Abstract
Since its inception in 2012, CRISPR-Cas technologies have taken the life science community by storm. Maize genetics research is no exception. Investigators around the world have adapted CRISPR tools to advance maize genetics research in many ways. The principle application has been targeted mutagenesis to confirm candidate genes identified using map-based methods. Researchers are also developing tools to more effectively apply CRISPR-Cas technologies to maize because successful application of CRISPR-Cas relies on target gene identification, guide RNA development, vector design and construction, CRISPR-Cas reagent delivery to maize tissues, and plant characterization, each contributing unique challenges to CRISPR-Cas efficacy. Recent advances continue to chip away at major barriers that prevent more widespread use of CRISPR-Cas technologies in maize, including germplasm-independent delivery of CRISPR-Cas reagents and production of high-resolution genomic data in relevant germplasm to facilitate CRISPR-Cas experimental design. This has led to the development of novel breeding tools to advance maize genetics and demonstrations of how CRISPR-Cas technologies might be used to enhance maize germplasm.
Similar content being viewed by others
Data availability
Not applicable.
References
Agarwal A, Yadava P, Kumar K, Singh I, Kaul T, Pattanayak A, Agrawal PK (2018) Insights into maize genome editing via CRISPR/Cas9. Physiol Mol Biol Plants Int J Funct Plant Biol 24:175–183. https://doi.org/10.1007/s12298-017-0502-3
Agrotis A, Ketteler R (2015) A new age in functional genomics using CRISPR/Cas9 in arrayed library screening. Front Genet 6. https://doi.org/10.3389/fgene.2015.00300
Altpeter F, Springer NM, Bartley LE, Blechl A, Brutnell TP, Citovsky V, Conrad L, Gelvin SB, Jackson D, Kausch AP, Lemaux PG, Medford JI, Orozo-Cardenas M, Tricoli D, VanEck J, Voytas DF, Walbot V, Wang K, Zhang ZJ, Stewart CN Jr (2016) Advancing crop transformation in the era of genome editing. Plant Cell 28:1510–1520. https://doi.org/10.1105/tpc.16.00196
Andorf C, Beavis WD, Hufford M, Smith S, Suza WP, Wang K, Woodhouse M, Yu J, Lübberstedt T (2019) Technological advances in maize breeding: past, present and future. Theor Appl Genet 132:817–849. https://doi.org/10.1007/s00122-019-03306-3
Anzalone AV, Randolph PB, Davis JR et al (2019) Search-and-replace genome editing without double-strand breaks or donor DNA. Nature:1–9. https://doi.org/10.1038/s41586-019-1711-4
Armario Najera V, Twyman RM, Christou P, Zhu C (2019) Applications of multiplex genome editing in higher plants. Curr Opin Biotechnol 59:93–102. https://doi.org/10.1016/j.copbio.2019.02.015
Bae S, Park J, Kim J-S (2014) Cas-OFFinder: a fast and versatile algorithm that searches for potential off-target sites of Cas9 RNA-guided endonucleases. Bioinformatics 30:1473–1475. https://doi.org/10.1093/bioinformatics/btu048
Barone P, Wu E, Lenderts B, Anand A, Gordon-Kamm W, Svitashev S, Kumar S (2020) Efficient gene targeting in maize using inducible CRISPR-Cas9 and marker-free donor template. Mol Plant. 13:1219–1227. https://doi.org/10.1016/j.molp.2020.06.008
Bayer PE, Golicz AA, Scheben A, Batley J, Edwards D (2020) Plant pan-genomes are the new reference. Nat Plants 6:914–920. https://doi.org/10.1038/s41477-020-0733-0
Boyle EA, Li YI, Pritchard JK (2017) An expanded view of complex traits: from polygenic to omnigenic. Cell 169:1177–1186. https://doi.org/10.1016/j.cell.2017.05.038
Brazelton VA, Zarecor S, Wright DA et al (2015) A quick guide to CRISPR sgRNA design tools. GM Crops Food 6:266–276. https://doi.org/10.1080/21645698.2015.1137690
Budhagatapalli N, Halbach T, Hiekel S, Büchner H, Müller AE, Kumlehn J (2020) Site-directed mutagenesis in bread and durum wheat via pollination by cas9/guide RNA-transgenic maize used as haploidy inducer. Plant Biotechnol J n/a 18:2376–2378. https://doi.org/10.1111/pbi.13415
Campa CC, Weisbach NR, Santinha AJ, Incarnato D, Platt RJ (2019) Multiplexed genome engineering by Cas12a and CRISPR arrays encoded on single transcripts. Nat Methods 16:887–893. https://doi.org/10.1038/s41592-019-0508-6
Cao Y, Lim E, Xu M, et al (2020) Precision delivery of multiscale payloads to tissue-specific targets in plants. Adv Sci n/a:1903551. https://doi.org/10.1002/advs.201903551
Čermák T, Curtin SJ, Gil-Humanes J, Čegan R, Kono TJY, Konečná E, Belanto JJ, Starker CG, Mathre JW, Greenstein RL, Voytas DF (2017) A multipurpose toolkit to enable advanced genome engineering in plants. Plant Cell Online 29:1196–1217. https://doi.org/10.1105/tpc.16.00922
Char SN, Unger-Wallace E, Frame B, Briggs SA, Main M, Spalding MH, Vollbrecht E, Wang K, Yang B (2015) Heritable site-specific mutagenesis using TALENs in maize. Plant Biotechnol J 13:1002–1010. https://doi.org/10.1111/pbi.12344
Char SN, Neelakandan AK, Nahampun H, Frame B, Main M, Spalding MH, Becraft PW, Meyers BC, Walbot V, Wang K, Yang B (2017) An agrobacterium-delivered CRISPR/Cas9 system for high-frequency targeted mutagenesis in maize. Plant Biotechnol J 15:257–268. https://doi.org/10.1111/pbi.12611
Chavas J-P, Shi G, Lauer J (2014) The effects of GM technology on maize yield. Crop Sci 54:1331–1335. https://doi.org/10.2135/cropsci2013.10.0709
Chen Q, Han Y, Liu H, Wang X, Sun J, Zhao B, Li W, Tian J, Liang Y, Yan J, Yang X, Tian F (2018a) Genome-wide association analyses reveal the importance of alternative splicing in diversifying gene function and regulating phenotypic variation in maize. Plant Cell 30:1404–1423. https://doi.org/10.1105/tpc.18.00109
Chen R, Xu Q, Liu Y, Zhang J, Ren D, Wang G, Liu Y (2018b) Generation of Transgene-free maize male sterile lines using the CRISPR/Cas9 system. Front Plant Sci 9. https://doi.org/10.3389/fpls.2018.01180
Chen K, Wang Y, Zhang R, Zhang H, Gao C (2019) CRISPR/Cas genome editing and precision plant breeding in agriculture. Annu Rev Plant Biol 70:667–697. https://doi.org/10.1146/annurev-arplant-050718-100049
Chilcoat D, Liu Z-B, Sander J (2017) Use of CRISPR/Cas9 for crop improvement in maize and soybean. Prog Mol Biol Transl Sci 149:27–46. https://doi.org/10.1016/bs.pmbts.2017.04.005
Chuai G, Ma H, Yan J, Chen M, Hong N, Xue D, Zhou C, Zhu C, Chen K, Duan B, Gu F, Qu S, Huang D, Wei J, Liu Q (2018) DeepCRISPR: optimized CRISPR guide RNA design by deep learning. Genome Biol 19:80. https://doi.org/10.1186/s13059-018-1459-4
Claeys H, Vi SL, Xu X, Satoh-Nagasawa N, Eveland AL, Goldshmidt A, Feil R, Beggs GA, Sakai H, Brennan RG, Lunn JE, Jackson D (2019) Control of meristem determinacy by trehalose 6-phosphate phosphatases is uncoupled from enzymatic activity. Nat Plants 5:352–357. https://doi.org/10.1038/s41477-019-0394-z
Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA, Zhang F (2013) Multiplex genome engineering using CRISPR/Cas systems. Science 339:819–823. https://doi.org/10.1126/science.1231143
Datlinger P, Rendeiro AF, Schmidl C, Krausgruber T, Traxler P, Klughammer J, Schuster LC, Kuchler A, Alpar D, Bock C (2017) Pooled CRISPR screening with single-cell transcriptome readout. Nat Methods 14:297–301. https://doi.org/10.1038/nmeth.4177
Davern SM, McKnight TE, Standaert RF et al (2016) Carbon nanofiber arrays: a novel tool for microdelivery of biomolecules to plants. PLoS ONE 11:e0153621. https://doi.org/10.1371/journal.pone.0153621
Debernardi JM, Tricoli DM, Ercoli MF, Hayta S, Ronald P, Palatnik JF, Dubcovsky J (2020) A GRF–GIF chimeric protein improves the regeneration efficiency of transgenic plants. Nat Biotechnol 38:1–6. https://doi.org/10.1038/s41587-020-0703-0
Demirer GS, Zhang H, Matos JL, Goh NS, Cunningham FJ, Sung Y, Chang R, Aditham AJ, Chio L, Cho MJ, Staskawicz B, Landry MP (2019) High aspect ratio nanomaterials enable delivery of functional genetic material without DNA integration in mature plants. Nat Nanotechnol 14:456–464. https://doi.org/10.1038/s41565-019-0382-5
Deodhar GV, Adams ML, Trewyn BG (2017) Controlled release and intracellular protein delivery from mesoporous silica nanoparticles. Biotechnol J 12:1600408. https://doi.org/10.1002/biot.201600408
Dixit A, Parnas O, Li B et al (2016) Perturb-seq: dissecting molecular circuits with scalable single cell RNA profiling of pooled genetic screens. Cell 167:1853–1866.e17. https://doi.org/10.1016/j.cell.2016.11.038
Doll NM, Gilles LM, Gérentes M-F, Richard C, Just J, Fierlej Y, Borrelli VMG, Gendrot G, Ingram GC, Rogowsky PM, Widiez T (2019) Single and multiple gene knockouts by CRISPR–Cas9 in maize. Plant Cell Rep. 38:487–501. https://doi.org/10.1007/s00299-019-02378-1
Dong L, Li L, Liu C, Liu C, Geng S, Li X, Huang C, Mao L, Chen S, Xie C (2018) Genome editing and double-fluorescence proteins enable robust maternal haploid induction and identification in maize. Mol Plant 11:1214–1217. https://doi.org/10.1016/j.molp.2018.06.011
Duvick DN (2005) The contribution of breeding to yield advances in maize (Zea mays L.). In: Advances in Agronomy. Academic Press, pp 83–145
Ellison EE, Nagalakshmi U, Gamo ME, Huang PJ, Dinesh-Kumar S, Voytas DF (2020) Multiplexed heritable gene editing using RNA viruses and mobile single guide RNAs. Nat Plants 6:620–624. https://doi.org/10.1038/s41477-020-0670-y
El-Mounadi K, Morales-Floriano ML, Garcia-Ruiz H (2020) Principles, applications, and biosafety of plant genome editing using CRISPR-Cas9. Front Plant Sci 11. https://doi.org/10.3389/fpls.2020.00056
Endo M, Mikami M, Endo A, Kaya H, Itoh T, Nishimasu H, Nureki O, Toki S (2019) Genome editing in plants by engineered CRISPR–Cas9 recognizing NG PAM. Nat Plants 5:14–17. https://doi.org/10.1038/s41477-018-0321-8
Feng C, Yuan J, Wang R, Liu Y, Birchler JA, Han F (2016) Efficient targeted genome modification in maize using CRISPR/Cas9 system. J Genet Genomics 43:37–43. https://doi.org/10.1016/j.jgg.2015.10.002
Feng C, Su H, Bai H, Wang R, Liu Y, Guo X, Liu C, Zhang J, Yuan J, Birchler JA, Han F (2018) High-efficiency genome editing using a dmc1 promoter-controlled CRISPR/Cas9 system in maize. Plant Biotechnol J 16:1848–1857. https://doi.org/10.1111/pbi.12920
Fuglie K, Clancy M, Heisey P, Macdonald J (2017) Research, productivity, and output growth in U.S. agriculture. J Agric Appl Econ 49:514–554. https://doi.org/10.1017/aae.2017.13
Gao H, Gadlage MJ, Lafitte HR, Lenderts B, Yang M, Schroder M, Farrell J, Snopek K, Peterson D, Feigenbutz L, Jones S, St Clair G, Rahe M, Sanyour-Doyel N, Peng C, Wang L, Young JK, Beatty M, Dahlke B, Hazebroek J, Greene TW, Cigan AM, Chilcoat ND, Meeley RB (2020a) Superior field performance of waxy corn engineered using CRISPR–Cas9. Nat Biotechnol 38:579–581. https://doi.org/10.1038/s41587-020-0444-0
Gao H, Mutti J, Young JK, Yang M, Schroder M, Lenderts B, Wang L, Peterson D, St. Clair G, Jones S, Feigenbutz L, Marsh W, Zeng M, Wagner S, Farrell J, Snopek K, Scelonge C, Sopko X, Sander JD, Betts S, Cigan AM, Chilcoat ND (2020b) Complex trait loci in maize enabled by CRISPR-Cas9 mediated gene insertion. Front Plant Sci 11:535. https://doi.org/10.3389/fpls.2020.00535
Grünewald J, Zhou R, Iyer S, Lareau CA, Garcia SP, Aryee MJ, Joung JK (2019) CRISPR DNA base editors with reduced RNA off-target and self-editing activities. Nat Biotechnol 37:1041–1048. https://doi.org/10.1038/s41587-019-0236-6
Hoerster G, Wang N, Ryan L, Wu E, Anand A, McBride K, Lowe K, Jones T, Gordon-Kamm B (2020) Use of non-integrating Zm-Wus2 vectors to enhance maize transformation. Vitro Cell Dev Biol Plant. 56:265–279. https://doi.org/10.1007/s11627-019-10042-2
Hu J, Li S, Li Z, Li H, Song W, Zhao H, Lai J, Xia L, Li D, Zhang Y (2019) A barley stripe mosaic virus-based guide RNA delivery system for targeted mutagenesis in wheat and maize. Mol Plant Pathol 0: https://doi.org/10.1111/mpp.12849
Huang C, Sun H, Xu D, Chen Q, Liang Y, Wang X, Xu G, Tian J, Wang C, Li D, Wu L, Yang X, Jin W, Doebley JF, Tian F (2018) ZmCCT9 enhances maize adaptation to higher latitudes. Proc Natl Acad Sci U S A 115:E334–E341. https://doi.org/10.1073/pnas.1718058115
Imai R, Hamada H, Liu Y, Linghu Q, Kumagai Y, Nagira Y, Miki R, Taoka N (2020) In planta particle bombardment (iPB): a new method for plant transformation and genome editing. Plant Biotechnol 37:171–176. https://doi.org/10.5511/plantbiotechnology.20.0206a
Jaitin DA, Weiner A, Yofe I et al (2016) Dissecting immune circuits by linking CRISPR-pooled screens with single-cell RNA-Seq. Cell 167:1883–1896.e15. https://doi.org/10.1016/j.cell.2016.11.039
Jaqueth JS, Hou Z, Zheng P, Ren R, Nagel BA, Cutter G, Niu X, Vollbrecht E, Greene TW, Kumpatla SP (2020) Fertility restoration of maize CMS-C altered by a single amino acid substitution within the Rf4 bHLH transcription factor. Plant J Cell Mol Biol 101:101–111. https://doi.org/10.1111/tpj.14521
Jiang S, Cheng Q, Yan J, Fu R, Wang X (2020a) Genome optimization for improvement of maize breeding. Theor Appl Genet 133:1491–1502. https://doi.org/10.1007/s00122-019-03493-z
Jiang Y-Y, Chai Y-P, Lu M-H, et al (2020b) Prime editing efficiently generates W542L and S621I double mutations in two ALS genes of maize. bioRxiv 2020.07.06.188896. https://doi.org/10.1101/2020.07.06.188896
Jiao Y, Peluso P, Shi J, Liang T, Stitzer MC, Wang B, Campbell MS, Stein JC, Wei X, Chin CS, Guill K, Regulski M, Kumari S, Olson A, Gent J, Schneider KL, Wolfgruber TK, May MR, Springer NM, Antoniou E, McCombie WR, Presting GG, McMullen M, Ross-Ibarra J, Dawe RK, Hastie A, Rank DR, Ware D (2017) Improved maize reference genome with single-molecule technologies. Nature 546:524–527. https://doi.org/10.1038/nature22971
Jin S, Zong Y, Gao Q, Zhu Z, Wang Y, Qin P, Liang C, Wang D, Qiu JL, Zhang F, Gao C (2019) Cytosine, but not adenine, base editors induce genome-wide off-target mutations in rice. Science 364:292–295. https://doi.org/10.1126/science.aaw7166
Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337:816–821. https://doi.org/10.1126/science.1225829
Jorasch P (2020) Potential, Challenges, and Threats for the Application of New Breeding Techniques by the Private Plant Breeding Sector in the EU. Front Plant Sci 11. https://doi.org/10.3389/fpls.2020.582011
Kannan B, Jung JH, Moxley GW, Lee SM, Altpeter F (2018) TALEN-mediated targeted mutagenesis of more than 100 COMT copies/alleles in highly polyploid sugarcane improves saccharification efficiency without compromising biomass yield. Plant Biotechnol J 16:856–866. https://doi.org/10.1111/pbi.12833
Kelliher T, Starr D, Su X, Tang G, Chen Z, Carter J, Wittich PE, Dong S, Green J, Burch E, McCuiston J, Gu W, Sun Y, Strebe T, Roberts J, Bate NJ, Que Q (2019) One-step genome editing of elite crop germplasm during haploid induction. Nat Biotechnol 37:287–292. https://doi.org/10.1038/s41587-019-0038-x
Khumsupan P, Donovan S, McCormick AJ (2019) CRISPR/Cas in Arabidopsis: overcoming challenges to accelerate improvements in crop photosynthetic efficiencies. Physiol Plant 166:428–437. https://doi.org/10.1111/ppl.12937
Kim HK, Min S, Song M, Jung S, Choi JW, Kim Y, Lee S, Yoon S, Kim H(H) (2018) Deep learning improves prediction of CRISPR–Cpf1 guide RNA activity. Nat Biotechnol 36:239–241. https://doi.org/10.1038/nbt.4061
Klein M, Eslami-Mossallam B, Arroyo DG, Depken M (2018) Hybridization kinetics explains CRISPR-Cas off-targeting rules. Cell Rep 22:1413–1423. https://doi.org/10.1016/j.celrep.2018.01.045
Kleter GA, Kuiper HA, Kok EJ (2019) Gene-edited crops: towards a harmonized safety assessment. Trends Biotechnol 37:443–447. https://doi.org/10.1016/j.tibtech.2018.11.014
Knott GJ, Doudna JA (2018) CRISPR-Cas guides the future of genetic engineering. Science 361:866–869. https://doi.org/10.1126/science.aat5011
Koiso N, Toda E, Ichikawa M, Kato N, Okamoto T (2017) Development of gene expression system in egg cells and zygotes isolated from rice and maize. Plant Direct:1. https://doi.org/10.1002/pld3.10
Kumar K, Gambhir G, Dass A, Tripathi AK, Singh A, Jha AK, Yadava P, Choudhary M, Rakshit S (2020) Genetically modified crops: current status and future prospects. Planta 251:91. https://doi.org/10.1007/s00425-020-03372-8
Lawrence-Dill CJ, Schnable PS, Springer NM (2019) Idea factory: the maize genomes to fields initiative. Crop Sci 59:1406–1410. https://doi.org/10.2135/cropsci2019.02.0071
Lee K, Zhang Y, Kleinstiver BP, Guo JA, Aryee MJ, Miller J, Malzahn A, Zarecor S, Lawrence-Dill CJ, Joung JK, Qi Y, Wang K (2019a) Activities and specificities of CRISPR/Cas9 and Cas12a nucleases for targeted mutagenesis in maize. Plant Biotechnol J 17:362–372. https://doi.org/10.1111/pbi.12982
Lee K, Zhu H, Yang B, Wang K (2019b) An agrobacterium-Mediated CRISPR/Cas9 platform for genome editing in maize. Methods Mol Biol Clifton NJ 1917:121–143. https://doi.org/10.1007/978-1-4939-8991-1_10
Lei Y, Lu L, Liu H-Y, Li S, Xing F, Chen LL (2014) CRISPR-P: a web tool for synthetic single-guide RNA design of CRISPR-system in plants. Mol Plant 7:1494–1496. https://doi.org/10.1093/mp/ssu044
Li C, Liu C, Qi X, Wu Y, Fei X, Mao L, Cheng B, Li X, Xie C (2017a) RNA-guided Cas9 as an in vivo desired-target mutator in maize. Plant Biotechnol J 15:1566–1576. https://doi.org/10.1111/pbi.12739
Li J, Zhang H, Si X, Tian Y, Chen K, Liu J, Chen H, Gao C (2017b) Generation of thermosensitive male-sterile maize by targeted knockout of the ZmTMS5 gene. J Genet Genomics 44:465–468. https://doi.org/10.1016/j.jgg.2017.02.002
Li C, Yue Y, Chen H, Qi W, Song R (2018) The ZmbZIP22 transcription factor regulates 27-kD γ-Zein gene transcription during maize endosperm development. Plant Cell 30:2402–2424. https://doi.org/10.1105/tpc.18.00422
Li C, Song W, Luo Y, Gao S, Zhang R, Shi Z, Wang X, Wang R, Wang F, Wang J, Zhao Y, Su A, Wang S, Li X, Luo M, Wang S, Zhang Y, Ge J, Tan X, Yuan Y, Bi X, He H, Yan J, Wang Y, Hu S, Zhao J (2019a) The HuangZaoSi maize genome provides insights into genomic variation and improvement history of maize. Mol Plant 12:402–409. https://doi.org/10.1016/j.molp.2019.02.009
Li S, Li J, He Y, Xu M, Zhang J, du W, Zhao Y, Xia L (2019b) Precise gene replacement in rice by RNA transcript-templated homologous recombination. Nat Biotechnol 37:445–450. https://doi.org/10.1038/s41587-019-0065-7
Li H, Feng X, Chu C (2020a) The design and construction of reference pangenome graphs. ArXiv200306079 Q-Bio
Li Q, Wu G, Zhao Y, Wang B, Zhao B, Kong D, Wei H, Chen C, Wang H (2020b) CRISPR/Cas9-mediated knockout and overexpression studies reveal a role of maize phytochrome C in regulating flowering time and plant height. Plant Biotechnol J. 18:2520–2532. https://doi.org/10.1111/pbi.13429
Liang Z, Zhang K, Chen K, Gao C (2014) Targeted mutagenesis in Zea mays Using TALENs and the CRISPR/Cas system. J Genet Genomics 41:63–68. https://doi.org/10.1016/j.jgg.2013.12.001
Liang G, Zhang H, Lou D, Yu D (2016) Selection of highly efficient sgRNAs for CRISPR/Cas9-based plant genome editing. Sci Rep 6:21451. https://doi.org/10.1038/srep21451
Lin G, He C, Zheng J, et al (2020) Chromosome-level genome assembly of a regenerable maize inbred line A188. bioRxiv 2020.09.09.289611. https://doi.org/10.1101/2020.09.09.289611
Liu H, Ding Y, Zhou Y, Jin W, Xie K, Chen LL (2017a) CRISPR-P 2.0: an improved CRISPR-Cas9 tool for genome editing in plants. Mol Plant 10:530–532. https://doi.org/10.1016/j.molp.2017.01.003
Liu X, Zhang Y, Chen Y et al (2017b) In situ capture of chromatin interactions by biotinylated dCas9. Cell 170:1028–1043.e19. https://doi.org/10.1016/j.cell.2017.08.003
Liu G, Yin K, Zhang Q, Gao C, Qiu JL (2019) Modulating chromatin accessibility by transactivation and targeting proximal dsgRNAs enhances Cas9 editing efficiency in vivo. Genome Biol 20:145. https://doi.org/10.1186/s13059-019-1762-8
Liu H, Jian L, Xu J et al (2020a) High-throughput CRISPR/Cas9 mutagenesis streamlines trait gene identification in maize. Plant Cell. 32:1397–1413. https://doi.org/10.1105/tpc.19.00934
Liu J, Fernie AR, Yan J (2020b) The past, present, and future of maize improvement: domestication, genomics, and functional genomic routes toward crop enhancement. Plant Commun 1:100010. https://doi.org/10.1016/j.xplc.2019.100010
Lowder LG, Zhang D, Baltes NJ, Paul JW III, Tang X, Zheng X, Voytas DF, Hsieh TF, Zhang Y, Qi Y (2015) A CRISPR/Cas9 toolbox for multiplexed plant genome editing and transcriptional regulation. Plant Physiol 169:971–985. https://doi.org/10.1104/pp.15.00636
Maher MF, Nasti RA, Vollbrecht M, Starker CG, Clark MD, Voytas DF (2020) Plant gene editing through de novo induction of meristems. Nat Biotechnol 38:84–89. https://doi.org/10.1038/s41587-019-0337-2
Malzahn AA, Tang X, Lee K, Ren Q, Sretenovic S, Zhang Y, Chen H, Kang M, Bao Y, Zheng X, Deng K, Zhang T, Salcedo V, Wang K, Zhang Y, Qi Y (2019) Application of CRISPR-Cas12a temperature sensitivity for improved genome editing in rice, maize, and Arabidopsis. BMC Biol 17:9. https://doi.org/10.1186/s12915-019-0629-5
Manghwar H, Li B, Ding X, Hussain A, Lindsey K, Zhang X, Jin S (2020) CRISPR/Cas systems in genome editing: methodologies and tools for sgRNA design, off-target evaluation, and strategies to mitigate off-target effects. Adv Sci 7:1902312. https://doi.org/10.1002/advs.201902312
Martin-Ortigosa S, Peterson DJ, Valenstein JS, Lin VSY, Trewyn BG, Lyznik LA, Wang K (2014) Mesoporous silica nanoparticle-mediated intracellular Cre protein delivery for maize genome editing via loxP site excision. Plant Physiol 164:537–547. https://doi.org/10.1104/pp.113.233650
McFarland BA, AlKhalifah N, Bohn M et al (2020) Maize genomes to fields (G2F): 2014–2017 field seasons: genotype, phenotype, climatic, soil, and inbred ear image datasets. BMC Res Notes 13:71. https://doi.org/10.1186/s13104-020-4922-8
Mei Y, Beernink BM, Ellison EE, Konečná E, Neelakandan AK, Voytas DF, Whitham SA (2019) Protein expression and gene editing in monocots using foxtail mosaic virus vectors. Plant Direct 3:e00181. https://doi.org/10.1002/pld3.181
Ming M, Ren Q, Pan C, He Y, Zhang Y, Liu S, Zhong Z, Wang J, Malzahn AA, Wu J, Zheng X, Zhang Y, Qi Y (2020) CRISPR–Cas12b enables efficient plant genome engineering. Nat Plants 6:202–208. https://doi.org/10.1038/s41477-020-0614-6
Minkenberg B, Zhang J, Xie K, Yang Y (2019) CRISPR-PLANT v2: an online resource for highly specific guide RNA spacers based on improved off-target analysis. Plant Biotechnol J 17:5–8. https://doi.org/10.1111/pbi.13025
Mishra R, Joshi RK, Zhao K (2018) Genome editing in rice: recent advances, challenges, and future implications. Front Plant Sci 9:1361. https://doi.org/10.3389/fpls.2018.01361
Moradpour M, Abdulah SNA (2020) CRISPR/dCas9 platforms in plants: strategies and applications beyond genome editing. Plant Biotechnol J 18:32–44. https://doi.org/10.1111/pbi.13232
Naim F, Shand K, Hayashi S, O’Brien M, McGree J, Johnson AAT, Dugdale B, Waterhouse PM (2020) Are the current gRNA ranking prediction algorithms useful for genome editing in plants? PLOS ONE 15:e0227994. https://doi.org/10.1371/journal.pone.0227994
Němečková A, Wäsch C, Schubert V, Ishii T, Hřibová E, Houben A (2019) CRISPR/Cas9-based RGEN-ISL allows the simultaneous and specific visualization of proteins, DNA repeats, and sites of DNA replication. Cytogenet Genome Res 159:48–53. https://doi.org/10.1159/000502600
Nepolean T, Kaul J, Mukri G, Mittal S (2018) Genomics-enabled next-generation breeding approaches for developing system-specific drought tolerant hybrids in maize. Front Plant Sci 9:361. https://doi.org/10.3389/fpls.2018.00361
OECD, Nations F and AO of the U (2020) OECD-FAO Agricultural Outlook 2020-2029
Perez-Pinera P, Kocak DD, Vockley CM, Adler AF, Kabadi AM, Polstein LR, Thakore PI, Glass KA, Ousterout DG, Leong KW, Guilak F, Crawford GE, Reddy TE, Gersbach CA (2013) RNA-guided gene activation by CRISPR-Cas9-based transcription factors. Nat Methods 10:973–976. https://doi.org/10.1038/nmeth.2600
Piatek A, Ali Z, Baazim H, Li L, Abulfaraj A, al-Shareef S, Aouida M, Mahfouz MM (2015) RNA-guided transcriptional regulation in planta via synthetic dCas9-based transcription factors. Plant Biotechnol J 13:578–589. https://doi.org/10.1111/pbi.12284
Portwood JL, Woodhouse MR, Cannon EK et al (2019) MaizeGDB 2018: the maize multi-genome genetics and genomics database. Nucleic Acids Res 47:D1146–D1154. https://doi.org/10.1093/nar/gky1046
Potlapalli BP, Schubert V, Metje-Sprink J, Liehr T, Houben A (2020) Application of Tris-HCl allows the specific labeling of regularly prepared chromosomes by CRISPR-FISH. Cytogenet Genome Res 160:156–165. https://doi.org/10.1159/000506720
Qi LS, Larson MH, Gilbert LA, Doudna JA, Weissman JS, Arkin AP, Lim WA (2013) Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell 152:1173–1183. https://doi.org/10.1016/j.cell.2013.02.022
Qi W, Zhu T, Tian Z, Li C, Zhang W, Song R (2016) High-efficiency CRISPR/Cas9 multiplex gene editing using the glycine tRNA-processing system-based strategy in maize. BMC Biotechnol 16:58. https://doi.org/10.1186/s12896-016-0289-2
Qi X, Zhang C, Zhu J, Liu C, Huang C, Li X, Xie C (2020) Genome editing enables next-generation hybrid seed production technology. Mol Plant. 13:1262–1269. https://doi.org/10.1016/j.molp.2020.06.003
Que Q, Chilton M-DM, Elumalai S et al (2019) Repurposing macromolecule delivery tools for plant genetic modification in the era of precision genome engineering. In: Kumar S, Barone P, Smith M (eds) Transgenic plants: methods and protocols. Springer, New York, pp 3–18
Replogle JM, Xu A, Norman TM, et al (2018) Direct capture of CRISPR guides enables scalable, multiplexed, and multi-omic Perturb-seq. bioRxiv 503367. https://doi.org/10.1101/503367
Reynolds MP, Hellin J, Govaerts B, Kosina P, Sonder K, Hobbs P, Braun H (2012) Global crop improvement networks to bridge technology gaps. J Exp Bot 63:1–12. https://doi.org/10.1093/jxb/err241
Rodriguez-Leal D, Lemmon ZH, Man J et al (2017) Engineering quantitative trait variation for crop improvement by genome editing. Cell 171:470–480.e8. https://doi.org/10.1016/j.cell.2017.08.030
Sánchez-León S, Gil-Humanes J, Ozuna CV, Giménez MJ, Sousa C, Voytas DF, Barro F (2018) Low-gluten, nontransgenic wheat engineered with CRISPR/Cas9. Plant Biotechnol J 16:902–910. https://doi.org/10.1111/pbi.12837
Schinkel H, Schillberg S (2016) Genome editing: intellectual property and product development in plant biotechnology. Plant Cell Rep 35:1487–1491. https://doi.org/10.1007/s00299-016-1988-9
Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, Liang C, Zhang J, Fulton L, Graves TA, Minx P, Reily AD, Courtney L, Kruchowski SS, Tomlinson C, Strong C, Delehaunty K, Fronick C, Courtney B, Rock SM, Belter E, du F, Kim K, Abbott RM, Cotton M, Levy A, Marchetto P, Ochoa K, Jackson SM, Gillam B, Chen W, Yan L, Higginbotham J, Cardenas M, Waligorski J, Applebaum E, Phelps L, Falcone J, Kanchi K, Thane T, Scimone A, Thane N, Henke J, Wang T, Ruppert J, Shah N, Rotter K, Hodges J, Ingenthron E, Cordes M, Kohlberg S, Sgro J, Delgado B, Mead K, Chinwalla A, Leonard S, Crouse K, Collura K, Kudrna D, Currie J, He R, Angelova A, Rajasekar S, Mueller T, Lomeli R, Scara G, Ko A, Delaney K, Wissotski M, Lopez G, Campos D, Braidotti M, Ashley E, Golser W, Kim H, Lee S, Lin J, Dujmic Z, Kim W, Talag J, Zuccolo A, Fan C, Sebastian A, Kramer M, Spiegel L, Nascimento L, Zutavern T, Miller B, Ambroise C, Muller S, Spooner W, Narechania A, Ren L, Wei S, Kumari S, Faga B, Levy MJ, McMahan L, van Buren P, Vaughn MW, Ying K, Yeh CT, Emrich SJ, Jia Y, Kalyanaraman A, Hsia AP, Barbazuk WB, Baucom RS, Brutnell TP, Carpita NC, Chaparro C, Chia JM, Deragon JM, Estill JC, Fu Y, Jeddeloh JA, Han Y, Lee H, Li P, Lisch DR, Liu S, Liu Z, Nagel DH, McCann MC, SanMiguel P, Myers AM, Nettleton D, Nguyen J, Penning BW, Ponnala L, Schneider KL, Schwartz DC, Sharma A, Soderlund C, Springer NM, Sun Q, Wang H, Waterman M, Westerman R, Wolfgruber TK, Yang L, Yu Y, Zhang L, Zhou S, Zhu Q, Bennetzen JL, Dawe RK, Jiang J, Jiang N, Presting GG, Wessler SR, Aluru S, Martienssen RA, Clifton SW, McCombie WR, Wing RA, Wilson RK (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115. https://doi.org/10.1126/science.1178534
Semenova E, Jore MM, Datsenko KA, Semenova A, Westra ER, Wanner B, van der Oost J, Brouns SJJ, Severinov K (2011) Interference by clustered regularly interspaced short palindromic repeat (CRISPR) RNA is governed by a seed sequence. Proc Natl Acad Sci U S A 108:10098–10103. https://doi.org/10.1073/pnas.1104144108
Shalem O, Sanjana NE, Hartenian E, Shi X, Scott DA, Mikkelsen TS, Heckl D, Ebert BL, Root DE, Doench JG, Zhang F (2014) Genome-scale CRISPR-Cas9 knockout screening in human cells. Science 343:84–87. https://doi.org/10.1126/science.1247005
Shi J, Gao H, Wang H, Lafitte HR, Archibald RL, Yang M, Hakimi SM, Mo H, Habben JE (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
Shukla VK, Doyon Y, Miller JC, DeKelver RC, Moehle EA, Worden SE, Mitchell JC, Arnold NL, Gopalan S, Meng X, Choi VM, Rock JM, Wu YY, Katibah GE, Zhifang G, McCaskill D, Simpson MA, Blakeslee B, Greenwalt SA, Butler HJ, Hinkley SJ, Zhang L, Rebar EJ, Gregory PD, Urnov FD (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 M, Kim HK, Lee S, et al (2020) Sequence-specific prediction of the efficiencies of adenine and cytosine base editors. Nat Biotechnol 1–7. https://doi.org/10.1038/s41587-020-0573-5
Sretenovic S, Yin D, Levav A, et al (2020) Expanding plant genome-editing scope by an engineered iSpyMacCas9 system that targets a-rich PAM sequences. Plant Commun 100101. https://doi.org/10.1016/j.xplc.2020.100101
Sun J, Liu H, Liu J, Cheng S, Peng Y, Zhang Q, Yan J, Liu HJ, Chen LL (2019) CRISPR-Local: a local single-guide RNA (sgRNA) design tool for non-reference plant genomes. Bioinforma Oxf Engl 35:2501–2503. https://doi.org/10.1093/bioinformatics/bty970
Svitashev S, Young J, Schwartz C et al (2015) Targeted mutagenesis, precise gene editing and site-specific gene insertion in maize using Cas9 and guide RNA. Plant Physiol:00793.2015. https://doi.org/10.1104/pp.15.00793
Svitashev S, Schwartz C, Lenderts B, et al (2016) Genome editing in maize directed by CRISPR–Cas9 ribonucleoprotein complexes. Nat Commun 7:. https://doi.org/10.1038/ncomms13274
Tang X, Ren Q, Yang L, Bao Y, Zhong Z, He Y, Liu S, Qi C, Liu B, Wang Y, Sretenovic S, Zhang Y, Zheng X, Zhang T, Qi Y, Zhang Y (2019) Single transcript unit CRISPR 2.0 systems for robust Cas9 and Cas12a mediated plant genome editing. Plant Biotechnol J 17:1431–1445. https://doi.org/10.1111/pbi.13068
Taylor AP (2019) Companies use CRISPR to improve crops. Sci Mag
Teng C, Zhang H, Hammond R, Huang K, Meyers BC, Walbot V (2020) Dicer-like 5 deficiency confers temperature-sensitive male sterility in maize. Nat Commun 11:2912. https://doi.org/10.1038/s41467-020-16634-6
USDA (2020) World Agricultural Production. United States Department of Agriculture. https://apps.fas.usda.gov/psdonline/circulars/production.pdf
Uusi-Mäkelä MIE, Barker HR, Bäuerlein CA et al (2018) Chromatin accessibility is associated with CRISPR-Cas9 efficiency in the zebrafish (Danio rerio). PLoS ONE 13. https://doi.org/10.1371/journal.pone.0196238
Wang M, Lu Y, Botella JR, Mao Y, Hua K, Zhu JK (2017) Gene targeting by homology-directed repair in rice using a geminivirus-based CRISPR/Cas9 system. Mol Plant 10:1007–1010. https://doi.org/10.1016/j.molp.2017.03.002
Wang M, Mao Y, Lu Y, Wang Z, Tao X, Zhu JK (2018) Multiplex gene editing in rice with simplified CRISPR-Cpf1 and CRISPR-Cas9 systems. J Integr Plant Biol 60:626–631. https://doi.org/10.1111/jipb.12667
Wang B, Zhu L, Zhao B, Zhao Y, Xie Y, Zheng Z, Li Y, Sun J, Wang H (2019a) Development of a haploid-inducer mediated genome editing system for accelerating maize breeding. Mol Plant 12:597–602. https://doi.org/10.1016/j.molp.2019.03.006
Wang H, Yan S, Xin H, Huang W, Zhang H, Teng S, Yu YC, Fernie AR, Lu X, Li P, Li S, Zhang C, Ruan YL, Chen LQ, Lang Z (2019b) A subsidiary cell-localized glucose transporter promotes stomatal conductance and photosynthesis. Plant Cell 31:1328–1343. https://doi.org/10.1105/tpc.18.00736
Wang F, Cui P-J, Tian Y, Huang Y, Wang HF, Liu F, Chen YF (2020) Maize ZmPT7 regulates Pi uptake and redistribution which is modulated by phosphorylation. Plant Biotechnol J. 18:2406–2419. https://doi.org/10.1111/pbi.13414
Wolter F, Schindele P, Puchta H (2019) Plant breeding at the speed of light: the power of CRISPR/Cas to generate directed genetic diversity at multiple sites. BMC Plant Biol 19:176. https://doi.org/10.1186/s12870-019-1775-1
Wu Q, Regan M, Furukawa H, Jackson D (2018) Role of heterotrimeric Gα proteins in maize development and enhancement of agronomic traits. PLoS Genet 14:e1007374. https://doi.org/10.1371/journal.pgen.1007374
Wu G, Zhao Y, Shen R, Wang B, Xie Y, Ma X, Zheng Z, Wang H (2019a) Characterization of maize phytochrome-interacting factors in light signaling and photomorphogenesis. Plant Physiol:00239.2019. https://doi.org/10.1104/pp.19.00239
Wu T-M, Huang J-Z, Oung H-M et al (2019b) H2O2-based method for rapid detection of transgene-free rice plants from segregating CRISPR/Cas9 genome-edited progenies. Int J Mol Sci 20. https://doi.org/10.3390/ijms20163885
Wu H, Qian C, Wu C, Wang Z, Wang D, Ye Z, Ping J, Wu J, Ji F (2020a) End-point dual specific detection of nucleic acids using CRISPR/Cas12a based portable biosensor. Biosens Bioelectron 157:112153. https://doi.org/10.1016/j.bios.2020.112153
Wu Q, Xu F, Liu L, Char SN, Ding Y, Je BI, Schmelz E, Yang B, Jackson D (2020b) The maize heterotrimeric G protein β subunit controls shoot meristem development and immune responses. Proc Natl Acad Sci U S A 117:1799–1805. https://doi.org/10.1073/pnas.1917577116
Xie K, Wu S, Li Z, Zhou Y, Zhang D, Dong Z, An X, Zhu T, Zhang S, Liu S, Li J, Wan X (2018) Map-based cloning and characterization of Zea mays male sterility33 (ZmMs33) gene, encoding a glycerol-3-phosphate acyltransferase. TAG Theor Appl Genet Theor Angew Genet 131:1363–1378. https://doi.org/10.1007/s00122-018-3083-9
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. https://doi.org/10.1186/s12870-014-0327-y
Xu W, Zhang C, Yang Y, Zhao S, Kang G, He X, Song J, Yang J (2020) Versatile nucleotides substitution in plant using an improved prime editing system. Mol Plant 13:675–678. https://doi.org/10.1016/j.molp.2020.03.012
Yadava P, Abhishek A, Singh R, Singh I, Kaul T, Pattanayak A, Agrawal PK (2016) Advances in maize transformation technologies and development of transgenic maize. Front Plant Sci 7:1949. https://doi.org/10.3389/fpls.2016.01949
Yin K, Gao C, Qiu J-L (2017) Progress and prospects in plant genome editing. Nat Plants 3:nplants2017107. https://doi.org/10.1038/nplants.2017.107
Young J, Zastrow-Hayes G, Deschamps S, Svitashev S, Zaremba M, Acharya A, Paulraj S, Peterson-Burch B, Schwartz C, Djukanovic V, Lenderts B, Feigenbutz L, Wang L, Alarcon C, Siksnys V, May G, Chilcoat ND, Kumar S (2019) CRISPR-Cas9 editing in maize: systematic evaluation of off-target activity and its relevance in crop improvement. Sci Rep 9:6729. https://doi.org/10.1038/s41598-019-43141-6
Zhang Q, Zhang Y, Lu M-H, Chai YP, Jiang YY, Zhou Y, Wang XC, Chen QJ (2019a) A novel ternary vector system united with morphogenic genes enhances CRISPR/Cas delivery in maize. Plant Physiol 181:1441–1448. https://doi.org/10.1104/pp.19.00767
Zhang Y, Malzahn AA, Sretenovic S, Qi Y (2019b) The emerging and uncultivated potential of CRISPR technology in plant science. Nat Plants 5:778–794. https://doi.org/10.1038/s41477-019-0461-5
Zhang J, Feng C, Su H, Liu Y, Liu Y, Han F (2020a) The cohesion complex subunit ZmSMC3 participates in meiotic centromere pairing in maize. Plant Cell 32:1323–1336. https://doi.org/10.1105/tpc.19.00834
Zhang Y, Pribil M, Palmgren M, Gao C (2020b) A CRISPR way for accelerating improvement of food crops. Nat Food 1:200–205. https://doi.org/10.1038/s43016-020-0051-8
Zhang Z, Zhang X, Lin Z, Wang J, Liu H, Zhou L, Zhong S, Li Y, Zhu C, Lai J, Li X, Yu J, Lin Z (2020c) A large transposon insertion in the stiff1 promoter increases stalk strength in maize. Plant Cell 32:152–165. https://doi.org/10.1105/tpc.19.00486
Zhao H, Qin Y, Xiao Z, Li Q, Yang N, Pan Z, Gong D, Sun Q, Yang F, Zhang Z, Wu Y, Xu C, Qiu F (2020) Loss of function of an RNAPIII subunit leads to impaired maize kernel development. Plant Physiol. 184:359–373. https://doi.org/10.1104/pp.20.00502
Zhong Y, Liu C, Qi X, Jiao Y, Wang D, Wang Y, Liu Z, Chen C, Chen B, Tian X, Li J, Chen M, Dong X, Xu X, Li L, Li W, Liu W, Jin W, Lai J, Chen S (2019a) Mutation of ZmDMP enhances haploid induction in maize. Nat Plants 5:575–580. https://doi.org/10.1038/s41477-019-0443-7
Zhong Z, Sretenovic S, Ren Q, Yang L, Bao Y, Qi C, Yuan M, He Y, Liu S, Liu X, Wang J, Huang L, Wang Y, Baby D, Wang D, Zhang T, Qi Y, Zhang Y (2019b) Improving plant genome editing with high-fidelity xCas9 and non-canonical PAM-targeting Cas9-NG. Mol Plant 12:1027–1036. https://doi.org/10.1016/j.molp.2019.03.011
Zhu J, Song N, Sun S, Yang W, Zhao H, Song W, Lai J (2016) Efficiency and inheritance of targeted mutagenesis in maize using CRISPR-Cas9. J Genet Genomics 43:25–36. https://doi.org/10.1016/j.jgg.2015.10.006
Zlobin NE, Lebedeva MV, Taranov VV (2020) CRISPR/Cas9 genome editing through in planta transformation. Crit Rev Biotechnol 40:153–168. https://doi.org/10.1080/07388551.2019.1709795
Zong Y, Wang Y, Li C, Zhang R, Chen K, Ran Y, Qiu JL, Wang D, Gao C (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
Zuo Y, Feng F, Qi W, Song R (2019) Dek42 encodes an RNA-binding protein that affects alternative pre-mRNA splicing and maize kernel development. J Integr Plant Biol 61:728–748. https://doi.org/10.1111/jipb.12798
Acknowledgments
We would like to thank Dave Jackson for the invitation to write this review, Nathan Springer, Yiping Qi, and Christy Gault for constructive feedback on early drafts of the manuscript, Catherine Feuillet for support and our many colleagues at Inari Agriculture for stimulating discussions and suggestions.
Author information
Authors and Affiliations
Contributions
MLN conceived the project, outlined the research, contributed to the research, and wrote the paper. HC and KSH contributed to the research and wrote the paper.
Corresponding author
Ethics declarations
Conflict of interest
The authors are employees of Inari Agriculture, Inc. (MLN) and Inari Agriculture, NV (HC, KSH), each a for profit agricultural biotechnology company.
Ethics approval and consent to participate
Not applicable.
Consent for publication
Not applicable.
Code availability
Not applicable.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
This article is part of the Topical Collection on Maize Genetics, Genomics and Sustainable Improvement.
Supplementary Information
ESM 1
(XLSX 99.2 kb)
Rights and permissions
About this article
Cite this article
Nuccio, M.L., Claeys, H. & Heyndrickx, K.S. CRISPR-Cas technology in corn: a new key to unlock genetic knowledge and create novel products. Mol Breeding 41, 11 (2021). https://doi.org/10.1007/s11032-021-01200-9
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11032-021-01200-9