Abstract
Identifying and characterizing genes that control important agronomic traits and finding ways to alter them are vital for crop improvement. Map-based cloning, heterologous gene expression, RNAi mediated gene silencing, T-DNA insertional mutation and TILLING technologies have enabled cloning, characterization, and deployment of a few important genes. Revolution in sequencing technologies and bioinformatics has facilitated us to quickly predict and annotate plethora of genes and regulatory elements with improved precision and spatio-temporal expression of genes in almost all cereal crops. However, their functional validation forms a bottleneck in exploiting useful genetic elements for crop improvement. The CRISPR/Cas9 mediated gene editing has become the tool of choice for precisely introducing targeted modifications in the genome to knock out/in a gene, introducing specific mutation in sequence or modulating its expression in diverse crop species. This can help to rapidly characterize plenty of genes in terms of understanding the function of individual gene/ gene family, involvement in a particular biochemical pathway or interaction of the crop plant with external stimuli at a reasonable cost. In this review, we discuss the power of gene editing for rapid functional characterization of genetic elements as a fundamental requirement to harness the power of precision genetic technologies for increasing crop yield, progress made so far, opportunities and challenges.
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Abbreviations
- Cas9:
-
CRISPR associated protein 9
- CLE:
-
CLAVATA3/embryo surrounding region-related
- Cpf1:
-
CRISPR from Prevotella and Francisella 1
- CRISPR:
-
Clustered regularly interspaced short palindromic repeats
- CSSL:
-
Chromosome segment substitution line
- DSB:
-
Double strand break
- DEG:
-
Differentially expressed gene
- EMS:
-
Ethyl methane sulfonate
- GMO:
-
Genetically modified organism
- GS:
-
Grain size
- GW:
-
Grain weight
- GWAS:
-
Genome-wide association studies
- HDR:
-
Homology-directed repair
- MAS:
-
Marker-assisted selection
- NHEJ:
-
Non-homologous end jointing
- PAM:
-
Protospacer adjacent motif
- QTL:
-
Quantitative trait locus
- RBSDVD:
-
Rice black-streaked dwarf virus disease
- RIL:
-
Recombinant inbred line
- RNAi:
-
RNA interference
- ROS:
-
Reactive oxygen species
- sgRNA:
-
Single guide RNA
- sRBSDVD:
-
Southern rice black-streaked dwarf virus disease
- TALEN:
-
Transcription activator-like effector nuclease
- T-DNA:
-
Transfer DNA
- TILLING:
-
Targeting induced local lesions in genomes
- VIGS:
-
Virus-induced gene silencing
- ZFN:
-
Zinc finger nuclease
References
Alonso JM, Stepanova AN, Leisse TJ et al (2003) Genome-wide insertional mutagenesis of arabidopsis thaliana. Science 80(301):653–657. https://doi.org/10.1126/science.1086391
An Y, Chen L, Li Y-X et al (2022) Fine mapping qKRN5.04 provides a functional gene negatively regulating maize kernel row number. Theor Appl Genet 135:1997–2007. https://doi.org/10.1007/s00122-022-04089-w
Andrade-Sanchez P, Gore MA, Heun JT et al (2013) Development and evaluation of a field-based high-throughput phenotyping platform. Funct Plant Physiol 41:68–79. https://doi.org/10.1071/fp13126
Araus JL, Cairns JE (2014) Field high-throughput phenotyping: the new crop breeding frontier. Trends Plant Sci 19:52–61. https://doi.org/10.1016/j.tplants.2013.09.008
Azpiroz-Leehan R, Feldmann KA (1997) T-DNA insertion mutagenesis in arabidopsis: going back and forth. Trends Genet 13:152–156. https://doi.org/10.1016/S0168-9525(97)01094-9
Bhavani S, Singh PK, Qureshi N et al (2021) Globally important wheat diseases: Status, challenges, breeding and genomic tools to enhance resistance durability. In: Kole C (ed) Genomic designing for biotic stress resistant cereal crops. Springer International Publishing, Cham, pp 59–128
Biswal AK, Mangrauthia SK, Reddy MR, Yugandhar P (2019) CRISPR mediated genome engineering to develop climate smart rice: challenges and opportunities. Semin Cell Dev Biol 96:100–106. https://doi.org/10.1016/j.semcdb.2019.04.005
Biswal AK, Wu T-Y, Urano D et al (2022) Novel mutant alleles reveal a role of the extra-large G protein in rice grain filling, panicle architecture, plant growth, and disease resistance. Front Plant Sci 12:2821. https://doi.org/10.3389/fpls.2021.782960
Biswal AK, Hernandez LRB, Castillo AIR et al (2023) An efficient transformation method for genome editing of elite bread wheat cultivars. Front Plant Sci 14:1–15. https://doi.org/10.3389/fpls.2023.1135047
Blankenagel S, Eggels S, Frey M et al (2022) Natural alleles of the abscisic acid catabolism gene ZmAbh4 modulate water use efficiency and carbon isotope discrimination in maize. Plant Cell 34:3860–3872. https://doi.org/10.1093/PLCELL/KOAC200
Bo W, Zhaohui Z, Huanhuan Z et al (2019) Targeted mutagenesis of NAC transcription factor gene, OsNAC041, leading to salt sensitivity in rice. Rice Sci 26:98–108. https://doi.org/10.1016/J.RSCI.2018.12.005
Brenchley R, Spannagl M, Pfeifer M et al (2012) Analysis of the bread wheat genome using whole-genome shotgun sequencing. Nature 491:705–710. https://doi.org/10.1038/nature11650
Butt H, Jamil M, Wang JY et al (2018) Engineering plant architecture via CRISPR/Cas9-mediated alteration of strigolactone biosynthesis. BMC Plant Biol 18:1–9. https://doi.org/10.1186/s12870-018-1387-1
Cao Y, Liang X, Yin P et al (2019) A domestication-associated reduction in K + -preferring HKT transporter activity underlies maize shoot K + accumulation and salt tolerance. New Phytol 222:301–317. https://doi.org/10.1111/nph.15605
Choulet F, Wicker T, Rustenholz C et al (2010) Megabase level sequencing reveals contrasted organization and evolution patterns of the wheat gene and transposable element spaces. Plant Cell 22:1686–1701. https://doi.org/10.1105/TPC.110.074187
Cram D, Kulkarni M, Buchwaldt M et al (2019) WheatCRISPR: a web-based guide RNA design tool for CRISPR/Cas9-mediated genome editing in wheat. BMC Plant Biol 19:474. https://doi.org/10.1186/s12870-019-2097-z
Debernardi JM, Tricoli DM, Ercoli MF et al (2020) A GRF–GIF chimeric protein improves the regeneration efficiency of transgenic plants. Nat Biotechnol 38:1274–1279. https://doi.org/10.1038/s41587-020-0703-0
Doudna JA, Charpentier E (2014) The new frontier of genome engineering with CRISPR-Cas9. Science 346(6213):1258096. https://doi.org/10.1126/science.1258096
Feng Z, Zhang B, Ding W et al (2013) Efficient genome editing in plants using a CRISPR/Cas system. Cell Res 23:1229–1232. https://doi.org/10.1038/cr.2013.114
Feng X, Xiong J, Zhang W et al (2022) ZmLBD5, a class-II LBD gene, negatively regulates drought tolerance by impairing abscisic acid synthesis. Plant J 112:1364–1376. https://doi.org/10.1111/tpj.16015
Garrett KA, Bebber DP, Etherton BA et al (2022) Climate change effects on pathogen emergence: artificial intelligence to translate big data for mitigation. Annu Rev Phytopathol 60:357–378. https://doi.org/10.1146/annurev-phyto-021021-042636
Goff SA, Ricke D, Lan T-H et al (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 80(296):92–100. https://doi.org/10.1126/science.1068275
Gullino ML, Albajes R, Al-Jboory I et al (2022) Climate change and pathways used by pests as challenges to plant health in agriculture and forestry. Sustainability 14:12421. https://doi.org/10.3390/su141912421
Guo H, Du Q, Xie Y et al (2021a) Identification of rice blast loss-of-function mutant alleles in the wheat genome as a new strategy for wheat blast resistance breeding. Front Genet 12:1–11. https://doi.org/10.3389/fgene.2021.623419
Guo M, Wang Q, Zong Y et al (2021b) Genetic manipulations of TaARE1 boost nitrogen utilization and grain yield in wheat. J Genet Genom 48:950–953. https://doi.org/10.1016/J.JGG.2021.07.003
Hsing YI, Chern CG, Fan MJ et al (2007) A rice gene activation/knockout mutant resource for high throughput functional genomics. Plant Mol Biol 63:351–364. https://doi.org/10.1007/S11103-006-9093-Z/METRICS
Huang X, Han B (2014) Natural variations and genome-wide association studies in crop plants. Annu Rev Plant Biol 65:531–551. https://doi.org/10.1146/annurev-arplant-050213-035715
IPCC (2018) Summary for Policymakers. In: Masson-Delmotte V, Zhai P, H.-O.Pörtner, et al. (eds) Global Warming of 1.5 °C. An IPCC special report on the impacts of global warming of 1.5 °C above pre-industrial levels and related global greenhouse gas emission pathways, in the context of strengthening the global response to the threat of climate change,. Cambridge University Press, Cambridge, UK and New York, NY, USA, pp 3–24
Jiang W, Zhou H, Bi H et al (2013) Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice. Nucleic Acids Res 41:e188. https://doi.org/10.1093/nar/gkt780
Jinek M, Chylinski K, Fonfara I et al (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 80(337):816–821. https://doi.org/10.1126/science.1225829
Juroszek P, Laborde M, Kleinhenz B et al (2022) A review on the potential effects of temperature on fungicide effectiveness. Plant Pathol 71:775–784. https://doi.org/10.1111/PPA.13531
Kan J, Cai Y, Cheng C et al (2022) Simultaneous editing of host factor gene TaPDIL5-1 homoeoalleles confers wheat yellow mosaic virus resistance in hexaploid wheat. New Phytol 234:340–344. https://doi.org/10.1111/nph.18002
Kan J, Cai Y, Cheng C et al (2023) CRISPR/Cas9-guided knockout of eIF4E improves wheat yellow mosaic virus resistance without yield penalty. Plant Biotechnol J 21:893–895. https://doi.org/10.1111/pbi.14002
Kulkarni KP, Vishwakarma C, Sahoo SP et al (2014) A substitution mutation in OsCCD7 cosegregates with dwarf and increased tillering phenotype in rice. J Genet 93:389–401. https://doi.org/10.1007/s12041-014-0389-5
Leng G (2021) Maize yield loss risk under droughts in observations and crop models in the United States. Environ Res Lett. https://doi.org/10.1088/1748-9326/abd500
Li W, Teng F, Li T, Zhou Q (2013) Simultaneous generation and germline transmission of multiple gene mutations in rat using CRISPR-Cas systems. Nat Biotechnol 31:684–686. https://doi.org/10.1038/nbt.2652
Li J-Y, Wang J, Zeigler RS (2014a) The 3000 rice genomes project: new opportunities and challenges for future rice research. Gigascience 3:8. https://doi.org/10.1186/2047-217X-3-8
Li Y, Fan C, Xing Y et al (2014b) (2014b) Chalk5 encodes a vacuolar H+-translocating pyrophosphatase influencing grain chalkiness in rice. Nat Genet 464(46):398–404. https://doi.org/10.1038/ng.2923
Li M, Li X, Zhou Z et al (2016a) Reassessment of the four yield-related genes Gn1a, DEP1, GS3, and IPA1 in rice using a CRISPR/Cas9 system. Front Plant Sci 7:1–13. https://doi.org/10.3389/fpls.2016.00377
Li S, Gao F, Xie K et al (2016b) The OsmiR396c-OsGRF4-OsGIF1 regulatory module determines grain size and yield in rice. Plant Biotechnol J 14:2134–2146. https://doi.org/10.1111/pbi.12569
Li X, Zhou W, Ren Y et al (2017) High-efficiency breeding of early-maturing rice cultivars via CRISPR/Cas9-mediated genome editing. J Genet Genom 44:175–178. https://doi.org/10.1016/J.JGG.2017.02.001
Li C, Li W, Zhou Z et al (2020) A new rice breeding method: CRISPR/Cas9 system editing of the Xa13 promoter to cultivate transgene-free bacterial blight-resistant rice. Plant Biotechnol J 18:313–315. https://doi.org/10.1111/PBI.13217
Li S, Lin D, Zhang Y et al (2022) Genome-edited powdery mildew resistance in wheat without growth penalties. Nature 602:455–460. https://doi.org/10.1038/s41586-022-04395-9
Liu D, Chen X, Liu J et al (2012) The rice ERF transcription factor OsERF922 negatively regulates resistance to Magnaporthe oryzae and salt tolerance. J Exp Bot 63:3899–3911. https://doi.org/10.1093/jxb/ers079
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. https://doi.org/10.1038/nplants.2017.43
Liu H, Jian L, Xu J et al (2020) High-throughput CRISPR/Cas9 mutagenesis streamlines trait gene identification in maize. Plant Cell. https://doi.org/10.1105/tpc.19.00934
Liu L, Gallagher J, Arevalo ED et al (2021) Enhancing grain-yield-related traits by CRISPR–Cas9 promoter editing of maize CLE genes. Nat Plants 7:287–294. https://doi.org/10.1038/s41477-021-00858-5
Liu C, Kong M, Yang F et al (2022a) Targeted generation of null mutants in ZmGDIα confers resistance against maize rough dwarf disease without agronomic penalty. Plant Biotechnol J 20:803–805. https://doi.org/10.1111/pbi.13793
Liu C, Kong M, Zhu J et al (2022b) Engineering null mutants in ZmFER1 confers resistance to ear rot caused by Fusarium verticillioides in maize. Plant Biotechnol J 20:2045–2047. https://doi.org/10.1111/PBI.13914
Lo SF, Fan MJ, Hsing YI et al (2016) Genetic resources offer efficient tools for rice functional genomics research. Plant Cell Environ 39:998–1013. https://doi.org/10.1111/PCE.12632
Lobell DB, Bänziger M, Magorokosho C, Vivek B (2011) Nonlinear heat effects on African maize as evidenced by historical yield trials. Nat Clim Chang 11(1):42–45. https://doi.org/10.1038/nclimate1043
Lou D, Wang H, Liang G, Yu D (2017) OsSAPK2 confers abscisic acid sensitivity and tolerance to drought stress in rice. Front Plant Sci. https://doi.org/10.3389/fpls.2017.00993
Lowder LG, Paul JW, Baltes NJ et al (2015) A CRISPR/Cas9 toolbox for multiplexed plant genome editing and transcriptional regulation. Plant Physiol 169:00636. https://doi.org/10.1104/pp.15.00636
Lu Y, Ye X, Guo R et al (2017) Genome-wide targeted mutagenesis in rice using the CRISPR/Cas9 system. Mol Plant 10:1242–1245. https://doi.org/10.1016/j.molp.2017.06.007
Lu K, Wu B, Wang J et al (2018) Blocking amino acid transporter OsAAP3 improves grain yield by promoting outgrowth buds and increasing tiller number in rice. Plant Biotechnol J 16:1710–1722. https://doi.org/10.1111/PBI.12907
Lu J, Wang C, Zeng D et al (2021) Genome-wide association study dissects resistance loci against bacterial blight in a diverse rice panel from the 3000 rice genomes project. Rice. https://doi.org/10.1186/s12284-021-00462-3
Luo M, Zhang Y, Li J et al (2021) Molecular dissection of maize seedling salt tolerance using a genome-wide association analysis method. Plant Biotechnol J 19:1937–1951. https://doi.org/10.1111/PBI.13607
Macovei A, Sevilla NR, Cantos C et al (2018) Novel alleles of rice eIF4G generated by CRISPR/Cas9-targeted mutagenesis confer resistance to rice tungro spherical virus. Plant Biotechnol J 16:1918–1927. https://doi.org/10.1111/pbi.12927
Makarova KS, Wolf YI, Koonin EV (2018) Classification and nomenclature of CRISPR-Cas systems: where from here? Cris J 1:325–336. https://doi.org/10.1089/crispr.2018.0033
Manmathan H, Shaner D, Snelling J et al (2013) Virus-induced gene silencing of Arabidopsis thaliana gene homologues in wheat identifies genes conferring improved drought tolerance. J Exp Bot 64:1381–1392. https://doi.org/10.1093/jxb/ert003
Mao X, Zheng Y, Xiao K et al (2018) OsPRX2 contributes to stomatal closure and improves potassium deficiency tolerance in rice. Biochem Biophys Res Commun 495:461–467. https://doi.org/10.1016/j.bbrc.2017.11.045
Meng X, Yu H, Zhang Y et al (2017) Construction of a genome-wide mutant library in rice using CRISPR/Cas9. Mol Plant 10:1238–1241. https://doi.org/10.1016/j.molp.2017.06.006
Miao C, Xiao L, Hua K et al (2018) Mutations in a subfamily of abscisic acid recepto genes promote rice growth and productivity. Proc Natl Acad Sci USA 115:6058–6063. https://doi.org/10.1073/PNAS.1804774115
Mohr T, Horstman J, Gu YQ et al (2022) CRISPR-Cas9 gene editing of the Sal1 gene family in wheat. Plants 11:1–16. https://doi.org/10.3390/plants11172259
Moin M, Bakshi A, Madhav MS, Kirti PB (2018) Cas9/sgRNA-based genome editing and other reverse genetic approaches for functional genomic studies in rice. Brief Funct Genom 17:339–351. https://doi.org/10.1093/bfgp/ely010
Mondal S, Sallam A, Sehgal D et al (2021) Advances in breeding for abiotic stress tolerance in wheat. In: Kole C (ed) Genomic designing for abiotic stress resistant cereal crops. Springer International Publishing, Cham, pp 71–103
Morran S, Eini O, Pyvovarenko T et al (2011) Improvement of stress tolerance of wheat and barley by modulation of expression of DREB/CBF factors. Plant Biotechnol J 9:230–249. https://doi.org/10.1111/j.1467-7652.2010.00547.x
Nuss ET, Tanumihardjo SA (2010) Maize: a paramount staple crop in the context of global nutrition. Compr Rev Food Sci Food Saf 9:417–436. https://doi.org/10.1111/j.1541-4337.2010.00117.x
Puchta H, Dujon B, Hohn B (1996) Two different but related mechanisms are used in plants for the repair of genomic double-strand breaks by homologous recombination. Proc Natl Acad Sci 93:5055–5060. https://doi.org/10.1073/pnas.93.10.5055
Purugganan MD, Jackson SA (2021) Advancing crop genomics from lab to field. Nat Genet 535(53):595–601. https://doi.org/10.1038/s41588-021-00866-3
Rajendrakumar P, Biswal AK, Balachandran SM et al (2007) Simple sequence repeats in organellar genomes of rice: frequency and distribution in genic and intergenic regions. Bioinformatics 23:1–4. https://doi.org/10.1093/bioinformatics/btl547
Ren Y, Huang Z, Jiang H et al (2021) A heat stress responsive NAC transcription factor heterodimer plays key roles in rice grain filling. J Exp Bot 72:2947–2964. https://doi.org/10.1093/jxb/erab027
Richard W, Hayashi H, Schell J (1991) T-DNA as a gene tag. Plant J 1:281–288. https://doi.org/10.1046/j.1365-313X.1991.t01-6-00999.x
Rong W, Qi L, Wang A et al (2014) The ERF transcription factor TaERF3 promotes tolerance to salt and drought stresses in wheat. Plant Biotechnol J 12:468–479. https://doi.org/10.1111/PBI.12153
Sánchez-León S, Gil-Humanes J, Ozuna CV et al (2018) Low-gluten, nontransgenic wheat engineered with CRISPR/Cas9. Plant Biotechnol J 16:902–910. https://doi.org/10.1111/pbi.12837
Savary S, Willocquet L, Pethybridge SJ et al (2019) The global burden of pathogens and pests on major food crops. Nat Ecol Evol 3:430–439. https://doi.org/10.1038/s41559-018-0793-y
Schnable PS, Ware D, Fulton RS et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 80(326):1112–1115. https://doi.org/10.1126/science.1178534
Schneider HM, Lor VS, Zhang X et al (2023) Transcription factor bHLH121 regulates root cortical aerenchyma formation in maize. Proc Natl Acad Sci 120:e2219668120. https://doi.org/10.1073/pnas.2219668120
Shan Q, Wang Y, Li J et al (2013) Targeted genome modification of crop plants using a CRISPR-Cas system. Nat Biotechnol 31:686–688. https://doi.org/10.1038/nbt.2650
Shan Q, Zhang Y, Chen K et al (2015) Creation of fragrant rice by targeted knockout of the OsBADH2 gene using TALEN technology. Plant Biotechnol J 13:791–800. https://doi.org/10.1111/pbi.12312
Shen C, Que Z, Xia Y et al (2017) Knock out of the annexin gene OsAnn3 via CRISPR/Cas9-mediated genome editing decreased cold tolerance in rice. J Plant Biol 60:539–547. https://doi.org/10.1007/s12374-016-0400-1
Shi J, Gao H, Wang H et al (2017) ARGOS8 variants generated by CRISPR-Cas9 improve maize grain yield under field drought stress conditions. Plant Biotechnol J 15:207–216. https://doi.org/10.1111/pbi.12603
Shomura A, Izawa T, Ebana K et al (2008) Deletion in a gene associated with grain size increased yields during rice domestication. Nat Genet 40:1023–1028. https://doi.org/10.1038/ng.169
Shufen C, Yicong C, Baobing F et al (2019) Editing of rice isoamylase gene ISA1 provides insights into its function in starch formation. Rice Sci 26:77–87. https://doi.org/10.1016/j.rsci.2018.07.001
Shukla VK, Doyon Y, Miller JC et al (2009) Precise genome modification in the crop species Zea mays using zinc-finger nucleases. Nature 459:437–441. https://doi.org/10.1038/nature07992
Song Y, Linderholm HW, Luo Y et al (2020) Climatic causes of maize production loss under global warming in Northeast China. Sustain 12:1–13. https://doi.org/10.3390/SU12187829
Sun Y, Jiao G, Liu Z et al (2017) Generation of high-amylose rice through CRISPR/Cas9-mediated targeted mutagenesis of starch branching enzymes. Front Plant Sci 8:249451. https://doi.org/10.3389/fpls.2017.00298
Svitashev S, Young JK, Schwartz C et al (2015) Targeted mutagenesis, precise gene editing, and site-specific gene insertion in maize using Cas9 and guide RNA. Plant Physiol 169:931–945. https://doi.org/10.1104/pp.15.00793
Symington LS, Gautier J (2011) Double-strand break end resection and repair pathway choice. Annu Rev Genet 45:247–271. https://doi.org/10.1146/ANNUREV-GENET-110410-132435
Takagi H, Tamiru M, Abe A et al (2015) MutMap accelerates breeding of a salt-tolerant rice cultivar. Nat Biotechnol 33:445–449. https://doi.org/10.1038/nbt.3188
Tester M, Langridge P (2010) Breeding technologies to increase crop production in a changing world. Science 80(327):818–822. https://doi.org/10.1126/science.1183700
The Royal Soceity (2020) If the world is warming, why are some winters and summers still very cold? In: Clim Chang Evid Causes. https://royalsociety.org/topics-policy/projects/climate-change-evidence-causes/question-11/. Accessed 30 Oct 2023
Tian X, Qin Z, Zhao Y et al (2022) Stress granule-associated TaMBF1c confers thermotolerance through regulating specific mRNA translation in wheat (Triticum aestivum). New Phytol 233:1719–1731. https://doi.org/10.1111/nph.17865
Varshney RK, Thudi M, Roorkiwal M et al (2019) (2019) Resequencing of 429 chickpea accessions from 45 countries provides insights into genome diversity, domestication and agronomic traits. Nat Genet 515(51):857–864. https://doi.org/10.1038/s41588-019-0401-3
Voytas DF, Gao C (2014) Precision genome engineering and agriculture: opportunities and regulatory challenges. PLoS Biol 12:1–6. https://doi.org/10.1371/journal.pbio.1001877
Wang H, Qin F (2017) Genome-wide association study reveals natural variations contributing to drought resistance in crops. Front Plant Sci 8:1–12. https://doi.org/10.3389/fpls.2017.01110
Wang N, Long T, Yao W et al (2013) Mutant resources for the functional analysis of the rice genome. Mol Plant 6:596–604. https://doi.org/10.1093/mp/sss142
Wang Y, Cheng X, Shan Q et al (2014) Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat Biotechnol 32:947–951. https://doi.org/10.1038/nbt.2969
Wang F, Wang C, Liu P et al (2016) Enhanced rice blast resistance by CRISPR/Cas9-targeted mutagenesis of the ERF transcription factor gene OsERF922. PLoS ONE 11:e0154027. https://doi.org/10.1371/journal.pone.0154027
Wang N, Fan X, He M et al (2022a) Transcriptional repression of TaNOX10 by TaWRKY19 compromises ROS generation and enhances wheat susceptibility to stripe rust. Plant Cell 34:1784–1803. https://doi.org/10.1093/plcell/koac001
Wang Z, Zhou L, Lan Y et al (2022b) An aspartic protease 47 causes quantitative recessive resistance to rice black-streaked dwarf virus disease and southern rice black-streaked dwarf virus disease. New Phytol 233:2520–2533. https://doi.org/10.1111/nph.17961
Weeks DP, Spalding MH, Yang B (2015) Use of designer nucleases for targeted gene and genome editing in plants. Plant Biotechnol J. https://doi.org/10.1111/pbi.12448
Wei FJ, Tsai YC, Hsu YM et al (2016) Lack of genotype and phenotype correlation in a rice T-DNA tagged line is likely caused by introgression in the seed source. PLoS ONE 11:1–17. https://doi.org/10.1371/journal.pone.0155768
Wellings CR (2011) Global status of stripe rust: a review of historical and current threats. Euphytica 179:129–141. https://doi.org/10.1007/s10681-011-0360-y
Weng J, Gu S, Wan X et al (2008) Isolation and initial characterization of GW5, a major QTL associated with rice grain width and weight. Cell Res 18:1199–1209. https://doi.org/10.1038/cr.2008.307
Wu X, Scott DA, Kriz AJ et al (2014) (2014) Genome-wide binding of the CRISPR endonuclease Cas9 in mammalian cells. Nat Biotechnol 327(32):670–676. https://doi.org/10.1038/nbt.2889
Wu T, Ali A, Wang J, Song J, Fang Y, Zhou T, Wu X (2021) A homologous gene of OsREL2/ASP1, ASP-LSL regulates pleiotropic phenotype including long sterile lemma in rice. BMC Plant Biol 21(1):1–15. https://doi.org/10.1186/S12870-021-03163-7
Wulff BBH, Dhugga KS (2018) Wheat-the cereal abandoned by GM. Science 80(361):451–452. https://doi.org/10.1126/science.aat5119
Xie K, Minkenberg B, Yang Y (2015) Boosting CRISPR/Cas9 multiplex editing capability with the endogenous tRNA-processing system. Proc Natl Acad Sci 112:3570–3575. https://doi.org/10.1073/pnas.1420294112
Xing H-L, Dong L, Wang Z-P et al (2014) A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biol 14:327. https://doi.org/10.1186/s12870-014-0327-y
Xu R, Yang Y, Qin R et al (2016) Rapid improvement of grain weight via highly efficient CRISPR/Cas9-mediated multiplex genome editing in rice. J Genet Genom 43:529–532. https://doi.org/10.1016/J.JGG.2016.07.003
Xu R, Li Y, Sui Z et al (2021) A C-terminal encoded peptide, ZmCEP1, is essential for kernel development in maize. J Exp Bot 72:5390–5406. https://doi.org/10.1093/JXB/ERAB224
Yin X, Biswal AK, Dionora J et al (2017) CRISPR-Cas9 and CRISPR-Cpf1 mediated targeting of a stomatal developmental gene EPFL9 in rice. Plant Cell Rep 36:745–757. https://doi.org/10.1007/s00299-017-2118-z
Yu J, Hu S, Wang J et al (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 80(296):79–92. https://doi.org/10.1126/science.1068037
Zhang H, Zhao Q, Sun ZZ et al (2011) Development and high-throughput genotyping of substitution lines carring the chromosome segments of indica 9311 in the background of japonica Nipponbare. J Genet Genom 38:603–611. https://doi.org/10.1016/J.JGG.2011.11.004
Zhang J, Zhang H, Botella JR, Zhu JK (2018a) Generation of new glutinous rice by CRISPR/Cas9-targeted mutagenesis of the Waxy gene in elite rice varieties. J Integr Plant Biol 60:369–375. https://doi.org/10.1111/JIPB.12620
Zhang Y, Li D, Zhang D et al (2018b) Analysis of the functions of TaGW2 homoeologs in wheat grain weight and protein content traits. Plant J 94:857–866. https://doi.org/10.1111/TPJ.13903
Zhang A, Liu Y, Wang F et al (2019a) Enhanced rice salinity tolerance via CRISPR/Cas9-targeted mutagenesis of the OsRR22 gene. Mol Breed 39:47. https://doi.org/10.1007/s11032-019-0954-y
Zhang Z, Guo J, Zhao Y, Chen J (2019b) Identification and characterization of maize ACD6 -like gene reveal ZmACD6 as the maize orthologue conferring resistance to Ustilago maydis. Plant Signal Behav 14:e1651604. https://doi.org/10.1080/15592324.2019.1651604
Zhao DS, Li QF, Zhang CQ et al (2018) GS9 acts as a transcriptional activator to regulate rice grain shape and appearance quality. Nat Commun. https://doi.org/10.1038/s41467-018-03616-y
Zheng M, Lin J, Liu X et al (2021) Histone acetyltransferase TaHAG1 acts as a crucial regulator to strengthen salt tolerance of hexaploid wheat. Plant Physiol 186:1951–1969. https://doi.org/10.1093/plphys/kiab187
Zhou J, Peng Z, Long J et al (2015) Gene targeting by the TAL effector PthXo2 reveals cryptic resistance gene for bacterial blight of rice. Plant J 82(4):632–643. https://doi.org/10.1111/tpj.12838
Zhou X, Liao H, Chern M et al (2018) Loss of function of a rice TPR-domain RNA-binding protein confers broad-spectrum disease resistance. Proc Natl Acad Sci 115:3174–3179. https://doi.org/10.1073/pnas.1705927115
Zong Y, Wang Y, Li C et al (2017) Precise base editing in rice, wheat and maize with a Cas9-cytidine deaminase fusion. Nat Biotechnol 35:438–440. https://doi.org/10.1038/nbt.3811
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Liang, Y., Li, C., Mangauthia, S.K. et al. Precision genetic technologies for cereal functional genomics. J. Plant Biochem. Biotechnol. 32, 673–687 (2023). https://doi.org/10.1007/s13562-023-00862-0
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DOI: https://doi.org/10.1007/s13562-023-00862-0