ZmGolS1 underlies natural variation of raffinose content and salt tolerance in maize

Xiaoyan Liang; Pan Yin; Fenrong Li; Yibo Cao; Caifu Jiang

doi:10.1016/j.jgg.2024.12.013

Volume 52 Issue 3

Mar. 2025

Turn off MathJax

Article Contents

Article Navigation > Journal of Genetics and Genomics > 2025 > 52(3): 346-355

PDF( 0 KB)

ZmGolS1 underlies natural variation of raffinose content and salt tolerance in maize

doi: 10.1016/j.jgg.2024.12.013

a. State Key Laboratory of Plant Environmental Resilience, Frontiers Science Center for Molecular Design Breeding, College of Biological Sciences, China Agricultural University, Beijing 100193, China;
b. Key Laboratory of Forest Silviculture and Conservation of the Ministry of Education, College of Forestry, Beijing Forestry University, Beijing 100083, China

Funds:

D Program of China (2022YFF1001601), the National Science Fund for Distinguished Young Scholars (32325037), the National Natural Science Foundation of China (32201718 and 32401756), the Postdoctoral Innovation Talents Support Program (BX20240420), and the China Postdoctoral Science Foundation (2024T171011 and 2023M743817).

The authors acknowledge financial support from the National Key R&

Received Date: 2024-11-11
Accepted Date: 2024-12-17
Rev Recd Date: 2024-12-17

Available Online: 2025-07-11

Publish Date: 2024-12-24

Abstract

Abstract

Salt stress significantly inhibits crop growth and development, and mitigating this can enhance salt tolerance in various crops. Previous studies have shown that regulating saccharide biosynthesis is a key aspect of plant salt tolerance; however, the underlying molecular mechanisms remain largely unexplored. In this study, we demonstrate that overexpression of a salt-inducible galactinol synthase gene, ZmGolS1, alleviates salt-induced growth inhibition, likely by promoting raffinose synthesis. Additionally, we show that natural variation in ZmGolS1 transcript levels contributes to the diversity of raffinose content and salt tolerance in maize. We further reveal that ZmRR18, a type-B response regulator transcription factor, binds to the AATC element in the promoter of ZmGolS1, with this binding increases the transcript levels of ZmGolS1 under salt conditions. Moreover, a single nucleotide polymorphism (termed SNP-302T) within the ZmGolS1 promoter significantly reduces its binding affinity for ZmRR18, resulting in decreased ZmGolS1 expression and diminished raffinose content, ultimately leading to a salt-hypersensitive phenotype. Collectively, our findings reveal the molecular mechanisms by which the ZmRR18-ZmGolS1 module enhances raffinose biosynthesis, thereby promoting maize growth under salt conditions. This research provides important insights into salt tolerance mechanisms associated with saccharide biosynthesis and identifies valuable genetic loci for breeding salt-tolerant maize varieties.
- Maize,
- Salt tolerance,
- Biomass,
- Raffinose content,
- Transcriptional regulation

FullText(HTML)

References(62)

References

Byrt, C.S., Platten, J.D., Spielmeyer, W., James, R.A., Lagudah, E.S., Dennis, E.S., Tester, M., Munns, R., 2007. HKT1;5-like cation transporters linked to Na⁺ exclusion loci in wheat, Nax2 and Kna1. Plant Physiol. 143, 1918-1928.

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.

Cao, Y., Zhou, X., Song, H., Zhang, M., Jiang, C., 2023. Advances in deciphering salt tolerance mechanism in maize. Crop J. 11, 1001-1010.

Cortleven, A., Leuendorf, J.E., Frank, M., Pezzetta, D., Bolt, S., Schmulling, T., 2018. Cytokinin action in response to abiotic and biotic stresses in plants. Plant Cell Environ. 42, 998-1018.

Cui, M., Li, Y., Li, J., Yin, F., Chen, X., Qin, L., Wei, L., Xia, G., Liu, S., 2023. Ca²⁺-dependent TaCCD1 cooperates with TaSAUR215 to enhance plasma membrane H⁺-ATPase activity and alkali stress tolerance by inhibiting PP2C-mediated dephosphorylation of TaHA2 in wheat. Mol. Plant 16, 571-587.

Dai, H.B., Zhu, Z.H., Wang, Z.G., Zhang, Z.P., Kong, W.W., Miao, M.M., 2022. Galactinol synthase 1 improves cucumber performance under cold stress by enhancing assimilate translocation. Hortic Res 9, uhab063.

D’Agostino, I.B., Kieber, J.J., 1999. Phosphorelay signal transduction: the emerging family of plant response regulators. Trends Biochem. Sci. 24, 452-456.

ElSayed, A.I., Rafudeen, M.S., Golldack, D., 2014. Physiological aspects of raffinose family oligosaccharides in plants: protection against abiotic stress. Plant Biol (Stuttg) 16, 1-8.

Eveland, A.L., Jackson, D.P., 2012. Sugars, signalling, and plant development. J. Exp. Bot. 63, 3367-3377.

Gu, H., Lu, M., Zhang, Z., Xu, J., Cao, W., Miao, M., 2018. Metabolic process of raffinose family oligosaccharides during cold stress and recovery in cucumber leaves. J. Plant Physiol. 224, 112-120.

Gu, L., Zhang, Y., Zhang, M., Li, T., Dirk, L.M., Downie, B. et al. 2016. ZmGOLS2, a target of transcription factor ZmDREB2A, offers similar protection against abiotic stress as ZmDREB2A. Plant Mol. Bio. 90, 157-170.

Han, Q., Qi, J., Hao, G., Zhang, C., Wang, C., Dirk, L.M.A., Downie, A.B., Zhao, T., 2020. ZmDREB1A regulates RAFFINOSE SYNTHASE controlling raffinose accumulation and plant chilling stress tolerance in maize. Plant Cell Physiol. 61, 331-341.

Hanks, R.J., Ashcroft, G.L., Rasmussen, V.P., Wilson, G.D., 1978. Corn production as influenced by irrigation and salinity-Utah studies. Irrig. Sci. 1, 47-59.

Hwang, I., Sheen, J., 2001. Two-component circuitry in Arabidopsis cytokinin signal transduction. Nature 413, 383-389.

Jang, J.H., Shang, Y., Kang, H.K., Kim, S.Y., Kim, B.H., Nam, K.H., 2018. Arabidopsis galactinol synthases 1 (AtGOLS1) negatively regulates seed germination. Plant Sci. 267, 94-101.

Jiao, Y., Zhao, H., Ren, L., Song, W., Zeng, B., Guo, J., Wang, B., Liu, Z., Chen, J., Li, W., Zhang, M., Xie, S., Lai, J., 2012. Genome-wide genetic changes during modern breeding of maize. Nat. Genet. 44, 812-815.

Kieber, J., Schaller, G.E., 2018. Cytokinin signaling in plant development. Development. 145, dev149344.

Kong, W., Gong, Z., Zhong, H., Zhang, Y., Zhao, G., Gautam, M., Deng, X., Liu, C., Zhang, C., Li, Y., 2019. Expansion and evolutionary patterns of glycosyltransferase family 8 in gramineae crop genomes and their expression under salt and cold stresses in Oryza sativa ssp. japonica. Biomolecules 9, 188.

Lang, S., Liu, X., Xue, H., Li, X., Wang, X., 2017. Functional characterization of BnHSFA4a as a heat shock transcription factor in controlling the re-establishment of desiccation tolerance in seeds. J. Exp. Bot. 9, 2361-2375.

Li, T., Zhang, Y.M., Liu, Y., Li, X.D., Hao, G.L., Han, Q.H., Dirk, M.A.L., Downie, B., Ruan, Y.L., Wang, J.M., Wang, G.Y., Zhao, T.Y., 2020. Raffinose synthase enhances drought tolerance through raffinose synthesis or galactinol hydrolysis in maize and Arabidopsis plants. J. Biol. Chem. 295, 8064-8077.

Li, T., Zhang, Y., Wang, D., Liu, Y., Dirk, L.M.A., Goodman, J., Downie, A.B., Wang, J., Wang, G., Zhao, T., 2017. Regulation of seed vigor by manipulation of raffinose family oligosaccharides in maize and Arabidopsis thaliana. Mol. Plant 10, 1540-1555.

Liang, X., Liu, S., Wang, T., Li, F., Cheng, J., Lai, J., Qin, F., Li, Z., Wang, X., Jiang, C., 2021. Metabolomics-driven gene mining and genetic improvement of tolerance to salt-induced osmotic stress in maize. New Phytol. 230, 2355-2370.

Liang, X., Li, J., Yang, Y., Jiang, C., Guo, Y., 2024. Designing salt stress-resilient crops: current progress and future challenges. J. Integr. Plant Biol. 66, 303-329.

Luo, X., Wang, B., Gao, S., Zhang, F., Terzaghi, W., Dai, M., 2019. Genome-wide association study dissects the genetic bases of salt tolerance in maize seedlings. J. Integr. Plant Biol. 61, 658-674.

Luo, M., Zhang, Y., Li, J., Zhang, P., Chen, K., Song, W., Wang, X., Yang, J., Lu, X., Lu, B., Zhao, Y., Zhao, J., 2021. Molecular dissection of maize seedling salt tolerance using a genome-wide association analysis method. Plant Biotechnol. J. 19, 1937-1951.

Mason, M.G., Jha, D., Salt, D.E., Tester, M., Hill, K., Kieber, J.J., Schaller, G.E., 2010. Type-B response regulators ARR1 and ARR12 regulate expression of AtHKT1;1 and accumulation of sodium in Arabidopsis shoots. Plant J. 64, 753-763.

Mason, M.G., Mathews, D.E., Argyros, D.A., Maxwell, B.B., Kieber, J.J., Alonso, J.M., Ecker, J.R., Schaller, G.E., 2005. Multiple type-B response regulators mediate cytokinin signal transduction in. Plant Cell 17, 3007-3018.

Martins, C.P.S., Fernandes, D., Guimaraes, V.M., Du, D.L., Silva, D.C., Almeida, A.A.F., Gmitter Jr, F.G., Otoni, W.C., Costa, M.G., 2022. Comprehensive analysis of the GALACTINOL SYNTHASE (GolS) gene family in citrus and the function of CsGolS6 in stress tolerance. PLoS One 9, e0274791.

Munns, R., Tester, M., 2008. Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 59, 651-681.

Munns, R., Passioura, J.B., Colmer, T.D., Byrt, C.S., 2020. Osmotic adjustment and energy limitations to plant growth in saline soil. New Phytol. 225, 1091-1096.

Nishizawa, A., Yabuta, Y., Shigeoka, S., 2008. Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol. 147, 1251-1263.

Peterbauer, T., Richter, A., 2001. Biochemistry and physiology of raffinose family oligosaccharides and galactosyl cyclitols in seeds. Seed Sci Res. 11, 185-197.

Ren, Z., Gao, J., Li, L., Cai, X., Huang, W., Chao, D., Zhu, M., Wang, Z., Luan, S., Lin, H., 2005. A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nat. Genet. 37, 1141-1146.

Ruan, Y.L., Sucrose metabolism: Gateway to diverse carbon use and sugar signaling. Annu. Rev. Plant Biol. 2014. 65, 33-67.

Salvi, P., Kamble, N.U., Majee, M., 2018. Stress-inducible galactinol synthase of chickpea (CaGolS) is implicated in heat and oxidative stress tolerance through reducing stress-induced excessive reactive oxygen species accumulation. Plant Cell Physiol. 59, 155-166.

Sami, F., Yusuf, M., Faizan, M., Faraz, A., Hayat, S., 2016. Role of sugars under abiotic stress. Plant Physiol Bioch 16, 30355.-2.

Schnable, J.C., 2015. Genome evolution in maize: from genomes back to genes. Annu. Rev. Plant Biol. 66, 329-343.

Sengupta, S., Mukherjee, S., Basak, P., Majumder, A.L., 2015. Significance of galactinol and raffinose family oligosaccharide synthesis in plants. Front Plant Sci 6, 656.

Sengupta, S., Mukherjee, S., Parween, S., Majumder, A.L., 2012. Galactinol synthase across evolutionary diverse taxa: functional preference for higher plants? FEBS Lett. 586, 1488-1496.

Song, C., Chung, W.S., Lim, C., 2016. Overexpression of heat shock factor gene HsfA3 increases galactinol levels and oxidative stress tolerance in Arabidopsis. Mol. Cells 6, 477-483.

Sun, Z., Qi, X., Wang, Z., Li, P., Wu, C., Zhang, H., Zhao, Y., 2013. Overexpression of TsGOLS2, a galactinol synthase, in Arabidopsis thaliana enhances tolerance to high salinity and osmotic stresses. Plant Physiol Biochem 69, 82-89.

Taji, T., Ohsumi, C., Iuchi, S., Seki, M., Kasuga, M., Kobayashi, M., Yamaguchi-Shinozaki, K., Shinozaki, K., 2002. Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J 29, 417-426.

Thomson, M.J., de Ocampo, M., Egdane, J., Rahman, M.A., Sajise, A. G., Adorada, D.L., Tumimbang-Raiz, E., Blumwald, E., Seraj, Z.I., Singh, R.K., et al., 2010. Characterizing the Saltol quantitative trait locus for salinity tolerance in rice. Rice 3, 148-160.

To, J.P.C., Haberer, G., Ferreira, F.J., Derue`re, J., Mason, M.G.,Schaller, G.E., Alonso, J.M., Ecker, J.R., Kieber, J.J., 2004. Type-A Arabidopsis response regulators are partially redundant negative regulators of cytokinin signaling. Plant Cell 16, 658-671.

To, J.P.C., and Kieber, J.J., 2008. Cytokinin signaling: two-components and more. Trends Plant Sci. 13, 85-92.

van Zelm, E., Zhang, Y., Testerink, C., 2020. Salt tolerance mechanisms of plants. Annu. Rev. Plant Biol. 71, 403-433.

Wang, L., Wang, Y., Yin, P., Jiang, C., Zhang, M., 2024. ZmHAK17 encodes a Na⁺-selective transporter that promotes maize seed germination under salt conditions. New Crops 1, 100024.

Wang, Q., Liu, P., Jing, H., Zhou, X., Zhao, B., Li, Y., Jin, J., 2021. JMJ27-mediated histone H3K9 demethylation positively regulates drought-stress responses in Arabidopsis. New Phytol. 232, 221-236.

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

Xing, H.L., Dong, L., Wang, Z.P., Zhang, H.Y., Han, C.Y., Liu, B., Wang, X.C., Chen, Q.J., 2014. A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biol. 14, 327.

Yan, Z., Wang, J., Wang, F., Xie, C., Lv, B., Yu, Z., Dai, S., Liu, X., Xia, G., Tian, H., Li, C., D, Z., 2021. MPK3/6-induced degradation of ARR1/10/12 promotes salt tolerance in Arabidopsis. EMBO Rep. 22, e52457.

Yan, C., Fan, M., Yang, M., Zhao, J., Zhang, W., Su, Y., Xiao, L., Deng, H., Xie, D., 2018. Injury activates Ca²⁺/Calmodulin-dependent phosphorylation of JAV1-JAZ8-WRKY51 complex for jasmonate biosynthesis. Mol. Cell, 70, 136-149.

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

Yang, Z., Cao, Y., Shi, Y., Qin, F., Jiang, C., Yang, S., 2023. Genetic and molecular exploration of maize environmental stress resilience: Toward sustainable agriculture. Mol. Plant 16, 1496-1517.

Yin, P., Liang, X., Zhao, H., Xu, Z., Chen, L., Yang, X., Qin, F., Zhang, J., Jiang, C., 2023. Cytokinin signaling promotes salt tolerance by modulating shoot chloride exclusion in maize. Mol. Plant 16, 1031-1047.

Zhang, M., Cao, Y., Wang, Z., Wang, Z.Q., 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.

Zhang, P., He, R., Yang, J., Cai, J., Qu, Z., Yang, R., Gu, J., Wang, Z., Adelson, D. L., Zhu, Y., Cao, X., 2023. The long non-coding RNA DANA2 positively regulates drought tolerance by recruiting ERF84 to promote JMJ29-mediated histone demethylation. Mol. Plant 16, 1339-1353.

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 Biotechnol. J. 21, 97-108.

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.

Zhang, H., Yu, F., Xie, P., Sun, S., Qiao, X., Tang, S., Chen, C., Yang, S., Mei, C., Yang, D., et al., 2023. A Gγ protein regulates alkaline sensitivity in crops. Science 379, eade8416.

Zhao, T., Thacker, R., Corum III, J. W., Snyder, J.C., Meeley, R.B., Obendorf, R.L., Downie, B., 2004. Expression of the maize GALACTINOL SYNTHASE gene family: (I) Expression of two different genes during seed development and germination. Physilol Plantarum, 21, 634-646.

Zhou, X., Li, J., Wang, Y., Liang, X., Zhang, M., Lu, M., Guo, Y., Qin, F., Jiang, C., 2022. The classical SOS pathway confers natural variation of salt tolerance in maize. New Phytol. 236, 479-494.

Relative Articles

Supplements(0)

Cited By

Proportional views