Abstract
As a staple food for more than half of the world’s population, the importance of rice is self-evident. Compared with ordinary rice, rice cultivars with superior eating quality and appearance quality are more popular with consumers due to their unique taste and ornamental value, even if their price is much higher. Appearance quality and CEQ (cooking and eating quality) are two very important aspects in the evaluation of rice quality. Here, we performed a genome-wide association study on floury endosperm in a diverse panel of 533 cultivated rice accessions. We identified a batch of potential floury genes and prioritize one (LOC_Os03g48060) for functional analyses. Two floury outer endosperm mutants (flo19-1 and flo19-2) were generated through editing LOC_Os03g48060 (named as FLO19 in this study), which encodes a class I glutamine amidotransferase. The different performances of the two mutants in various storage substances directly led to completely different changes in CEQ. The mutation of FLO19 gene caused the damage of carbon and nitrogen metabolism in rice, which affected the normal growth and development of rice, including decreased plant height and yield loss by decreased grain filling rate. Through haplotype analysis, we identified a haplotype of FLO19 that can improve both CEQ and appearance quality of rice, Hap2, which provides a selection target for rice quality improvement, especially for high-yield indica rice varieties.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The variation information of 533 rice accessions can be obtained through the website RiceVarMap (http://ricevarmap.ncpgr.cn/). The phenotypic data of 533 rice accessions can be obtained from the references mentioned in the main text or the Supplementary Data part of this study. For materials, please contact the corresponding author’s email address.
References
Bello B, Hou Y, Zhao J, Jiao G, Wu Y, Li Z, Wang Y, Tong X, Wang W, Yuan W, Wei r, Zhang J (2018) NF‐YB1‐YC12‐bHLH144 complex directly activates Wx to regulate grain quality in rice ( Oryza sativa L.). Plant Biotechnol J. https://doi.org/10.1111/pbi.13048
Beninati S, Piacentini M (2004) The transglutaminase family: an overview. Minireview article. Amino Acids 26:367–372. https://doi.org/10.1007/s00726-004-0091-7
Bhattarai U, Subudhi P (2018) Genetic analysis of yield and agronomic traits under reproductive stage drought stress in rice using a high-resolution linkage map. Gene 669. https://doi.org/10.1016/j.gene.2018.05.086
Büttner K, Hertel T, Pietzsch M (2011) Increased thermostability of microbial transglutaminase by combination of several hot spots evolved by random and saturation mutagenesis. Amino Acids 42:987–996. https://doi.org/10.1007/s00726-011-1015-y
Chen P, Shen Z, Ming L, Li Y, Dan W, Lou G, Peng B, Wu B, Li Y, Zhao D, Gao G, Zhang Q, Xiao J, Li X, Wang G, He Y (2018) Genetic basis of variation in rice seed storage protein (albumin, globulin, prolamin, and glutelin) content revealed by genome-wide association analysis. Front Plant Sci 9. https://doi.org/10.3389/fpls.2018.00612
Fu F, Xue H (2010) Coexpression analysis identifies rice starch regulator1, a rice AP2/EREBP family transcription factor, as a novel rice starch biosynthesis regulator. Plant Physiol 154:927–938. https://doi.org/10.1104/pp.110.159517
Fusi N, Lippert C, Lawrence ND, Stegle O (2014) Warped linear mixed models for the genetic analysis of transformed phenotypes. Nat Commun 5:4890. https://doi.org/10.1038/ncomms5890
Gao Z, Zeng D, Cheng F, Tian Z, Guo L, Su Y, Yan M, Jiang H, Dong G, Huang Y, Han B, Li J, Qian Q (2011) ALK, the key gene for gelatinization temperature, is a modifier gene for gel consistency in rice. J Integr Plant Biol 53(9):756–765. https://doi.org/10.1111/j.1744-7909.2011.01065.x
Gurka M, Edwards L, Muller K, Kupper L (2006) Extending the Box-Cox transformation to the linear mixed model. J Roy Stat Soc Ser A (Stat Soc) 169(2):273–288. https://doi.org/10.1111/j.1467-985X.2005.00391.x
Hori K, Suzuki K, Iijima K, Ebana K (2016) Variation in cooking and eating quality traits in Japanese rice germplasm accessions. Breed Sci 66(2):309–318. https://doi.org/10.1270/jsbbs.66.309
Hori K, Suzuki K, Ishikawa H, Nonoue Y, Nagata K, Fukuoka S, Tanaka J (2021) Genomic regions involved in differences in eating and cooking quality other than Wx and Alk Genes between indica and japonica rice cultivars. Rice (N Y) 14(1):8. https://doi.org/10.1186/s12284-020-00447-8
Hu B, Wei W, Ou S, Tang J, Hua L, Che R, Zhang Z, Chai X, Wang H, Wang Y, Liang C, Liu L, Piao Z, Deng Q, Deng K, Xu C, Liang Y, Zhang L, Li L, Chu C (2015) Variation in NRT1.1B contributes to nitrate-use divergence between rice subspecies. Nat Genet 47:834–838. https://doi.org/10.1038/ng.3337
Hu T, Tian Y, Zhu J, Wang Y, Jing R, Lei J, Sun Y, Yu Y, Li J, Chen X, Zhu X, Hao Y, Liu L, Wang Y, Wan J (2018) OsNDUFA9 encoding a mitochondrial complex I subunit is essential for embryo development and starch synthesis in rice. Plant Cell Rep 37. https://doi.org/10.1007/s00299-018-2338-x
Huang L, Li Q, Zhang C, Chu R, Gu Z, Tan H, Zhao D, Fan X, Liu Q (2020) Creating novel Wx alleles with fine‐tuned amylose levels and improved grain quality in rice by promoter editing using CRISPR/Cas9 system. Plant Biotechnol J 18. https://doi.org/10.1111/pbi.13391
Islam S, Zhang J, Zhao Y, She M, Ma W (2021) Genetic regulation of the traits contributing to wheat nitrogen use efficiency. Plant Sci 303:110759. https://doi.org/10.1016/j.plantsci.2020.110759
Kang H, Sul J, Service S, Zaitlen N, Kong S, Freimer N, Sabatti C, Eskin E (2010) Variance component model to account for sample structure in genome-wide association studies. Nat Genet 42(4):348–354. https://doi.org/10.1038/ng.548
Kang H, Park S, Matsuoka M, An G (2005) White-core endosperm flour endosperm-4 in rice is generated by knockout mutations in the C4-type pyruvate orthophosphate dikinase gene (OsPPDKB). Plant J 42:901–911. https://doi.org/10.1111/j.1365-313X.2005.02423.x
Kashiwagi T, Munakata J (2018) Identification and characteristics of quantitative trait locus for grain protein content, TGP12, in rice (Oryza sativa L.). Euphytica 214. https://doi.org/10.1007/s10681-018-2249-5
Kawakatsu T, Yamamoto M, Touno S, Yasuda H, Takaiwa F (2009) Compensation and interaction between RISBZ1 and RPBF during grain filling in rice. Plant J 59:908–920. https://doi.org/10.1111/j.1365-313X.2009.03925.x
Kieliszek M, Misiewicz A (2014) Microbial transglutaminase and its application in the food industry. A review. Folia Microbiol 241–250. https://doi.org/10.1007/s12223-013-0287-x
Li M, Yeung J, Cherny S, Sham P (2012) Evaluating the effective numbers of independent tests and significant p-value thresholds in commercial genotyping arrays and public imputation reference datasets. Hum Genet 131(5):747–756. https://doi.org/10.1007/s00439-011-1118-2
Li S, Tian Y, Wu K, Ye Y, Yu J, Zhang J, Liu Q, Hu M, Li H, Tong Y, Harberd NP, Fu X (2018) Modulating plant growth-metabolism coordination for sustainable agriculture. Nature 560(7720):595–600. https://doi.org/10.1038/s41586-018-0415-5
Li Y, Fan C, Xing Y, Yun P, Luo L, Yan B, Peng B, Xie W, Wang G, Li X, Xiao J, Xu C, He Y (2014) Chalk5 encodes a vacuolar H+ -translocating pyrophosphatase influencing grain chalkiness in rice. Nat Genet 46:398
Liu F, Ren Y, Wang Y, Cheng P, Zhou K, Lv J, Guo X, Zhang X, Zhong M, Zhao S, Jiang L, Wang H, Bao Y, Wan J (2013) OsVPS9A functions cooperatively with OsRAB5A to regulate post-Golgi dense vesicle-mediated storage protein trafficking to the protein storage vacuole in rice Endosperm Cells. Mol Plant 6. https://doi.org/10.1093/mp/sst081
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(1):852. https://doi.org/10.1038/s41467-018-03047-9
Long W, Dong B, Wang Y, Pan P, Wang Y, Liu L, Chen X, Liu X, Liu S, Tian Y, Chen L, Wan J (2017) FLOURY ENDOSPERM8, encoding the UDP-glucose pyrophosphorylase 1, affects the synthesis and structure of starch in rice endosperm. J Plant Biol 60:513–522. https://doi.org/10.1007/s12374-017-0066-3
Mariotti M, Fongaro L, Catenacci F (2010) Alkali spreading value and image analysis. J Cereal Sci 52(2):227–235. https://doi.org/10.1016/j.jcs.2010.05.011
Martin M, Fitzgerald M (2002) Proteins in rice grains influence cooking properties! J Cereal Sci 36:285–294. https://doi.org/10.1006/jcrs.2001.0465
Nelson O, Pan D (2003) Starch synthesis in Maize endosperms. Annu Rev Plant Physiol Plant Mol Biol 46:475–496. https://doi.org/10.1146/annurev.pp.46.060195.002355
Okadome H (2005) Application of instrument-based multiple texture measurement of cooked milled-rice grains to rice quality evaluation. JARQ 39:261–268. https://doi.org/10.6090/jarq.39.261
Peng B, Kong H, Li Y, Wang L, Zhong M, Sun L, Gao G, Zhang Q, Luo L, Wang G, Xie W, Chen J, Yao W, Peng Y, Lei L, Lian X, Xiao J, Xu C, Li X, He Y (2014) OsAAP6 functions as an important regulator of grain protein content and nutritional quality in rice. Nat Commun 5:4847. https://doi.org/10.1038/ncomms5847
Pietrocola F, Galluzzi L, Bravo San Pedro J, Madeo F, Kroemer G (2015) Acetyl coenzyme A: a central metabolite and second messenger. Cell Metab 21:805–821. https://doi.org/10.1016/j.cmet.2015.05.014
Ren Y, Wang Y, Liu F, Zhou K, Ding Y, Zhou F, Wang Y, Liu K, Gan L, Ma W, Han X, Zhang X, Guo X, Wu F, Cheng Z, Wang J, Lei C, Lin Q, Jiang L, Wan J (2014) GLUTELIN PRECURSOR ACCUMULATION3 encodes a regulator of post-Golgi vesicular traffic essential for vacuolar protein sorting in rice endosperm. Plant Cell 26. https://doi.org/10.1105/tpc.113.121376
Ren Y, Wang Y, Pan T, Wang Y, Wang Y, Gan L, Wei Z, Fan W, Wu M, Jing R, Wang J, Wan G, Bao X, Zhang B, Zhang P, Zhang Y, Ji Y, Lei C, Zhang X, Wan J (2020) GPA5 encodes a Rab5a effector required for post-Golgi trafficking of rice storage proteins. Plant Cell 32. https://doi.org/10.1105/tpc.19.00863
Ryoo N, Yu C, Park C-S, Baik M-Y, Park I, Cho M-H, Bhoo S, An G, Hahn T-R, Jeon J-S (2007) Knockout of a starch synthase gene OsSSIIIa/Flo5 causes white-core floury endosperm in rice (Oryza sativa L.). Plant Cell Rep 26:1083–1095. https://doi.org/10.1007/s00299-007-0309-8
Satoh H, Omura T (1981) New endosperm mutations induced by chemical mutagens in rice Oryza sativa L. Ikushugaku zasshi 31:316–326. https://doi.org/10.1270/jsbbs1951.31.316
Shurubor Y, D’Aurelio M, Clark Matott J, Isakova E, Deryabina Y, Beal M, Cooper A, Krasnikov B (2017) Determination of coenzyme A and acetyl-coenzyme A in biological samples using HPLC with UV detection. Molecules 22:1388. https://doi.org/10.3390/molecules22091388
Sun S, Wei H, Lin H (2006) Identification of QTLs for cooking and eating quality of rice grain. Rice Sci 13:161–169
Tan Y, Li J, Yu S, Xing Y, Xu C, Zhang Q (1999) The three important traits for cooking and eating quality of rice grains are controlled by a single locus in an elite rice hybrid, Shanyou 63. Theor Appl Genet 99:642–648. https://doi.org/10.1007/s001220051279
Tanaka N, Fujita N, Nishi A, Satoh H, Hosaka Y, Ugaki M, Kawasaki S, Nakamura Y (2004) The structure of starch can be manipulated by changing the expression levels of starch branching enzyme IIb in rice endosperm. Plant Biotechnol J 2:507–516. https://doi.org/10.1111/j.1467-7652.2004.00097.x
Teng X, Zhong M, Zhu X, Wang C, Ren Y, Wang Y, Zhang H, Jiang L, Wang D, Hao Y, Wu M, Zhu J, Zhang X, Guo X, Wang Y, Wan J (2019) FLOURY ENDOSPERM16 encoding a NAD-dependent cytosolic malate dehydrogenase plays an important role in starch synthesis and seed development in rice. Plant Biotechnol J 17. https://doi.org/10.1111/pbi.13108
Wang C, Shen L, Fu Y, Yan C, Wang K (2015) A simple CRISPR/Cas9 system for multiplex genome editing in rice. J Genet Genom 42(12):703–706. https://doi.org/10.1016/j.jgg.2015.09.011
Wang J, Xu H, Zhu Y, Liu Q, Cai X (2013) OsbZIP58, a basic leucine zipper transcription factor, regulates starch biosynthesis in rice endosperm. J Exp Bot 64. https://doi.org/10.1093/jxb/ert187
Wang Y, Liu F, Ren Y, Wang Y, Liu X, Long W, Wang D, Zhu J, Zhu X, Jing R, Wu M, Hao Y, Jiang L, Wang C, Wang H, Bao Y, Wan J (2016) GOLGI TRANSPORT 1B regulates protein export from endoplasmic reticulum in rice endosperm cells. Plant Cell 28. https://doi.org/10.1105/tpc.16.00717
Wang Y, Ren Y, Liu X, Jiang L, Chen L, Han X, Jin M, Liu S, Liu F, Lv J, Zhou K, Su N, Bao Y, Wan J (2010) OsRab5a regulates endomembrane organization and storage protein trafficking in rice endosperm cells. Plant J 64:812–824. https://doi.org/10.1111/j.1365-313X.2010.04370.x
Wei X, Jiao G, Lin H, Sheng Z, Shao G, Xie L, Tang S, Xu Q, Hu P (2016) GRAIN INCOMPLETE FILLING 2 regulates grain filling and starch synthesis during rice caryopsis development: GIF2 regulates grain filling and starch synthesis. J Integr Plant Biol 59. https://doi.org/10.1111/jipb.12510
Wu Y, Li G, Zhu Y, Cheng Y, Yang J, Chen H, Song X, Ying J (2020) Genome-wide identification of QTLs for grain protein content based on genotyping-by-resequencing and verification of qGPC1-1 in rice. Inter J Mol Sci 21. https://doi.org/10.3390/ijms21020408
Xie W, Wang G, Yuan M, Yao W, Lyu K, Zhao H, Yang M, Li P, Zhang X, Yuan J, Wang Q, Liu F, Dong H, Zhang L, Li X, Meng X, Zhang W, Xiong L, He Y, Zhang Q (2015) Breeding signatures of rice improvement revealed by a genomic variation map from a large germplasm collection. Proc Natl Acad Sci U S A 112. https://doi.org/10.1073/pnas.1515919112
Xu Y, Lin Q, Li X, Wang F, Chen Z, Wang J, Li W, Fan F, Tao Y, Jiang Y, Wei X, Zhang R, Zhu Q, Bu Q, Yang J, Gao C (2020) Fine‐tuning the amylose content of rice by precise base editing of the Wx gene. Plant Biotechnol J 19. https://doi.org/10.1111/pbi.13433
Xue M, Liu L, Yu Y, Zhu J, Gao H, Wang Y, Wan J (2019) Lose-of-function of a rice nucleolus-localized pentatricopeptide repeat protein is responsible for the floury endosperm14 mutant phenotypes. Rice 12. https://doi.org/10.1186/s12284-019-0359-x
Yang B, Xu S, Xu L, You H, Xiang X (2018) Effects of Wx and its interaction with SSIII-2 on rice eating and cooking qualities. Front Plant Sci 9:456. https://doi.org/10.3389/fpls.2018.00456
Yang M, Kai L, Zhao F, Xie W, Ramakrishna P, Wang G, Du Q, Liang L, Sun C, Zhao H, Zhang Z, Liu Z, Tian J, Huang X, Wang W, Dong H, Hu J, Ming L, Xing Y, Lian X (2018b) Genetic basis of rice ionomic variation revealed by genome-wide association studies. Plant Cell 30:tpc.00375.02018. https://doi.org/10.1105/tpc.18.00375
Yang Y, Guo M, Sun S, Zou Y, Yin S, Liu Y, Tang S, Gu M, Yang Z, Yan C (2019) Natural variation of OsGluA2 is involved in grain protein content regulation in rice. Nat Commun 10:1949. https://doi.org/10.1038/s41467-019-09919-y
Yano K, Yamamoto E, Aya K, Takeuchi H, Lo P, Hu L, Yamasaki M, Yoshida S, Kitano H, Hirano K, Matsuoka M (2016) Genome-wide association study using whole-genome sequencing rapidly identifies new genes influencing agronomic traits in rice. Nat Genet 48. https://doi.org/10.1038/ng.3596
You X, Zhang W, Hu J, Jing R, Cai Y, Feng Z, Kong F, Zhang J, Yan H, Chen W, Xingang C, Ma J, Tang X, Wang P, Zhu S, Liu L, Jiang L, Wan J (2019) FLOURY ENDOSPERM15 encodes a glyoxalase I involved in compound granule formation and starch synthesis in rice endosperm. Plant Cell Rep 38. https://doi.org/10.1007/s00299-019-02370-9
Yu M, Wu M, Ren Y, Wang Y, Li J, Lei C, Sun Y, Bao X, Wu H, Yang H, Pan T, Wang Y, Jing R, Yan M, Zhang H, Zhao L, Zhao Z, Zhang X, Guo X, Wan J (2020) Rice FLOURY ENDOSPERM 18 encodes a pentatricopeptide repeat protein required for 5′ processing of mitochondrial nad5 mRNA and endosperm development. J Integr Plant Biol. https://doi.org/10.1111/jipb.13049
Zeng D, Liu T, Ma X, Wang B, Zheng Z, Zhang Y, Xie X, Yang B, Zhao Z, Zhu Q, Liu Y (2020) Quantitative regulation of Waxy expression by CRISPR/Cas9‐based promoter and 5′UTR‐intron editing improves grain quality in rice. Plant Biotechnol J 18. https://doi.org/10.1111/pbi.13427
Zhang A, Gao Y, Li Y, Ruan B, Yang S, Liu C, Zhang B, Jiang H, Fang G, Ding S, Jahan N, Xie L, Dong G, Xu Z, Gao Z, Guo L, Qian Q (2020a) Genetic analysis for cooking and eating quality of super rice and fine mapping of a novel locus qGC10 for gel consistency. Front Plant Sci 11:342. https://doi.org/10.3389/fpls.2020.00342
Zhang C, Yang Y, Chen S, Liu X, Zhu J, Zhou L, Lu Y, Li Q, Fan X, Tang S, Gu M, Liu Q (2020b) A rare Waxy allele coordinately improves rice eating and cooking quality and grain transparency. J Integr Plant Biol. https://doi.org/10.1111/jipb.13010
Zhang C, Zhu J, Chen S, Fan X, Li Q, Lu Y, Wang M, Yu H, Yi C, Tang S, Gu M, Liu Q (2019) Wxlv, the ancestral allele of rice Waxy gene. Mol Plant 12(8):1157–1166. https://doi.org/10.1016/j.molp.2019.05.011
Zhang L, Qi Y, Wu M, Zhao L, Zhao Z, Lei C, Hao Y, Yu X, Sun Y, Zhang X, Guo X, Ren Y, Wan J (2020c) Mitochondrion-targeted PENTATRICOPEPTIDE REPEAT5 is required for cis-splicing of nad4 intron 3 and endosperm development in rice. Crop J. https://doi.org/10.1016/j.cj.2020.09.002
Zhang L, Ren Y, Lu B, Yang C, Feng Z, Liu Z, Chen J, Ma W, Wang Y, Yu X, Wang Y, Zhang W, Wang Y, Liu S, Wu F, Zhang X, Guo X, Bao Y, Jiang L, Wan J (2015) FLOURY ENDOSPERM7 encodes a regulator of starch synthesis and amyloplast development essential for peripheral endosperm development in rice. J Exp Bot 67. https://doi.org/10.1093/jxb/erv469
Zhao K, Tung C, Eizenga G, Wright M, Ali M, Price A, Norton G, Islam M, Reynolds A, Mezey J, McClung A, Bustamante C, McCouch S (2011) Genome-wide association mapping reveals a rich genetic architecture of complex traits in Oryza sativa. Nat Commun 2:467. https://doi.org/10.1038/ncomms1467
Zhou H, Li P, Xie W, Hussain S, Li Y, Xia D, Zhao H, Shengyuan S, Chen J, Ye H, Hou J, Zhao D, Gao G, Zhang Q, Wang G, Lian X, Xiao J, Yu S, Li X, He Y (2017) Genome-wide association analyses reveal the genetic basis of stigma exsertion in rice. Mol Plant 10. https://doi.org/10.1016/j.molp.2017.01.001
Zhou H, Xia D, Zhao D, Li Y, Li P, Wu B, Gao G, Zhang Q, Wang G, Xiao J, Li X, Yu S, Lian X, He Y (2020) The origin of Wxla provides new insights into the improvement of grain quality in rice. J Integr Plant Biol. https://doi.org/10.1111/jipb.13011
Zhu H, Kranz R (2012) A nitrogen-regulated glutamine amidotransferase (GAT1_2.1) represses shoot branching in Arabidopsis. Plant Physiol 160. https://doi.org/10.1104/pp.112.199364
Funding
This work was supported by grants from the National Natural Science Foundation of China (91435202, 31821005, 31901533) and earmarked fund for Agriculture Research System (CARS-01–03) in China.
Author information
Authors and Affiliations
Contributions
Guangming Lou and Pingli Chen performed most of the experiments; Jiawang Xiong, Shanshan Wan, Yuanyuan Zheng, Mufid Alam, Rongjia Liu, Yin Zhou, Hanyuan Yang, Yahong Tian, Jingjing Bai, Wenting Rao, Xuan Tan, and Haozhou Gao participated in part of phenotyping, genotyping, and biochemical experiments; Guangming Lou, Pingli Chen, and Hao Zhou performed various data analysis; Guanjun Gao and Qinglu Zhang participated in partial field experiments. Hao Zhou and Yanhua Li provided guidance for the determination of partial quality traits. Guangming Lou, Pingli Chen, and Yuqing He designed experiments. Guangming Lou wrote the manuscript and Pingbo Li improved it. All authors discussed and commented on the manuscript.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Lou, G., Chen, P., Zhou, H. et al. FLOURY ENDOSPERM19 encoding a class I glutamine amidotransferase affects grain quality in rice. Mol Breeding 41, 36 (2021). https://doi.org/10.1007/s11032-021-01226-z
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11032-021-01226-z