The quantitative trait locus <i>stiff2</i> controls stalk bending strength and root architecture in maize

Shuyang Zhong; Le Xu; Zhihai Zhang; Yan Li; Zhongwei Lin

doi:10.1016/j.jgg.2025.11.014

The quantitative trait locus stiff2 controls stalk bending strength and root architecture in maize

doi: 10.1016/j.jgg.2025.11.014

a. State Key Laboratory of Maize Bio-Breeding; National Maize Improvement Center, Department of Crop Genetics and Breeding, China Agricultural University, Beijing 100193, China;
b. Beijing DaBeiNong Biotechnology Co., Ltd., Beijing, 100194, China;
c. Sanya Institute of China Agricultural University, Sanya, Hainan 572025, China

基金项目:

We thank Mingliang Xu from China Agricultural University for generously providing the ZmCCT transgenic events. This work was supported by the National Key Research and Development Program of China (2023YFD1200501 to Z.L.).

详细信息

通讯作者:
Zhongwei Lin,E-mail:zlin@cau.edu.cn

计量
- 文章访问数: 172
- HTML全文浏览量: 79
- PDF下载量: 0
- 被引次数: 0
出版历程
- 收稿日期: 2025-07-29
- 录用日期: 2025-11-24
- 修回日期: 2025-11-24
- 网络出版日期: 2025-12-05

The quantitative trait locus stiff2 controls stalk bending strength and root architecture in maize

Shuyang Zhong^a,b,
Le Xu^a,c,
Zhihai Zhang^a,
Yan Li^a,
Zhongwei Lin^{a,c
, ,}

a. State Key Laboratory of Maize Bio-Breeding; National Maize Improvement Center, Department of Crop Genetics and Breeding, China Agricultural University, Beijing 100193, China;
b. Beijing DaBeiNong Biotechnology Co., Ltd., Beijing, 100194, China;
c. Sanya Institute of China Agricultural University, Sanya, Hainan 572025, China

Funds:

摘要

摘要: Stalk lodging is a major threat to global maize production, which causes great annual yield losses. Stalk bending strength (SBS) is highly associated with resistance to stalk lodging in maize. However, the genetic basis of SBS remains largely unknown. In this study, we identify a quantitative trait locus (QTL), stiff2, corresponding to a known flowering-time gene ZmCCT, by integrating QTL mapping and association mapping. A 5-kilobase (kb) transposable element inserted in the promoter region of ZmCCT significantly reduces SBS, while upregulated expression of ZmCCT through transformation significantly enhances SBS. Gene regulatory network analysis reveals that ZmCCT may indirectly regulate a set of downstream genes, which contain nrt5 for nitrogen transport, Tu1, d8, and d9 for stalk elongation, ub2, ub3, and ch1 for stalk thickening, and myb69 and bm4 for lignin biosynthesis. These genes collectively increase stalk strength and improve lodging resistance aboveground. Additionally, stiff2 regulates not only aboveground resistance to stalk bending and breakage but also influences root system architecture, which enhances resistance to root lodging belowground. The identification of stiff2 and its downstream targets provides critical insights into the genetic control of maize lodging and offers powerful tools for breeding lodging-resistant cultivars.
- Stalk lodging /
- Maize /
- QTL /
- stiff2 /
- Gene regulatory network
Abstract: Stalk lodging is a major threat to global maize production, which causes great annual yield losses. Stalk bending strength (SBS) is highly associated with resistance to stalk lodging in maize. However, the genetic basis of SBS remains largely unknown. In this study, we identify a quantitative trait locus (QTL), stiff2, corresponding to a known flowering-time gene ZmCCT, by integrating QTL mapping and association mapping. A 5-kilobase (kb) transposable element inserted in the promoter region of ZmCCT significantly reduces SBS, while upregulated expression of ZmCCT through transformation significantly enhances SBS. Gene regulatory network analysis reveals that ZmCCT may indirectly regulate a set of downstream genes, which contain nrt5 for nitrogen transport, Tu1, d8, and d9 for stalk elongation, ub2, ub3, and ch1 for stalk thickening, and myb69 and bm4 for lignin biosynthesis. These genes collectively increase stalk strength and improve lodging resistance aboveground. Additionally, stiff2 regulates not only aboveground resistance to stalk bending and breakage but also influences root system architecture, which enhances resistance to root lodging belowground. The identification of stiff2 and its downstream targets provides critical insights into the genetic control of maize lodging and offers powerful tools for breeding lodging-resistant cultivars.
- Stalk lodging /
- Maize /
- QTL /
- stiff2 /
- Gene regulatory network

HTML全文

参考文献(34)

Buckler, E.S., Holland, J.B., Bradbury, P.J., Acharya, C.B., Brown, P.J., Browne, C., Ersoz, E., Flint-Garcia, S., Garcia, A., Glaubitz, J.C., et al., 2009. The genetic architecture of maize flowering time. Science 325, 714-718.

Chuck, G.S., Brown, P.J., Meeley, R., Hake, S., 2014. Maize SBP-box transcription factors unbranched2 and unbranched3 affect yield traits by regulating the rate of lateral primordia initiation. Proc. Natl. Acad. Sci. U. S. A. 111, 18775-18780.

Flint-Garcia, S.A., Jampatong, C., Darrah, L.L., McMullen, M.D., 2003. Quantitative trait locus analysis of stalk strength in four maize populations. Crop Sci. 43, 13-22.

Flint-Garcia, S.A., Thuillet, A.C., Yu, J.M., Pressoir, G., Romero, S.M., Mitchell, S.E., Doebley, J., Kresovich, S., Goodman, M.M., Buckler, E.S., 2005. Maize association population: a high-resolution platform for quantitative trait locus dissection. Plant J. 44, 1054-1064.

Fujioka, S., Yamane, H., Spray, C.R., Katsumi, M., Phinney, B.O., Gaskin, P., Macmillan, J., Takahashi, N., 1988. The dominant non-gibberellin-responding dwarf mutant (D8) of maize accumulates native gibberellins. Proc. Natl. Acad. Sci. U. S. A. 85, 9031-9035.

Hu, H., Liu, W., Fu, Z., Homann, L., Technow, F., Wang, H., Song, C., Li, S., Melchinger, A.E., Chen, S., 2013. QTL mapping of stalk bending strength in a recombinant inbred line maize population. Theor. Appl. Genet. 126, 2257-2266.

Hung, H., Shannon, L.M., Tian, F., Bradbury, P.J., Chen, C., Flint-Garcia, S.A., McMullen, M.D., Ware, D., Buckler, E.S., Doebley, J.F., et al., 2012. ZmCCT and the genetic basis of day-length adaptation underlying the postdomestication spread of maize. Proc. Natl. Acad. Sci. U. S. A. 109, E1913-E1921.

Jiao, Y., Wang, Y., Xue, D., Wang, J., Yan, M., Liu, G., Dong, G., Zeng, D., Lu, Z., Zhu, X., et al., 2010. Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat. Genet. 42, 536-541.

Klimyuk, V.I., Persello-Cartieaux, F., Havaux, M., Contard-David, P., Schuenemann, D., Meiherhoff, K., Gouet, P., Jones, J., Hoffman, N.E., Nussaume, L., 1999. A chromodomain protein encoded by the Arabidopsis CAO gene is a plant-specific component of the chloroplast signal recognition particle pathway that is involved in LHCP targeting. Plant Cell 11, 87-99.

Lawit, S.J., Wych, H.M., Xu, D., Kundu, S., Tomes, D.T., 2010. Maize DELLA proteins dwarf plant8 and dwarf plant9 as modulators of plant development. Plant Cell Physiol. 51, 1854-1868.

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

Li, Y., 2017. The function of different alleles and mechanism underlying transcription regulatory of ZmCCT, in Ph. D. thesis: China Agricultural University.

Li, Y., Wang, J., Zhong, S., Huo, Q., Wang, Q., Shi, Y., Liu, H., Liu, J., Song, Y., Fang, X., et al., 2024. MADS-box encoding gene Tunicate1 positively controls maize yield by increasing leaf number above the ear. Nat. Commun. 15, 9799.

Lipka, A.E., Tian, F., Wang, Q., Peiffer, J., Li, M., Bradbury, P.J., Gore, M.A., Buckler, E.S., Zhang, Z., 2012. GAPIT: genome association and prediction integrated tool. Bioinformatics 28, 2397-2399.

Livak, K.J., Schmittgen, T.D., 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta c(t)) method. Methods 25, 402-408.

Lou, G., Chen, P., Li, P., Gao, H., Xiong, J., Wan, S., Zheng, Y., Wang, Y., Alam, M., Chen, Y., et al., 2025. Antagonistic Ghd7-OsNAC42 complexes modulate carbon and nitrogen metabolism to achieves superior quality and high yield in rice. Adv. Sci. 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, 14.

Qiang, Z., Sun, H., Ge, F., Li, W., Li, C., Wang, S., Zhang, B., Zhu, L., Zhang, S., Wang, X., et al., 2022. The transcription factor ZmMYB69 represses lignin biosynthesis by activating ZmMYB31/42 expression in maize. Plant Physiol. 189, 1916-1919.

Robertson, D.J., Julias, M., Lee, S.Y., Cook, D.D., 2017. Maize stalk lodging: morphological determinants of stalk strength. Crop Sci. 57, 926-934.

Sekhon, R.S., Joyner, C.N., Ackerman, A.J., McMahan, C.S., Cook, D.D., Robertson, D.J., 2020. Stalk bending strength is strongly associated with maize stalk lodging incidence across multiple environments. Field Crops Res. 249, 10.

Silva, L.D.C.E., Wang, S., Zeng, Z., 2012. Composite interval mapping and multiple interval mapping: procedures and guidelines for using windows QTL cartographer. Methods Mol. Biol. 871, 75-119.

Sluiter, A., Hames, B., Ruiz, R., Scarlata, C., Sluiter, J., Templeton, D., Crocker, D., 2011. Determination of structural carbohydrates and lignin in biomass: laboratory analytical procedure. (Golden, CO: National Renewable Energy Laboratory).

Wang, C., Yang, Q., Wang, W., Li, Y., Guo, Y., Zhang, D., Ma, X., Song, W., Zhao, J., Xu, M., 2017. A transposon-directed epigenetic change in ZmCCT underlies quantitative resistance to gibberella stalk rot in maize. New Phytol. 215, 1503-1515.

Wang, Q., Su, Q., Nian, J., Zhang, J., Guo, M., Dong, G., Hu, J., Wang, R., Wei, C., Li, G., et al., 2021. The Ghd7 transcription factor represses ARE1 expression to enhance nitrogen utilization and grain yield in rice. Mol. Plant 14, 1012-1023.

Wang, Q., Wang, M., Xia, A., Wang, J., Wang, Z., Xu, T., Jia, D., Lu, M., Tan, W., Luo, J., et al., 2025. Natural variation in ZmNRT2.5 modulates husk leaf width and promotes seed protein content in maize. Plant Biotechnol. J. 23, 1039-1052.

Wang, X., Shi, Z., Zhang, R., Sun, X., Wang, J., Wang, S., Zhang, Y., Zhao, Y., Su, A., Li, C., et al., 2020. Stalk architecture, cell wall composition, and QTL underlying high stalk flexibility for improved lodging resistance in maize. BMC Plant Biol. 20, 12.

Yang, Q., Li, Z., Li, W., Ku, L., Wang, C., Ye, J., Li, K., Yang, N., Li, Y., Zhong, T., et al., 2013. CACTA-like transposable element in ZmCCT attenuated photoperiod sensitivity and accelerated the postdomestication spread of maize. Proc. Natl. Acad. Sci. U. S. A. 110, 16969-16974.

Zhai, J., Zhang, Y., Zhang, G., Tian, M., Xie, R., Ming, B., Hou, P., Wang, K., Xue, J., Li, S., 2022. Effects of nitrogen fertilizer management on stalk lodging resistance traits in summer maize. Agriculture-Basel 12, 16.

Zhang, P., Gu, S., Wang, Y., Yang, R., Yan, Y., Zhang, S., Sheng, D., Cui, T., Huang, S., Wang, P., 2021. Morphological and mechanical variables associated with lodging in maize. Field Crops Res. 269, 14.

Zhang, Y., Zhou, Z., Xiao, S., Li, Y., Hao, S., Que, F., Liu, Z., Shi, L., Shi, Y., Zhang, Z., et al., 2025. The nuclear transcription factor ZmCCT positively regulates salt and low nitrogen stress response in maize. Plant Stress 16, 100893.

Zhang, Z., Zhang, X., Lin, Z., Wang, J., Liu, H., Zhou, L., Zhong, S., Li, Y., Zhu, C., Lai, J., et al., 2020. A large transposon insertion in the stiff1 promoter increases stalk strength in maize. Plant Cell 32, 152-165.

Zhang, Z., Zhang, X., Lin, Z., Wang, J., Xu, M., Lai, J., Yu, J., Lin, Z., 2018. The genetic architecture of nodal root number in maize. Plant J. 93, 1032-1044.

Zheng, Z., Wang, B., Zhuo, C., Xie, Y., Zhang, X., Liu, Y., Zhang, G., Ding, H., Zhao, B., Tian, M., Xu, M., Kong, D., Shen, R., Liu, Q., Wu, G., Huang, J., Wang, H., 2023. Local auxin biosynthesis regulates brace root angle and lodging resistance in maize. New Phytol. 238, 142-154.

Zhong, S., Liu, H., Li, Y., Lin, Z., 2021. Opposite response of maize ZmCCT to photoperiod due to transposon jumping. Theor. Appl. Genet. 134, 2841-2855.

施引文献

资源附件(0)

访问统计

点击查看大图

计量

文章访问数: 172
HTML全文浏览量: 79
PDF下载量: 0
被引次数: 0

姓名
邮箱
手机号码
标题
留言内容
验证码

留言板

The quantitative trait locus stiff2 controls stalk bending strength and root architecture in maize

doi: 10.1016/j.jgg.2025.11.014

通讯作者:
Zhongwei Lin,E-mail:zlin@cau.edu.cn

计量

The quantitative trait locus stiff2 controls stalk bending strength and root architecture in maize

计量

目录

留言板

The quantitative trait locus stiff2 controls stalk bending strength and root architecture in maize

doi: 10.1016/j.jgg.2025.11.014

通讯作者: Zhongwei Lin,E-mail:zlin@cau.edu.cn

计量

出版历程

The quantitative trait locus stiff2 controls stalk bending strength and root architecture in maize

计量

出版历程

目录

通讯作者:
Zhongwei Lin,E-mail:zlin@cau.edu.cn