A quantitative trait locus GW6 controls rice grain size and yield through the gibberellin pathway.
Oryza sativa
cell expansion
domestication
gibberellin biosynthesis
grain size
quantitative trait locus
rice yield
Journal
The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397
Informations de publication
Date de publication:
08 2020
08 2020
Historique:
received:
16
01
2020
revised:
14
04
2020
accepted:
22
04
2020
pubmed:
5
5
2020
medline:
2
3
2021
entrez:
5
5
2020
Statut:
ppublish
Résumé
Grain size is one of the essential components determining rice yield and is a target for both domestication and artificial breeding. Gibberellins (GAs) are diterpenoid phytohormones that influence diverse aspects of plant growth and development. Several quantitative trait loci (QTLs) have been identified that control grain size through phytohormone regulation. However, little is known about the role of GAs in the control of grain size. Here we report the cloning and characterization of a QTL, GW6 (GRAIN WIDTH 6), which encodes a GA-regulated GAST family protein and positively regulates grain width and weight. GW6 is highly expressed in the young panicle and increases grain width by promoting cell expansion in the spikelet hull. Knockout of GW6 exhibits reduced grain size and weight, whereas overexpression of GW6 results in increased grain size and weight. GW6 is induced by GA and its knockout downregulates the expression of GA biosynthesis genes and decreases GA content in the young panicle. We found that a natural variation in the cis element CAAT-box in the promoter of GW6 is associated with its expression level and grain width and weight. Furthermore, introduction of GW6 to Oryza indica variety HJX74 can lead to a 10.44% increase in rice grain yield, indicating that GW6 has great potential to improve grain yield in rice.
Substances chimiques
Gibberellins
0
Plant Growth Regulators
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1174-1188Informations de copyright
© 2020 Society for Experimental Biology and John Wiley & Sons Ltd.
Références
Daviere, J.M. and Achard, P. (2013) Gibberellin signaling in plants. Development, 140, 1147-1151.
de Lucas, M., Daviere, J.M., Rodriguez-Falcon, M., Pontin, M., Iglesias-Pedraz, J.M., Lorrain, S., Fankhauser, C., Blazquez, M.A., Titarenko, E. and Prat, S. (2008) A molecular framework for light and gibberellin control of cell elongation. Nature, 451, 480-484.
Fan, C., Xing, Y., Mao, H., Lu, T., Han, B., Xu, C., Li, X. and 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.
Furukawa, T., Sakaguchi, N. and Shimada, H. (2006) Two OsGASR genes, rice GAST homologue genes that are abundant in proliferating tissues, show different expression patterns in developing panicles. Genes Genet Syst. 81, 171-180.
Gao, X., Zhang, J.Q., Zhang, X. et al. (2019) Rice qGL3/OsPPKL1 Functions with the GSK3/SHAGGY-Like Kinase OsGSK3 to Modulate Brassinosteroid Signaling. Plant Cell, 31, 1077-1093.
Guo, T., Chen, K., Dong, N.Q., Shi, C.L., Ye, W.W., Gao, J.P., Shan, J.X. and Lin, H.X. (2018) GRAIN SIZE AND NUMBER1 negatively regulates the OsMKKK10-OsMKK4-OsMPK6 cascade to coordinate the trade-off between grain number per panicle and grain size in rice. Plant Cell, 30, 871-888.
Guo, T., Chen, K., Dong, N.Q., Ye, W.W., Shan, J.X. and Lin, H.X. (2020) Tillering and small grain 1 dominates the tryptophan aminotransferase family required for local auxin biosynthesis in rice. J. Integr. Plant Biol. 62, 581-600.
Hedden, P. and Sponsel, V. (2015) A century of gibberellin research. J. Plant Growth Regul. 34, 740-760.
Hu, J., Wang, Y., Fang, Y. et al. (2015) A rare allele of GS2 enhances grain size and grain yield in rice. Mol. Plant, 8, 1455-1465.
Hu, Z., Lu, S.J., Wang, M.J. et al. (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.
Huo, X., Wu, S., Zhu, Z. et al. (2017) NOG1 increases grain production in rice. Nat. Commun. 8, 1497.
Ikeda, A., Ueguchi-Tanaka, M., Sonoda, Y., Kitano, H., Koshioka, M., Futsuhara, Y., Matsuoka, M. and Yamaguchi, J. (2001) slender rice, a constitutive gibberellin response mutant, is caused by a null mutation of the SLR1 gene, an ortholog of the height-regulating gene GAI/RGA/RHT/D8. Plant Cell, 13, 999-1010.
International Rice Genome Sequencing, P. (2005) The map-based sequence of the rice genome. Nature, 436, 793-800.
Ishimaru, K., Hirotsu, N., Madoka, Y. et al. (2013) Loss of function of the IAA-glucose hydrolase gene TGW6 enhances rice grain weight and increases yield. Nat. Genet., 45, 707-711.
Kumar, A., Singh, A., Kumar, P. and Sarkar, A.K. (2019) Giberellic acid-stimulated transcript proteins evolved through successive conjugation of novel motifs and their subfunctionalization. Plant Physiol. 180, 998-1012.
Kuroha, T., Nagai, K., Gamuyao, R. et al. (2018) Ethylene-gibberellin signaling underlies adaptation of rice to periodic flooding. Science, 361, 181-186.
Kwon, C.T. and Paek, N.C. (2016) Gibberellic acid: a key phytohormone for spikelet fertility in rice grain production. Int. J. Mol. Sci. 17(5), 794.
Li, N. and Li, Y. (2016) Signaling pathways of seed size control in plants. Curr. Opin. Plant Biol. 33, 23-32.
Li, N., Xu, R. and Li, Y. (2019a) Molecular networks of seed size control in plants. Annu. Rev. Plant Biol. 70, 435-463.
Li, X., Shi, S., Tao, Q., Tao, Y., Miao, J., Peng, X., Li, C., Yang, Z., Zhou, Y. and Liang, G. (2019b) OsGASR9 positively regulates grain size and yield in rice (Oryza sativa). Plant Sci. 286, 17-27.
Li, Y., Fan, C., Xing, Y. et al. (2011) Natural variation in GS5 plays an important role in regulating grain size and yield in rice. Nat. Genet. 43, 1266-1269.
Liu, J., Chen, J., Zheng, X. et al. (2017) GW5 acts in the brassinosteroid signalling pathway to regulate grain width and weight in rice. Nat. Plants, 3, 17043.
Liu, L., Tong, H., Xiao, Y., Che, R., Xu, F., Hu, B., Liang, C., Chu, J., Li, J. and Chu, C. (2015) Activation of Big Grain1 significantly improves grain size by regulating auxin transport in rice. Proc. Natl. Acad. Sci. U S A, 112, 11102-11107.
Ma, X., Zhang, Q., Zhu, Q. et al. (2015) A robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants. Mol. Plant, 8, 1274-1284.
Maity, S.N. and de Crombrugghe, B. (1998) Role of the CCAAT-binding protein CBF/NF-Y in transcription. Trends Biochem. Sci. 23, 174-178.
Maity, S.N., Golumbek, P.T., Karsenty, G. and de Crombrugghe, B. (1988) Selective activation of transcription by a novel CCAAT binding factor. Science, 241, 582-585.
Mao, H., Sun, S., Yao, J., Wang, C., Yu, S., Xu, C., Li, X. and 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.
Porto, W.F. and Franco, O.L. (2013) Theoretical structural insights into the snakin/GASA family. Peptides, 44, 163-167.
Qi, P., Lin, Y.S., Song, X.J., Shen, J.B., Huang, W., Shan, J.X., Zhu, M.Z., Jiang, L., Gao, J.P. and Lin, H.X. (2012) The novel quantitative trait locus GL3.1 controls rice grain size and yield by regulating Cyclin-T1;3. Cell Res, 22, 1666-1680.
Roxrud, I., Lid, S.E., Fletcher, J.C., Schmidt, E.D. and Opsahl-Sorteberg, H.G. (2007) GASA4, one of the 14-member Arabidopsis GASA family of small polypeptides, regulates flowering and seed development. Plant Cell Physiol. 48, 471-483.
Rubinovich, L., Ruthstein, S. and Weiss, D. (2014) The Arabidopsis cysteine-rich GASA5 is a redox-active metalloprotein that suppresses gibberellin responses. Mol. Plant, 7, 244-247.
Sasaki, A., Ashikari, M., Ueguchi-Tanaka, M. et al. (2002) Green revolution: a mutant gibberellin-synthesis gene in rice. Nature, 416, 701-702.
Shi, L., Gast, R.T., Gopalraj, M. and Olszewski, N.E. (1992) Characterization of a shoot-specific, GA3- and ABA-regulated gene from tomato. Plant J. 2, 153-159.
Si, L., Chen, J., Huang, X. et al. (2016) OsSPL13 controls grain size in cultivated rice. Nat. Genet. 48, 447-456.
Song, X.J., Huang, W., Shi, M., Zhu, M.Z. and Lin, H.X. (2007) A QTL for rice grain width and weight encodes a previously unknown RING-type E3 ubiquitin ligase. Nat. Genet. 39, 623-630.
Song, X.J., Kuroha, T., Ayano, M. et al. (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.
Wang, L., Wang, Z., Xu, Y., Joo, S.H., Kim, S.K., Xue, Z., Xu, Z., Wang, Z. and Chong, K. (2009) OsGSR1 is involved in crosstalk between gibberellins and brassinosteroids in rice. Plant J. 57, 498-510.
Wang, S., Li, S., Liu, Q. et al. (2015a) The OsSPL16-GW7 regulatory module determines grain shape and simultaneously improves rice yield and grain quality. Nat. Genet. 47, 949-954.
Wang, S., Wu, K., Yuan, Q. et al. (2012) Control of grain size, shape and quality by OsSPL16 in rice. Nat. Genet. 44, 950-954.
Wang, W., Mauleon, R., Hu, Z. et al. (2018) Genomic variation in 3,010 diverse accessions of Asian cultivated rice. Nature, 557, 43-49.
Wang, Y., Xiong, G., Hu, J. et al. (2015b) Copy number variation at the GL7 locus contributes to grain size diversity in rice. Nat. Genet. 47, 944-948.
Wang, Y., Zhao, J., Lu, W. and Deng, D. (2017) Gibberellin in plant height control: old player, new story. Plant Cell Rep. 36, 391-398.
Wu, Y., Wang, Y., Mi, X.F., Shan, J.X., Li, X.M., Xu, J.L. and Lin, H.X. (2016) The QTL GNP1 encodes GA20ox1, which increases grain number and yield by increasing Cytokinin activity in rice panicle meristems. PLoS Genet. 12, e1006386.
Xu, C., Liu, Y., Li, Y., Xu, X., Xu, C., Li, X., Xiao, J. and Zhang, Q. (2015) Differential expression of GS5 regulates grain size in rice. J. Exp. Bot. 66, 2611-2623.
Zhang, L., Yu, H., Ma, B. et al. (2017) A natural tandem array alleviates epigenetic repression of IPA1 and leads to superior yielding rice. Nat. Commun. 8, 14789.
Zhang, S., Yang, C., Peng, J., Sun, S. and Wang, X. (2009) GASA5, a regulator of flowering time and stem growth in Arabidopsis thaliana. Plant Mol. Biol. 69, 745-759.
Zhang, X., Wang, J., Huang, J. et al. (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.
Zhao, Q., Feng, Q., Lu, H. et al. (2018) Pan-genome analysis highlights the extent of genomic variation in cultivated and wild rice. Nat. Genet. 50, 278-284.