Skip to main content
Log in

A minor QTL, SG3, encoding an R2R3-MYB protein, negatively controls grain length in rice

  • Original Article
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Key message

SG3 , an R2R3 MYB protein coding gene that tightly linked to a major QTL GS3 , negatively regulates grain length while dependent on the status of GS3 in rice.

Abstract

It is often very difficult to isolate a minor QTL that is closely linked to a major QTL in rice. In this study, we focused on the isolation of a minor grain length QTL, small grain 3 (SG3), which is closely linked to the major QTL grain size 3 (GS3). The genetic effect of SG3 on grain length was dependent on GS3 status. Its genetic effect was larger in the presence of nonfunctional sg3 than functional SG3. A large number of near-isogenic F2 plants in which GS3 was fixed with nonfunctional alleles were developed to clone SG3. A gene encoding an R2R3 MYB domain transcriptional regulator was identified as the candidate gene for SG3. SG3 overexpression and knockdown plants showed shortened and elongated grains, respectively, which demonstrated that SG3 acts as a negative regulator of grain length. SG3 was preferentially expressed in panicles after flowering, and SG3 acted as a transcription activator. Comparative sequencing analysis identified a 12-bp insertion in the third exon of NYZ that led to a frameshift and resulted in a premature stop codon. The insertion/deletion was associated with grain length in the presence of functional GS3 in the indica subspecies. SG3 and GS3 were frequently in coupling phase in indica rice, making them good targets for the breeding of cultivars with short or long grains. The isolation of the SG3 MYB gene provides new gene resource and contributes to the regulatory network of grain length in rice.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Bai XF, Luo LJ, Yan WH, Kovi MR, Zhan W, Xing YZ (2010) Genetic dissection of rice grain shape using a recombinant inbred line population derived from two contrasting parents and fine mapping a pleiotropic quantitative trait locus qGL7. BMC Genet 11:16

    PubMed  PubMed Central  Google Scholar 

  • Bai XF, Huang Y, Hu Y, Liu HY, Zhang B, Smaczniak C, Hu G, Han ZM, Xing YZ (2017) Duplication of an upstream silencer of FZP increases grain yield in rice. Nat Plants 3:885–893

    CAS  PubMed  Google Scholar 

  • De Souza AT, Dai X, Spencer AG, Reppen T, Menzie A, Roesch PL, He Y, Caguyong MJ, Bloomer S, Herweijer H, Wolff JA, Hagstrom JE, Lewis DL, Linsley PS, Ulrich RG (2006) Transcriptional and phenotypic comparisons of Ppara knockout and siRNA knockdown mice. Nucleic Acids Res 34:4486–4494

    PubMed  PubMed Central  Google Scholar 

  • Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci 15:573–581

    CAS  PubMed  Google Scholar 

  • El-Brolosy MA, Kontarakis Z, Rossi A, Kuenne C, Gunther S, Fukuda N, Kikhi K, Boezio GLM, Takacs CM, Lai SL, Fukuda R, Gerri C, Giraldez AJ, Stainier DYR (2019) Genetic compensation triggered by mutant mRNA degradation. Nature 568:193–197

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fan C, Xing Y, Mao H, Lu T, Han B, Xu C, Li X, Zhang Q (2006) 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

    CAS  PubMed  Google Scholar 

  • Fan C, Yu S, Wang C, Xing Y (2009) A causal C-A mutation in the second exon of GS3 highly associated with rice grain length and validated as a functional marker. Theor Appl Genet 118:465–472

    CAS  PubMed  Google Scholar 

  • Gao Y, Zhang Y, Zhang D, Dai X, Estelle M, Zhao Y (2015) Auxin binding protein 1 (ABP1) is not required for either auxin signaling or Arabidopsis development. Proc Natl Acad Sci USA 112:2275–2280

    CAS  PubMed  Google Scholar 

  • Gubler F, Kalla R, Roberts JK, Jacobsen JV (1995) Gibberellin-regulated expression of a Myb gene in barley aleurone cells—evidence for Myb transactivation of a high-Pl alpha-amylase gene promoter. Plant Cell 7:1879–1891

    CAS  PubMed  PubMed Central  Google Scholar 

  • Heang D, Sassa H (2012a) Antagonistic actions of HLH/bHLH proteins are involved in grain length and weight in rice. PLoS ONE 7:e31325

    CAS  PubMed  PubMed Central  Google Scholar 

  • Heang D, Sassa H (2012b) Overexpression of a basic helix-loop-helix gene Antagonist of PGL1 (APG) decreases grain length of rice. Plant Biotechnol 29:65–69

    CAS  Google Scholar 

  • Heang D, Sassa H (2012c) An atypical bHLH protein encoded by POSITIVE REGULATOR OF GRAIN LENGTH 2 is involved in controlling grain length and weight of rice through interaction with a typical bHLH protein APG. Breed Sci 62:133–141

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hu Z, Lu SJ, Wang MJ, He H, Sun L, Wang H, Liu XH, Jiang L, Sun JL, Xin X, Kong W, Chu C, Xue HW, Yang J, Luo X, Liu JX (2018) A novel QTL qTGW3 encodes the GSK3/SHAGGY-like kinase OsGSK5/OsSK41 that interacts with OsARF4 to negatively regulate grain size and weight in rice. Mol Plant 11:736–749

    CAS  PubMed  Google Scholar 

  • Huang X, Kurata N, Wei X, Wang ZX, Wang A, Zhao Q, Zhao Y, Liu K, Lu H, Li W, Guo Y, Lu Y, Zhou C, Fan D, Weng Q, Zhu C, Huang T, Zhang L, Wang Y, Feng L et al (2012) A map of rice genome variation reveals the origin of cultivated rice. Nature 490:497–501

    CAS  PubMed  Google Scholar 

  • Huang Y, Bai XF, Cheng NN, Xiao JH, Li XH, Xing YZ (2019) Wide Grain 7 increases grain width by enhancing H3K4me3 enrichment in the OsMADS1 promoter in rice (Oryza sativa L.). Plant J. https://doi.org/10.1111/tpj.14646

    Article  PubMed  PubMed Central  Google Scholar 

  • Kranz HD, Denekamp M, Greco R, Jin H, Leyva A, Meissner RC, Petroni K, Urzainqui A, Bevan M, Martin C, Smeekens S, Tonelli C, Paz-Ares J, Weisshaar B (1998) Towards functional characterisation of the members of the R2R3-MYB gene family from Arabidopsis thaliana. Plant J 16:263–276

    CAS  PubMed  Google Scholar 

  • Kuwano M, Masumura T, Yoshida KT (2011) A novel endosperm transfer cell-containing region-specific gene and its promoter in rice. Plant Mol Biol 76:47–56

    CAS  PubMed  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and clustal X version 2.0. Bioinformatics 23:2947–2948

    CAS  PubMed  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    CAS  PubMed  Google Scholar 

  • Lin YJ, Zhang QF (2005) Optimising the tissue culture conditions for high efficiency transformation of indica rice. Plant Cell Rep 23:540–547

    CAS  PubMed  Google Scholar 

  • Liu Q, Han R, Wu K, Zhang J, Ye Y, Wang S, Chen J, Pan Y, Li Q, Xu X, Zhou J, Tao D, Wu Y, Fu X (2018) G-protein betagamma subunits determine grain size through interaction with MADS-domain transcription factors in rice. Nat Commun 9:852

    PubMed  PubMed Central  Google Scholar 

  • Lu L, Shao D, Qiu X, Sun L, Yan W, Zhou X, Yang L, He Y, Yu S, Xing Y (2013) Natural variation and artificial selection in four genes determine grain shape in rice. New Phytol 200:1269–1280

    CAS  PubMed  Google Scholar 

  • Ma Z, Zhu P, Shi H, Guo L, Zhang Q, Chen Y, Chen S, Zhang Z, Peng J, Chen J (2019) PTC-bearing mRNA elicits a genetic compensation response via Upf3a and COMPASS components. Nature 568:259–263

    CAS  PubMed  Google Scholar 

  • Mao H, Sun S, Yao J, Wang C, Yu S, Xu C, Li X, Zhang Q (2010) Linking differential domain functions of the GS3 protein to natural variation of grain size in rice. Proc Natl Acad Sci USA 107:19579–19584

    CAS  PubMed  Google Scholar 

  • Nesi N, Jond C, Debeaujon I, Caboche M, Lepiniec L (2001) The Arabidopsis TT2 gene encodes an R2R3 MYB domain protein that acts as a key determinant for proanthocyanidin accumulation in developing seed. Plant Cell 13:2099–2114

    CAS  PubMed  PubMed Central  Google Scholar 

  • Payne CT, Zhang F, Lloyd AM (2000) GL3 encodes a bHLH protein that regulates trichome development in Arabidopsis through interaction with GL1 and TTG1. Genetics 156:1349–1362

    CAS  PubMed  PubMed Central  Google Scholar 

  • Qi P, Lin YS, Song XJ, Shen JB, Huang W, Shan JX, Zhu MZ, Jiang L, Gao JP, Lin HX (2012) The novel quantitative trait locus GL3.1 controls rice grain size and yield by regulating Cyclin-T1;3. Cell Res 22:1666–1680

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ren D, Cui Y, Hu H, Xu Q, Rao Y, Yu X, Zhang Y, Wang Y, Peng Y, Zeng D, Hu J, Zhang G, Gao Z, Zhu L, Chen G, Shen L, Zhang Q, Guo L, Qian Q (2019) AH2 encodes a MYB domain protein that determines hull fate and affects grain yield and quality in rice. Plant J. https://doi.org/10.1111/tpj.14481

    Article  PubMed  PubMed Central  Google Scholar 

  • Rossi A, Kontarakis Z, Gerri C, Nolte H, Holper S, Kruger M, Stainier DY (2015) Genetic compensation induced by deleterious mutations but not gene knockdowns. Nature 524:230–233

    CAS  PubMed  Google Scholar 

  • Song XJ, Kuroha T, Ayano M, Furuta T, Nagai K, Komeda N, Segami S, Miura K, Ogawa D, Kamura T, Suzuki T, Higashiyama T, Yamasaki M, Mori H, Inukai Y, Wu J, Kitano H, Sakakibara H, Jacobsen SE, Ashikari M (2015) Rare allele of a previously unidentified histone H4 acetyltransferase enhances grain weight, yield, and plant biomass in rice. Proc Natl Acad Sci USA 112:76–81

    CAS  PubMed  Google Scholar 

  • Sun S, Wang L, Mao H, Shao L, Li X, Xiao J, Ouyang Y, Zhang Q (2018) A G-protein pathway determines grain size in rice. Nat Commun 9:851

    PubMed  PubMed Central  Google Scholar 

  • Suzuki A, Suzuki T, Tanabe F, Toki S, Washida H, Wu CY, Takaiwa F (1997) Cloning and expression of five myb-related genes from rice seed. Gene 198:393–398

    PubMed  Google Scholar 

  • Todaka D, Nakashima K, Maruyama K, Kidokoro S, Osakabe Y, Ito Y, Matsukura S, Fujita Y, Yoshiwara K, Ohme-Takagi M, Kojima M, Sakakibara H, Shinozaki K, Yamaguchi-Shinozaki K (2012) Rice phytochrome-interacting factor-like protein OsPIL1 functions as a key regulator of internode elongation and induces a morphological response to drought stress. Proc Natl Acad Sci USA 109:15947–15952

    CAS  PubMed  Google Scholar 

  • Wang S, Li S, Liu Q, Wu K, Zhang J, Wang S, Wang Y, Chen X, Zhang Y, Gao C, Wang F, Huang H, Fu X (2015a) The OsSPL16-GW7 regulatory module determines grain shape and simultaneously improves rice yield and grain quality. Nat Genet 47:949–954

    CAS  PubMed  Google Scholar 

  • Wang Y, Xiong G, Hu J, Jiang L, Yu H, Xu J, Fang Y, Zeng L, Xu E, Xu J, Ye W, Meng X, Liu R, Chen H, Jing Y, Wang Y, Zhu X, Li J, Qian Q (2015b) Copy number variation at the GL7 locus contributes to grain size diversity in rice. Nat Genet 47:944–948

    CAS  PubMed  Google Scholar 

  • Wen J, Li Y, Qi T, Gao H, Liu B, Zhang M, Huang H, Song S (2018) The C-terminal domains of Arabidopsis GL3/EGL3/TT8 interact with JAZ proteins and mediate dimeric interactions. Plant Signal Behav 13:e1422460

    PubMed  PubMed Central  Google Scholar 

  • Xia D, Zhou H, Liu R, Dan W, Li P, Wu B, Chen J, Wang L, Gao G, Zhang Q, He Y (2018) GL3.3, a novel QTL encoding a GSK3/SHAGGY-like kinase, epistatically interacts with GS3 to produce extra-long grains in rice. Mol Plant 11:754–756

    CAS  PubMed  Google Scholar 

  • Xu W, Grain D, Bobet S, Le Gourrierec J, Thevenin J, Kelemen Z, Lepiniec L, Dubos C (2014) Complexity and robustness of the flavonoid transcriptional regulatory network revealed by comprehensive analyses of MYB-bHLH-WDR complexes and their targets in Arabidopsis seed. New Phytol 202:132–144

    CAS  PubMed  Google Scholar 

  • Xu WJ, Dubos C, Lepiniec L (2015) Transcriptional control of flavonoid biosynthesis by MYB-bHLH-WDR complexes. Trends Plant Sci 20:176–185

    CAS  PubMed  Google Scholar 

  • Xue WY, Xing YZ, Weng XY, Zhao Y, Tang WJ, Wang L, Zhou HJ, Yu SB, Xu CG, Li XH, Zhang QF (2008) Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat Genet 40:761–767

    CAS  PubMed  Google Scholar 

  • Yang A, Dai XY, Zhang WH (2012) A R2R3-type MYB gene, OsMYB2, is involved in salt, cold, and dehydration tolerance in rice. J Exp Bot 63:2541–2556

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang W, Guo Z, Huang C, Duan L, Chen G, Jiang N, Fang W, Feng H, Xie W, Lian X, Wang G, Luo Q, Zhang Q, Liu Q, Xiong L (2014) Combining high-throughput phenotyping and genome-wide association studies to reveal natural genetic variation in rice. Nat Commun 5:5087

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang XM, Ren YL, Cai Y, Niu M, Feng ZM, Jing RN, Mou CL, Liu X, Xiao LJ, Zhang X, Wu FQ, Guo XP, Jiang L, Wan JM (2018) Overexpression of OsbHLH107, a member of the basic helix-loop-helix transcription factor family, enhances grain size in rice (Oryza sativa L.). Rice (N Y) 11:1–12

    Google Scholar 

  • Ying JZ, Ma M, Bai C, Huang XH, Liu JL, Fan YY, Song XJ (2018) TGW3, a major QTL that negatively modulates grain length and weight in rice. Mol Plant 11:750–753

    CAS  PubMed  Google Scholar 

  • Yu J, Xiong H, Zhu X, Zhang H, Li H, Miao J, Wang W, Tang Z, Zhang Z, Yao G, Zhang Q, Pan Y, Wang X, Rashid MAR, Li J, Gao Y, Li Z, Yang W, Fu X, Li Z (2017) OsLG3 contributing to rice grain length and yield was mined by Ho-LAMap. BMC Biol 15:28

    PubMed  PubMed Central  Google Scholar 

  • Yu J, Miao J, Zhang Z, Xiong H, Zhu X, Sun X, Pan Y, Liang Y, Zhang Q, Abdul Rehman RM, Li J, Zhang H, Li Z (2018) Alternative splicing of OsLG3b controls grain length and yield in japonica rice. Plant Biotechnol J. https://doi.org/10.1111/pbi.12903

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang XJ, Wang JF, Huang J, Lan HX, Wang CL, Yin CF, Wu YY, Tang HJ, Qian Q, Li JY, Zhang HS (2012) Rare allele of OsPPKL1 associated with grain length causes extra-large grain and a significant yield increase in rice. Proc Natl Acad Sci USA 109:21534–21539

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Zhou Y, Li S, Qian Q, Zeng D, Zhang M, Guo L, Liu X, Zhang B, Deng L, Liu X, Luo G, Wang X, Li J (2009) BC10, a DUF266-containing and Golgi-located type II membrane protein, is required for cell-wall biosynthesis in rice (Oryza sativa L.). Plant J 57:446–462

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Mr. JB Wang for his excellent work in the field. This work was supported by grants from the National Natural Science Foundation of China (91935302) and the National Basic Research Program of China (2016YFD0100403).

Author information

Authors and Affiliations

Authors

Contributions

LQP performed most of the experiments, analyzed the data, and wrote the article; LL contributed to sequencing and reviewed the manuscript; LHY, WB, and BXF provided material. ZX, YMQ, and YL contributed to genotyping and data collection the phenotypes; XYZ designed the experiments, supervised and completed the writing, and reviewed the manuscript.

Corresponding author

Correspondence to Yongzhong Xing.

Ethics declarations

Conflict of interest

The authors declare that there are no conflicts of interest in the reported research.

Ethical standards

The authors note that this research was performed and reported in accordance with the ethical standards for scientific conduct.

Additional information

Communicated by Takuji Sasaki.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 1766 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, Q., Lu, L., Liu, H. et al. A minor QTL, SG3, encoding an R2R3-MYB protein, negatively controls grain length in rice. Theor Appl Genet 133, 2387–2399 (2020). https://doi.org/10.1007/s00122-020-03606-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-020-03606-z

Navigation