Abstract
Grain weight is one of the most important components of grain yield and is controlled by quantitative trait loci (QTLs) derived from natural variations in crops. However, the molecular roles of QTLs in the regulation of grain weight have not been fully elucidated. Here, we report the cloning and characterization of GW2, a new QTL that controls rice grain width and weight. Our data show that GW2 encodes a previously unknown RING-type protein with E3 ubiquitin ligase activity, which is known to function in the degradation by the ubiquitin-proteasome pathway. Loss of GW2 function increased cell numbers, resulting in a larger (wider) spikelet hull, and it accelerated the grain milk filling rate, resulting in enhanced grain width, weight and yield. Our results suggest that GW2 negatively regulates cell division by targeting its substrate(s) to proteasomes for regulated proteolysis. The functional characterization of GW2 provides insight into the mechanism of seed development and is a potential tool for improving grain yield in crops.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
Accession codes
References
Tanksley, S.D. Mapping polygenes. Annu. Rev. Genet. 27, 205–233 (1993).
Yano, M. Genetic and molecular dissection of naturally occurring variations. Curr. Opin. Plant Biol. 4, 130–135 (2001).
Frary, A. et al. fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. Science 289, 85–88 (2000).
Yano, M. et al. Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell 12, 2473–2484 (2000).
El-Din El-Assal, S., Alonso-Blanco, C., Peeters, A.J., Raz, V. & Koornneef, M.A. A QTL for flowering time in Arabidopsis reveals a novel allele of CRY2. Nat. Genet. 29, 435–440 (2001).
Liu, J., Eck, J.V., Cong, B. & Tanksley, S.D. A new class of regulatory genes underlying the cause of pear-shaped tomato fruit. Proc. Natl. Acad. Sci. USA 99, 13302–13306 (2002).
Takahashi, Y., Shomura, A., Sasaki, T. & Yano, M. Hd6, a rice quantitative trait locus involved in photoperiod sensitivity, encodes the alpha subunit of protein kinase CK2. Proc. Natl. Acad. Sci. USA 98, 7922–7927 (2001).
Ren, Z.H. et al. A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nat. Genet. 37, 1141–1146 (2005).
Ashikari, M. et al. Cytokinin oxidase regulates rice grain production. Science 309, 741–745 (2005).
Konishi, S. et al. An SNP caused loss of seed shattering during rice domestication. Science 312, 1392–1396 (2006).
Evans, L.T. Storage capacity as a limitation on grain yield. in Rice Breeding (International Rice Research Institute, Manila, 1972).
Xu, J.Y., Xue, Q.Z., Luo, L.J. & Li, Z.K. Genetic dissection of grain weight and its related traits in rice (Oryza sativa L.). Chin J Rice Sci 16, 6–10 (2002).
Lin, H.X. et al. RFLP mapping of QTLs for yield and related characters in rice (Oryza sativa L.). Theor. Appl. Genet. 92, 920–927 (1996).
Huang, N. et al. RFLP mapping of isozymes, RAPD, and QTLs for grain shape, brown planthopper resistance in a doubled-haploid rice population. Mol. Breed. 3, 105–113 (1997).
Redona, E.D. & Mackill, D.J. Quantitative trait locus analysis for rice panicle and grain characteristics. Theor. Appl. Genet. 96, 957–963 (1998).
Thomson, M.J. et al. Mapping quantitative trait loci for yield, yield components and morphological traits in an advanced backcross population between Oryza rufipogon and the Oryza sativa cultivar Jefferson. Theor. Appl. Genet. 107, 479–493 (2003).
Li, J., Thomson, M. & McCouch, S.R. Fine mapping of a grain weight quantitative trait locus in the pericentromeric region of rice chromosome 3. Genetics 168, 2187–2195 (2004).
Fan, C. 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).
Lin, H.X. et al. RFLP mapping of QTLs for grain shape traits in indica rice (Oryza sativa L. subsp. indica). Scientia Agricultura Sinica 28, 1–7 (1995).
Yoon, D.B. et al. Mapping quantitative trait loci for yield components and morphological traits in an advanced backcross population between Oryza grandiglumis and the O. sativa japonica cultivar Hwaseongbyeo. Theor. Appl. Genet. 112, 1052–1062 (2006).
Freemont, P.S., Hanson, I.M. & Trowsdale, J. A novel cysteine-rich sequence motif. Cell 64, 483–484 (1991).
Borden, K.L. & Freemont, P.S. The RING finger domain: a recent example of a sequence-structure family. Curr. Opin. Struct. Biol. 6, 395–401 (1996).
Saurin, A.J., Borden, K.L., Boddy, M.N. & Freemont, P.S. Does this have a familiar RING? Trends Biochem Sci. 21, 208–214 (1996).
Stone, S.L. et al. Functional analysis of the RING-type ubiquitin ligase family of Arabidopsis. Plant Physiol. 137, 13–30 (2005).
Hewitt, E.W. et al. Ubiquitylation of MHC class I by the K3 viral protein signals internalization and TSG101-dependent degradation. EMBO J. 21, 2418–2429 (2002).
Dasgupta, A., Ramsey, K.L., Smith, J.S. & Auble, D.T. Sir Antagonist 1 (San1) is a ubiquitin ligase. J. Biol. Chem. 279, 26830–26838 (2004).
Albert, T.K. et al. Identification of a ubiquitin-protein ligase subunit within the CCR4-NOT transcription repressor complex. EMBO J. 21, 355–364 (2002).
Lorick, K.L. et al. RING fingers mediate ubiquitin-conjugating enzyme (E2)-dependent ubiquitination. Proc. Natl. Acad. Sci. USA 96, 11364–11369 (1999).
Joazeiro, C.A. et al. The tyrosine kinase negative regulator c-Cbl as a RING-type, E2 dependent ubiquitin-protein ligase. Science 286, 309–312 (1999).
Xie, Q. et al. SINAT5 promotes ubiquitin-related degradation of NAC1 to attenuate auxin signals. Nature 419, 167–170 (2002).
Saijo, Y. et al. The COP1–SPA1 interaction defines a critical step in phytochrome A-mediated regulation of HY5 activity. Genes Dev. 17, 2642–2647 (2003).
Deng, X.W., Caspar, T. & Quail, P.H. cop1: A regulatory locus involved in light-controlled development and gene expression in Arabidopsis. Genes Dev. 5, 1172–1182 (1991).
Moon, J., Parry, G. & Estelle, M. The ubiquitin-proteasome pathway and plant development. Plant Cell 16, 3181–3195 (2004).
Alonso-Blanco, C., Blankestijn-De Vries, H., Hanhart, C.J. & Koornneef, M. Natural allelic variation at seed size loci in relation to other life history traits of Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 96, 4710–4717 (1999).
Luo, M., Dennis, E.S., Berge, F., Peacock, W.J. & Chaudhury, A. MINISEED3 (MINI3), a WRKY family gene, and HAIKU2 (IKU2), a leucine-rich repeat (LRR) KINASE gene, are regulators of seed size in Arabidopsis. Proc. Natl. Acad. Sci. USA 102, 17531–17536 (2005).
Xie, X. et al. Fine mapping of a grain weight quantitative trait locus on rice chromosome 8 using near-isogenic lines derived from a cross between Oryza sativa and Oryza rufipogon. Theor. Appl. Genet. 113, 885–894 (2006).
Tan, Y.F. et al. Genetic bases of appearance quality of rice grains in Shanyou 63, an elite rice hybrid. Theor. Appl. Genet. 101, 823–829 (2000).
Dornan, D. et al. The ubiquitin ligase COP1 is a critical negative regulator of p53. Nature 429, 86–92 (2004).
Disch, S. et al. The E3 ubiquitin ligase BIG BROTHER controls Arabidopsis organ size in a dosage-dependent manner. Curr. Biol. 16, 272–279 (2006).
Osterlund, M.T., Hardtke, C.S., Wei, N. & Deng, X.W. Targeted destabilization of HY5 during light-regulated development of Arabidopsis. Nature 405, 462–466 (2000).
Miki, Y. et al. A strong candidate for the breast and ovarian cancer susceptibility gene BRCA1. Science 266, 66–71 (1994).
Venkitaraman, A.R. Cancer susceptibility and the functions of BRCA1 and BRCA2. Cell 108, 171–182 (2002).
Reddy, V.M. & Daynard, T.B. Endosperm characteristics associated with rate of grain filling and kernel size in corn. Maydica 28, 339–355 (1983).
Chojecki, A.J.S., Bayliss, M.W. & Gale, M.D. Cell production and DNA accumulation in the wheat endosperm, and their association with grain weight. Ann. Bot. (Lond.) 58, 809–817 (1986).
Schruff, M.C. et al. The AUXIN RESPONSE FACTOR 2 gene of Arabidopsis links auxin signalling, cell division, and the size of seeds and other organs. Development 133, 251–261 (2005).
Lander, E.S. & Botstein, D. Mapping Mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121, 185–199 (1989).
Mao, J., Zhang, Y.C., Sang, Y., Li, Q.H. & Yang, H.Q. A role for Arabidopsis cryptochromes and COP1 in the regulation of stomatal opening. Proc. Natl. Acad. Sci. USA 102, 12270–12275 (2005).
Hiei, Y., Ohta, S., Komari, T. & Kumashiro, T. Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J. 6, 271–282 (1994).
Zhang, X., Garreton, V. & Chua, N.H. The AIP2 E3 ligase acts as a novel negative regulator of ABA signaling by promoting ABI3 degradation. Genes Dev. 19, 1532–1543 (2005).
Acknowledgements
We thank P. Qi and Z.-Z. Piao for technical assistance. We thank S. Luan for critically reading the manuscript. This work was supported by grants from the Ministry of Science and Technology of China and the Shanghai Science and Technology Development Fund to H.-X.L.
Author information
Authors and Affiliations
Contributions
H.-X.L. designed the experiments. X.J.S. and W.H. performed most of the experiments. H.-X.L., S.M. and M.Z.Z. performed some of the experiments. H.-X.L. wrote the manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Supplementary Fig. 1
Grain phenotypes of FAZ1, WY3 and Oochikara. (PDF 29 kb)
Supplementary Fig. 2
GW2 expression in transgenic lines. (PDF 29 kb)
Supplementary Fig. 3
Comparison of plant height, flag leaf width, panicle number per plant, days to heading and main panicle length in FAZ1 and NIL(GW2). (PDF 34 kb)
Supplementary Fig. 4
Phenotypic characterization of grains in reciprocal crosses between FAZ1 and NIL(GW2). (PDF 31 kb)
Supplementary Fig. 5
Endosperm at various time points after fertilization. (PDF 52 kb)
Supplementary Fig. 6
Comparison of the six rice grain quality traits in FAZ1 and NIL1(GW2). (PDF 56 kb)
Supplementary Table 1
Molecular marker primers and primers for GW2 molecular analysis. (PDF 11 kb)
Rights and permissions
About this article
Cite this article
Song, XJ., Huang, W., Shi, M. et al. A QTL for rice grain width and weight encodes a previously unknown RING-type E3 ubiquitin ligase. Nat Genet 39, 623–630 (2007). https://doi.org/10.1038/ng2014
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/ng2014
This article is cited by
-
OsMAPK6 phosphorylation and CLG1 ubiquitylation of GW6a non-additively enhance rice grain size through stabilization of the substrate
Nature Communications (2024)
-
Genomic analyses reveal the stepwise domestication and genetic mechanism of curd biogenesis in cauliflower
Nature Genetics (2024)
-
MADS1-regulated lemma and awn development benefits barley yield
Nature Communications (2024)
-
Development of introgression lines and mapping of qGW2, a novel QTL that confers grain width, in rice (Oryza sativa L.)
Molecular Breeding (2024)
-
Genetic and functional mechanisms of yield-related genes in rice
Acta Physiologiae Plantarum (2024)