<i>LG1</i> promotes preligule band formation through directly activating <i>ZmPIN1</i> genes in maize

Zhuojun Zhong; Minhao Yao; Yingying Cao; Dexin Kong; Baobao Wang; Yanli Wang; Rongxin Shen; Haiyang Wang; Qing Liu

doi:10.1016/j.jgg.2025.01.014

Volume 52 Issue 3

Mar. 2025

Turn off MathJax

Article Contents

Article Navigation > Journal of Genetics and Genomics > 2025 > 52(3): 356-366

PDF( 0 KB)

LG1 promotes preligule band formation through directly activating ZmPIN1 genes in maize

doi: 10.1016/j.jgg.2025.01.014

a. State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangdong Laboratory for Lingnan Modern Agriculture, College of Life Sciences, South China Agricultural University, Guangzhou, Guangdong 510642, China;
b. Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing 100081, China;
c. Hebei Key Laboratory of Horticultural Germplasm Excavation and Innovative Utilization, College of Horticultural Science&Technology, HeBei Normal University of Science & Technology, Qinhuangdao, Hebei 066004, China

Funds:

We greatly thank Prof. Fang Yang (Sun Yat-Sen University) for sharing the pDR5 rev::RFP marker line seeds. We thank Prof. Yueqin heng and Jinshun Zhong (South China Agricultural University) for proof reading and comments on the manuscript. This work was supported by the National Key Research and Development Program of China (2021YFF1000301), the National Natural Science Foundation of China (32472179, 32130077, 32201835), the Natural Science Foundation of Hebei Province (C2022407068), the Natural Science Foundation of Guangdong Province (2024A1515030237, 2022A1515011002), and the Hainan Yazhou Bay Seed Lab (B21HJ8101).

Received Date: 2024-12-10
Accepted Date: 2025-01-22
Rev Recd Date: 2025-01-14

Available Online: 2025-07-11

Publish Date: 2025-01-27

Abstract

Abstract

Increasing plant density is an effective strategy for enhancing crop yield per unit land area. A key architectural trait for crops adapting to high planting density is a smaller leaf angle (LA). Previous studies have demonstrated that LG1, a SQUAMOSA BINDING PROTEIN (SBP) transcription factor, plays a critical role in LA establishment. However, the molecular mechanisms underlying the regulation of LG1 on LA formation remain largely unclear. In this study, we conduct comparative RNA-seq analysis of the preligule band (PLB) region of wild type and lg1 mutant leaves. Gene Ontology (GO) term enrichment analysis reveals enrichment of phytohormone pathways and transcription factors, including three auxin transporter genes ZmPIN1a, ZmPIN1b, and ZmPIN1c. Further molecular experiments demonstrate that LG1 can directly bind to the promoter region of these auxin transporter genes and activate their transcription. We also show that double and triple mutants of these ZmPINs genes exhibit varying degrees of auricle size reduction and thus decreased LA. On the contrary, overexpression of ZmPIN1a causes larger auricle and LA. Taken together, our findings establish a functional link between LG1 and auxin transport in regulating PLB formation and provide valuable targets for genetic improvement of LA for breeding high-density tolerant maize cultivars.
- Maize (Zea mays L.),
- LG1,
- Leaf angle (LA),
- Preligule band,
- Auxin transport

FullText(HTML)

References(55)

References

Assefa, Y., Carter, P., Hinds, M., Bhalla, G., Schon, R., Jeschke, M., Paszkiewicz, S., Smith, S., Ciampitti, I.A., 2018. Analysis of long term study indicates both agronomic optimal plant density and increase maize yield per plant contributed to yield gain. Sci. Rep. 8, 4937.

Becraft, P.W., Freeling, M., 1991. Sectors of liguleless-1 tissue interrupt an inductive signal during maize leaf development. Plant Cell 3, 801-807.

Becraft, P.W., Bongard-Pierce, D.K., Sylvester, A.W., Poethig, R.S., Freeling, M., 1990. The liguleless-1 gene acts tissue specifically in maize leaf development. Dev. Biol. 141, 220-232.

Best, N.B., Hartwig, T., Budka, J., Fujioka, S., Johal, G., Schulz, B., Dilkes, B.P., 2016. nana plant2 encodes a maize ortholog of the Arabidopsis brassinosteroid biosynthesis gene DWARF1, identifying developmental interactions between brassinosteroids and gibberellins. Plant Physiol. 171, 2633-2647.

Bortiri, E., Chuck, G., Vollbrecht, E., Rocheford, T., Martienssen, R., Hake, S., 2006. ramosa2 encodes a LATERAL ORGAN BOUNDARY domain protein that determines the fate of stem cells in branch meristems of maize. Plant Cell 18, 574-585.

Cao, Y., Zhong, Z., Wang, H., Shen, R., 2022. Leaf angle: a target of genetic improvement in cereal crops tailored for high-density planting. Plant Biotechnol. J. 20, 426-436.

Dong, L., Shi, Y., Li, P., Zhong, S., Sun, Y., Yang, F., 2023. Constructing the maize inflorescence regulatory network by using efficient tsCUT&Tag assay. Crop J. 11, 951-956.

Duncan, W.G., 1971. Leaf Angles, Leaf Area, and Canopy Photosynthesis. Crop Sci. 11, 482-485.

Duvick, D. N., 2005. Genetic progress in yield of United States maize (Zea mays L.). Maydica (Italy).

Duvick, Donald N., 2005. The contribution of breeding to yield advances in maize (Zea mays L.), in: Advances in Agronomy. Elsevier, pp. 83-145.

Duvick, D.N., Smith, J.S.C., Cooper, M., 2003. Long-Term selection in a commercial hybrid maize breeding program, in: Plant Breeding Reviews. pp. 109-151.

Emerson, R.A., 1912. The inheritance of the ligule and auricles of corn leaves. Nebr. Agric. Exp. Stn. Annu. Rep. 25, 81-88.

Gallavotti, A., Yang, Y., Schmidt, R.J., Jackson, D., 2008. The relationship between auxin transport and maize branching. Plant Physiol. 147, 1913-1923.

Galli, M., Khakhar, A., Lu, Z., Chen, Z., Sen, S., Joshi, T., Nemhauser, J.L., Schmitz, R.J., Gallavotti, A., 2018. The DNA binding landscape of the maize AUXIN RESPONSE FACTOR family. Nat. Commun. 9, 4526.

Huang, G., Hu, H., van de Meene, A., Zhang, J., Dong, L., Zheng, S., Zhang, F., Betts, N.S., Liang, W., Bennett, M.J., et al., 2021. AUXIN RESPONSE FACTORS 6 and 17 control the flag leaf angle in rice by regulating secondary cell wall biosynthesis of lamina joints. Plant Cell 33, 3120-3133.

Jackson, D., 1992. In situ hybridization in plants, in: Gurr, S.J., Mcpherson, M.J., Bowles, D.J. (Eds.), Molecular Plant Pathology. Oxford University Press, pp. 163-174.

Jafari, F., Wang, B., Wang, H., Zou, J., 2024. Breeding maize of ideal plant architecture for high-density planting tolerance through modulating shade avoidance response and beyond. J. Integr. Plant Biol. 66, 849-864.

Johnston, R., Wang, M., Sun, Q., Sylvester, A.W., Hake, S., Scanlon, M.J., 2015. Transcriptomic analyses indicate that maize ligule development recapitulates gene expression patterns that occur during lateral organ initiation. Plant Cell 26, 4718-4732.

Kong, D., Pan, X., Jing, Y., Zhao, Y., Duan, Y., Yang, J., Wang, B., Liu, Y., Shen, R., Cao, Y., et al., 2021. ZmSPL10/14/26 are required for epidermal hair cell fate specification on maize leaf. New Phytol. 230, 1533–1549.

Langmead, B., Salzberg, S.L., 2012. Fast gapped-read alignment with bowtie 2. Nat. Methods 9, 357-359.

Lewis, M.W., Bolduc, N., Hake, K., Htike, Y., Hay, A., Candela, H., Hake, S., 2014. Gene regulatory interactions at lateral organ boundaries in maize. Development 141, 4590-4597.

Li, X., Wu, P., Lu, Y., Guo, S., Zhong, Z., Shen, R., Xie, Q., 2020. Synergistic interaction of phytohormones in determining leaf angle in crops. Int. J. Mol. Sci. 21, 5052.

Lin, R., Ding, L., Casola, C., Ripoll, D.R., Feschotte, C., Wang, H., 2007. Transposase-derived transcription factors regulate light signaling in arabidopsis. Science 318, 1302-1305.

Liu, K., Cao, J., Yu, K., Liu, X., Gao, Y., Chen, Q., Zhang, W., Peng, H., Du, J., Xin, M., et al., 2019. Wheat TaSPL8 modulates leaf angle through auxin and brassinosteroid signaling. Plant Physiol. 181, 179-194.

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.

Luo, X., Zheng, J., Huang, R., Huang, Y., Wang, H., Jiang, L., Fang, X., 2016. Phytohormones signaling and crosstalk regulating leaf angle in rice. Plant Cell Rep. 35, 2423-2433.

Mi, G., Chen, F., Wu, Q., Lai, N., Yuan, L., Zhang, F., 2010. Ideotype root architecture for efficient nitrogen acquisition by maize in intensive cropping systems. Sci. China Life Sci. 53, 1369-1373.

Moon, J., Candela, H., Hake, S., 2013. The Liguleless narrow mutation affects proximal-distal signaling and leaf growth. Development 140, 405-412.

Moreno, M.A., Harper, L.C., Krueger, R.W., Dellaporta, S.L., Freeling, M., 1997. liguleless1 encodes a nuclear-localized protein required for induction of ligules and auricles during maize leaf organogenesis. Genes Dev. 11, 616-628.

O’Malley, R.C., Huang, S.C., Song, L., Lewsey, M.G., Bartlett, A., Nery, J.R., Galli, M., Gallavotti, A., Ecker, J.R., 2016. Cistrome and Epicistrome Features Shape the Regulatory DNA Landscape. Cell 165, 1280-1292.

Ray, D.K., Mueller, N.D., West, P.C., Foley, J.A., 2013. Yield trends are insufficient to double global crop production by 2050. PLoS One 8, e66428.

Sharman, B.C., 1942. Developmental Anatomy of the Shoot of Zea mays L. Ann. Bot. 6, 245-282.

Shi, Q., Xia, Y., Wang, Q., Lv, K., Yang, H., Cui, L., Sun, Y., Wang, X., Tao, Q., Song, X., et al., 2024. Phytochrome B interacts with LIGULELESS1 to control plant architecture and density tolerance in maize. Mol. Plant 17, 1255-1271.

Strable, J., Wallace, J.G., Unger-Wallace, E., Briggs, S., Bradbury, P.J., Buckler, E.S., Vollbrecht, E., 2017. Maize YABBY genes drooping leaf1 and drooping leaf2 regulate plant architecture. Plant Cell 29, 1622-1641.

Sylvester, A.W., Cande, W.Z., Freeling, M., 1990. Division and differentiation during normal and liguleless-1 maize leaf development. Development 110, 985-1000.

Tamura, K., Stecher, G., Kumar, S., 2021. MEGA11: molecular evolutionary genetics analysis version 11. Mol. Biol. Evol. 38, 3022–3027.

Tian, F., Bradbury, P.J., Brown, P.J., Hung, H., Sun, Q., Flint-Garcia, S., Rocheford, T.R., McMullen, M.D., Holland, J.B., Buckler, E.S., 2011. Genome-wide association study of leaf architecture in the maize nested association mapping population. Nat. Genet. 43, 159-162.

Tian, J., Wang, C., Xia, J., Wu, L., Xu, G., Wu, W., Li, D., Qin, W., Han, X., Chen, Q., et al., 2019. Teosinte ligule allele narrows plant architecture and enhances high-density maize yields. Science 365, 658-664.

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.

Tsiantis, M., Brown, M.I.N., Skibinski, G., Langdale, J.A., 1999. Disruption of auxin transport is associated with aberrant leaf development in maize. Plant Physiol 121, 1163-1168.

Tu, X., Mejía-Guerra, M.K., Valdes Franco, J.A., Tzeng, D., Chu, P.Y., Shen, W., Wei, Y., Dai, X., Li, P., et al., 2020. Reconstructing the maize leaf regulatory network using ChIP-seq data of 104 transcription factors. Nat. Commun. 11, 5089.

United Nations 2024. World Population Prospects 2024: Summary of Results. United Nations Department of Economic and Social Affairs, Population Division.

van Dijk, M., Morley, T., Rau, M.L., Saghai, Y., 2021. A meta-analysis of projected global food demand and population at risk of hunger for the period 2010-2050. Nat. Food 2, 494-501.

Walsh, J., Waters, C.A., Freeling, M., 1998. The maize gene liguleless2 encodes a basic leucine zipper protein involved in the establishment of the leaf blade-sheath boundary. Genes Dev. 12, 208-218.

Wang, B., Lin, Z., Li, X., Zhao, Y., Zhao, B., Wu, G., Ma, X., Wang, H., Xie, Y., Li, Q., et al., 2020. Genome-wide selection and genetic improvement during modern maize breeding. Nat. Genet. 52, 565-571.

Wang, R., Liu, C., Chen, Z., Sun, S., Wang, X., 2021. Oryza sativa LIGULELESS 2s determine lamina joint positioning and differentiation by inhibiting auxin signaling. New Phytol. 229, 1832-1839.

Wu, G., Zhao, Y., Shen, R., Wang, B., Xie, Y., Ma, X., Zheng, Z., Wang, H., 2019. Characterization of maize phytochrome-interacting factors in light signaling and photomorphogenesis. Plant Physiol. 181, 789–803.

Xu, J., Wang, J., Xue, H., Zhang, G., 2021. Leaf direction: Lamina joint development and environmental responses. Plant Cell Environ. 44, 2441-2454.

Yamamuro, C., Ihara, Y., Wu, X., Noguchi, T., Fujioka, S., Takatsuto, S., Ashikari, M., Kitano, H., Matsuoka, M., 2000. Loss of function of a rice brassinosteroid insensitive1 homolog prevents internode elongation and bending of the lamina joint. Plant Cell 12, 1591-1605.

Yuan, H., Xu, Z., Chen, W., Deng, C., Liu, Y., Yuan, M., Gao, P., Shi, H., Tu, B., Li, T., et al., 2022. OsBSK2, a putative brassinosteroid-signalling kinase, positively controls grain size in rice. J. Exp. Bot. 73, 5529-5542.

Zhao, S.Q., Xiang, J.J., Xue, H.W., 2013. Studies on the rice LEAF INCLINATION1 (LC1), an IAA-amido synthetase, reveal the effects of auxin in leaf inclination control. Mol. Plant 6, 174-187.

Zhang, Y., Liu, T., Meyer, C.A., Eeckhoute, J., Johnson, D.S., Bernstein, B.E., Nusbaum, C., Myers, R.M., Brown, M., Li, W., et al., 2008. Model-based analysis of ChIP-seq (MACS). Genome Biol. 9, R137.

Zhao, M., Tang, S., Zhang, H., He, M., Liu, J., Zhi, H., Sui, Y., Liu, X., Jia, G., Zhao, Z., et al., 2020. DROOPY LEAF1 controls leaf architecture by orchestrating early brassinosteroid signaling. Proc. Natl. Acad. Sci. U.S.A. 117, 21766-21774.

Zhao, Y., Zhang, C., Liu, W., Gao, W., Liu, C., Song, G., Li, W.X., Mao, L., Chen, B., Xu, Y., et al., 2016. An alternative strategy for targeted gene replacement in plants using a dual-sgRNA/Cas9 design. Sci. Rep. 6, 23890.

Zhong, J., van Esse, G.W., Bi, X., Lan, T., Walla, A., Sang, Q., Franzen, R., von Korff, M., 2021. INTERMEDIUM-M encodes an HvAP2L-H5 ortholog and is required for inflorescence indeterminacy and spikelet determinacy in barley. Proc. Natl. Acad. Sci. U.S.A. 118, e2011779118.

Relative Articles

Supplements(0)

Cited By

Proportional views