Natural variation in SlSOS2 promoter hinders salt resistance during tomato domestication

Abstract

Increasing soil salinization seriously impairs plant growth and development, resulting in crop loss. The Salt-Overly-Sensitive (SOS) pathway is indispensable to the mitigation of Na⁺ toxicity in plants under high salinity. However, whether natural variations of SOS2 contribute to salt tolerance has not been reported. Here a natural variation in the SlSOS2 promoter region was identified to be associated with root Na⁺/K⁺ ratio and the loss of salt resistance during tomato domestication. This natural variation contains an ABI4-binding cis-element and plays an important role in the repression of SlSOS2 expression. Genetic evidence revealed that SlSOS2 mutations increase root Na⁺/K⁺ ratio under salt stress conditions and thus attenuate salt resistance in tomato. Together, our findings uncovered a critical but previously unknown natural variation of SOS2 in salt resistance, which provides valuable natural resources for genetic breeding for salt resistance in cultivated tomatoes and other crops.

Acknowledgements

This work was supported by the National Natural Science Foundation of China (grant 32000206 to Z.W.) and the Natural Science Foundation of Anhui Province (grant 2208085Y08 to Z.W.).

Author contributions

Z.W., G.Z., S.H., and J.-K.Z. conceived the project; Z.W. and G.Z. designed the experiments and analyzed the data; Z.W. and Y.H. performed most of the experiments; G.Z. and X.G. carried out the association mapping; X.W., Z.Q.W., D.K., S.Y., Y.Y., Z.-F.C., and X.L. provided technical assistance; Z.W. and Y.H. drafted the article; Z.W. and G.Z. revised and finalized the manuscript.

Data availability

The authors declare that all the data supporting the findings of this study are available within the paper and its supplementary information files.

Conflict of interest

The authors declare no competing financial interests.

References

[1] Shabala S, Bose J, Hedrich R . Salt bladders: do they matter? Trends Plant Sci. 2014; 19: 687-91.

[2] Zhu JK . Salt and drought stress signal transduction in plants. Annu Rev Plant Biol. 2002; 53: 247-73.

[3] Zhu JK . Abiotic stress signaling and responses in plants. Cell. 2016; 167: 313-24.

[4] Horie T, Schroeder JI . Sodium transporters in plants. Diverse genes and physiological functions. Plant Physiol. 2004; 136: 2457-62.

[5] Ishitani M, Liu J, Halfter U et al. SOS3 function in plant salt tolerance requires N-myristoylation and calcium binding. Plant Cell. 2000; 12: 1667-77.

[6] Qiu QS, Guo Y, Dietrich MA et al. Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc Natl Acad Sci USA. 2002; 99: 8436-41.

[7] Shi H, Quintero FJ, Pardo JM et al. The putative plasma membrane Na(+)/H(+) antiporter SOS1 controls long-distance Na(+) transport in plants. Plant Cell. 2002; 14: 465-77.

[8] Quan R, Lin H, Mendoza I et al. SCABP8/CBL10, a putative calcium sensor, interacts with the protein kinase SOS2 to protect Arabidopsis shoots from salt stress. Plant Cell. 2007; 19: 1415-31.

[9] Rubio F, Gassmann W, Schroeder JI . Sodium-driven potassium uptake by the plant potassium transporter HKT1 and mutations conferring salt tolerance. Science. 1995; 270: 1660-3.

[10] Bose J, Xie Y, Shen W et al. Haem oxygenase modifies salinity tolerance in Arabidopsis by controlling K(+) retention via regulation of the plasma membrane H(+)-ATPase and by altering SOS1 transcript levels in roots. J Exp Bot. 2013; 64: 471-81.

[11] An D, Chen JG, Gao YQ et al. AtHKT1 drives adaptation of Arabidopsis thaliana to salinity by reducing floral sodium content. PLoS Genet. 2017; 13: e1007086.

[12] Ren ZH, Gao JP, Li LG et al. A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nat Genet. 2005; 37: 1141-6.

[13] Chao DY, Chen Y, Chen J et al. Genome-wide association mapping identifies a new arsenate reductase enzyme critical for limiting arsenic accumulation in plants. PLoS Biol. 2014; 12: e1002009.

[14] Chao ZF, Wang YL, Chen YY et al. NPF transporters in synaptic-like vesicles control delivery of iron and copper to seeds. Sci Adv. 2021; 7: eabh2450.

[15] Wang Z, Hong Y, Zhu G et al. Loss of salt tolerance during tomato domestication conferred by variation in a Na(+)/K(+) transporter. EMBO J. 2020; 39: e103256.

[16] Wang Z, Hong Y, Li Y et al. Natural variations in SlSOS1 contribute to the loss of salt tolerance during tomato domestication. Plant Biotechnol J. 2021; 19: 20-2.

[17] Zhou X, Li J, Wang Y et al. The classical SOS pathway confers natural variation of salt tolerance in maize. New Phytol. 2022; 236: 479-94.

[18] Sato S, Tabata S, Hirakawa S et al. The tomato genome sequence provides insights into fleshy fruit evolution. Nature. 2012; 485: 635-41.

[19] Lin T, Zhu G, Zhang J et al. Genomic analyses provide insights into the history of tomato breeding. Nat Genet. 2014; 46: 1220-6.

[20] Tieman D, Zhu G, Resende MFR Jr et al. A chemical genetic roadmap to improved tomato flavor. Science. 2017; 355: 391-4.

[21] Arciniegas Vega JP, Melino VJ . Uncovering natural genetic variants of the SOS pathway to improve salinity tolerance in maize. New Phytol. 2022; 236: 313-5.

[22] Huertas R, Olias R, Eljakaoui Z et al. Overexpression of SlSOS2 (SlCIPK24) confers salt tolerance to transgenic tomato. Plant Cell Environ. 2012; 35: 1467-82.

[23] Giraud E, Van Aken O, Ho LHM et al. The transcription factor ABI4 is a regulator of mitochondrial retrograde expression of ALTERNATIVE OXIDASE1a. Plant Physiol. 2009; 150: 1286-96.

[24] Luo L, Wan Q, Zhang K et al. AhABI4s negatively regulate salt-stress response in peanut. Front Plant Sci. 2021; 12: 741641.

[25] Shkolnik-Inbar D, Adler G, Bar-Zvi D . ABI4 downregulates expression of the sodium transporter HKT1;1 in Arabidopsis roots and affects salt tolerance. Plant J. 2013; 73: 993-1005.

[26] Luo X, Dai Y, Zheng C et al. The ABI4-RbohD/VTC2 regulatory module promotes reactive oxygen species (ROS) accumulation to decrease seed germination under salinity stress. New Phytol. 2021; 229: 950-62.

[27] Guo Y, Halfter U, Ishitani M et al. Molecular characterization of functional domains in the protein kinase SOS2 that is required for plant salt tolerance. Plant Cell. 2001; 13: 1383-400.

[28] Chen X, Ding Y, Yang Y et al. Protein kinases in plant responses to drought, salt, and cold stress. J Integr Plant Biol. 2021; 63: 53-78.

[29] Yang Y, Guo Y . Unraveling salt stress signaling in plants. J Integr Plant Biol. 2018; 60: 796-804.

[30] Roy SJ, Negrao S, Tester M . Salt resistant crop plants. Curr Opin Biotechnol. 2014; 26: 115-24.

[31] van Zelm E, Zhang Y, Testerink C . Salt tolerance mechanisms of plants. Annu Rev Plant Biol. 2020; 71: 403-33.

[32] Zhang H, Zhu J, Gong Z et al. Abiotic stress responses in plants. Nat Rev Genet. 2022; 23: 104-19.

[33] Yang ZM, Li GX, Tieman D et al. Genomics approaches to domestication studies of horticultural crops. Hortic Plant J. 2019; 5: 240-6.

[34] Shi H, Lee BH, Wu SJ et al. Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nat Biotechnol. 2003; 21: 81-5.

[35] Quintero FJ, Ohta M, Shi HZ et al. Reconstitution in yeast of the Arabidopsis SOS signaling pathway for Na+ homeostasis. Proc Natl Acad Sci USA. 2002; 99: 9061-6.

[36] Quintero FJ, Martinez-Atienza J, Villalta I et al. Activation of the plasma membrane Na/H antiporter Salt-Overly-Sensitive 1 (SOS1) by phosphorylation of an auto-inhibitory C-terminal domain. Proc Natl Acad Sci USA. 2011; 108: 2611-6.

[37] Ren ZZ, Wang Z, Zhou XE et al. Structure determination and activity manipulation of the turfgrass ABA receptor FePYR1. Sci Rep. 2017; 7: 14022.

[38] Lescot M, Déhais P, Thijs G et al. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res. 2002; 30: 325-7.

[39] Hong YC, Wang Z, Liu X et al. Two chloroplast proteins negatively regulate plant drought resistance through separate pathways. Plant Physiol. 2020; 182: 1007-21.

[40] Miao C, Wang Z, Zhang L et al. The grain yield modulator miR156 regulates seed dormancy through the gibberellin pathway in rice. Nat Commun. 2019; 10: 3822.