Abstract
Increased crop yields are required to support rapid population growth worldwide. Grain weight is a key component of rice yield, but the underlying molecular mechanisms that control it remain elusive. Here, we report the cloning and characterization of a new quantitative trait locus (QTL) for the control of rice grain length, weight and yield. This locus, GL3.1, encodes a protein phosphatase kelch (PPKL) family — Ser/Thr phosphatase. GL3.1 is a member of the large grain WY3 variety, which is associated with weaker dephosphorylation activity than the small grain FAZ1 variety. GL3.1-WY3 influences protein phosphorylation in the spikelet to accelerate cell division, thereby resulting in longer grains and higher yields. Further studies have shown that GL3.1 directly dephosphorylates its substrate, Cyclin-T1;3, which has only been rarely studied in plants. The downregulation of Cyclin-T1;3 in rice resulted in a shorter grain, which indicates a novel function for Cyclin-T in cell cycle regulation. Our findings suggest a new mechanism for the regulation of grain size and yield that is driven through a novel phosphatase-mediated process that affects the phosphorylation of Cyclin-T1;3 during cell cycle progression, and thus provide new insight into the mechanisms underlying crop seed development. We bred a new variety containing the natural GL3.1 allele that demonstrated increased grain yield, which indicates that GL3.1 is a powerful tool for breeding high-yield crops.
Similar content being viewed by others
Log in or create a free account to read this content
Gain free access to this article, as well as selected content from this journal and more on nature.com
or
References
Tilman D, Fargione J, Wolff B, et al. Forecasting agriculturally driven global environmental change. Science 292:281–284.
Hibberd JM, Sheehy JE, Langdale JA . Using C4 photosynthesis to increase the yield of rice-rationale and feasibility. Curr Opin Plant Biol 2008; 11:228–231.
Khush GS . Green revolution: preparing for the 21st century. Genome 1999; 42:646–655.
Khush GS . What it will take to feed 5.0 billion rice consumers in 2030. Plant Mol Biol 2005; 59:1–6.
Zhang Q . Strategies for developing Green Super Rice. Proc Natl Acad Sci USA 2007; 104:16402–16409.
Kropff M, Cassman K, Peng S, Matthews R, Setter T . Quantitative understanding of yield potential. In: Cassman K, ed. Breaking the Yield Barrier. Los Baños, Philippines: International Rice Research Institute, 1994:21–38.
Song XJ, Huang W, Shi M, Zhu MZ, Lin HX . A QTL for rice grain width and weight encodes a previously unknown RING-type E3 ubiquitin ligase. Nat Genet 2007; 39:623–630.
Shomura A, Izawa T, Ebana K, et al. Deletion in a gene associated with grain size increased yields during rice domestication. Nat Genet 2008; 40:1023–1028.
Weng J, Gu S, Wan X, et al. Isolation and initial characterization of GW5, a major QTL associated with rice grain width and weight. Cell Res 2008; 18:1199–1209.
Mao H, Sun S, Yao J, et al. Linking differential domain functions of the GS3 protein to natural variation of grain size in rice. Proc Natl Acad Sci USA 2010; 107:19579–19584.
Fan C, Xing Y, Mao 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 2006; 112:1164–1171.
Li Y, Fan C, Xing Y, et al. Natural variation in GS5 plays an important role in regulating grain size and yield in rice. Nat Genet 2011; 43:1266–1269.
Wang E, Wang J, Zhu X, et al. Control of rice grain-filling and yield by a gene with a potential signature of domestication. Nat Genet 2008; 40:1370–1374.
Ashikari M, Sakakibara H, Lin S, et al. Cytokinin oxidase regulates rice grain production. Science 2005; 309:741–745.
Xue W, Xing Y, Weng X, et al. Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat Genet 2008; 40:761–767.
Huang X, Qian Q, Liu Z, et al. Natural variation at the DEP1 locus enhances grain yield in rice. Nat Genet 2009; 41:494–497.
Li X, Qian Q, Fu Z, et al. Control of tillering in rice. Nature 2003; 422:618–621.
Jiao Y, Wang Y, Xue D, et al. Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat Genet 2010; 42:541–544.
Miura K, Ikeda M, Matsubara A, et al. OsSPL14 promoters panicles branching and higher grain productivity in rice. Nat Genet 2010; 42:545–549.
Jin J, Huang W, Gao JP, et al. Genetic control of rice plant architecture under domestication. Nat Genet 2008; 40:1365–1369.
Tan L, Li X, Liu F, et al. Control of a key transition from prostrate to erect growth in rice domestication. Nat Genet 2008; 40:1360–1364.
Olsen JV, Blagoev B, Gnad F, et al. Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 2006; 127:635–648.
Cohen P . The regulation of protein function by multisite phosphorylation--a 25 year update. Trends Biochem Sci 2000; 25:596–601.
Farkas I, Dombradi V, Miskei M, Szabados L, Koncz C . Arabidopsis PPP family of serine/threonine phosphatases. Trends Plant Sci 2007; 12:169–176.
Denu JM, Stuckey JA, Saper MA, Dixon JE . Form and function in protein dephosphorylation. Cell 1996; 87:361–364.
Janssens V, Goris J . Protein phosphatase 2A: a highly regulated family of serine/threonine phosphatases implicated in cell growth and signalling. Biochem J 2001; 353:417–439.
Luan S . Protein phosphatases in plants. Annu Rev Plant Biol 2003; 54:63–92.
Goldberg J, Huang HB, Kwon YG, Greengard P, Nairn AC, Kuriyan J . Three-dimensional structure of the catalytic subunit of protein serine/threonine phosphatase-1. Nature 1995; 376:745–753.
Barton GJ, Cohen PT, Barford D . Conservation analysis and structure prediction of the protein serine/threonine phosphatases. Sequence similarity with diadenosine tetraphosphatase from Escherichia coli suggests homology to the protein phosphatases. Eur J Biochem 1994; 220:225–237.
Kutuzov MA, Andreeva AV . Protein Ser/Thr phosphatases with kelch-like repeat domains. Cell Signal 2002; 14:745–750.
Li JL, Baker DA . A putative protein serine/threonine phosphatase from Plasmodium falciparum contains a large N-terminal extension and five unique inserts in the catalytic domain. Mol Biochem Parasitol 1998; 95:287–295.
Mora-Garcia S, Vert G, Yin Y, Cano-Delgado A, Cheong H, Chory J . Nuclear protein phosphatases with Kelch-repeat domains modulate the response to brassinosteroids in Arabidopsis. Genes Dev 2004; 18:448–460.
Kerk D, Bulgrien J, Smith DW, Barsam B, Veretnik s, Gribskov M . The complement of protein phosphatase catalytic subunits encoded in the genome of Arabidopsis. Plant Physiol 2002; 129:908–925.
Kim TW, Guan S, Sun Y, et al. Brassinosteroid signal transduction from cell-surface receptor kinases to nuclear transcription factors. Nat Cell Biol 2009; 11:1254–1260.
Aluko G, Martinez C, Tohme J, et al. QTL mapping of grain quantity traits from the interspecific cross Oryza sativa × O. glaberrima. Theor Appl Genet 2004; 109:630–639.
Li JM, Michael T, Susan RM . Fine mapping of a grain-weight quantitative trait locus in the pericentromeric region of rice chromosome 3. Genetics 2004; 168:2187–2195.
Liu TM, Mao DH, Zhang SP, Xu CG, Xing YZ . Fine mapping SPP1, a QTL controlling the number of spikelets per panicle, to a BAC clone in rice (Oryza sativa). Theor Appl Genet 2009; 118:1509–1517.
Wang JK, Wan XY, Jose C, Jonathan C, Weng JF, Zhai HQ, Wan JM . QTL mapping of grain length in rice (Oryza sativa L.) using chromosome segment substitution lines. Genet Res 2006; 88:93–104.
Ren ZH, Gao JP, Li LG, et al. A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nat Genet 2005; 37:1141–1146.
Shigeto K, Hiroshi S, Teruo A, Minoru T, Takash S, Minako N . Analysis by in vitro mutagenesis of PP2Aα okadaic acid responsive sequences. Biochem and Biophys Res Commun 1995; 214:518–523.
Adams J, Kelso R, Cooley L . The kelch repeat superfamily of proteins: propellers of cell function. Trends Cell Biol 2000; 10:17–24.
Weber AP, Linka M, Bhattacharya D . Single, ancient origin of a plastid metabolite translocator family in Plantae from an endomembrane-derived ancestor. Eukaryot Cell 2006; 5:609–612.
Cavalier-Smith T . Principles of protein and lipid targeting in secondary symbiogenesis: euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryote family tree. J Eukaryot Microbiol 1999; 46:347–366.
Eichinger L, Bomblies L, Vandekerckhove J, Schleicher M, Gettemans J . A novel type of protein kinase phosphorylates actin in the actin-fragmin complex. EMBO J 1996; 15:5547–5556.
Kim IF, Mohammadi E, Huang RC . Isolation and characterization of IPP, a novel human gene encoding an actin-binding, kelch-like protein. Gene 1999; 228:73–83.
Philips J, Herskowitz I . Identification of Kel1p, a kelch domain-containing protein involved in cell fusion and morphology in Saccharomyces cerevisiae. J Cell Biol 1998; 143:375–389.
Duke-Cohan JS, Gu J, McLaughlin DF, et al. Attractin (DPPT-L), a member of the CUB family of cell adhesion and guidance proteins, is secreted by activated human T lymphocytes and modulates immune cell interactions. Proc Natl Acad Sci USA 1998; 95:11336–11341.
Herrmann CH, Mancini MA . The Cdk9 and cyclin T subunits of TAK/P-TEFb localize to splicing factor-rich nuclear speckle regions. J Cell Sci 2001; 114:1491–1503.
Moiola C, De Luca P, Gardner K, Vazquez E, De Siervi A . Cyclin T1 overexpression induces malignant transformation and tumor growth. Cell Cycle 2010; 9:3119–3126 ().
De Wulf P, Montani F, Visintin R . Protein phosphatases take the mitotic stage. Curr Opin Cell Biol 2009; 21:806–815.
Sun SY, Chao DY, Li XM, et al. OsHAL3 mediates a new pathway in the light-regulated growth of rice. Nat Cell Biol 2009; 11:845–851.
Miao Y, Jiang L . Transient expression of fluorescent fusion proteins in protoplasts of suspension cultured cells. Nat Protoc 2007; 2:2348–2353.
Mao J, Zhang YC, Sang Y, Li QH, Yang HQ . A role for Arabidopsis cryptochromes and COP1 in the regulation of stomatal opening. Proc Natl Acad Sci USA 2005; 102:12270–12275.
Shi S, Chen W, Sun W . Comparative proteomic analysis of the Arabidopsis cbl1 mutant in response to salt stress. Proteomics 2011; 11:4712–4725.
Ross PL, Huang YN, Marchese JN, et al. Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol Cell Proteomics 2004; 12:1154–1169.
Acknowledgements
We would like to thank Mr Xiao-Yan Gao, Mr Xiao-Shu Gao and Mr Wei-fang Jiang for assistance with transmission electron microscopy, confocal laser scanning microscopy and flow cytometry, respectively. This work was supported by the Ministry of Science and Technology of China (2012CB944800 and 2012AA10A302), the National Natural Science Foundation of China (31130071 and 31121063), the Ministry of Agriculture of China (2009ZX08009-102B), the Chinese Academy of Sciences (KSCX3-EW-N-01), the Research Grants Council of Hong Kong (CUHK466011 and CUHK2/CRF/11G) and the CAS-Croucher Foundation.
Author information
Authors and Affiliations
Corresponding authors
Additional information
( Supplementary information is linked to the online version of the paper on the Cell Research website.)
Supplementary information
Supplementary information, Figure S1
FAZ1 and NIL agricultural traits and grain quality. (PDF 458 kb)
Supplementary information, Figure S2
Phenotypic characterization of Huanghuazhan and Huanghuazhan (GL3.1) grains. (PDF 258 kb)
Supplementary information, Figure S3
Sequence alignment of GL3.1 from FAZ1 and WY3 with other large grain rice varieties. (PDF 1085 kb)
Supplementary information, Figure S4
Analysis of transgenic lines overexpressing GL3.1-WY3, GL3.1-M1, GL3.1-M2. (PDF 430 kb)
Supplementary information, Figure S5
Sequence alignment of GL3.1's promoter from FAZ1 and WY3. (PDF 693 kb)
Supplementary information, Figure S6
The expression pattern of GL3.1 in FAZ1 and NIL. (PDF 307 kb)
Supplementary information, Figure S7
Sequence alignment of phopshatase domain of GL3.1 and PP2A. (PDF 309 kb)
Supplementary information, Figure S8
The expression pattern of Cyclin-T1;3 in FAZ1 and NIL. (PDF 217 kb)
Supplementary information, Figure S9
Genomic alignment of GL3.1 from a variety of species. (PDF 382 kb)
Table S1
Influence of GL3 on differential protein expression in young FAZ1 and NIL spikelets. (PDF 19 kb)
Table S2
Proteins with different phosphorylation status between FAZ1 and NIL. (PDF 36 kb)
Table S3
Gene Ontology analysis of phosphoproteins. (PDF 19 kb)
Table S4
The primers used for GL3 study. (PDF 21 kb)
Rights and permissions
About this article
Cite this article
Qi, P., Lin, YS., Song, XJ. et al. The novel quantitative trait locus GL3.1 controls rice grain size and yield by regulating Cyclin-T1;3. Cell Res 22, 1666–1680 (2012). https://doi.org/10.1038/cr.2012.151
Received:
Revised:
Accepted:
Published:
Issue date:
DOI: https://doi.org/10.1038/cr.2012.151
Keywords
This article is cited by
-
Natural variation of Grain size 3 allele differentially functions in regulating grain length in xian/indica and geng/japonica rice
Euphytica (2024)
-
Identification of qGL4.1 and qGL4.2, two closely linked QTL controlling grain length in rice
Molecular Breeding (2024)
-
Development of introgression lines and mapping of qGW2, a novel QTL that confers grain width, in rice (Oryza sativa L.)
Molecular Breeding (2024)
-
Identification of Increased Grain Length 1 (IGL1), a novel gene encoded by a major QTL for modulating grain length in rice
Theoretical and Applied Genetics (2024)
-
T-DNA insertion mutants of Arabidopsis DA1 orthologous genes displayed altered plant height and yield-related traits in rice (O. Sativa L.)
Genes & Genomics (2024)


