<i>ZmPRX38</i> is required for improving stalk strength and yield in maize

Xiaqing Wang; Tianyi Wang; Ruyang Zhang; Min Deng; Xuan Sun; Jinghuan Li; Dongmei Chen; Yanxin Zhao; Jidong Wang; Shuai Wang; Zhiyong Li; Ruibin Xu; Ronghuan Wang; Wei Song; Jiuran Zhao

doi:10.1016/j.jgg.2025.10.009

ZmPRX38 is required for improving stalk strength and yield in maize

doi: 10.1016/j.jgg.2025.10.009

a. Beijing Key Laboratory of Maize DNA Fingerprinting and Molecular Breeding, Maize Research Institute, Beijing Academy of Agriculture and Forestry Sciences, Shuguang Garden Middle Road No. 9, Haidian District, Beijing 10009, China;
b. College of Agronomy, Hunan Agricultural University, Yuelushan Laboratory, Changsha, 410128, China

基金项目:

This work was supported by grants of the Beijing Municipal Natural Science Foundation 6244040, Outstanding Youth Foundation of Beijing Academy of Agriculture and Forestry Sciences (YXQN202401), the National Natural Science Foundation of China (32201815), the Beijing Scholars Program (BSP041).

详细信息

通讯作者:
Ronghuan Wang,E-mail:wangronghuan@baafs.net.cn

Wei Song,E-mail:songwei@baafs.net.cn

Jiuran Zhao,E-mail:maizezhao@126.com

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出版历程
- 收稿日期: 2025-07-15
- 录用日期: 2025-10-31
- 修回日期: 2025-10-30
- 网络出版日期: 2025-11-07

ZmPRX38 is required for improving stalk strength and yield in maize

a. Beijing Key Laboratory of Maize DNA Fingerprinting and Molecular Breeding, Maize Research Institute, Beijing Academy of Agriculture and Forestry Sciences, Shuguang Garden Middle Road No. 9, Haidian District, Beijing 10009, China;
b. College of Agronomy, Hunan Agricultural University, Yuelushan Laboratory, Changsha, 410128, China

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摘要

摘要: Stalk lodging is a major problem in maize production, usually causing significant yield losses due to weak stalk strength. Understanding the genetic basis of stalk strength is crucial for improving maize lodging resistance. In this study, we identify 31 quantitative trait loci (QTLs) related to maize stalk strength and clone ZmPRX38 (encoding peroxidase 38) responsible for a hotspot QTL region of stalk strength. ZmPRX38 is highly expressed in maize stalk during vegetative growth stage, and its protein is localized in the cell membrane, cytoplasm and apoplast. Knockout of ZmPRX38 decreases stalk strength and yield in maize, while overexpressing ZmPRX38 increases stalk strength and yield. ZmPRX38 in phenylpropanoid pathway is involved in the biosynthesis of guaiacyl lignin, p-hydroxy-phenyl lignin, and syringyl lignin. Additionally, we identify a favorable haplotype of ZmPRX38, which enhances stalk strength, containing 3 loci distributed in the 5’ untranslated region (UTR), exon 1, and 3’UTR of ZmPRX38, respectively. Although 91.46% of maize natural lines contain this favorable haplotype, most of the Huang-gai (HG) lines, a backbone maize germplasm, contain the unfavorable haplotypes. Therefore, targeted improvement of ZmPRX38 by editing unfavorable haplotypes may be an effective strategy for increasing maize stalk strength, thereby improving maize lodging resistance and yield.
- Maize /
- Stalk Strength /
- Lodging Resistance /
- Peroxidase /
- QTL /
- Lignin
Abstract: Stalk lodging is a major problem in maize production, usually causing significant yield losses due to weak stalk strength. Understanding the genetic basis of stalk strength is crucial for improving maize lodging resistance. In this study, we identify 31 quantitative trait loci (QTLs) related to maize stalk strength and clone ZmPRX38 (encoding peroxidase 38) responsible for a hotspot QTL region of stalk strength. ZmPRX38 is highly expressed in maize stalk during vegetative growth stage, and its protein is localized in the cell membrane, cytoplasm and apoplast. Knockout of ZmPRX38 decreases stalk strength and yield in maize, while overexpressing ZmPRX38 increases stalk strength and yield. ZmPRX38 in phenylpropanoid pathway is involved in the biosynthesis of guaiacyl lignin, p-hydroxy-phenyl lignin, and syringyl lignin. Additionally, we identify a favorable haplotype of ZmPRX38, which enhances stalk strength, containing 3 loci distributed in the 5’ untranslated region (UTR), exon 1, and 3’UTR of ZmPRX38, respectively. Although 91.46% of maize natural lines contain this favorable haplotype, most of the Huang-gai (HG) lines, a backbone maize germplasm, contain the unfavorable haplotypes. Therefore, targeted improvement of ZmPRX38 by editing unfavorable haplotypes may be an effective strategy for increasing maize stalk strength, thereby improving maize lodging resistance and yield.
- Maize /
- Stalk Strength /
- Lodging Resistance /
- Peroxidase /
- QTL /
- Lignin

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参考文献(54)

Besseau, S., Hoffmann, L., Geoffroy, P., Lapierre, C., Pollet, B., Legrand, M., 2007. Flavonoid accumulation in Arabidopsis repressed in lignin synthesis affects auxin transport and plant growth. Plant Cell 19, 148-162.

Blee, K.A., Choi, J.W., O'Connell, A.P., Schuch, W., Lewis, N.G., Bolwell, G.P., 2003. A lignin-specific peroxidase in tobacco whose antisense suppression leads to vascular tissue modification. Phytochemistry 64, 163-176.

Cui, J.J., Cui, Z.G., Lu, Y., Lv, X.F., Cao, Q.J., Hou, Y.L., Yang, X.Y., Gu, Y., 2022. Maize grain yield enhancement in modern hybrids associated with greater stalk lodging resistance at a high planting density: a case study in northeast China. Sci. Rep. 12, 14647.

Duan, C.X., Cao, Y.Y., Dong, H.Y., Xia, Y.S., Li, H., Hu, Q.Y., Yang, Z.H., Wang, X.M., 2022. Precise characterization of maize germplasm for resistance to pythium stalk rot and gibberella stalk rot. Scientia Agricultura Sinica 55, 265-279.

Fernandez-Perez, F., Pomar, F., Pedreno, M.A., Novo-Uzal, E., 2015a. The suppression of AtPrx52 affects fibers but not xylem lignification in Arabidopsis by altering the proportion of syringyl units. Physiol Plant. 154, 395-406.

Fernandez-Perez, F., Vivar, T., Pomar, F., Pedreno, M.A., Novo-Uzal, E., 2015b. Peroxidase 4 is involved in syringyl lignin formation in Arabidopsis thaliana. J. Plant Physiol. 175, 86-94.

Francisco, J.S., Moraes, H.P., Dias, E.P., 2004. Evaluation of the Image-Pro Plus 4.5 software for automatic counting of labeled nuclei by PCNA immunohistochemistry. Braz. Oral Res. 18, 100-104.

Halpin, C., Holt, K., Chojecki, J., Oliver, D., Chabbert, B., Monties, B., Edwards, K., Barakate, A., Foxon, G.A., 1998. Brown-midrib maize (bm1)-a mutation affecting the cinnamyl alcohol dehydrogenase gene. Plant J. 14, 545-553.

Jeong, Y.J., Kim, Y.C., Lee, J.S., Kim, D.G., Lee, J.H., 2022. Reduced expression of PRX2/ATPRX1, PRX8, PRX35, and PRX73 affects cell elongation, vegetative growth, and vasculature structures in Arabidopsis thaliana. Plants (Basel). 11, 3353.

Jiao, S.P., Hazebroek, J.P., Chamberlin, M.A., Perkins, M., Sandhu, A.S., Gupta, R., Simcox, K.D., Li, Y.H., Prall, A., Heetland, L., et al., 2019. Chitinase-like1 plays a role in stalk tensile strength in maize. Plant Physiol. 181, 1127-1147.

Kanehisa, M., Sato, Y., Furumichi, M., Morishima, K., Tanabe, M., 2019. New approach for understanding genome variations in KEGG. Nucleic Acids Res 47(D1), D590-D595.

Kebrom, T.H., McKinley, B., Mullet, J.E., 2017. Dynamics of gene expression during development and expansion of vegetative stem internodes of bioenergy sorghum. Biotechnol Biofuels 10, 159.

Kidwai, M., Dhar, Y. V., Gautam, N., Tiwari, M., Ahmad, I. Z., Asif, M. H., Chakrabarty, D., 2019. Oryza sativa class III peroxidase (OsPRX38) overexpression in Arabidopsis thaliana reduces arsenic accumulation due to apoplastic lignification. J Hazard Mater., 362, 383-393.

Lapierre, C., Monties, B., and Rolando, C., 1986. Thioacidolysis of poplar lignins: identification of monomeric syringyl products and characterization of guaiacyl-syringyl lignin fractions. Holzforschung 40, 113-118.

Li, C.H., Song, W., Luo, Y.F., Gao, S.H., Zhang, R.Y., Shi, Z., Wang, X.Q., Wang, R.H., Wang, F.G., Wang, J.D., et al., 2019. The HuangZaoSi maize genome provides insights into genomic variation and improvement history of maize. Mol. Plant 12, 402-409.

Li, D.D., Li, X.M., Wang, Z.C., Wang, H.C., Gao, J.Z., Liu, X.T., Zhang, Z., 2024. Transcription factors RhbZIP17 and RhWRKY30 enhance resistance to Botrytis cinerea by increasing lignin content in rose petals. J. Exp. Bot. 75, 1633-1646.

Li, L., Hill-Skinner, S., Liu, S.Z., Beuchle, D., Tang, H.M., Yeh, C.T., Nettleton, D., Schnable, P.S., 2015. The maize brown midrib4 (bm4) gene encodes a functional folylpolyglutamate synthase. Plant J. 81, 493-504.

Li, M. X., Yeung, J. M., Cherny, S. S., Sham, P. C., 2012. Evaluating the effective numbers of independent tests and significant p-value thresholds in commercial genotyping arrays and public imputation reference datasets. Hum Genet, 131(5), 747-756.

Li, P., Zhu, T., Wang, Y., Zhang, X., Yang, X., Fang, S., Li, W., Rui, W., Yang, A., Duan, Y., et al., 2025. Natural variation in a cortex/epidermis-specific transcription factor bZIP89 determines lateral root development and drought resilience in maize. Sci. Adv. 11, eadt1113.

Li, Q., Fu, C.F., Liang, C.L., Ni, X.J., Zhao, X.H., Chen, M., Ou, L.J., 2022. Crop lodging and the roles of lignin, cellulose, and hemicellulose in lodging resistance. Agronomy 12, 1795.

Li, Q.G., Nie, S.J., Li, G.K., Du, J.Y., Ren, R.C., Yang, X., Liu, B.Y., Gao, X.L., Liu, T.J., Zhang, Z.M., et al., 2022. Identification and fine mapping of the recessive gene BK-5, which affects cell wall biosynthesis and plant brittleness in maize. Int. J. Mol. Sci. 23, 814.

Lin, C.Y., Li, Q.Z., Tunlaya-Anukit, S., Shi, R., Sun, Y.H., Wang, J.P., Liu, J., Loziuk, P., Edmunds, C.W., Miller, Z.D., et al., 2016. A cell wall-bound anionic peroxidase, PtrPO21, is involved in lignin polymerization in Populus trichocarpa. Tree Genet Genomics 12, 1-18.

Lin, G., Li, P., Li, L., Wang, R., Zhao, W., Tian, M., Wu, J., Xu, S., Chen, Y., Feng, X., 2024. Discovery of ElABCG39: a key player in ingenol transmembrane efflux identified through genome-wide analysis of ABC transporters in Euphorbia lathyris L. Plant Cell Rep 43, 274.

Liu, H.J., Wang, X.Q., Xiao, Y.J., Luo, J.Y., Qiao, F., Yang, W.Y., Zhang, R.Y., Meng, Y.J., Sun, J.M., Yan, S.J., et al., 2020. CUBIC: an atlas of genetic architecture promises directed maize improvement. Genome Biol. 21, 20.

Liu, X., Hu, X., Li, K., Liu, Z., Wu, Y., Wang, H., Huang, C., 2020. Genetic mapping and genomic selection for maize stalk strength. BMC Plant Biol. 20, 196.

Marjamaa, K., Kukkola, E.M., Fagerstedt, K.V., 2009. The role of xylem class III peroxidases in lignification. J. Exp. Bot. 60, 367-376.

Mazaheri, M., Heckwolf, M., Vaillancourt, B., Gage, J.L., Burdo, B., Heckwolf, S., Barry, K., Lipzen, A., Ribeiro, C.B., Kono, T.J.Y., et al., 2019. Genome-wide association analysis of stalk biomass and anatomical traits in maize. BMC Plant Biol. 19, 1-17.

Peiffer, J.A., Flint-Garcia, S.A., De Leon, N., McMullen, M.D., Kaeppler, S.M., Buckler, E.S., 2013. The genetic architecture of maize stalk strength. PLoS One 8, e67066.

Savidge, R.A., Forster, H., 2001. Coniferyl alcohol metabolism in conifers -- II. Coniferyl alcohol and dihydroconiferyl alcohol biosynthesis. Phytochemistry 57, 1095-1103.

Shigeto, J., Itoh, Y., Hirao, S., Ohira, K., Fujita, K., Tsutsumi, Y., 2015. Simultaneously disrupting AtPrx2, AtPrx25 and AtPrx71 alters lignin content and structure in Arabidopsis stem. J Integr Plant Biol. 57, 349-356.

Sindhu, A., Langewisch, T., Olek, A., Multani, D.S., McCann, M.C., Vermerris, W., Carpita, N.C., Johal, G., 2007. Maize Brittle stalk2 encodes a COBRA-like protein expressed in early organ development but required for tissue flexibility at maturity. Plant Physiol. 145, 1444-1459.

Srivastava, A.K., Lu, Y., Zinta, G., Lang, Z., Zhu, J.K., 2018. UTR-dependent control of gene expression in plants. Trends Plant Sci. 23, 248-259.

Stubbs, C.J., Larson, R., Cook, D.D., 2022. Maize stalk stiffness and strength are primarily determined by morphological factors. Sci. Rep. 12, 720.

Tang, H.M., Liu, S., Hill-Skinner, S., Wu, W., Reed, D., Yeh, C.T., Nettleton, D., Schnable, P.S., 2014. The maize brown midrib2 (bm2) gene encodes a methylenetetrahydrofolate reductase that contributes to lignin accumulation. Plant J. 77, 380-392.

Tatusov, R.L., Fedorova, N.D., Jackson, J.D., Jacobs, A.R., Kiryutin, B., Koonin, E.V., Krylov, D.M., Mazumder, R., Mekhedov, S.L., Nikolskaya, A.N., et al., 2003. The COG database: an updated version includes eukaryotes. BMC Bioinformatics. 4, 41.

Vera Alvarez, R., Pongor, L.S., Marino-Ramirez, L., Landsman, D., 2019. TPMCalculator: one-step software to quantify mRNA abundance of genomic features. Bioinformatics 35, 1960-1962.

Vignols, F., Rigau, J., Torres, M.A., Capellades, M., Puigdomenech, P., 1995. The brown midrib3 (bm3) mutation in maize occurs in the gene encoding caffeic acid O-methyltransferase. Plant Cell 7, 407-416.

Wang, X.Q., Chen, Y.N., Sun, X., Li, J.H., Zhang, R.Y., Jiao, Y.Y., Wang, R.H., Song, W., Zhao, J.R., 2022. Characteristics and candidate genes associated with excellent stalk strength in maize (Zea mays L.). Front. Plant Sci. 13, 957566.

Wang, X.Q., Shi, Z., Zhang, R.Y., Sun, X., Wang, J.D., Wang, S., Zhang, Y., Zhao, Y.X., Su, A.G., Li, C.H., et al., 2020. Stalk architecture, cell wall composition, and QTL underlying high stalk flexibility for improved lodging resistance in maize. BMC Plant Biol. 20, 515.

Wang, X.Q., Zhang, R.Y., Shi, Z., Zhang, Y., Sun, X., Ji, Y., Zhao, Y.X., Wang, J.D., Zhang, Y.X., Xing, J.F., et al., 2019. Multi-omics analysis of the development and fracture resistance for maize internode. Sci Rep, 9(1), 8183.

Wang, Y., Wang, Q.Q., Zhao, Y., Han, G.M., Zhu, S.W., 2015. Systematic analysis of maize class III peroxidase gene family reveals a conserved subfamily involved in abiotic stress response. Gene 566, 95-108.

Xiao, S.L., Li, Z.Y., Zhang, H.X., Su, A.G., Li, C.H., Zhang, R.Y, Zhao, Y.X., Xing, J.F., Song, W., Zhao, J.R., 2023. An iTRAQ-based quantitative proteomic analysis reveals the role of mitochondrial complex I subunits in S-type cytoplasmic male sterility of maize. Agric Commun 1(2):100013.

Xiao, Y., Tong, H., Yang, X., et al., 2016. Genome-wide dissection of the maize ear genetic architecture using multiple populations. New Phytol 210(3):1095-1106.

Xie, L.Y., Wen, D.X., Wu, C.L., Zhang, C.Q., 2022. Transcriptome analysis reveals the mechanism of internode development affecting maize stalk strength. BMC Plant Biol. 22, 49.

Xiong, W.D., Wu, Z.Y., Liu, Y.C., Li, Y., Su, K.L., Bai, Z.T., Guo, S.Y., Hu, Z.B., Zhang, Z.M., Bao, Y., et al., 2019. Mutation of 4-coumarate: coenzyme A ligase 1 gene affects lignin biosynthesis and increases the cell wall digestibility in maize brown midrib5 mutants. Biotechnol Biofuels. 12, 82.

Xu, B.Q., Hao, Y., Li, S.T., Du, D.D., Xiao, D.D., Chen, M.M., Song, Y.G., Wei, G.L., Zong, W.B., Guo, X.T., et al., 2025. Fine regulation of heading date by editing the untranslated regions of heading-related genes in rice. Plant Biotechnol J. 10.1111/pbi.70114.

Xue, J., Xie, R.Z., Zhang, W.F., Wang, K.R., Hou, P., Ming, B., Guo, L., Li, S.K., 2017. Research progress on reduced lodging of high-yield and -density maize. J. Integr. Agric. 16, 2717-2725.

Yang, X.H., Gao, S.B., Xu, S.T., Zhang, Z.X., M. Prasanna, B., Li, L., Li, J.S., Yan, J.B., 2011. Characterization of a global germplasm collection and its potential utilization for analysis of complex quantitative traits in maize. Mol. Breed. 28, 511-526.

Yoo, S.D., Cho, Y.H., Sheen, J., 2007. Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat. Protoc. 2, 1565-1572.

Yoon, J., Choi, H., An, G., 2015. Roles of lignin biosynthesis and regulatory genes in plant development. J. Integr. Plant Biol. 57, 902-912.

Zhai, X.Z., Yan, X.C., Zenda, T.S., Wang, N., Dong, A.Y., Yang, Q., Zhong, Y., Xing, Y., Duan, H.J., 2024. Overexpression of the peroxidase gene ZmPRX1 increases maize seedling drought tolerance by promoting root development and lignification. Crop J. 12, 753-765.

Zhang, F., Niu, L., Li, Y., Zhou, X., Zhang, H., Wu, X., Liu, H., Wang, W., 2025. Maize peroxidase ZmPrx25 modulates apoplastic ROS homeostasis and promotes seed germination and growth under osmotic and drought stresses. Antioxidants. 14, 1067.

Zhang, Y.L., Liu, P., Zhang, X.X., Zheng, Q., Chen, M., Ge, F., Li, Z.L., Sun, W.T., Guan, Z.R., Liang, T.H., et al., 2018. Multi-locus genome-wide association study reveals the genetic architecture of stalk lodging resistance-related traits in maize. Front Plant Sci. 9, 611.

Zhao, B.H., Li, K., Wang, M., Liu, Z.Y., Yin, P.F., Wang, W.D., Li, Z.G., Li, X.W., Zhang, L.L., Han, Y.J., et al., 2024. Genetic basis of maize stalk strength decoded via linkage and association mapping. Plant J. 117, 1558-1573.

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