article  CAS  PubMed  Google Scholar 

  • Demidchik V, Maathuis FJ (2007) Physiological roles of nonselective cation channels in plants: from salt stress to signalling and development. New Phytol 175:387–404

    Article  CAS  PubMed  Google Scholar 

  • Eggert E, Obata T, Gerstenberger A, Gier K, Brandt T, Fernie AR, Schulze W, Kühn C (2016) A sucrose transporter-interacting protein disulphide isomerase affects redox homeostasis and links sucrose partitioning with abiotic stress tolerance. Plant Cell Environ 39:1366–1380

    Article  CAS  PubMed  Google Scholar 

  • El Mahi H, Pérez-Hormaeche J, De Luca A, Villalta I, Espartero J, Gámez-Arjona F, Fernández JL, Bundó M, Mendoza I, Mieulet D, Lalanne E, Lee SY, Yun DJ, Guiderdoni E, Aguilar M, Leidi EO, Pardo JM, Quintero FJ (2019) A critical role of sodium flux via the plasma membrane Na+/H+ exchanger SOS1 in the salt tolerance of rice. Plant Physiol 180:1046–1065

    Article  PubMed  PubMed Central  Google Scholar 

  • Gong Z, **ong L, Shi H, Yang S, Herrera-Estrella LR, Xu G, Chao DY, Li J, Wang PY, Qin F, Li J, Ding Y, Shi Y, Wang Y, Yang Y, Guo Y, Zhu JK (2020) Plant abiotic stress response and nutrient use efficiency. Sci China Life Sci 63:635–674

    Article  PubMed  Google Scholar 

  • Ismail AM, Horie T (2017) Genomics, physiology, and molecular breeding approaches for improving salt tolerance. Annu Rev Plant Biol 68:405–434

    Article  CAS  PubMed  Google Scholar 

  • Jiang Z, Zhou X, Tao M, Yuan F, Liu L, Wu F, Wu X, **ang Y, Niu Y, Liu F, Li C, Ye R, Byeon B, Xue Y, Zhao H, Wang HN, Crawford BM, Johnson DM, Hu C, Pei C, Zhou W, Swift GB, Zhang H, Vo-Dinh T, Hu Z, Siedow JN, Pei ZM (2019) Plant cell-surface GIPC sphingolipids sense salt to trigger Ca2+ influx. Nature 572:341–346

    Article  CAS  PubMed  Google Scholar 

  • Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12:357–360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar S, Beena AS, Awana M, Singh A (2017) Salt-induced tissue-specific cytosine methylation downregulates expression of HKT genes in contrasting wheat (Triticum aestivum L.) genotypes. DNA Cell Biol 36:283–294

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT Method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Lu Y, Zhang S, Shah T, ** is a powerful approach to detecting quantitative trait loci underlying drought tolerance in maize. Proc Natl Acad Sci USA 107:19585–19590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma L, Ye J, Yang Y, Lin H, Yue L, Luo J, Long Y, Fu H, Liu X, Zhang Y, Wang Y, Chen L, Kudla J, Wang Y, Han S, Song CP, Guo Y (2019) The SOS2-SCaBP8 complex generates and fine-tunes an AtANN4-dependent calcium signature under salt stress. Dev Cell 48:697–709

    Article  CAS  PubMed  Google Scholar 

  • Meloni DA, Oliva MA, Martinez CA, Cambraia J (2003) Photosynthesis and activity of superoxide dismutase, peroxidase and glutathione reductase in cotton under salt stress. Environ Exp Bot 49:69–76

    Article  CAS  Google Scholar 

  • Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signaling during drought and salinity stresses. Plant Cell Environ 33:453–467

    Article  CAS  PubMed  Google Scholar 

  • Monihan SM, Ryu CH, Magness CA, Schumaker KS (2019) Linking duplication of a calcium sensor to salt tolerance in Eutrema salsugineum. Plant Physiol 179:176–1192

    Article  Google Scholar 

  • Ren ZH, Gao JP, Li LG, Cai XL, Huang W, Chao DY, Zhu MZ, Wang ZY, Luan S, Lin HX (2005) A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nat Genet 37:1141–1146

    Article  CAS  PubMed  Google Scholar 

  • Shabala S, Demidchik V, Shabala L, Cuin TA, Smith SJ, Miller AJ, Davies JM, Newman IA (2006) Extracellular Ca2+ ameliorates NaCl-induced K+ loss from Arabidopsis root and leaf cells by controlling plasma membrane K+-permeable channels. Plant Physiol 141:1653–1665

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D, Huerta-Cepas J, Simonovic M, Roth A, Santos A, Tsafou KP, Kuhn M, Bork P, Jensen LJ, von Mering C (2015) STRING v10: protein-protein interaction networks, integrated over the tree of life. Nucleic Acids Res 43:D447–D452

    Article  CAS  PubMed  Google Scholar 

  • Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7:562–578

    Article  CAS  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 

  • Wong TH, Li MW, Yao XQ, Lam HM (2013) The GmCLC1 protein from soybean functions as a chloride ion transporter. J Plant Physiol 170:101–104

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi T, Blumwald E (2005) Develo** salt-tolerant crop plants: challenges and opportunities. Trends Plant Sci 10:615–620

    Article  CAS  PubMed  Google Scholar 

  • Yang Y, Guo Y (2018) Elucidating the molecular mechanisms mediating plant salt-stress responses. New Phytol 217:523–539

    Article  CAS  PubMed  Google Scholar 

  • Yang T, Zhang S, Hu Y, Wu F, Hu Q, Chen G, Cai J, Wu T, Moran N, Yu L, Xu G (2014) The role of a potassium transporter OsHAK5 in potassium acquisition and transport from roots to shoots in rice at low potassium supply levels. Plant Physiol 166:945–959

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang Z, Wang C, Xue Y, Liu X, Chen S, Song C, Yang Y, Guo Y (2019) Calcium-activated 14-3-3 proteins as a molecular switch in salt stress tolerance. Nat Commun 10:1199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yin YG, Kobayashi Y, Sanuki A, Kondo S, Fukuda N, Ezura H, Sugaya S, Matsukura C (2010) Salinity induces carbohydrate accumulation and sugar-regulated starch biosynthetic genes in tomato (Solanum lycopersicum L. cv. ’Micro-Tom’) fruits in an ABA- and osmotic stress-independent manner. J Exp Bot 61:563–574

    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 M, Cao Y, Wang Z, Wang ZQ, Shi J, Liang X, Song W, Chen Q, Lai J, Jiang C (2018) 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 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 X, Liu P, Qing C, Yang C, Shen Y, Ma L (2021) Comparative transcriptome analyses of maize seedling root responses to salt stress. PeerJ 9:e10765

    Article  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 

  • Zhu JK (2016) Abiotic stress signaling and responses in plants. Cell 167:313–324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (31571671), the High-end Talent Project of Yangzhou University (18HTYZU12), and the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).

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YJW: designed the research. SSW, WHD, YDC, and YWS: performed the experiments. YHD: analyzed the data. YJW and YHD: wrote the manuscript.

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Correspondence to Yijun Wang.

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Ding, Y., Wang, S., Du, W. et al. Identification of Germplasm and Sugar Transporter Gene ZmSWEET1b Associated with Salt Tolerance in Maize. J Plant Growth Regul 42, 7580–7590 (2023). https://doi.org/10.1007/s00344-023-11033-9

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