The OsCLV2s-OsCRN1 co-receptor regulates grain shape in rice

Xingxing Li; Meng-en Wu; Juncheng Zhang; Jingyue Xu; Yuanfei Diao; Yibo Li

doi:10.1016/j.jgg.2024.03.011

Volume 51 Issue 7

Jul. 2024

Turn off MathJax

Article Contents

Article Navigation > Journal of Genetics and Genomics > 2024 > 51(7): 691-702

PDF( 4978 KB)

The OsCLV2s-OsCRN1 co-receptor regulates grain shape in rice

doi: 10.1016/j.jgg.2024.03.011

a. National Key Laboratory of Crop Genetic Improvement and National Centre of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan, Hubei 430070, China;
b. Hubei Hongshan Laboratory, Wuhan, Hubei 430070, China

Funds:

This study is supported by grants from STI 2030-Major Projects (2023ZD0406902), the National Key Research and Development Program of China (2022YFD1200103, 2023ZD04073), the National Natural Science Foundation of China (U22A20470, 32072042, 31821005), Hubei Hongshan Laboratory (2022hszd025, 2021hszd005), the Key Research and Development Program of Hubei (2023BBB135, 2022BBA0033), and the Fundamental Research Funds for the Central Universities (2662023PY002).

Received Date: 2024-01-05
Accepted Date: 2024-03-29
Rev Recd Date: 2024-03-29

Available Online: 2025-06-06

Publish Date: 2024-04-03

Abstract

Abstract

The highly conserved CLV-WUS negative feedback pathway plays a decisive role in regulating stem cell maintenance in shoot and floral meristems in higher plants, including Arabidopsis, rice, maize, and tomato. Here, we find significant natural variations in the OsCLV2c, OsCLV2d, and OsCRN1 loci in a genome-wide association study of grain shape in rice. OsCLV2a, OsCLV2c, OsCLV2d, and OsCRN1 negatively regulate grain length-width ratio and show distinctive geographical distribution, indica-japonica differentiation, and artificial selection signatures. Notably, OsCLV2a and OsCRN1 interact biochemically and genetically, suggesting that the two components function in a complex to regulate grain shape of rice. Furthermore, the genetic contributions of the haplotypes combining OsCLV2a, OsCLV2c, and OsCRN1 are significantly higher than those of each single gene alone in controlling key yield traits. These findings identify two groups of receptor-like kinases that may function as distinct co-receptors to control grain size in rice, thereby revealing a previously unrecognized role of the CLV class genes in regulating seed development and proposing a framework to understand the molecular mechanisms of the CLV-WUS pathway in rice and other crops.
- Rice,
- Grain shape,
- OsCLV2s,
- OsCRN1,
- Natural variations,
- Indica-japonica differentiation

FullText(HTML)

References(47)

References

Bleckmann, A., Weidtkamp-Peters, S., Seidel, C., Simon, R., 2010. Stem cell signaling in Arabidopsis requires CRN to localize CLV2 to the plasma membrane. Plant Physiol., 152, 166-176.

Bommert, P., Lunde, C., Nardmann, J., Vollbrecht, E., Running, M., Jackson, D., Hake, S., Werr, W., 2005. Thick tassel dwarf1 encodes a putative maize ortholog of the Arabidopsis CLAVATA1 leucine-rich repeat receptor-like kinase. Development 132, 1235-1245.

Bommert, P., Nagasawa, N., Jackson, D., 2013. Quantitative variation in maize kernel row number is controlled by the FASCIATED EAR2 locus. Nat. Genet. 45, 334-337.

Chen, H., Zou, Y., Shang, Y., Lin, H., Wang, Y., Cai, R., Tang, X., Zhou, J., 2008. Firefly luciferase complementation imaging assay for protein-protein interactions in plants. Plant Physiol. 146, 368-376.

Fan, Y., Li, Y., 2019. Molecular, cellular and Yin-Yang regulation of grain size and number in rice. Mol. Breed. 39, 163-188.

Fleming, A., 2015. Sweet size control in tomato. Nat. Genet. 47, 698-699.

Fletcher J., 2018. The CLV-WUS stem cell signaling pathway: a roadmap to crop yield optimization. Plants 7, 87.

Gao, Y., Zhao, Y., 2014. Self-processing of ribozyme-flanked RNAs into guide RNAs in vitro and in vivo for CRISPR-mediated genome editing. J. Integr. Plant Biol. 56, 343-349.

Gupta, P., Kulwal, P., Jaiswal, V., 2019. Association mapping in plants in the post-GWAS genomics era. Adv. Genet. 104, 75-154.

Hanks, S., Quinn, A., Hunter, T., 1988. The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241, 42-52.

Harberd, N., 2015. Shaping taste: the molecular discovery of rice genes improving grain size, shape and quality. J. Genet. Genom. 42, 597-599.

Hong, L., Fletcher, J., 2023. Stem cells: engines of plant growth and development. Int. J. Mol. Sci. 24, 14889.

Hu, C., Zhu, Y., Cui, Y., Cheng, K., Liang, W., Wei, Z., Zhu, M., Yin, H., Zeng, L., Xiao, Y., et al., 2018. A group of receptor kinases are essential for CLAVATA signalling to maintain stem cell homeostasis. Nat. Plants 4, 205-211.

Je, B., et al., 2016. Signaling from maize organ primordia via FASCIATED EAR3 regulates stem cell proliferation and yield traits. Nat. Genet. 48, 785-791.

Je, B., Xu, F., Wu, Q., Liu, L., Meeley, R., Gallagher, J., Corcilius, L., Payne, R., Bartlett, M., Jackson, D., 2018. The CLAVATA receptor FASCIATED EAR2 responds to distinct CLE peptides by signaling through two downstream effectors. Elife 7, e35673.

Jones, D., John, A., VanDerMolen, K., Nimchuk, Z., 2021. CLAVATA signaling ensures reproductive development in plants across thermal environments. Curr. Biol. 31, 220-227.

Kitagawa, M., Jackson, D., 2019. Control of meristem size. Annu. Rev. Plant Biol. 70, 269-291.

Li, N., Xu, R., Li, Y., 2019. Molecular networks of seed size control in plants. Annu. Rev. Plant Biol. 70, 435-463.

Li, T., Yang, X., Yu, Y., Si, X., Zhai, X., Zhang, H., Dong, W., Gao, C., Xu, C., 2018. Domestication of wild tomato is accelerated by genome editing. Nat. Biotechnol. 36, 1160-1163.

Lippert, C., Listgarten, J., Liu, Y., Kadie, C., Davidson, R., Heckerman, D., 2011. FaST linear mixed models for genome-wide association studies. Nat. Methods 8, 833e835.

Liu, Q., et al., 2022. Insights into the genomic regions and candidate genes of senescence-related traits in upland cotton via GWAS. Int. J. Mol. Sci. 23, 8584.

Liu, Y., et al., 2021b. Genomic basis of geographical adaptation to soil nitrogen in rice. Nature 590, 600-605.

Liu, L., Gallagher, J., Arevalo, E., Chen, R., Skopelitis, T., Wu, Q., Bartlett, M., Jackson, D., 2021a. Enhancing grain-yield-related traits by CRISPR-Cas9 promoter editing of maize CLE genes. Nat. Plants 7, 287-294.

Meng, L., Feldman, L., 2010. CLE14/CLE20 peptides may interact with CLAVATA2/CORYNE receptor-like kinases to irreversibly inhibit cell division in the root meristem of Arabidopsis. Planta 232, 1061-1074.

Muller, R., Bleckmann, A., Simon, R., 2008. The receptor kinase CORYNE of Arabidopsis transmits the stem cell-limiting signal CLAVATA3 independently of CLAVATA1. Plant Cell 20, 934-946.

Nimchuk, Z., 2017. CLAVATA1 controls distinct signaling outputs that buffer shoot stem cell proliferation through a two-step transcriptional compensation loop. PLoS Genet. 13, e1006681.

Purcell, S., Neale, B., Todd-Brown, K., Thomas, L., Ferreira, M., Bender, D., Maller, J., Sklar, P., de Bakker, P., Daly, M.J., et al., 2007. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559e575.

Purugganan, M., Jackson, S., 2021. Advancing crop genomics from lab to field. Nat. Genet. 53, 595-601.

Rodriguez-Leal, D., Lemmon, Z., Man, J., Bartlett, M., Lippman, Z., 2017. Engineering quantitative trait variation for crop improvement by genome editing. Cell 171, 470-480.

Shinohara, H., Matsubayashi, Y. 2015. Reevaluation of the CLV3-receptor interaction in the shoot apical meristem: dissection of the CLV3 signaling pathway from a direct ligand-binding point of view. Plant J. 82, 328-336.

Somssich, M., Je, B., Simon, R., Jackson, D., 2016b. CLAVATA-WUSCHEL signaling in the shoot meristem. Development 143, 3238-3248.

Somssich, M., Bleckmann, A., Simon, R., 2016a. Shared and distinct functions of the pseudokinase CORYNE (CRN) in shoot and root stem cell maintenance of Arabidopsis. J. Exp. Bot. 67, 4901-4915.

Somssich, M., Ma, Q., Weidtkamp-Peters, S., Stahl, Y., Felekyan, S., Bleckmann, A., Seidel, C., Simon, R., 2015. Real-time dynamics of peptide ligand-dependent receptor complex formation in planta. Sci. Signal. 8, ra76.

Song, Y., Yang, H., Zhu, W., Wang, H., Zhang, J., Li, Y., 2023. The Os14-3-3 family genes regulate grain size in rice. J. Genet. Genom. Online.

Wang, C., Yu, H., Huang, J., Wang, W., Faruquee, M., Zhang, F., Zhao, X., Fu, B., Chen, K., Zhang, H., et al., 2020. Towards a deeper haplotype mining of complex traits in rice with RFGB v2.0. Plant Biotechnol. J. 18, 14-16.

Tao, Y. et al., 2020. Large-scale GWAS in sorghum reveals common genetic control of grain size among cereals. Plant Biotechnol. J. 18, 1093-1105.

Wang, W., Hu, C., Li, X., Zhu, Y., Tao, L., Cui, Y., Deng, D., Fan, X., Zhang, H., Li, J., et al., 2022. Receptor-like cytoplasmic kinases PBL34/35/36 are required for CLE peptide-mediated signaling to maintain shoot apical meristem and root apical meristem homeostasis in Arabidopsis. Plant Cell 34, 1289-1307.

Xu, C., Liberatore, K., MacAlister, C., Huang, Z., Chu, Y., Jiang, K., Brooks, C., Ogawa-Ohnishi, M., Xiong, G., Pauly, M., 2015. A cascade of arabinosyltransferases controls shoot meristem size in tomato. Nat. Genet. 47, 784-792.

Ying, J., Gao, J., Shan, J., Zhu, M., Shi, M., Lin, H., 2012. Dissecting the genetic basis of extremely large grain shape in rice cultivar ‘JZ1560’. J. Genet. Genom. 39, 325-333.

Yu, S., Ali, J., Zhou, S., Ren, G., Xie, H., Xu, J., Yu, X., Zhou, F., Peng, S., Ma, L., et al., 2022. From Green Super Rice to green agriculture: reaping the promise of functional genomics research. Mol. Plant 15, 9-26.

Zhang, J., Zhang, D., Fan, Y., Li, C., Xu, P., Li, W., Sun, Q., Huang, X., Zhang, C., Wu, L., et al., 2021. The identification of grain size genes by RapMap reveals directional selection during rice domestication. Nat. Commun. 12, 5673.

Zhang, Q., 2007. Strategies for developing green super rice. Proc. Natl. Acad. Sci. U. S. A. 104, 16402-16409.

Zhao, H., Li, J., Yang, L., Qin, G., Xia, C., Xu, X., Su, Y., Liu,Y., Ming, L., Chen, L., et al., 2021. An inferred functional impact map of genetic variants in rice. Mol. Plant 14, 1584-1599.

Zhao, H., Yao, W., Ouyang, Y., Yang, W., Wang, G., Lian, X., Xing, Y., Chen, L., Xie, W., 2015. RiceVarMap: a comprehensive database of rice genomic variations. Nucleic Acids Res. 43, D1018-D1022.

Zhu, Y., Wang, Y., Li, R., Song, X., Wang, Q., Huang, S., Jin, J., Liu, C., Lin, J., 2010. Analysis of interactions among the CLAVATA3 receptors reveals a direct interaction between CLAVATA2 and CORYNE in Arabidopsis. Plant J. 61, 223-233.

Zsogon, A., Cermak, T., Naves, E., Notini, M., Edel, K., Weinl, S., Freschi, L., Voytas, D., Kudla, J., Peres, L., 2018. De novo domestication of wild tomato using genome editing. Nat. Biotechnol. 36, 1211-1216.

Zuo, J., Li, J., 2014. Molecular genetic dissection of quantitative trait loci regulating rice grain size. Annu. Rev. Genet. 48, 99-118.

Relative Articles

Supplements(0)

Cited By

Proportional views