ZmFBL41 variants enhance maize resistance to <i>Rhizoctonia solani</i> by attenuating ZmFAH degradation and increasing fumaric acid accumulation

Jicheng Qu; Bao Lin; Tiantian Geng; Mingyue Lai; Yunya Bi; Fangyu Liang; Bin Yuan; Daolin Fu; Jiajie Wu; Haifeng Liu; Zhaohui Chu

doi:10.1016/j.jgg.2026.04.009

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ZmFBL41 variants enhance maize resistance to Rhizoctonia solani by attenuating ZmFAH degradation and increasing fumaric acid accumulation

doi: 10.1016/j.jgg.2026.04.009

a. State Key Laboratory of Hybrid Rice, Hubei Hongshan Laboratory, College of Life Sciences, Wuhan University, Wuhan, Hubei 430072, China;
b. State Key Laboratory of Wheat Improvement, College of Agronomy, Shandong Agricultural University, Taian, Shandong 271018, China;
c. Frontier Science Center for Immunology and Metabolism, Medical Research Institute, Zhongnan Hospital of Wuhan University, Wuhan University, Wuhan, Hubei 430071, China;
d. Institute of Plant Protection and Soil Fertilizer, Hubei Academy of Agricultural Sciences, Wuhan, Hubei 430064, China

Funds:

This project was funded by the STI 2030-Major Projects (2023ZD04070), the Innovation Team Project for Modern Agricultural Industrious Technology System of Shandong Province (SDAIT-17-06), the Key Research and Development Program of Hubei Province (2022BFE003), and the Hubei Agriculture Science and Technology Innovation Center Program (2025-620-000-001-030).

Received Date: 2026-01-18
Accepted Date: 2026-04-13
Rev Recd Date: 2026-04-11

Available Online: 2026-04-22

Abstract

Abstract

The F-box protein ZmFBL41, which targets ZmCAD and ZmNCED6, increases susceptibility to maize banded leaf and sheath blight (BLSB). Here, we report significantly reduced BLSB resistance in maize expressing the susceptible haplotype ZmFBL41^B73, and the identification of ZmFBL41^B73-interacting protein, fumarylacetoacetate hydrolase (FAH). In contrast to ZmCAD, which interacts with the LRR3 motif, ZmFAH interacts with each LRR motif of ZmFBL41^B73. ZmFAH positively regulates plant resistance to Rhizoctonia solani and decrease BLSB resistance in zmfah maize but increase sheath blight (ShB) resistance in ZmFAH-overexpressing rice. ZmFAH is involved in fumaric acid (FA) metabolism, which inhibits fungal growth and invasion in plants. Compared with the susceptible allele of ZmFBL41^B73, the resistant haplotype ZmFBL41^Chang7-2, with two amino acid substitutions, exhibits weaker interactions with and promotes the degradation of ZmFAH, thereby resulting in greater FA accumulation and increased resistance to BLSB in the inbred lines of the Chang7-2 haplotype than in those of the B73 haplotype. Additionally, field fumarate pretreatment significantly increases rice resistance to bacterial blight and ShB. Collectively, our findings reveal the dual functions of ZmFBL41^Chang7-2 in strengthening the host’s chemical barrier through FA accumulation in addition to the previously identified physical barrier protection through lignin accumulation during fungal infection.
- Banded leaf and sheath blight,
- Fumaric acid,
- Rhizoctonia solani,
- Rice sheath blight,
- Zea mays

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References

Ahuja, I., Kissen, R. Bones, A. M., 2012. Phytoalexins in defense against pathogens. Trends Plant Sci. 17, 73-90.

Akram, M., 2014. Citric acid cycle and role of its intermediates in metabolism. Cell Biochem. Biophys. 68, 475-478.

Arias-Barrau, E., Olivera, E. R., Luengo, J. M., Fernandez, C., Galan, B., Garcia, J. L., Diaz, E., Minambres, B., 2004. The homogentisate pathway: a central catabolic pathway involved in the degradation of L-phenylalanine, L-tyrosine, and 3-hydroxyphenylacetate in Pseudomonas putida. J. Bacteriol. 186, 5062-5077.

Arts, R. J., Novakovic, B., Ter Horst, R., Carvalho, A., Bekkering, S., Lachmandas, E., Rodrigues, F., Silvestre, R., Cheng, S. C., Wang, S. Y., et al., 2016. Glutaminolysis and fumarate accumulation integrate immunometabolic and epigenetic programs in trained immunity. Cell Metab. 24, 807-819.

Balmer, A., Pastor, V., Glauser, G., Mauch-Mani, B., 2018. Tricarboxylates induce defense priming against bacteria in Arabidopsis thaliana. Front. Plant Sci. 9, 1221.

Bard, J. A. M., Goodall, E. A., Greene, E. R., Jonsson, E., Dong, K. C., Martin, A., 2018. Structure and function of the 26S proteasome. Annu. Rev. Biochem. 87, 697-724.

Batiru, G., Lubberstedt, T. 2024. Polyploidy in maize: from evolution to breeding. Theor. Appl. Genet. 137, 182.

Cai, H., Chen, X., Liu, Y., Chen, Y., Zhong, G., Chen, X., Rong, S., Zeng, H., Zhang, L., Li, Z., et al., 2025. Lactate activates trained immunity by fueling the tricarboxylic acid cycle and regulating histone lactylation. Nat. Commun., 16, 3230.

Choi, I., Son, H., Baek, J. H., 2021. Tricarboxylic Acid TCA. Cycle intermediates: regulators of immune responses. Life (Basel) 11, 69.

Ding, M., Zhou, Y., Becker, D., Yang, S., Krischke, M., Scherzer, S., Yu-Strzelczyk, J., Mueller, M. J., Hedrich, R., Nagel, G., et al., 2024. Probing plant signal processing optogenetically by two channelrhodopsins. Nature 633, 872-877.

Doyle, J., 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem. Bull. 19.

Fabregas, N., Fernie, A. R., 2021. The interface of central metabolism with hormone signaling in plants. Curr. Biol. 31, R1535-R1548.

Fan, Y., Zhou, W., Xian, B., Shu, K., 2025. K48- and K63-linked ubiquitination in plant development and stress responses. J. Genet. Genomics S1673-8527(25)00354-00356.

Feiz, L., Shyu, C., Wu, S., Ahern, K. R., Gull, I., Rong, Y., Artymowicz, C. J., Pineros, M. A., Fei, Z., Brutnell, T. P., et al., 2024. COI1 F-box proteins regulate DELLA protein levels, growth, and photosynthetic efficiency in maize. Plant Cell 36, 3237-3259.

Feng, Z., Gao, P., Wang, G., Kang, H., Zhao, J., Xie, W., Chen, R., Ju, R., Wang, X., Wei, Z., et al., 2025. Natural variation in SBRR1 shows high potential for sheath blight resistance breeding in rice. Nat. Genet. 57, 2004-2016.

Gao, L. L., Dong, Y., Cun, Z., Zhang, J. Y., Chen, J. W., 2025. Moderate shading elicits succinic acid accumulation aligning with simultaneous expression of genes involved in TCA cycle and photosynthetic pathway in a medicinal plant Pinellia ternata. Plant Physiol. Biochem. 224, 109911.

Greene, G. H., McGary, K. L., Rokas, A., Slot, J. C., 2014. Ecology drives the distribution of specialized tyrosine metabolism modules in fungi. Genome Biol. Evol. 6, 121-132.

Han, C., Ren, C., Zhi, T., Zhou, Z., Liu, Y., Chen, F., Peng, W., Xie, D., 2013. Disruption of fumarylacetoacetate hydrolase causes spontaneous cell death under short-day conditions in Arabidopsis. Plant Physiol. 162, 1956-1964.

Hao, B., Zheng, N., Schulman, B. A., Wu, G., Miller, J. J., Pagano, M., Pavletich, N. P., 2005. Structural basis of the Cks1-dependent recognition of p27Kip1. by the SCFSkp2. ubiquitin ligase. Mol. Cell 20, 9-19.

Hu, Z., Liu, H., Guo, M., Han, X., Li, Y., Chen, R., Guo, Y., Yang, Y., Sun, S., Zhou, Y., et al., 2025. Natural variation of an E3 ubiquitin ligase encoding gene Chalk9 regulates grain chalkiness in rice. Nat. Commun. 16, 6653.

Ilica, R. A., Kloetzer, L., Galaction, A. I., Cascaval, D., 2019. Fumaric acid: production and separation. Biotechnol. Lett. 41, 47-57.

Inigo, M., Deja, S., Burgess, S. C., 2021. Ins and Outs of the TCA Cycle: The central role of anaplerosis. Annu. Rev. Nutr. 41, 19-47.

Kitagawa, T., 2012. Hepatorenal tyrosinemia. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci. 88, 192-200.

Kuchay, S., Wang, H., Marzio, A., Jain, K., Homer, H., Fehrenbacher, N., Philips, M. R., Zheng, N., Pagano, M., 2019. GGTase3 is a newly identified geranylgeranyltransferase targeting a ubiquitin ligase. Nat. Struct. Mol. Biol. 26, 628-636.

Kumar, N., Goel, N., 2019. Phenolic acids: Natural versatile molecules with promising therapeutic applications. Biotechnol. Rep. 24, e00370.

Lechner, E., Achard, P., Vansiri, A., Potuschak, T., Genschik, P., 2006. F-box proteins everywhere. Curr. Opin. Plant Biol. 9, 631-638.

Li, N., Lin, B., Wang, H., Li, X., Yang, F., Ding, X., Yan, J., Chu, Z., 2019. Natural variation in ZmFBL41 confers banded leaf and sheath blight resistance in maize. Nat. Genet. 51, 1540-1548.

Liu, H., Lu, C., Li, Y., Wu, T., Zhang, B., Liu, B., Feng, W., Xu, Q., Dong, H., He, S., et al., 2022. The bacterial effector AvrRxo1 inhibits vitamin B6 biosynthesis to promote infection in rice. Plant Commun. 3, 100324.

Liu, Y., Zhang, H., Wang, J., Gao, W., Sun, X., Xiong, Q., Shu, X., Miao, Y., Shen, Q., Xun, W., Zhang, R., 2024. Nonpathogenic Pseudomonas syringae derivatives and its metabolites trigger the plant "cry for help" response to assemble disease suppressing and growth promoting rhizomicrobiome. Nat. Commun. 15, 1907.

Mason, B., Laman, H., 2020. The FBXL family of F-box proteins: variations on a theme. Open Biol. 10, 200319.

Meteignier, L. V., Nutzmann, H. W., Papon, N., Osbourn, A., Courdavault, V., 2023. Emerging mechanistic insights into the regulation of specialized metabolism in plants. Nat. Plants 9, 22-30.

Miao, P., Wang, H., Wang, W., Wang, Z., Ke, H., Cheng, H., Ni, J., Liang, J., Yao, Y. F., Wang, J., et al., 2025. A widespread plant defense compound disarms bacterial type III injectisome assembly. Science 387, eads0377.

Mou, B., Zhao, G., Wang, J., Wang, S., He, F., Ning, Y., Li, D., Zheng, X., Cui, F., Xue, F., et al., 2023. The OsCPK17-OsPUB12-OsRLCK176 module regulates immune homeostasis in rice. Plant Cell 36, 987-1006.

Navarro-Quezada, A., Schumann, N., Quint, M., 2013. Plant F-box protein evolution is determined by lineage-specific timing of major gene family expansion waves. PLoS ONE 8, e68672.

Roussin-Leveillee, C., Rossi, C. A. M., Castroverde, C. D. M., Moffett, P., 2024. The plant disease triangle facing climate change: a molecular perspective. Trends Plant Sci. 29, 895-914.

Schmittgen, T. D., Livak, K. J., 2008. Analyzing real-time PCR data by the comparative CT. method. Nat. Protoc. 3, 1101-1108.

Sciacovelli, M., Goncalves, E., Johnson, T.I., Zecchini, V. R., da Costa, A. S., Gaude, E., Drubbel, A. V., Theobald, S. J., Abbo, S. R., Tran, M. G., et al. 2016. Fumarate is an epigenetic modifier that elicits epithelial-to-mesenchymal transition. Nature 537, 544-547.

Shang, S., He, Y., Zhao, R., Li, H., Fang, Y., Hu, Q., Fan, Y., Wang, Y., Zhou, X., Wang, P., et al., 2025. Fumarylacetoacetate hydrolase targeted by a Fusarium graminearum effector positively regulates wheat FHB resistance. Nat. Commun. 16, 5582.

Singh, B. K., Delgado-Baquerizo, M., Egidi, E., Guirado, E., Leach, J. E., Liu, H., Trivedi, P., 2023. Climate change impacts on plant pathogens, food security and paths forward. Nat. Rev. Microbiol. 21, 640-656.

Sweetlove, L. J., Beard, K. F., Nunes-Nesi, A., Fernie, A. R., Ratcliffe, R. G., 2010. Not just a circle: flux modes in the plant TCA cycle. Trends Plant Sci. 15, 462-470.

Tal, L., Palayam, M., Ron, M., Young, A., Britt, A., Shabek, N., 2022. A conformational switch in the SCF-D3/MAX2 ubiquitin ligase facilitates strigolactone signalling. Nat. Plants 8, 561-573.

Tian, J., Wang, C., Chen, F., Qin, W., Yang, H., Zhao, S., Xia, J., Du, X., Zhu, Y., Wu, L., et al., 2024. Maize smart-canopy architecture enhances yield at high densities. Nature 632, 576-584.

Vierstra, R. D., 2009. The ubiquitin-26S proteasome system at the nexus of plant biology. Nat. Rev. Mol. Cell Biol. 10, 385-397.

Wang, A., Shu, X., Jing, X., Jiao, C., Chen, L., Zhang, J., Ma, L., Jiang, Y., Yamamoto, N., Li, S., et al., 2021. Identification of rice Oryza sativa L. genes involved in sheath blight resistance via a genome-wide association study. Plant Biotechnol. J. 19, 1553-1566.

Wang, L., Xia, Y., Hou, Y., 2024a. Candy or poison: Plant metabolites as swing factors against microbes. Mol. Plant 17, 1341-1343.

Wang, S., Zhang, X., Gong, D. H., Huang, Q. Q., Kandegama, W., Georgiev, M. I., Gao, Y. Y., Liao, P., Hao, G. F., 2025. Sophisticated crosstalk of tryptophan-derived metabolites in plant stress responses. Plant Commun. 6, 101425.

Wang, X., Ju, Y., Wu, T., Kong, L., Yuan, M., Liu, H., Chen, X., Chu, Z., 2024b. The clade III subfamily of OsSWEETs directly suppresses rice immunity by interacting with OsHMGB1 and OsHsp20L. Plant Biotechnol. J. 22, 2186-2200.

Wei, L., Chen, J., Liu, C., Liu, D., Du, M., He, S., Cheng, W., Bhadauria, V., Peng, Y.L., Zhu, W., 2025. Allelic variation in maize malata dehydrogenase 7 shapes promoter methylation and banded leaf and sheath blight resistance. Adv. Sci. 13, e11356.

Weiss, A. K. H., Loeffler, J. R., Liedl, K. R., Gstach, H., Jansen-Durr, P., 2018. The fumarylacetoacetate hydrolase FAH superfamily of enzymes: multifunctional enzymes from microbes to mitochondria. Biochem. Soc. Trans. 46, 295-309.

Wu, Z., Pope, S. D., Ahmed, N. S., Leung, D. L., Hong, Y., Hajjar, S., Krabak, C., Zhong, Z., Raghunathan, K., Yue, Q., et al., 2025. Regulation of inflammatory responses by pH-dependent transcriptional condensates. Cell 188, 5632-5652.e5625.

Xie, W., Xue, X., Wang, Y., Zhang, G., Zhao, J., Zhang, H., Wang, G., Li, L., Wang, Y., Shan, W., et al., 2025. Natural mutation in Stay-Green OsSGR confers enhanced resistance to rice sheath blight through elevating cytokinin content. Plant Biotechnol. J. 23, 807-823.

Xing, W., Busino, L., Hinds, T. R., Marionni, S. T., Saifee, N. H., Bush, M. F., Pagano, M., Zheng, N., 2013. SCFFBXL3 ubiquitin ligase targets cryptochromes at their cofactor pocket. Nature 496, 64-68.

Xue, X., Chen, X., Wang, X., Wang, T., Liao, R., Liu, H., Zhu, C., Jones, J. D. G., Chu, Z., 2026. Two Phytophthora effectors mitigate plant immunity by manipulating intracellular pH through interaction with V-ATPase in potato. Mol. Hortic. 6, 4.

Yang, Z., Liang, G., Liu, C., Chu, Z., Li, N., 2024. The F-box protein ZmFBL41 negatively regulates disease resistance to Rhizoctonia solani by degrading the abscisic acid synthase ZmNCED6 in maize. Plant Cell Rep. 43, 48.

You, X., Wang, J., Wang, G. L., Ning, Y., 2025. Disruption of E3 ubiquitin ligase confers disease resistance. Trends Plant Sci. 30, 1183-1185.

Zhang, M., Li, W., Zhang, T., Liu, Y., Liu, L., 2024. Botrytis cinerea-induced F-box protein 1 enhances disease resistance by inhibiting JAO/JOX-mediated jasmonic acid catabolism in Arabidopsis. Mol. Plant 17, 297-311.

Zhao, P., Yang, H., Sun, Y., Zhang, J., Gao, K., Wu, J., Zhu, C., Yin, C., Chen, X., Liu, Q., et al., 2025. Targeted MYC2 stabilization confers citrus Huanglongbing resistance. Science 388, 191-198.

Zheng, A., Lin, R., Zhang, D., Qin, P., Xu, L., Ai, P., Ding, L., Wang, Y., Chen, Y., Liu, Y., et al., 2013. The evolution and pathogenic mechanisms of the rice sheath blight pathogen. Nat. Commun. 4, 1424.

Zhou, T., Chen, H., Jiang, X., Zhu, H., Lin, Q., Jung, K. H., Zhu, X., Xuan, Y. H., 2025. TCP19 regulates nitrogen-dependent sheath blight susceptibility by modulating nitrogen uptake and signalling in rice. Plant Biotechnol. J. 23, 4140-4157.

Zuo, S., Zhang, L., Wang, H., Yin, Y., Zhang, Y., Chen, Z., Ma, Y., Pan, X., 2008. Prospect of the QTL-qSB-9Tq utilized in molecular breeding program of japonica rice against sheath blight. J. Genet. Genomics 35, 499-505.

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