Abstract
Members of the permease gene family are responsible for important biological functions in the growth and development of rice. Here, we show that OsAAP8 is a constitutive expression gene, and its translated protein is localized on the cell membrane. Mutation of the OsAAP8 can promote the expression of genes related to protein and amylopectin synthesis, and also promote the enlargement of protein bodies in its endosperm, leading to an increase in the protein, amylopectin, and total amino acid content of grains in OsAAP8 mutants. Seeds produced by the OsAAP8 mutant were larger, and the chalkiness traits of the OsAAP8 mutants were significantly reduced, thereby improving the nutritional quality and appearance of rice grains. The OsAAP8 protein is involved in the transport of various amino acids; OsAAP8 mutation significantly enhanced the root absorption of a range of amino acids and might affect the distribution of various amino acids. Therefore, OsAAP8 is an important quality trait gene with multiple biological functions, which provides important clues for the molecular design of breeding strategies for developing new high-quality varieties of rice.
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References
Alam M, Tan X, Zhang H, Lou G, Yang H, Zhou Y, Hussain A, Bhantana P, Jiang G, He Y (2023) QTL Mining and validation of grain nutritional quality characters in rice (Oryza sativa L.) using two introgression line populations. Agriculture 13(9):1725. https://doi.org/10.3390/agriculture.13091725
Cai Y, Li S, Jiao G, Sheng Z, Wu Y, Shao G, Xie L, Peng C, Xu J, Tang S, Wei X, Hu P (2018) OsPK2 encodes a plastidic pyruvate kinase involved in rice endosperm starch synthesis, compound granule formation and grain filling. Plant Biotechnol J 16(11):1878–1891. https://doi.org/10.1111/pbi.12923
Chen C, Huang J, Zhu L, Shah F, Nie L, Cui K, Peng S (2013) Varietal difference in the response of rice chalkiness to temperature during ripening phase across different sowing dates. Field Crop Res 151:85–91. https://doi.org/10.1016/j.fcr.2013.07.016
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 9:612. https://doi.org/10.3389/fpls.2018.00612
Chen P, Lou G, Wang Y, Chen J, Chen W, Fan Z, Liu Q, Sun B, Mao X, Yu H, Jiang L, Zhang J, Lv S, Xing J, Pan D, Li C, He Y (2022) The genetic basis of grain protein content in rice by genome-wide association analysis. Mol Breed 43:1. https://doi.org/10.1007/s11032-022-01347-z
Fang Z, Wu BW, Ji Y (2021) The amino acid transporter OsAAP4 contributes to rice tillering and grain yield by regulating neutral amino acid allocation through two splicing variants. Rice 14(1):2. https://doi.org/10.1186/s12284-020-00446-9
Gao Y, Liu C, Li Y, Zhang A, Dong G, Xie L, Zhang B, Ruan B, Hong K, Xue D, Zeng D, Guo L, Qian Q, Gao Z (2016) QTL analysis for chalkiness of rice and fine mapping of a candidate gene for qACE9. Rice 9:41. https://doi.org/10.1186/s12284-016-0114-5
Guo T, Liu X, Wan X, Weng J, Liu S, Liu X, Chen M, Li J, Su N, Wu F, Cheng Z, Guo X, Lei C, Wang J, Jiang L, Wan J (2011) Identification of a stable quantitative trait locus for percentage grains with white chalkiness in rice (Oryza sativa). J Integr Plant Biol 53(8):598–607. https://doi.org/10.1111/j.1744-7909.2011.01041.x
Ji Y, Huang W, Wu B, Fang Z, Wang X (2020) The amino acid transporter AAP1 mediates growth and grain yield by regulating neutral amino acid uptake and reallocation in Oryza sativa. J Exp Bot 71(16):4763–4777. https://doi.org/10.1093/jxb/eraa256
Kong D, Peng B, Peng Y, Song X, Peng J, Huang C, Wang Y, Li J, Sun Y, Pang R (2018) Effect of sowing date on grain endosperm chalkiness of different rice varieties. J Plant Sci 6(2):41–51. https://doi.org/10.11648/J.JPS.20180602.12
Kusano M, Yang Z, Okazaki Y, Nakabayashi R, Fukushima A, Saito K (2015) Using metabolomic approaches to explore chemical diversity in rice. Mol Plant 8(1):58–67. https://doi.org/10.1016/j.molp.2014.11.010
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(4):398–404. https://doi.org/10.1038/ng.2923
Li S, Lin D, Zhang Y, Deng M, Chen Y, Lv B, Li B, Lei Y, Wang Y, Zhao L, Liang Y, Liu J, Chen K, Liu Z, Xiao J, Qiu J, Gao C (2022) Genome-edited powdery mildew resistance in wheat without growth penalties. Nature 602(7897):455–460. https://doi.org/10.1038/s41586-022-04395-9
Liu H, Zhang X, Huang W, Zhang Y, Zhao H (2018) Advances in research on plant amino acid transporters. Plant Sci J 36(4):9. https://doi.org/10.11913/PSJ.2095-0837.2018.40623
Liu Y, Li Y, Peng Y, Ma S, Yan S (2021) A feasibility quantitative analysis of free fatty acids in polished rice by fourier transform near-infrared spectroscopy and chemometrics. J Food Sci 86(8):3434–3446. https://doi.org/10.1111/1750-3841.15809
Lou G, Bhat M, Tan X, Wang Y, He Y (2023) Research progress on the relationship between rice protein content and cooking and eating quality and its influencing factors. Seed Biol 2:16. https://doi.org/10.48130/SeedBio-2023-0016
Lu Y, Song Z, Kai L, Lian X, Cai H (2012) Molecular characterization, expression and functional analysis of the amino acid transporter gene family (OsAATs) in rice. Acta Physiol Plant 34(5):1943–1962. https://doi.org/10.1007/s11738-012-0995-x
Peng B, Kong H, Li Y, 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 (2014a) 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
Peng B, Wang L, Fan C, Jiang G, Luo L, Li Y, He Y (2014b) Comparative mapping of chalkiness components in rice using five populations across two environments. BMC Genet 15:49. https://doi.org/10.1186/1471-2156-15-49
Peng B, Zuo Y, Tang J, Zhang G, Kong D (2017) Application of modern technologies in rice (Oryza sativa) quality improvement. J Agr Biotech 25(12):2027–2037. https://doi.org/10.3969/j.issn.1674-7968,2017.12.013
Peng B, Li J, Kong D, He L, Li M, Nassirou T, Peng Y, Song X, Peng J, Jiang Y (2018) Genetic improvement of grain quality promoted by high and new technology in rice. J Agr Sci 11(1):81–94. https://doi.org/10.5539/JAS.V11N1P81
Peng B, Sun X, Tian X, Kong D, He L, Peng J, Liu Y, Guo G, Sun Y, Pang R, Zhou W, Zhao J, Wang Q (2023) OsNAC74 affects grain protein content and various biological traits by regulating OsAAP6 expression in rice. Mol Breeding 43:87. https://doi.org/10.1007/s11032-023-01387-z
Ren D, Ding C, Qian Q (2023) Molecular bases of rice grain size and quality for optimized productivity. Sci Bull 68(3):314–314. https://doi.org/10.1016/j.scib.2023.01.026
Sanders A, Collier R, Trethewy A, Tegeder M (2009) AAP1 regulates import of amino acids into developing Arabidopsis embryos. Plant J 59(4):540–552. https://doi.org/10.1111/j.1365-313X.2009.03890.x
Santiago J, Tegeder M (2016) Connecting source with sink: the role of Arabidopsis AAP8 in phloem loading of amino acids. Plant Physiol 171(1):508. https://doi.org/10.1104/pp.16.00244
Schmidt R, Stransky H, Koch W (2007) The amino acid permease AAP8 is important for early seed development in Arabidopsis thaliana. Planta 226(4):805–813. https://doi.org/10.1007/s00425-007-0527-x
Su Y, Xiao L (2020) 3D visualization and volume-based quantification of rice chalkiness in vivo by using high resolution micro-CT. Rice 13(1):69. https://doi.org/10.21203/rs.2.21396/v1
Taylor M, Reinders A, Ward J (2015) Transport function of rice amino acid permeases (AAPs). Plant Cell Physiol 56(7):1355. https://doi.org/10.1093/pcp/pcv053
Tegeder M, Ward J (2012) Molecular evolution of plant AAP and LHT amino acid transporters. Front Plant Sci 3:21. https://doi.org/10.3389/fpls.2012.00021
Wang E, Wang J, Zhu X, Hao W, Wang L, Li Q, Zhang L, He W, Lu B, Lin H, Ma H, Zhang G, He Z (2008) Control of rice grain-filling and yield by a gene with a potential signature of domestication. Nat Genet 40(11):1370–1374. https://doi.org/10.1038/ng.220
Wang S, Li S, Liu Q, Zhang J, Wang S, Wang Y, Chen X, Zhang Y, Gao C (2015) The OsSPL16-GW7 regulatory module determines grain shape and simultaneously improves rice yield and grain quality. Nat Genet 47(8):949–954. https://doi.org/10.1038/ng.3352
Wang J, Wu B, Lu K, Wei Q, Qian J, Chen Y, Fang Z (2019) The amino acid permease 5 (OsAAP5) regulates tiller number and grain yield in rice. Plant Physiol 180(2):1031–1045. https://doi.org/10.1104/pp.19.00034
Wang S, Yang Y, Guo M, Zhong C, Sun S (2020) Targeted mutagenesis of amino acid transporter genes for rice quality improvement using the CRISPR/Cas9 system. Crop J 8(3):457–464. https://doi.org/10.1016/j.cj.2020.02.005
Wang T, Li Y, Huang Y, Zhao X, Dong Z, Jin W (2022) Huang W (2022) Amino acid permease 6 regulates grain protein content in maize. Crop J 10(6):1536–1544. https://doi.org/10.1016/j.cj.2022.03.007
Wang Q, Chen P, Wang H, Chao S, Guo W, Zhang Y, Miao C, Yuan H, Peng B (2023) Physiological and transcriptomic analysis of OsLHCB3 knockdown lines in rice. Mol Breed 43:38. https://doi.org/10.1007/s11032-023-01387-z
Wu B, Yun P, Zhou H, Xia D, Gu Y, Li P, Yao J, Zhou Z, Chen J, Liu R, Cheng S, Zhang H, Zheng Y, Lou G, Chen P, Wan S, Zhou M, Li Y, Gao G, Zhang Q, Li X, Lian X, He Y (2022) Natural variation in WHITE-CORE RATE 1 regulates redox homeostasis in rice endosperm to affect grain quality. Plant Cell 5:5. https://doi.org/10.1093/plcell/koac057
Xia D, Wang Y, Shi Q, Wu B, Yu X, Zhang C, Li Y, Fu P, Li M, Zhang Q, Liu Q, Gao G, Zhou H, He Y (2022) Effects of Wx genotype, nitrogen fertilization, and temperature on rice grain quality. Front Plant Sci 13(3):901541. https://doi.org/10.3389/fpls.2022.901541
Xu Y, Lin Q, Li X, Chen Z, Wang J, Li W, Fan F, Tao Y, Jiang Y (2021) Fine-tuning the amylose content of rice by precise base editing of the Wx gene. Plant Biotechnol J 19(1):11–13. https://doi.org/10.1111/pbi.13433
Yang Y, Shen Z, Li Y, Xu C, Xia H, Zhuang H, Sun S, Guo M, Yan C (2022) Rapid improvement of rice eating and cooking quality through gene editing toward glutelin as target. J Integr Plant Biol 64(10):1860–1865. https://doi.org/10.1111/jipb.13334
Yang X, Yang G, Wei X, Huang W, Fang Z (2023a) OsAAP15, an amino acid transporter in response to nitrogen concentration, mediates panicle branching and grain yield in rice. Plant Sci 330:111640. https://doi.org/10.1016/j.plantsci.2023.111640
Yang Y, Zhang Y, Sun Z, Shen Z, Li Y, Guo Y, Feng Y, Sun S, Guo M, Hu Z (2023b) Knocking out OsAAP11 to improve rice grain quality using CRISPR/Cas9 system. Int J Mol Sci 24:14360. https://doi.org/10.3390/ijms241814360
Yao X, Nie J, Bai R, Sui X (2020) Amino acid transporters in plants: identification and function. Plants 9(8):972. https://doi.org/10.3390/plants9080972
Yue H, Zhong M, Chong X (2023) Summary of the influencing factors of RVA spectrum characteristics and their relationship with rice taste quality. Jiangsu Agr Sci 51(1):16–22. https://doi.org/10.15889/j.issn.1002-1302.2023.01.003
Zhang Y, Mu H, Shao Z, Wang Y, Jing L, Wang Y, Yang L (2019) Effects of ozone stress on amylose content and starch RVA profile in grains located at different positions on a panicle. J Appl Ecol 30(12):4211–4221. https://doi.org/10.13287/j.1001-9332.201912.028
Zhao H, Ma H, Li Y, Xin W, Jie Z (2012) Genome-wide survey and expression analysis of amino acid transporter gene family in rice (Oryza sativa L.). PLoS One 7(11):e49210. https://doi.org/10.1371/journal.pone.0049210
Zhao M, Lin Y, Chen H (2020) Improving nutritional quality of rice for human health. Theor Appl Genet 133(5):1397–1413. https://doi.org/10.1007/s00122-019-03530-x
Zhou L, Chen L, Jiang L, Zhang W, Liu L, Liu X, Zhao Z, Liu S, Zhang L, Wang J, Wan J (2009) Fine mapping of the grain chalkiness QTL qPGWC-7 in rice (Oryza sativa L.). Theor Appl Genet 118(3):581–590. https://doi.org/10.1007/s00122-008-0922-0
Zhou H, Xia D, He Y (2020a) Rice grain quality-traditional traits for high quality rice and health-plus substances. Mol Breed 40:1. https://doi.org/10.1007/s11032-019-1080-6
Zhou H, Xia D, Li P, Ao Y, Xu X, Wan S, Li Y, Wu B, Shi H, Wang K, Gao G, Zhang Q, Wang G, Xiao J, Li X, Yu S, Lian X, He Y (2020b) Genetic architecture and key genes controlling the diversity of oil composition in rice grain. Mol Plant 14(3):456–469. https://doi.org/10.1016/j.molp.2020.12.001
Zhu Y (2022) Advances in CRISPR/Cas9. BioMed Res Int 8:9978571. https://doi.org/10.1155/2022/9978571
Zhu A, Zhang Y, Zhang Z, Wang B, Xue P, Cao Y, Chen Y, Li Z, Liu Q, Cheng S, Cao L (2018) Genetic dissection of for a quantitative trait locus for percentage of chalky grain in rice (Oryza sativa L.). Front Plant Sci 10(9):1173. https://doi.org/10.3389/fpls.2018.01173
Acknowledgements
This work was financially supported by National Natural Science Foundation of China (U2004141, 31801332; 12305399), Key Project of Science and Technology in Henan Province (222102110141; 222102110115; 212102110249), Key R&D and Promotion Project of Xinyang-Science and Technology Research Project (20230025), Graduate Research Innovation Fund Project of XYNU (2022KYJJ066, 2022KYJJ068), and Nanhu Scholars Program for Young Scholars of XYNU.
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Bo Peng and Quanxiu Wang designed the experiments. Bo Peng, Qingxi Zhang, Yan Liu, Xiaoyu Sun and Xiayu Tian carried out most of the experiments and analyzed the data. Qiang Zhao, Zhiguo Zhang, Yaqin Huang and Juan Peng contributed to the experiments and formal analysis. Yanfang Sun, Xiaohua Song and Guiying Guo contributed to the experiments. Jinhui Zhao, Ruihua Pang and Wei Zhou contributed to the experiments and analyzed the data. Bo Peng and Quanxiu Wang wrote the manuscript.
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Peng, B., Zhang, Q., Liu, Y. et al. OsAAP8 mutation leads to significant improvement in the nutritional quality and appearance of rice grains. Mol Breeding 44, 34 (2024). https://doi.org/10.1007/s11032-024-01473-w
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DOI: https://doi.org/10.1007/s11032-024-01473-w