Prospects for the Application of Gene Editing and Genomic Selection in Rice Breeding

doi:10.16819/j.1001-7216.2024.230503

Abstract

Abstract:

Rice is the main grain crop in China. Due to large population and limited land resources in China, rice breeding goals have long been yield oriented. Chinese researchers have continuously achieved breakthroughs in rice breeding technology, and the adoption of dwarf breeding and hybrid rice breeding technology has resulted in two significant leaps in rice yield in China. However, with the improvement of living standards and the increasing frequency of extreme weather events, higher demands have been placed on rice in terms of yield, quality, and resistance. At present, biotechnology is undergoing constant innovation, particularly with the rapid development of gene editing and genomic selection breeding technology. This progress is expected to provide robust support for the development of new rice varieties with high yield, superior quality, and resistance to multiple factors. It helps promote the green and sustainable development of rice production. This paper reviews the recent advancements in gene editing technology and genomic selection technology in rice breeding for high yield, superior quality, disease and insect resistance, stress tolerance, and heterosis. The goal is to provide breeding strategies for the efficient development of new varieties to meet demands.

Key words: rice, breeding techniques, gene editing, genomic selection

摘要：

水稻是我国主要的粮食作物。由于我国人多地少的现状，长期以来水稻的育种目标是以产量为导向。我国科研人员通过协同攻关实现了水稻育种技术突破，矮化育种和杂交水稻育种技术的利用促进了水稻产量两次大的飞跃。随着我国消费者生活水平的提高以及极端天气出现的频次上升，水稻育种对品质、抗性与耐逆等也提出了更高要求。目前，生物技术正在不断革新，特别是基因编辑和全基因组选择育种技术的迅速发展，为高产优质多抗耐逆的水稻新品种选育提供强有力支持，推动着我国水稻生产向绿色可持续发展。本文就基因编辑技术和全基因组选择技术在水稻高产优质、抗病虫、耐逆及杂种优势育种应用中的新进展进行简述，旨在为高效培育能够满足市场需求的水稻新品种提供一些育种思路。

关键词: 水稻, 育种技术, 基因编辑, 全基因组选择

LIANG Chuyan, WU Mingming, HUANG Fengming, ZHAI Rongrong, YE Jing, ZHU Guofu, YU Faming, ZHANG Xiaoming, YE Shenghai. Prospects for the Application of Gene Editing and Genomic Selection in Rice Breeding[J]. Chinese Journal OF Rice Science, 2024, 38(1): 1-12.

梁楚炎, 巫明明, 黄凤明, 翟荣荣, 叶靖, 朱国富, 俞法明, 张小明, 叶胜海. 基因编辑及全基因组选择技术在水稻育种中的应用展望[J]. 中国水稻科学, 2024, 38(1): 1-12.

Figures/Tables 2

References 78

[1]	刘定富, 尹合兴, 应继锋. 中国水稻百年育种的一些关键基因[J]. 中国稻米, 2022, 28(2): 1-11.
	Liu D G, Yi H X, Ying J F. Key genes century rice breeding in China[J]. China Rice, 2022, 28(2): 1-11. (in Chinese with English abstract)
[2]	Liao C, Yan W, Chen Z, Xie G, Deng X W, Tang X. Innovation and development of the third-generation hybrid rice technology[J]. The Crop Journal, 2021, 9(3): 693-701.
[3]	刘定富, 应继锋. 杂交水稻育种的新赛道[J]. 中国种业, 2022(2): 13-18.
	Liu D F, Ying J F. A new track for hybrid rice breeding[J]. China Seed Industry, 2022(2): 13-18. (in Chinese with English abstract)
[4]	Wen L X, Zhou F, Zou Y L. The research progress on herbicide resistant transgenic rice development[J]. Journal of Plant Protection, 2018, 45(5): 954-960.
[5]	Zhu Q L, Yu S Z, Zeng D C, Liu H M, Wang H, Yang Z F, Xie X R, Shen R X, Tan J T, Li H Y, Zhao X C, Zhang Q Y, Chen Y L, Guo J X, Chen L T, Liu Y G. Development of “purple endosperm rice” by engineering anthocyanin biosynthesis in the endosperm with a high-efficiency transgene stacking system[J]. Molecular Plant, 2017, 10(7): 918-929.
[6]	Zhou L, Yuan Q, Ai X, Chen J, Lu Y, Yan F. Transgenic rice plants expressing artificial miRNA targeting the rice stripe virus MP gene are highly resistant to the virus[J]. Biology, 2022, 11(2): 332.
[7]	黄耀辉, 王艺洁, 杨立桃, 焦悦, 付仲文. 生物育种新技术作物的安全管理[J]. 生物技术进展, 2022, 12(2): 198-204.
	Huang Y H, Wang Y J, Yang L T, Jiao Y, Fu Z W. Safety management of the crop produced by new breeding techniques[J]. Current Biotechnology, 2022, 12(2): 198-204. (in Chinese with English abstract)
[8]	黄耀辉, 焦悦, 吴小智, 叶纪明. 生物育种技术对种业科技创新的影响[J]. 南京农业大学学报, 2022(3): 1-10.
	Huang Y H, Jiao Y, Wu X Z, Ye J M. The influence of biological breeding on the science and technology innovation of seed industry[J]. Journal of Nanjing Agricultural University, 2022, 45(3): 413-421. (in Chinese with English abstract)
[9]	Joong C P, Hoyong C, Nuri O, Joohee C, Woon B S, Eun J S, Harin J, Sung S J, Kon K J. Efficiency of recombinant CRISPR/rCas9-mediated miRNA gene editing in rice[J]. International Journal of Molecular Sciences, 2020, 21(24): 9606. (in Chinese with English abstract)
[10]	任俊, 曹跃炫, 黄勇, 董慧荣, 刘庆, 王克剑. 基因编辑技术及其水稻中的发展和应用[J]. 中国稻米, 2021, 27(4): 92-100
	Ren J, Zao Y X, Huang Y, Dong H R, Liu Q, Wang K J. Development and application of genome editing technology in rice[J]. China Rice, 2021, 27(4): 92-100. (in Chinese with English abstract)
[11]	Komor A C, Kim Y B, Packer M S, Zuris J A, Liu D R. Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage[J]. Nature, 2016, 533(7603): 420-424.
[12]	刘尧, 周先辉, 黄舒泓, 王小龙. 引导编辑: 突破碱基编辑类型的新技术[J]. 遗传, 2022, 44(11): 993-1008.
	Liu Y, Zhou X H, Huang S H, Wang X L. Prime editing: A search and replace tool with versatile baes changes[J]. Hereditas, 2022, 44(11): 993-1008. (in Chinese with English abstract)
[13]	卢振万, 李雪琪, 黄金光, 周焕斌. 利用胞嘧啶碱基编辑技术创制耐草甘膦水稻[J]. 生物技术通报, 2023, 39(2): 63-69.
	Lu Z W, Li X Q, Huang J G, Zhou H B. Creation of glyphosate-tolerant rice by cytosine base editing[J]. Biotechnology Bulletin, 2023, 39(2): 63-69. (in Chinese with English abstract)
[14]	Gao C X. Genome engineering for crop improvement and future agriculture[J]. Cell, 2021, 184(6): 1621-1635.
[15]	Kumar J, Nian C S, Weiss T, Liu H, Liu B, Yang B, Zhang F. Efficient protein tagging and cis-regulatory element engineering via precise and directional oligonucleotide-based targeted insertion in plants[J]. The Plant Cell, 2023. DOI:10.1093/PLCELL/KOAD139
[16]	Lorenzo C D, Debray K, Herwegh D, Develtere W, Impens L, Schaumont D, Vandeputte W, Aesaert S, Coussens G, De Boe Y, Demuynck K, van Hautegem T, Pauwels L, Jacobs T B, Ruttink T, Nelissen H, Inzé D. BREEDIT: A multiplex genome editing strategy to improve complex quantitative traits in maize[J]. The Plant Cell, 2022, 35(1): 218-238.
[17]	卢跃磊, 荣克伟, 陈勇, 李生梅, 郝转芳, 高文伟. 全基因组选择概况及其在玉米育种中的研究进展[J/OL]. 分子植物育种, 2022: 1-21.
	Lu Y L, Rong K W, Chen Y, Li S M, Hao Z F, Gao W W. Genomic selection and its role in assisting maize breeding procedure[J/OL]. Molecular Plant Breeding, 2022: 1-21
[18]	Vincent P R, Justine K K, Shunsaku N, Daigo M, Kazuyuki D. Utilization of genotyping-by-sequencing (GBS) for rice pre-breeding and improvement: A review[J]. Life, 2022, 12(11): 1752.
[19]	He S, Liu H, Zhan J, Meng Y, Wang Y, Wang F, Ye G. Genomic prediction using composite training sets is an effective method for exploiting germplasm conserved in rice gene banks[J]. The Crop Journal, 2022, 10(4): 1073-1082.
[20]	Xu S, Zhu D, Zhang Q. Predicting hybrid performance in rice using genomic best linear unbiased prediction[J]. Proceedings of the National Academy of Sciences of the United States of America, 2014, 111(34): 12456-12461.
[21]	Song X, Meng X, Guo H, Cheng Q, Jing Y, Chen M, Liu G, Wang B, Wang Y, Li J, Yu H. Targeting a gene regulatory element enhances rice grain yield by decoupling panicle number and size[J]. Nature Biotechnology, 2022, 40(9): 1403-1411.
[22]	Qu R, Zhang P, Liu Q, Wang Y, Guo W, Du Z, Li X, Yang L, Yan S, Gu X. Genome-edited ATP BINDING CASSETTE B1 transporter SD8 knockouts have optimized rice architecture without yield penalty[J]. Plant Communications, 2022, 3(5): 100347.
[23]	Chen W, Chen L, Zhang X, Yang N, Guo J, Wang M, Ji S, Zhao X, Yin P, Cai L, Xu J, Zhang L, Han Y, Xiao Y, Xu G, Wang Y, Wang S, Wu S, Yang F, Jackson D, Cheng J, Chen S, Sun C, Qin F, Tian F, Fernie A R, Li J, Yan J, Yang X. Convergent selection of a WD40 protein that enhances grain yield in maize and rice[J]. Science, 2022, 375(6587): 7985.
[24]	Li Y, Wu S, Huang Y, Ma X, Tan L, Liu F, Lü Q, Zhu Z, Hu M, Fu Y, Zhang K, Gu P, Xie D, Sun H, Sun C. OsMADS17 simultaneously increases grain number and grain weight in rice[J]. Nature Communications, 2023, 14(1): 3098.
[25]	Xu R F, Yang Y C. Rapid improvement of grain weight via highly efficient CRISPR/Cas9-mediated multiplex genome editing in rice[J]. Journal of Genetics and Genomics, 2016, 43(8): 529-532.
[26]	Zeng Y, Wen J, Zhao W, Wang Q, Huang W. Rational improvement of rice yield and cold tolerance by editing the three genes OsPIN5b, GS3, and OsMYB30 with the CRISPR-Cas9 system[J]. Frontiers in Plant Science, 2019, 10: 1663.
[27]	Huang Y, Dong H, Mou C, Wang P, Hao Q, Zhang M, Wu H, Zhang F, Ma T, Miao R, Fu K, Chen Y, Zhu Z, Chen C, Tong Q, Wang Z, Zhou S, Liu X, Liu S, Tian Y, Jiang L, Wan J. Ribonuclease H-like gene SMALL GRAIN2 regulates grain size in rice through brassinosteroid signaling pathway[J]. Journal of Integrative Plant Biology, 2022, 64(10): 1883-1900.
[28]	Zeng D, Yan M, Wang Y, Liu X, Qian Q, Li J. Dul1, encoding a novel Prp1 protein, regulates starch biosynthesis through affecting the splicing of Wx^b pre-mRNAs in rice (Oryza sativa L.)[J]. Plant Molecular Biology, 2007, 65(4): 501-509.
[29]	Zhang H, Duan L, Dai J S, Zhang C Q, Li J, Gu M H, Liu Q, Zhu Y. Major QTLs reduce the deleterious effects of high temperature on rice amylose content by increasing splicing efficiency of Wx pre-mRNA[J]. Theoretical and Applied Genetics, 2014, 127(2): 273-82.
[30]	Cai Y, Zhang W, Fu Y, Shan Z, Xu J, Wang P, Kong F, Jin J, Yan H, Ge X, Wang Y, You X, Chen J, Li X, Chen W, Chen X, Ma J, Tang X, Zhang J, Bao Y, Jiang L, Wang H, Wan J. Du13 encodes a C2H2 zinc-finger protein that regulates Wx^b pre-mRNA splicing and microRNA biogenesis in rice endosperm[J]. Plant Biotechnology Journal, 2022, 20(7): 1387-1401
[31]	Liu X, Ding Q, Wang W, Pan Y, Tan C, Qiu Y, Chen Y, Li H, Li Y, Ye N, Xu N, Wu X, Ye R, Liu J, Ma C. Targeted deletion of the first intron of the Wx^b allele via CRISPR/Cas9 significantly increases grain amylose content in rice[J]. Rice, 2022, 15(1): 1-1.
[32]	Huang L, Li Q, Zhang C, Chu R, Gu Z, Tan H, Zhao D, Fan X, Liu Q. Creating novel Wx alleles with fine-tuned amylose levels and improved grain quality in rice by promoter editing using CRISPR/Cas9 system[J]. Plant Biotechnology Journal, 2020, 18(11): 2164-2166.
[33]	Zeng D, Liu T, Ma X, Wang B, Zheng Z, Zhang Y, Xie X, Yang B, Zhao Z, Zhu Q, Liu Y. Quantitative regulation of Waxy expression by CRISPR/Cas9-based promoter and 5'UTR-intron editing improves grain quality in rice[J]. Plant Biotechnology Journal, 2020, 18(12): 2385-2387.
[34]	Xu Y, Lin Q P, Li X F, Wang F Q, Chen Z H, Wang J, Li W Q, Fan F J, Tao Y J, Jiang Y J, Wei X D, Zhang R, Zhu Q H, Bu Q Y, Yang J, Gao C X. Fine-tuning the amylose content of rice by precise base editing of the Wx gene[J]. Plant Biotechnology Journal, 2020, 19(1): 11-13.
[35]	Huang L C, Xiao Y, Zhao W, Rao Y N, Shen H M, Gu Z W, Fan X L, Li Q F, Zhang C Q, Liu Q Q. Creating high-resistant starch rice by simultaneous editing of SS3a and SS3b[J]. Plant Biotechnology Journal, 2023: 1-4.
[36]	Hui S Z, Li H J, Mawia A M, Zhou L, Cai J Y, Ahmad S, Lai C K, Wang J X, Jiao G A, Xie L H, Shao G N, Sheng Z H, Tang S Q, Wang J L, Wei X J, Hu S K, Hu P S. Production of aromatic three-line hybrid rice using novel alleles of BADH2[J]. Plant Biotechnology Journal, 2021, 20(1): 59-73.
[37]	Yang Y H, Shen Z Y, Li Y G, Xu C D, Xia H, Zhuang H, Sun S Y, Guo M, Yan C J. Rapid improvement of rice eating and cooking quality through gene editing toward glutelin as target[J]. Journal of Integrative Plant Biology, 2022, 64(10): 1860-1865.
[38]	Huang H X, Ye Y F, Song W Z, Li Q, Han R X, Wu C C, Wang S X, Yu J P, Liu X Y, Fu X D, Liu Q, Wu K. Modulating the C-terminus of DEP1 synergistically enhances grain quality and yield in rice[J]. Journal of Genetics and Genomics, 2022, 49(5): 506-509.
[39]	李广伟. 水稻生殖隔离遗传结构解析、S5位点演化起源与基于全基因组预测的亚种间杂种优势利用研究[D]. 武汉: 华中农业大学, 2018
	Li G W. Genetic architecture of reproductive isolation in rice, evolutionary origination of S5 and utilization of inter-subspecific heterosis via genomic prediction[D]. Wuhan: Huazhong Agricultural University, 2018. (in Chinese with English abstract)
[40]	Won K K, Bhagwat N, Jungrye N, Ho C S, Jungmin H, Jin P Y. Development of an inclusive 580K SNP array and its application for genomic selection and genome-wide association studies in rice[J]. Frontiers in Plant Science, 2022, 13: 1036177.
[41]	Spindel J, Begum H, Akdemir D, Virk P, Collard B, Redoña E, Atlin G, Jannink J L, McCouch S R. Genomic selection and association mapping in rice (Oryza sativa): Effect of trait genetic architecture, training population composition, marker number and statistical model on accuracy of rice genomic selection in elite, tropical rice breeding lines[J]. PLoS Genetics, 2015, 11(2): 1004982.
[42]	Xu S Z, Zhu D, Zhang Q F. Predicting hybrid performance in rice using genomic best linear unbiased prediction[J]. Proceedings of the National Academy of Sciences of the United States of America, 2014, 111(34): 12456-124621.
[43]	Ryokei T, Tojo M S, Mbolatantely R, Nicole R H, Juan P T, Hiromi K K, Hiroyoshi I, Matthias W. From gene banks to farmer's fields: Using genomic selection to identify donors for a breeding program in rice to close the yield gap on smallholder farms[J]. Theoretical and Applied Genetics, 2021, 134(10): 1-14.
[44]	Zhou Y B, Xu S C, Jiang N, Zhao X, Bai Z N, Liu J L, Yao W, Tang Q Y, Xiao G, Lü C, Wang K, Hu X C, Tan J, Yang Y Z. Engineering of rice varieties with enhanced resistances to both blast and bacterial blight diseases via CRISPR/Cas9[J]. Plant Biotechnology Journal, 2022, 20(5): 876-885.
[45]	Zhang Y, Yu Q, Gao S L, Yu N G, Zhao L, Wang J B, Zhao J, Huang P, Yao L B, Wang M, Zhang K W. Disruption of the primary salicylic acid hydroxylases in rice enhances broad-spectrum resistance against pathogens[J]. Plant, Cell & Environment, 2022, 45(7): 2211-2225.
[46]	Li H, Zhang Y, Wu C Y, Bi J P, Chen Y C, Jiang C J, Cui M M, Chen Y D, Hou X, Yuan M, Xiong L Z, Yang Y N, Xie K B. Fine-tuning OsCPK18/OsCPK4 activity via genome editing of phosphorylation motif improves rice yield and immunity[J]. Plant Biotechnology Journal, 2022, 20(12): 2258-2271.
[47]	Li C Y, Li W, Zhou Z H, Chen H, Xie C H, Lin Y. A new rice breeding method: CRISPR/Cas9 system editing of the Xa13 promoter to cultivate transgene-free bacterial blight-resistant rice[J]. Plant Biotechnology Journal, 2020, 18(2): 313-315.
[48]	Xu Z Y, Xu X M, Gong Q, Li Z Y, Li Y, Wang S, Yang Y Y, Ma W X, Liu L Y, Zhu B, Zou L F, Chen G. Engineering broad-spectrum bacterial blight resistance by simultaneously disrupting variable tale-binding elements of multiple susceptibility genes in rice[J]. Molecular Plant, 2019, 12(11): 1434-1446.
[49]	Wang S X, Zong Y, Lin Q P, Zhang H W, Chai Z Z, Zhang D, Chen K L, Qiu J L, Gao C X. Precise, predictable multi-nucleotide deletions in rice and wheat using APOBEC-Cas9[J]. Nature Biotechnology, 2020, 38: 1460-1465.
[50]	Sun Y J, Gong Y W, He Q Z, Kuang S J, Gao Q, Ding W B, He H L, Xue J, Li Y Z, Li Q. FAR knockout significantly inhibits Chilo suppressalis survival and transgene expression of double-stranded FAR in rice exhibits strong pest resistance[J]. Plant Biotechnology Journal, 2022, 20(12): 2272-2283.
[51]	Hu L F, Ye M, Li R, Zhang T F, Zhou G X, Wang Q, Lu J, Lou Y G. The rice transcription factor WRKY53 suppresses herbivore-induced defenses by acting as a negative feedback modulator of mitogen-activated protein kinase activity[J]. Plant Physiology, 2015, 169(4): 2907-2921.
[52]	Huang Q L, Lin B R, Cao Y Q, Zhang Y, Song H D, Huang C H, Sun T L, Long C W, Liao J L, Zhuo K. CRISPR/Cas9-mediated mutagenesis of the susceptibility gene OsHPP04 in rice confers enhanced resistance to rice root-knot nematode[J]. Frontiers in Plant Science, 2023, 14: 1134653.
[53]	Wang X M, Cheng R, Xu D C, Huang R L, Li H X, Jin L, Wu Y F, Tang J Y, Sun C H, Peng D L, Chu C C, Guo X L. MG1 interacts with a protease inhibitor and confers resistance to rice root-knot nematode[J]. Nature Communications, 2023, 14(1): 3354.
[54]	Shen R D, Yao Q, Zhong D T, Zhang X N, Li X B, Cao X S, Dong C, Tian Y F, Zhu J K, Lu Y M. Targeted insertion of regulatory elements enables translational enhancement in rice[J]. Frontiers in Plant Science, 2023, 14: 1134209.
[55]	Gong X D, Huang Y Q, Liang Y, Yuan Y D, Liu Y H, Han T W, Li S J, Gao H B, Lü B, Huang X H, Linster E, Wang Y C, Wirtz M, Wang Y H. OsHYPK-mediated protein N-terminal acetylation coordinates plant development and abiotic stress responses in rice[J]. Molecular Plant, 2022, 15(4): 740-754.
[56]	陈银科, 滕振宁, 郑芹吕, 佳晗, 鲁丝琼, 刘伯涵, 叶能辉. 脱落酸调控水稻籽粒灌浆的机理研究进展[J/OL]. 分子植物育种, 2022(12): 1-18.
	Chen Y K, Teng Z N, Zheng Q, Lü J H, Lu S Q, Liu B H, Ye N H. Research advances in regulations by abscisic acid on grain filling in rice[J/OL]. Molecular Plant Breeding, 2022(12): 1-18. (in Chinese with English abstract)
[57]	周天顺, 余东, 刘玲, 欧阳宁, 袁贵龙, 段美娟, 袁定阳. 利用CRISPR/Cas9技术编辑AFP1基因提高水稻耐逆性[J]. 中国水稻科学, 2021, 35(1): 11-18.
	Zhou T S, Yu D, Liu L, Ouyang N, Yuan G L, Duan M J, Yuan D Y. CRISPR/Cas9-mediated editing of AFP1 improves rice stress tolerance[J]. Chinese Journal of Rice Science, 2021, 35(1): 11-18.
[58]	Kan Y, Mu X R, Zhang H, Gao J, Shan J X, Ye W W, Lin H X. TT2 controls rice thermo-tolerance through SCT1-dependent alteration of wax biosynthesis[J]. Nature Plants, 2021, 8(1): 53-67.
[59]	Tang J Q, Tian X J, Mei E Y, He M L, Gao J W, Yu J, Xu M, Liu J L, Song L, Li X F, Wang Z Y, Guan Q J, Zhao Z G, Wang C M, Bu Q Y. WRKY53 negatively regulates rice cold tolerance at the booting stage by fine-tuning anther gibberellin levels[J]. The Plant Cell, 2022, 34(11): 4495-4515.
[60]	李景芳, 温舒越, 赵利君, 陈庭木, 周振玲, 孙志广, 刘艳, 陈海元, 张云辉, 迟铭, 邢运高, 徐波, 徐大勇, 王宝祥. 基于CRISPR/Cas9技术创制耐盐香稻[J]. 中国水稻科学, 2023, 37(5): 478-485.
	Li J F, Wen S Y, Zhao L J, Chen T M, Zhou Z L, Sun Z G, Sun Z G, Liu Y, Chen H Y, Zhang Y H, Chi M, Xing Y G, Xu D Y, Wang B X. Development of aromatic salt-tolerant rice based on CRISPR/Cas9 technology[J]. Chinese Journal of Rice Science, 2023, 37(5): 478-485. (in Chinese with English abstract)
[61]	Lu Y, Wang J Y, Chen B, Mo S D, Lian L, Luo Y M, Ding D H, Ding Y H, Cao Q, Li Y C, Li Y, Liu G Z, Hou Q Q, Cheng T T, Wei J T, Zhang Y R, Chen G W, Song C, Hu Q, Sun S, Fan G Y, Wang Y T, Liu Z T, Song B A, Zhu J K, Li H R, Jiang L J. A donor-DNA-free CRISPR/Cas-based approach to gene knock-up in rice[J]. Nature Plants, 2021, 7(11): 1445-1452.
[62]	Yu H, Lin T, Meng X B, Du H L, Zhang J K, Liu G F, Chen M J, Jing Y H, Kou L Q, Li X X, Gao Q, Liang Y, Liu X D, Fan Z L, Liang Y T, Cheng Z K, Chen M S, Tian X, Li J Y. A route to de novo domestication of wild allotetraploid rice[J]. Cell, 2021, 184(5): 1156-1170.
[63]	Mahantesh G K, Sayan D, Saraswathi R, Gopalakrishnan C, Gnanam R, Amandeep K, Dhaliwal L K, Pannu P P S, Bernardo R, Yu J, Chen Z, Feng Z, Kang H, Zhao J, Chen T. Analysis of the efficiency of genomic selection models for predicting sheath blight resistance in rice (Oryza sativa L.)[J]. International Journal of Bio-resource and Stress Management, 2022, 13(3): 268-275
[64]	Huang M, Balimponya E G, Mgonja E M, McHale L K, Luzi-Kihupi A, Wang G L, Sneller C H. Use of genomic selection in breeding rice(Oryza sativa L.) for resistance to rice blast(Magnaporthe oryzae)[J]. Molecular Breeding, 2019, 39(8): 1-16.
[65]	肖韦宇, 刘英, 罗继景. 水稻苗期耐热遗传位点的全基因组关联分析[J/OL]. 分子植物育种: 1-17.
	Xiao W Y, Liu Y, Luo J J. CGenome wide association analysis of heat tolerance at the seedling stage in rice[J/OL]. Molecular Plant Breeding, 2022: 1-17.
[66]	Sandhu K S, Merrick L F, Sankaran S, Zhang Z W, Carter A H. Prospectus of genomic selection and phenomics in cereal, legume and oilseed breeding programs[J]. Frontiers in Genetics, 2022, 12: 829131.
[67]	Vernet A, Meynard D, Lian Q. High-frequency synthetic apomixis in hybrid rice[J]. Nature Communications, 2022, 13(1): 7963.
[68]	Wang C, Liu Q, Shen Y, Hua Y F, Wang J J, Lin J R, Wu M G, Sun T T, Cheng Z K, Mercier R, Wang K J. Clonal seeds from hybrid rice by simultaneous genome engineering of meiosis and fertilization genes[J]. Nature Biotechnology, 2019, 37(3): 283.
[69]	Xie E, Li Y F, Tang D, Lü Y L, Shen Y, Cheng Z K. A strategy for generating rice apomixis by gene editing[J]. Journal of Integrative Plant Biology, 2019, 61(8): 911-916.
[70]	Zhu X Y, Gou Y J, Heng Y Q, Ding W Y, Li Y J, Zhou D G, Li X Q, Liang C R, Wu C Y, Wang H Y, Shen R X. Targeted manipulation of grain shape genes effectively improves outcrossing rate and hybrid seed production in rice[J]. Plant Biotechnology Journal, 2023, 21(2): 381-390.
[71]	Wang M M, Zhu Q P, Peng G Q, Liu M L, Zhang S Q, Chen M H, Liao S T, Wei X Y, Xu P, Tan X Y, Li F P, Li Z C, Deng L, Luo Z L, Zhu L Y, Zhao S, Jiang D G, Li J, Liu Z L, Xie X R, Wang S K, Wu A M, Zhuang C X, Zhou H. Methylesterification of cell wall pectin controls the diurnal flower opening times in rice[J]. Molecular Plant, 2022, 4(4): 956-972.
[72]	Wu L B, Eom J S, Isoda R. OsSWEET11b, a potential sixth leaf blight susceptibility gene involved in sugar transport-dependent male fertility[J]. New Phytologist, 2022, 234(3): 975-989.
[73]	段敏, 谢留杰, 高秀莹, 唐海娟, 黄善军, 潘晓飚. 利用CRISPR/Cas9技术创制广亲和水稻温敏雄性不育系[J]. 中国水稻科学, 2023, 37(3): 233-243.
	Duan M, Xie L J, Gao X Y, Tang H J, Huang S J, Pan X B. Creation of thermo-sensitive genic male sterile rice lines with wide compatibility based on CRISPR/Cas9 Technology[J]. Chinese Journal of Rice Science, 2023, 37(3): 233-243. (in Chinese with English abstract)
[74]	Chen Y, Qasim S M, Wu J W, Deng R L, Chen Z X, Wang L, Liu G Q, Zhou H, Liu X D. Thermo-sensitive genic male sterile lines of neo-tetraploid rice developed through gene editing technology revealed high levels of hybrid vigor[J]. Plants, 2022, 11(11): 1390.
[75]	Cui Y R, Li R D, Li G W, Zhang F, Zhu T T, Zhang Q F, Jauhar A, Li Z K, Xu S Z. Hybrid breeding of rice via genomic selection[J]. Plant Biotechnology Journal, 2020, 18(1): 57-67.
[76]	Wang X, Li L, Yang Z, Zheng X, Yu S, Xu C, Hu Z. Predicting rice hybrid performance using univariate and multivariate GBLUP models based on North Carolina mating design II[J]. Heredity, 2017, 118(3): 302-310.
[77]	Xu Y, Wang X, Ding X W, Zheng X F, Yang Z F, Xu C W, Hu Z L. Genomic selection of agronomic traits in hybrid rice using an NCⅡ population[J]. Rice, 2018, 11(1): 32.
[78]	Xu Y B, Zhang X P, Li H H, Zheng H J, Zhang J N, Olsen M S, Varshney R K, Prasanna B M, Qian Q. Smart breeding driven by big data, artificial intelligence and integrated genomic-enviromic prediction[J]. Molecular Plant, 2022, 15(11): 1664-1695.

基因名称 Gene name			表型 Phenotype		参考文献 Reference
IPA1	敲除Knockout	顺式调控区 Cis-regulatory element	产量提高15.9% 15.9% increase in yield		[21]
SD8	敲除Knockout	外显子Exon	密植条件下增产10% 10% increase in yield		[22]
OsKRN2	敲除Knockout	外显子Exon	增产8% 8% increase in yield		[23]
OsMADS17	敲除Knockout	5′UTR	穗粒数、粒重增加Grain number and weight increased		[24]
GW2, GW5, TGW6	敲除Knockout	外显子Exon	粒重增加Grain weight increased		[25]
OsPIN56, GS3, OsMYB30	敲除Knockout	外显子Exon	高产、耐冷High yield and cold resistance increased		[26]
Dull	敲除Knockout	外显子Exon	直链淀粉含量下降Decreased amylose content		[30]
Wx^b	敲除Knockout	TATA box	微调直链淀粉含量Fine-tune amylose content		[32]
Wx^a	敲除Knockout	5′UTR	直链淀粉含量下降Decreased amylose content		[33]
Wx^b	敲除Knockout	N-末端结构域 N-terminal domain	低淀粉含量Low starch content		[34]
SS3a, SS3b	敲除Knockout	外显子Exon	抗性淀粉增加Resistant starch increased		[35]
OsBADH2	敲除Knockout	外显子Exon	稻米香味增加Aroma of rice increased		[35]
OsGlus	敲除Knockout	外显子Exon	稻米蛋白质含量下降Decreased protein content		[37]
DEP1	敲除Knockout	蛋白质C端 C-terminus	提高产量和稻米品质Improved yield and rice quality		[38]
Bsr-d1, Pi21, ERF922	敲除Knockout	外显子Exon	稻瘟病及白叶枯病抗性增强Resistance to rice blast and rice bacterial blight was enhanced		[44]
OsS5H1, OsS5H2	敲除Knockout	外显子Exon	稻瘟病及白叶枯病抗性增强Resistance to rice blast and rice bacterial blight was enhanced		[45]
OsMPK5	敲除Knockout	磷酸化位点Phosphorylation site	产量及稻瘟病抗性提高Yield and blast resistance improved		[46]
Xa13	敲除Knockout	启动子Promoter	产量不变、强白叶枯病抗性Unchanged yield and stronger resistance to rice bacterial blight		[47]
OsSWEET11, 13, 14	敲除Knockout	启动子Promoter	广谱白叶枯病抗性Broad-spectrum rice bacterial blight resistance		[48]
OsSWEET14	敲除Knockout	启动子Promoter	白叶枯病抗性增加Increased resistance to rice bacterial blight		[49]
FAS	HIGS		二化螟存活率下降Survival rate of C. suppressalis decreased		[50]
OsWRKY53	iRNA		二化螟抗性增加C. suppressalis resistance increased		[51]
OsHPP04	敲除Knockout	外显子Exon	对拟禾本科根结线虫抗性增加Resistance to Meloidogyne graminicola increased		[52]
OsWRKY71, OsSKC1	敲入Knock-in	增强子Enhancer	非生物胁迫抗性增加Increased resistance to abiotic stresses		[54]
OsHYPK	敲除Knockout	外显子Exon	抗旱耐盐Increased drought and salt tolerant		[55]
AFP1	敲除Knockout	外显子Exon	耐旱耐热Increased drought and heat tolerant		[57]
SCT1	敲除Knockout	外显子Exon	耐热性增加Increased heat resistance		[58]
SCT2	敲除Knockout	外显子Exon	耐热性增加Increased heat resistance		[58]
OsRR22	敲除Knockout	外显子Exon	耐盐性增加Increased salt tolerance		[60]
PP01, HPPD	敲除Knockout	启动子Promoter	抗除草剂Herbicide resistance		[61]
PAIR1, REC8, OSD1	敲除Knockout	外显子Exon	高效无性繁殖, 自留种 Efficient vegetative propagation, self-retaining seeds		[67]
PAIR1, REC8, OSD1, MTL	敲除Knockout	外显子Exon	无融合生殖Apomixis		[68]
PAIR1, OsPO11.1, OSD1, MTL	敲除Knockout	外显子Exon	无融合生殖Apomixis	[69]
GS3, GS9, GW8	敲除Knockout	外显子Exon	雄性不育柱头外露率和异交结实率提高Increased exposure rate of male sterile stigma and outcrossing seed setting	[70]
DFOT1	敲除Knockout	外显子Exon	促进开花Promoted flowering	[71]
OsSWEET11a, 11b	敲除Knockout	外显子Exon	雄配子不育Sterile male gametes	[72]
OsWRKY53	敲除Knockout	外显子Exon	结实率、孕穗期耐冷性和花粉活力增加Increased seed setting rate, cold tolerance at booting stage and pollen viability	[59]
TMS5	敲除Knockout	外显子Exon	不育Infertility	[73]
TMS5	敲除Knockout	外显子Exon	致使四倍体不育Causing tetraploid infertility	[74]

基因名称 Gene name			表型 Phenotype		参考文献 Reference
IPA1	敲除Knockout	顺式调控区 Cis-regulatory element	产量提高15.9% 15.9% increase in yield		[21]
SD8	敲除Knockout	外显子Exon	密植条件下增产10% 10% increase in yield		[22]
OsKRN2	敲除Knockout	外显子Exon	增产8% 8% increase in yield		[23]
OsMADS17	敲除Knockout	5′UTR	穗粒数、粒重增加Grain number and weight increased		[24]
GW2, GW5, TGW6	敲除Knockout	外显子Exon	粒重增加Grain weight increased		[25]
OsPIN56, GS3, OsMYB30	敲除Knockout	外显子Exon	高产、耐冷High yield and cold resistance increased		[26]
Dull	敲除Knockout	外显子Exon	直链淀粉含量下降Decreased amylose content		[30]
Wx^b	敲除Knockout	TATA box	微调直链淀粉含量Fine-tune amylose content		[32]
Wx^a	敲除Knockout	5′UTR	直链淀粉含量下降Decreased amylose content		[33]
Wx^b	敲除Knockout	N-末端结构域 N-terminal domain	低淀粉含量Low starch content		[34]
SS3a, SS3b	敲除Knockout	外显子Exon	抗性淀粉增加Resistant starch increased		[35]
OsBADH2	敲除Knockout	外显子Exon	稻米香味增加Aroma of rice increased		[35]
OsGlus	敲除Knockout	外显子Exon	稻米蛋白质含量下降Decreased protein content		[37]
DEP1	敲除Knockout	蛋白质C端 C-terminus	提高产量和稻米品质Improved yield and rice quality		[38]
Bsr-d1, Pi21, ERF922	敲除Knockout	外显子Exon	稻瘟病及白叶枯病抗性增强Resistance to rice blast and rice bacterial blight was enhanced		[44]
OsS5H1, OsS5H2	敲除Knockout	外显子Exon	稻瘟病及白叶枯病抗性增强Resistance to rice blast and rice bacterial blight was enhanced		[45]
OsMPK5	敲除Knockout	磷酸化位点Phosphorylation site	产量及稻瘟病抗性提高Yield and blast resistance improved		[46]
Xa13	敲除Knockout	启动子Promoter	产量不变、强白叶枯病抗性Unchanged yield and stronger resistance to rice bacterial blight		[47]
OsSWEET11, 13, 14	敲除Knockout	启动子Promoter	广谱白叶枯病抗性Broad-spectrum rice bacterial blight resistance		[48]
OsSWEET14	敲除Knockout	启动子Promoter	白叶枯病抗性增加Increased resistance to rice bacterial blight		[49]
FAS	HIGS		二化螟存活率下降Survival rate of C. suppressalis decreased		[50]
OsWRKY53	iRNA		二化螟抗性增加C. suppressalis resistance increased		[51]
OsHPP04	敲除Knockout	外显子Exon	对拟禾本科根结线虫抗性增加Resistance to Meloidogyne graminicola increased		[52]
OsWRKY71, OsSKC1	敲入Knock-in	增强子Enhancer	非生物胁迫抗性增加Increased resistance to abiotic stresses		[54]
OsHYPK	敲除Knockout	外显子Exon	抗旱耐盐Increased drought and salt tolerant		[55]
AFP1	敲除Knockout	外显子Exon	耐旱耐热Increased drought and heat tolerant		[57]
SCT1	敲除Knockout	外显子Exon	耐热性增加Increased heat resistance		[58]
SCT2	敲除Knockout	外显子Exon	耐热性增加Increased heat resistance		[58]
OsRR22	敲除Knockout	外显子Exon	耐盐性增加Increased salt tolerance		[60]
PP01, HPPD	敲除Knockout	启动子Promoter	抗除草剂Herbicide resistance		[61]
PAIR1, REC8, OSD1	敲除Knockout	外显子Exon	高效无性繁殖, 自留种 Efficient vegetative propagation, self-retaining seeds		[67]
PAIR1, REC8, OSD1, MTL	敲除Knockout	外显子Exon	无融合生殖Apomixis		[68]
PAIR1, OsPO11.1, OSD1, MTL	敲除Knockout	外显子Exon	无融合生殖Apomixis	[69]
GS3, GS9, GW8	敲除Knockout	外显子Exon	雄性不育柱头外露率和异交结实率提高Increased exposure rate of male sterile stigma and outcrossing seed setting	[70]
DFOT1	敲除Knockout	外显子Exon	促进开花Promoted flowering	[71]
OsSWEET11a, 11b	敲除Knockout	外显子Exon	雄配子不育Sterile male gametes	[72]
OsWRKY53	敲除Knockout	外显子Exon	结实率、孕穗期耐冷性和花粉活力增加Increased seed setting rate, cold tolerance at booting stage and pollen viability	[59]
TMS5	敲除Knockout	外显子Exon	不育Infertility	[73]
TMS5	敲除Knockout	外显子Exon	致使四倍体不育Causing tetraploid infertility	[74]

统计模型 Statistical model	预测的表型 Predicted phenotype	参考文献 Reference
GBLUP	每穗颖花数、分蘖数、千粒重、粒长粒宽、单株干质量、株高、杂种优势 Number of spikelets per panicle, number of tillers, 1000-grain weight, grain length and width, dry weight per plant, plant height, and heterosis	[39]
RR-BLUP, Convolutional neural network(CNN)	粒长、抽穗期、穗长Grain length, heading date, panicle length	[40]
RR-BLUP, Bayesian LASSO(BL), Reproducing Kernel Hilbert Spaces(RKHS), Ran-dom Forest(RF), Multiple Linear Regression (MLR), Pedigree-BLUP(PED)	产量、株高、开花时间 Yield, plant height, flowering time	[41]
GBLUP	产量Yield	[42]
GBLUP	产量、秸秆生物量、抽穗期 Yield, straw biomass, heading date	[43]
BayesB, GBLUP	纹枯病抗性Sheath blight resistance	[63]
GBLUP, fgBLUP, sgBLUP, mgBLUP, BayesA, BayesC, ML	稻瘟病抗性Rice blast resistance	[64]
BLUP	杂交优势Heterosis	[75]
GBLUP	杂交优势Heterosis	[76]

统计模型 Statistical model	预测的表型 Predicted phenotype	参考文献 Reference
GBLUP	每穗颖花数、分蘖数、千粒重、粒长粒宽、单株干质量、株高、杂种优势 Number of spikelets per panicle, number of tillers, 1000-grain weight, grain length and width, dry weight per plant, plant height, and heterosis	[39]
RR-BLUP, Convolutional neural network(CNN)	粒长、抽穗期、穗长Grain length, heading date, panicle length	[40]
RR-BLUP, Bayesian LASSO(BL), Reproducing Kernel Hilbert Spaces(RKHS), Ran-dom Forest(RF), Multiple Linear Regression (MLR), Pedigree-BLUP(PED)	产量、株高、开花时间 Yield, plant height, flowering time	[41]
GBLUP	产量Yield	[42]
GBLUP	产量、秸秆生物量、抽穗期 Yield, straw biomass, heading date	[43]
BayesB, GBLUP	纹枯病抗性Sheath blight resistance	[63]
GBLUP, fgBLUP, sgBLUP, mgBLUP, BayesA, BayesC, ML	稻瘟病抗性Rice blast resistance	[64]
BLUP	杂交优势Heterosis	[75]
GBLUP	杂交优势Heterosis	[76]