<i>ZmL75</i> is required for colonization by arbuscular mycorrhizal fungi and for saline–alkali tolerance in maize

Jie Liu; Boming Yang; Xunji Chen; Tengfei Zhang; Huairen Zhang; Yimo Du; Qian Zhao; Zhaogui Zhang; Darun Cai; Juan Liu; Huabang Chen; Li Zhao

doi:10.1016/j.jgg.2024.12.015

Volume 52 Issue 3

Mar. 2025

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ZmL75 is required for colonization by arbuscular mycorrhizal fungi and for saline–alkali tolerance in maize

doi: 10.1016/j.jgg.2024.12.015

a. Institute of Genetics and Developmental Biology, Key Laboratory of Seed Innovation, Chinese Academy of Sciences, Beijing 100101, China;
b. University of Chinese Academy of Sciences, Beijing 100049, China;
c. Institute of Nuclear Technology and Biotechnology, Xinjiang Academy of Agriculture/Xinjiang Key Laboratory of Crop Biotechnology, Urumqi, Xinjiang 830091, China

Funds:

We thank the National Natural Science Foundation of China (No. 32171947 and No. 31671699) which supported this research. We thank professors Jianru Zuo, Chengcai Chu, and Yang Bai for kindly advices during research and manuscript written.

Received Date: 2024-10-25
Accepted Date: 2024-12-18
Rev Recd Date: 2024-12-18

Available Online: 2025-07-11

Publish Date: 2024-12-28

Abstract

Abstract

Saline–alkali soil severely reduces the productivity of crops, including maize (Zea mays). Although several genes associated with saline–alkali tolerance have been identified in maize, the underlying regulatory mechanism remains elusive. Here, we report a direct link between colonization by arbuscular mycorrhizal fungi (AMF) and saline–alkali tolerance in maize. We identify s75, a natural maize mutant that cannot survive under moderate saline–alkali soil conditions or establish AM symbioses. The saline–alkali hypersensitive phenotype of s75 is caused by a 1340-bp deletion in Zm00001d033915, designated as ZmL75. This gene encodes a glycerol-3-phosphate acyltransferase localized in the endoplasmic reticulum, and is responsible for AMF colonization. ZmL75 expression levels in roots correspond with the root length colonization (RLC) rate during early vegetative development. Notably, the s75 mutant line shows a complete loss of AMF colonization, along with alterations in the diversity and structure of its root fungal microbiota. Conversely, overexpression of ZmL75 increases the RLC rate and enhances tolerance to saline–alkali soil conditions. These results suggest that ZmL75 is required for symbiosis with AMF, which directly improves saline–alkali tolerance. Our findings provide insights into maize–AMF interactions and offer a potential strategy for maize improvement.
- Maize,
- Saline–alkali,
- ZmL75,
- AMF colonization,
- Tolerance

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References

Aroca, R., Porcel, R., Ruiz-Lozano, J.M., 2007. How does arbuscular mycorrhizal symbiosis regulate root hydraulic properties and plasma membrane aquaporins in Phaseolus vulgaris under drought, cold or salinity stresses? New Phytol. 173, 808-816.

Auge, R.M., Toler, H.D., Saxton, A.M., 2015. Arbuscular mycorrhizal symbiosis alters stomatal conductance of host plants more under drought than under amply watered conditions: A meta-analysis. Mycorrhiza 25, 13-24.

Azcon-G de Aguilar, C., Azcon, R., Barea, J. M., 1979. Endomycorrhizal fungi and Rhizobium as biological fertilisers for Medicago sativa in normal cultivation. Nature 279, 325-327.

Bravo, A., Brands, M., Wewer, V., Dormann, P., Harrison, M.J., 2017. Arbuscular mycorrhiza-specific enzymes FatM and RAM2 fine-tune lipid biosynthesis to promote development of arbuscular mycorrhiza. New Phytol. 214, 1631-1645.

Bukowski, R., Guo, X.S., Lu, Y.L., Zou, C., He, B., Rong, Z.Q., Wang, B., Xu, D.W., Yang, B.C., Xie, C.X., et al., 2018. Construction of the third-generation Zea mays haplotype map. Gigascience 7, 1-12.

Butcher, K.W.A.F., de Sutter, T., Chatterjee, A., Harmon, J., 2016. Soil salinity: a threat to global food security. Agron. J. 108, 2189-2200.

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

Cao, Y.B., Song, H.F., Zhang, L.Y., 2022. New insight into plant saline-alkali tolerance mechanisms and application to breeding. Int. J. Mol. Sci. 23, 16048.

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

Chandrasekaran, M., Boughattas, S., Hu, S., Oh, S.H., Sa, T.A., 2014. Meta-analysis of arbuscular mycorrhizal effects on plants grown under salt stress. Mycorrhiza 24, 611-625.

Dai, H.L., Zhang, X.W., Zhao, B.Y., Shi, J.C., Zhang, C., Wang, G., Yu, N., Wang, E.T., 2022. Colonization of mutualistic mycorrhizal and parasitic blast fungi requires OsRAM2-regulated fatty acid biosynthesis in rice. Mol. Plant microbe interact. 35, 178-186.

Estrada, B., Beltran-Hermoso, M., Palenzuela, J., Iwase, K., Ruiz-Lozano, J.M., Barea, J., Oehl, F., 2013. Diversity of arbuscular mycorrhizal fungi in the rhizosphere of Asteriscus maritimus (L.) Less., a representative plant species in arid and saline Mediterranean ecosystems. J. Arid Environ. 97, 170-175.

Evelin, H., Devi, T.S., Gupta, S., Kapoor, R., 2019. Mitigation of salinity stress in plants by arbuscular mycorrhizal symbiosis: current understanding and new challenges. Front Plant Sci. 10, 470.

Evelin, H., Giri, B., Kapoor, R., 2012. Contribution of Glomus intraradices inoculation to nutrient acquisition and mitigation of ionic imbalance in NaCl stressed Trigonella foenum-graecum. Mycorrhiza 22, 203-217.

Gidda, S.K., Shockey, J.M., Rothstein, S.J., Dyer, J.M., Mullen, R.T., 2009. Arabidopsis thaliana GPAT8 and GPAT9 are localized to the ER and possess distinct ER retrieval signals: functional divergence of the dilysine ER retrieval motif in plant cells. Plant Physiol. Biochem. 47, 867-879.

Glassop, D., Smith, S.E., Smith, F.W., 2005. Cereal phosphate transporters associated with the mycorrhizal pathway of phosphate uptake into roots. Planta 222, 688-698.

Guo, R., Shi, L.X., Yan, C.R., Zhong, X.L., Gu, F.X., Liu, Q., Xia, X., Li, H.R., 2017. Ionomic and metabolic responses to neutral salt or alkaline salt stresses in maize (Zea mays L.) seedlings. BMC Plant Biol. 17, 41.

Hui, J., An, X., Li, Z.B., Neuhauser, B., Ludewig, U., Wu, X.N., Schulze, W.X., Chen, F.J., Feng, G., Lambers, H., et al., 2022. The mycorrhiza-specific ammonium transporter ZmAMT3;1 mediates mycorrhiza-dependent nitrogen uptake in maize roots. Plant Cell 34, 4066-4087.

Ismail, A.M., Horie, T., 2017. Genomics, physiology, and molecular breeding approaches for improving salt tolerance. Annu. Rev. Plant Biol. 68, 405-434.

Jiang, Y.N., Wang, W.X., Xie, Q.J., Liu, N., Liu, L.X., Wang, D.P., Zhang, X.W., Yang, C., Chen, X.Y., Tang, D.Z., et al., 2017. Plants transfer lipids to sustain colonization by mutualistic mycorrhizal and parasitic fungi. Science 356, 1172–1175.

Jung, S., Hutsch, B.W., Schubert, S., 2017. Salt stress reduces kernel number of corn by inhibiting plasma membrane H⁺-ATPase activity. Plant Physiol. Biochem. 113, 198-207.

Kim, D., Langmead, B., Salzberg, S.L., 2015. HISAT: a fast spliced aligner with low memory requirements. Nat. Methods 12, 357-360.

Li, J.W., Zhu, Q.L., Jiao, F.C., Yan, Z.W., Zhang, H.Y., Zhang, Y.M., Ding, Z.H., Mu, C.H., Liu, X., Li, Y., et al., 2023. Research progress on the mechanism of salt tolerance in maize: a classic field that needs new efforts. Plants 12, 2356.

Liu, Y.N., Liu, C.C., Zhu, A.Q., Niu, K.X., Guo, R., Tian, L., Wu, Y.N., Sun, B., Wang, B., 2022. OsRAM2 function in lipid biosynthesis is required for arbuscular mycorrhizal symbiosis in rice. Mol. Plant Microbe Interact. 35, 187-199.

Love, M.I., Huber, W., Anders, S., 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome biol. 15, 550.

Luginbuehl, L.H., Menard, G.N., Kurup, S., Van Erp, H., Radhakrishnan, G.V., Breakspear, A., Oldroyd, G.E.D., Eastmond, P.J., 2017. Fatty acids in arbuscular mycorrhizal fungi are synthesized by the host plant. Science 356, 1175-1178.

McGonigle, T.P., Miller, M.H., Evans, D.G., Fairchild, G.L., Swan, J.A., 1990. A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol. 115, 495-501.

Moulin, S., 2022. Get connected to the fungal network for improved transfer of nitrogen: the role of ZmAMT3;1 in ammonium transport in maize-arbuscular mycorrhizal symbiosis. Plant Cell 34, 3509-3511.

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.

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

Nadal, M., Sawers, R., Naseem, S., Bassin, B., Kulicke, C., Sharman, A., An, G., An, K., Ahern, K.R., Romag, A., et al., 2017. An N-acetylglucosamine transporter required for arbuscular mycorrhizal symbioses in rice and maize. Nat. Plants 3, 17073.

Nagy, R., Vasconcelos, M.J.V., Zhao, S., McElver, J., Bruce, W., Amrhein, N., Raghothama, K.G., Bucher, M., 2006. Differential regulation of five Pht1 phosphate transporters from maize (Zea mays L.). Plant Biol. 8, 186-197.

Pfeifer, B., Wittelsburger, U., Ramos-Onsins, S.E., Lercher, M.J., 2014. PopGenome: an efficient Swiss army knife for population genomic analyses in R. Mol. Biol. Evol. 31, 1929-1936.

Phillips, J.M., Hayman, D.S., 1970. Improved procedures for clearing and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Transactions of the British Mycological Society 55, 158–161.

Porcel, R., Aroca, R., Azcon, R., Ruiz-Lozano, J.M., 2016. Regulation of cation transporter genes by the arbuscular mycorrhizal symbiosis in rice plants subjected to salinity suggests improved salt tolerance due to reduced Na⁺ root-to-shoot distribution. Mycorrhiza 26, 673-684.

Porcel, R., Redondo-Gomez, S., Mateos-Naranjo, E., Aroca, R., Garcia, R., Ruiz-Lozano, J.M., 2015. Arbuscular mycorrhizal symbiosis ameliorates the optimum quantum yield of photosystem II and reduces non-photochemical quenching in rice plants subjected to salt stress. J. Plant Physiol. 185, 75-83.

Ramirez-Flores, M.R., Perez-Limon, S., Li, M., Barrales-Gamez, B., Albinsky, D., Paszkowski, U., Olalde-Portugal, V., Sawers, R.J.H., 2020. The genetic architecture of host response reveals the importance of arbuscular mycorrhizae to maize cultivation. eLife 9, e61701.

Ruiz-Lozano, J.M., Porcel, R., Azcon, C., Aroca, R., 2012. Regulation by arbuscular mycorrhizae of the integrated physiological response to salinity in plants: new challenges in physiological and molecular studies. J. Exp. Bot. 63, 4033-4044.

Sheng, M., Tang, M., Chen, H., Yang, B.W., Zhang, F.F., Huang, Y.H., 2008. Influence of arbuscular mycorrhizae on photosynthesis and water status of maize plants under salt stress. Mycorrhiza 18, 287-296.

Varet, H., Brillet-Gueguen, L., Coppee, J-Y., Dillies, M-A., 2016. SARTools: A DESeq2- and EdgeR-based R pipeline for comprehensive differential analysis of RNA-seq data. PLoS One 11, e0157022.

Wang, D.Y., Ni, Y., Xie, K.L., Li, Y.H., Wu, W.X., Shan, H.C., Cheng, B.J., Li, X.Y., 2024. Aquaporin ZmTIP2;3 promotes drought resistance of maize through symbiosis with arbuscular mycorrhizal fungi. Int. J. Mol. Sci. 25, 4205.

Wang, E.T., Schornack, S., Marsh, J.F., Gobbato, E., Schwessinger, B., Eastmond, P., Schultze, M., Kamoun, S., Oldroyd, G.E.D., 2012. A common signaling process that promotes mycorrhizal and oomycete colonization of plants. Curr. Biol. 22, 2242-2246.

Wang, M.Q., Wang, Y.F., Zhang, Y.F., Li, C.X., Gong, S.C., Yan, S.Q., Li, G.L., Hu, G.H., Ren, H.L., Yang, J.F., et al., 2019. Comparative transcriptome analysis of salt-sensitive and salt-tolerant maize reveals potential mechanisms to enhance salt resistance. Genes Genomics 41, 781-801.

Wu, N., Li, Z., Liu, H.G., Tang, M., 2015. Influence of arbuscular mycorrhiza on photosynthesis and water status of Populus cathayana Rehder males and females under salt stress. Acta. Physiol. Plant 37, 183-197.

Xie, K., Wu, S.W., Li, Z.W., Zhou, Y., Zhang, D.F., Dong, Z.Y., An, X.L., Zhu, T.T., Zhang, S.M., Liu, S.S., et al., 2018. Map-based cloning and characterization of Zea mays male sterility33 (ZmMs33) gene, encoding a glycerol-3-phosphate acyltransferase. Theor. Appl. Genet. 131, 1363-1378.

Xing, L.J., Zhu, M., Luan, M.D., Zhang, M., Jin, L., Liu, Y.P., Zou, J.J., Wang, L., Xu, M.Y., 2022. miR169q and NUCLEAR FACTOR YA8 enhance salt tolerance by activating PEROXIDASE1 expression in response to ROS. Plant Physiol. 188, 608-623.

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

Yu, H.M., Bai, F.X., Ji, C.Y., Fan, Z.Y., Luo, J.Y., Ouyang, B., Deng, X.X., Xiao, S.Y., Bisseling, T., Limpens, E., et al., 2023. Plant lysin motif extracellular proteins are required for arbuscular mycorrhizal symbiosis. Proc. Natl. Acad. Sci. U.S.A. 120, e2301884120.

Zhang, E.Y., Zhu, X.J., Wang, W.L., Sun, Y., Tian, X.M., Chen, Z.Y., Mou, X.S., Zhang, Y.L., Wei, Y.H., Fang, Z.X., et al., 2023. Metabolomics reveals the response of hydroprimed maize to mitigate the impact of soil salinization. Front. Plant Sci. 14, 1109460.

Zhang, L., Luo, H.B., Zhao, Y., Chen, X.Y., Huang, Y.M., Yan, S.S., Li, S.X., Liu, M.S., Huang, W., Zhang, X.L., et al., 2018a. Maize male sterile 33 encodes a putative glycerol-3-phosphate acyltransferase that mediates anther cuticle formation and microspore development. BMC Plant Biol. 18, 318.

Zhang, M., Cao, Y.B., Wang, Z.P., Wang, Z.Q., Shi, J.P., Liang, X.Y., Song, W.B., Chen, Q.J., Lai, J.S., Jiang, C.F., 2018b. 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, Q., Blaylock, L.A., Harrison, M.J., 2010. Two Medicago truncatula half-ABC transporters are essential for arbuscule development in arbuscular mycorrhizal symbiosis. Plant Cell 22, 1483-1497.

Zhang, X., Cai, H.L., Lu, M., Wei, Q.Y., Xu, L.J., Bo, C., Ma, Q., Zhao, Y., Cheng, B.J., 2019. A maize stress-responsive Di19 transcription factor, ZmDi19-1, confers enhanced tolerance to salt in transgenic Arabidopsis. Plant Cell Rep. 38, 1563-1578.

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

Zhu, T.T., Wu, S.W., Zhang, D.F., Li, Z.W., Xie, K., An, X.L., Ma, B., Hou, Q.C., Dong, Z.Y., Tian, Y.H., et al., 2019. Genome-wide analysis of maize GPAT gene family and cytological characterization and breeding application of ZmMs33/ZmGPAT6 gene. Theor. Appl. Genet. 132, 2137-2154.

Zorb, C., Geilfus, C-M., Dietz, K-J., 2019. Salinity and crop yield. Plant Biol. Suppl 1, 31-38.

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