Abstract
Given the continuously growing population and decreasing arable land, food shortage is becoming one of the most serious global problems in this century1. Grain size is one of the determining factors for grain yield and thus is a prime target for genetic breeding2,3. Although a number of quantitative trait loci (QTLs) associated with rice grain size have been identified in the past decade, mechanisms underlying their functions remain largely unknown4,5. Here we show that a grain-length-associated QTL, GL2, has the potential to improve grain weight and grain yield up to 27.1% and 16.6%, respectively. We also show that GL2 is allelic to OsGRF4 and that it contains mutations in the miR396 targeting sequence. Because of the mutation, GL2 has a moderately increased expression level, which consequently activates brassinosteroid responses by upregulating a large number of brassinosteroid-induced genes to promote grain development. Furthermore, we found that GSK2, the central negative regulator of rice brassinosteroid signalling, directly interacts with OsGRF4 and inhibits its transcription activation activity to mediate the specific regulation of grain length by the hormone. Thus, this work demonstrates the feasibility of modulating specific brassinosteroid responses to improve plant productivity.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 digital issues and online access to articles
$119.00 per year
only $9.92 per issue
Rent or buy this article
Prices vary by article type
from$1.95
to$39.95
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Rosegrant, M. W. & Cline, S. A. Global food security: challenges and policies. Science 302, 1917–1919 (2003).
Xing, Y. Z. & Zhang, Q. F. Genetic and molecular bases of rice yield. Annu. Rev. Plant Biol. 61, 421–442 (2010).
Ikeda, M., Miura, K., Aya, K., Kitano, H. & Matsuoka, M. Genes offering the potential for designing yield-related traits in rice. Curr. Opin. Plant Biol. 16, 213–220 (2013).
Zuo, J. & Li, J. Molecular genetic dissection of quantitative trait loci regulating rice grain size. Annu. Rev. Genet. 48, 99–118 (2014).
Miura, K., Ashikari, M. & Matsuoka, M. The role of QTLs in the breeding of high-yielding rice. Trends Plant Sci. 16, 319–326 (2011).
Horiguchi, G., Kim, G. T. & Tsukaya, H. The transcription factor AtGRF5 and the transcription coactivator AN3 regulate cell proliferation in leaf primordia of Arabidopsis thaliana. Plant J. 43, 68–78 (2005).
Wang, L. et al. miR396-targeted AtGRF transcription factors are required for coordination of cell division and differentiation during leaf development in Arabidopsis. J. Exp. Bot. 62, 761–773 (2011).
Liu, D. M., Song, Y., Chen, Z. X. & Yu, D. Q. Ectopic expression of miR396 suppresses GRF target gene expression and alters leaf growth in Arabidopsis. Physiol. Plant 136, 223–236 (2009).
van der Knaap, E., Kim, J. H. & Kende, H. A novel gibberellin-induced gene from rice and its potential regulatory role in stem growth. Plant Physiol. 122, 695–704 (2000).
Kim, J. H., Choi, D. S. & Kende, H. The AtGRF family of putative transcription factors is involved in leaf and cotyledon growth in Arabidopsis. Plant J. 36, 94–104 (2003).
Tong, H. N. et al. Brassinosteroid regulates cell elongation by modulating gibberellin metabolism in rice. Plant Cell 26, 4376–4393 (2014).
Zhu, X. L. et al. Brassinosteroids promote development of rice pollen grains and seeds by triggering expression of Carbon Starved Anther, a MYB domain protein. Plant J. 82, 570–581 (2015).
Tong, H. et al. DWARF AND LOW-TILLERING acts as a direct downstream target of a GSK3/SHAGGY-like kinase to mediate brassinosteroid responses in rice. Plant Cell 24, 2562–2577 (2012).
Wang, X. L. et al. Arabidopsis MICROTUBULE DESTABILIZING PROTEIN40 is involved in brassinosteroid regulation of hypocotyl elongation. Plant Cell 24, 5193–5193 (2012).
Yamamuro, C. et al. Loss of function of a rice brassinosteroid insensitive1 homolog prevents internode elongation and bending of the lamina joint. Plant Cell 12, 1591–1606 (2000).
Li, J. A. et al. Mutation of rice BC12/GDD1, which encodes a kinesin-like protein that binds to a GA biosynthesis gene promoter, leads to dwarfism with impaired cell elongation. Plant Cell 23, 628–640 (2011).
Kitagawa, K. et al. A novel Kinesin 13 protein regulating rice seed length. Plant Cell Physiol. 51, 1315–1329 (2010).
Fujikura, U. et al. Atkinesin-13A modulates cell-wall synthesis and cell expansion in Arabidopsis thaliana via the THESEUS1 pathway. PLoS Genet. 10, e1004627 (2014).
Kim, J. H. & Kende, H. A transcriptional coactivator, AtGIF1, is involved in regulating leaf growth and morphology in Arabidopsis. Proc. Natl Acad. Sci. USA 101, 13374–13379 (2004).
Tong, H. & Chu, C. Brassinosteroid signaling and application in rice. J. Genet. Genomics 39, 3–9 (2012).
Nelissen, H. et al. Dynamic changes in ANGUSTIFOLIA3 complex composition reveal a growth regulatory mechanism in the maize leaf. Plant Cell 27, 1605–1619 (2015).
Kim, J. H. & Tsukaya, H. Regulation of plant growth and development by the GROWTH-REGULATING FACTOR and GRF-INTERACTING FACTOR duo. J. Exp. Bot. 66, 6093–6107 (2015).
Omidbakhshfard, M. A., Proost, S., Fujikura, U. & Mueller-Roeber, B. Growth-regulating factors (GRFs): a small transcription factor family with important functions in plant biology. Mol. Plant 8, 998–1010 (2015).
Fan, C. H. et al. GS3, a major QTL for grain length and weight and minor QTL for grain width and thickness in rice, encodes a putative transmembrane protein. Theor. Appl. Genet. 112, 1164–1171 (2006).
Hu, J. et al. A rare allele of GS2 enhances grain size and grain yield in rice. Mol. Plant 8, 1455–1465 (2015).
Huang, X. H. et al. Genome-wide association studies of 14 agronomic traits in rice landraces. Nature Genet. 42, 961–967 (2010).
Jin, Y. et al. An AT-hook gene is required for palea formation and floral organ number control in rice. Dev. Biol. 359, 277–288 (2011).
Waadt, R. et al. Multicolor bimolecular fluorescence complementation reveals simultaneous formation of alternative CBL/CIPK complexes in planta. Plant J. 56, 505–516 (2008).
Sparkes, I. A., Runions, J., Kearns, A. & Hawes, C. Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants. Nature Protocols 1, 2019–2025 (2006).
Guo, X. et al. The rice GERMINATION DEFECTIVE 1, encoding a B3 domain transcriptional repressor, regulates seed germination and seedling development by integrating GA and carbohydrate metabolism. Plant J. 75, 403–416 (2013).
Fiil, B. K., Qiu, J. L., Petersen, K., Petersen, M. & Mundy, J. Coimmunoprecipitation (co-IP) of nuclear proteins and chromatin immunoprecipitation (ChIP) from Arabidopsis. Cold Spring Harb. Protoc. 2008, pdb.prot5049 (2008).
Chen, M. L. et al. Highly sensitive and quantitative profiling of acidic phytohormones using derivatization approach coupled with nano-LC-ESI-Q-TOF-MS analysis. J. Chromatogr. B 905, 67–74 (2012).
Ding, J., Mao, L. J., Wang, S. T., Yuan, B. F. & Feng, Y. Q. Determination of endogenous brassinosteroids in plant tissues using solid-phase extraction with double layered cartridge followed by high-performance liquid chromatography-tandem mass spectrometry. Phytochem. Anal. 24, 386–394 (2013).
Acknowledgements
This work was supported by grants from National Natural Science Foundation of China (91435106, 91335203, 31170715), Ministry of Agriculture of China (2014ZX08009), Natural Science Foundation of Fujian Province (B0420002) and Youth Innovation Promotion Association CAS (2015076).
Author information
Authors and Affiliations
Contributions
R.C. and H.T. designed the research, performed the experiments, analysed the data and wrote the paper. B.S, Y.L., S.F., Y.X., D.L., B.H., L.L. and H.W. performed the experiments. C.C. and M.Z. supervised the project, designed the research and analysed the data.
Corresponding authors
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Rights and permissions
About this article
Cite this article
Che, R., Tong, H., Shi, B. et al. Control of grain size and rice yield by GL2-mediated brassinosteroid responses. Nature Plants 2, 15195 (2016). https://doi.org/10.1038/nplants.2015.195
Received:
Accepted:
Published:
DOI: https://doi.org/10.1038/nplants.2015.195
This article is cited by
-
Identification of qGL4.1 and qGL4.2, two closely linked QTL controlling grain length in rice
Molecular Breeding (2024)
-
SPR9 encodes a 60 S ribosomal protein that modulates panicle spreading and affects resistance to false smut in rice (Oryza sativa. L)
BMC Plant Biology (2023)
-
Reducing brassinosteroid signalling enhances grain yield in semi-dwarf wheat
Nature (2023)
-
Deploying QTL-seq rapid identification and separation of the major QTLs of tassel branch number for fine-mapping in advanced maize populations
Molecular Breeding (2023)
-
Genome-wide analysis of growth-regulating factor genes in grape (Vitis vinifera L.): identification, characterization and their responsive expression to osmotic stress
Plant Cell Reports (2023)