Abstract
The advent of genome editing has opened new avenues for targeted trait enhancement in fruit, ornamental, industrial, and all specialty crops. In particular, CRISPR-based editing systems, derived from bacterial immune systems, have quickly become routinely used tools for research groups across the world seeking to edit plant genomes with a greater level of precision, higher efficiency, reduced off-target effects, and overall ease-of-use compared to ZFNs and TALENs. CRISPR systems have been applied successfully to a number of horticultural and industrial crops to enhance fruit ripening, increase stress tolerance, modify plant architecture, control the timing of flower development, and enhance the accumulation of desired metabolites, among other commercially-important traits. As editing technologies continue to advance, so too does the ability to generate improved crop varieties with non-transgenic modifications; in some crops, direct transgene-free edits have already been achieved, while in others, T-DNAs have successfully been segregated out through crossing. In addition to the potential to produce non-transgenic edited crops, and thereby circumvent regulatory impediments to the release of new, improved crop varieties, targeted gene editing can speed up trait improvement in crops with long juvenile phases, reducing inputs resulting in faster market introduction to the market. While many challenges remain regarding optimization of genome editing in ornamental, fruit, and industrial crops, the ongoing discovery of novel nucleases with niche specialties for engineering applications may form the basis for additional and potentially crop-specific editing strategies.
Similar content being viewed by others
References
Alagoz Y, Gurkok T, Zhang B, Unver T (2016) Manipulating the biosynthesis of bioactive compound alkaloids for next-generation metabolic engineering in opium poppy using CRISPR-Cas 9 genome editing technology. Sci Rep. https://doi.org/10.1038/srep30910
Ayar A, Wehrkamp-Richter S, Laffaire J et al (2013) Gene targeting in maize by somatic ectopic recombination. Plant Biotechnol J 11:305–314
Bahri BA, Daverdin G, Xu X et al (2018) Natural variation in genes potentially involved in plant architecture and adaptation in switchgrass (Panicum virgatum L.). BMC Evol Biol 18:91. https://doi.org/10.1186/s12862-018-1193-2
Bouasker M, Belayachi N, Hoxha D, Al-Makhtar M (2014) Physical characterization of natural straw fibers as aggregates for construction materials applications. Materials (Basel) 7:3034–3048. https://doi.org/10.3390/ma7043034
Bouis HE (2002) Plant breeding: a new tool for fighting micronutrient malnutrition. J Nutr 132:491S-494S. https://doi.org/10.1093/jn/132.3.491s
Braatz J, Harloff H-J, Mascher M, Stein N, Himmelbach A, Jung C (2017) CRISPR-Cas9 targeted mutagenesis leads to simultaneous modification of different homoeologous gene copies in polyploid oilseed rape (Brassica napus). Plant Physiol 174(2):935–942. https://doi.org/10.1104/pp.17.00426
Brooks C, Nekrasov V, Lippman ZB, Van Eck J (2014) Efficient gene editing in tomato in the first generation using the clustered regularly interspaced short palindromic repeats/CRISPR-Associated9 system. Plant Physiol 166:1292–1297. https://doi.org/10.1104/pp.114.247577
Budiani A, Nugroho IB, Sari AD, Palupi I, Putranto RA (2019) CRISPR/Cas9-mediated knockout of an oil palm defense-related gene to the pathogenic fungus Ganoderma boninense. Indonesian J Biotechnol 24(2):100. https://journal.ugm.ac.id/ijbiotech/article/view/52170/26701
Cai L, Zhang L, Fu Q, Xu ZF (2018) Identification and expression analysis of cytokinin metabolic genes IPTs, CYP735A and CKXs in the biofuel. PeerJ 6:e4812. https://doi.org/10.7717/peerj.4812
Čermák T, Baltes NJ, Čegan R et al (2015) High-frequency, precise modification of the tomato genome. Genome Biol. https://doi.org/10.1186/s13059-015-0796-9
Chandler SF, Brugliera F (2011) Genetic modification in floriculture. Biotechnol Lett 33:207–214. https://doi.org/10.1007/s10529-010-0424-4
Chandrasekaran J, Brumin M, Wolf D et al (2016) Development of broad virus resistance in non-transgenic cucumber using CRISPR/Cas9 technology. Mol Plant Pathol 17:1140–1153
Charrier A, Vergne E, Dousset N et al (2019) Efficient targeted mutagenesis in apple and first time edition of pear using the CRISPR-Cas9 system. Front Plant Sci 10:1–12. https://doi.org/10.3389/fpls.2019.00040
Cherney J, Small E (2016) Industrial hemp in North America: production. Politics Potential Agron 6:58. https://doi.org/10.3390/agronomy6040058
Cornille A, Giraud T, Smulders MJM et al (2014) The domestication and evolutionary ecology of apples. Trends Genet 30:57–65. https://doi.org/10.1016/j.tig.2013.10.002
Cornish K (2017) Alternative natural rubber crops: why should we care? Technol Innov 18:245–256. https://doi.org/10.21300/18.4.2017.245
Cornish K, Wenshuang X (2012) Natural rubber biosynthesis in plants: rubber transferase|Elsevier Enhanced Reader. In: Hopwood DA (ed) Methods in enzymology. Academic Press Inc, Cambridge, pp 63–82
Crosby JA, Janick J, Pecknold PC et al (1992) Breeding apples for scab resistance: 1945–1990. In: Acta horticulturae. International Society for Horticultural Science (ISHS), Leuven, pp 43–70
D’Ambrosio C, Stigliani AL, Giorio G (2018) CRISPR/Cas9 editing of carotenoid genes in tomato. Transgenic Res 27:367–378. https://doi.org/10.1007/s11248-018-0079-9
D’hont A, Denoeud F, Aury J-M et al (2012) The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature 488:213–217
Dai Y, Hu G, Dupas A, Medina L, Blandels N, San Clemente H, Ladouce N, Badawi M, Hernandez-Raquet G, Mounet F, Grima-Pettenati J, Cassan-Wang H (2020) Implementing the CRISPR/Cas9 technology in eucalyptus hairy roots using wood-related genes. Int J Mol Sci 21(10):3408. https://doi.org/10.3390/ijms21103408
Danilo B, Perrot L, Mara K et al (2019) Efficient and transgene-free gene targeting using Agrobacterium-mediated delivery of the CRISPR/Cas9 system in tomato. Plant Cell Rep 38:459–462. https://doi.org/10.1007/s00299-019-02373-6
Deguchi M, Kane S, Potlakayala S et al (2020) Metabolic engineering strategies of industrial hemp (Cannabis sativa L,): a brief review of the advances and challenges. Front. Plant Sci. 11:580621
Deng L, Wang H, Sun C et al (2018) Efficient generation of pink-fruited tomatoes using CRISPR/Cas9 system. J Genet Genomics 45:51–54. https://doi.org/10.1016/j.jgg.2017.10.002
Doudna JA, Charpentier E (2014) The new frontier of genome engineering with CRISPR-Cas9. Science (80-). https://doi.org/10.1126/science.1258096
Fan D, Liu T, Li C, Jiao B, Li S, Hou Y, Luo K (2015) Efficient CRISPR/Cas9-mediated targeted mutagenesis in populus in the first generation. Sci Rep. https://doi.org/10.1038/srep12217
Fan Y, Xin S, Dai X et al (2020) Efficient genome editing of rubber tree (Hevea brasiliensis) protoplasts using CRISPR/Cas9 ribonucleoproteins. Ind Crops Prod. https://doi.org/10.1016/j.indcrop.2020.112146
FAO (2020) Banana facts and figures
FAOSTAT (2016) Natural rubber gross production value 2016
FAOSTAT (2018) Fruit production value 2018
Feng S, Zhang J, Mu Z et al (2020) Recent progress on the molecular breeding of Cucumis sativus L. in China. Theor Appl Genet 133:1777–1790. https://doi.org/10.1007/s00122-019-03484-0
Fister AS, Landherr L, Maximova SN, Guiltinan MJ (2018) Transient expression of CRISPR/Cas9 machinery targeting TcNPR3 enhances defense response in Theobroma cacao. Front Plant Sci 9:1–15. https://doi.org/10.3389/fpls.2018.00268
Gao Y, Wei W, Zhao X et al (2018) A NAC transcription factor, NOR-like1, is a new positive regulator of tomato fruit ripening. Hortic Res. https://doi.org/10.1038/s41438-018-0111-5
Ghadge A, van der Werf S, Er Kara M et al (2020) Modelling the impact of climate change risk on bioethanol supply chains. Technol Forecast Soc Change. https://doi.org/10.1016/j.techfore.2020.120227
Ghogare R, Williamson-Benavides B, Ramírez-Torres F, Dhingra A (2019) CRISPR-associated nucleases: the Dawn of a new age of efficient crop improvement. Transgenic Res 29:1–35
Gonsalves D (2006) Transgenic papaya: development, release, impact and challenges. Adv Virus Res 67:317–354. https://doi.org/10.1016/S0065-3527(06)67009-7
Gottwald TR, Graham JH, Schubert TS (2002) Citrus canker: the pathogen and its impact. Plant Heal Prog. https://doi.org/10.1094/PHP-2002-0812-01-RV
Gurin D, Glacier A, Natura P et al (2014) Watch out for wildlife fact sheet. Pestic - Toxic Asp 4:451–456. https://doi.org/10.5772/57399
Hafiz M, Hazir M, Kadir RA, Karim YA (2018) IOP Conference Series: Earth and Environmental Science Projections on future impact and vulnerability of climate change towards rubber areas in Peninsular Malaysia. IOP Conf Ser Earth Environ Sci 169:12053. https://doi.org/10.1088/1755-1315/169/1/012053
Hayut SF, Bessudo CM, Levy AA (2017) Targeted recombination between homologous chromosomes for precise breeding in tomato. Nat Commun 8:1–9. https://doi.org/10.1038/ncomms15605
Hooghvorst I, López-Cristoffanini C, Nogués S (2019) Efficient knockout of phytoene desaturase gene using CRISPR/Cas9 in melon. Sci Rep 9:1–7. https://doi.org/10.1038/s41598-019-53710-4
Hu B, Li D, Liu X et al (2017) Engineering non-transgenic gynoecious cucumber using an improved transformation protocol and optimized CRISPR/Cas9 system. Mol Plant 10:1575–1578. https://doi.org/10.1016/j.molp.2017.09.005
Hu Y, Zhang J, Jia H et al (2014) Lateral organ boundaries 1 is a disease susceptibility gene for citrus bacterial canker disease. PNAS 111:E521–E529. https://doi.org/10.1073/pnas.1313271111
Huang X, Wang Y, Xu J, Wang N (2020) Development of multiplex genome editing toolkits for citrus with high efficacy in biallelic and homozygous mutations. Plant Mol Biol 104:297–307. https://doi.org/10.1007/s11103-020-01043-6
Iaffaldano B, Zhang Y, Cornish K (2016) CRISPR/Cas9 genome editing of rubber producing dandelion Taraxacum kok-saghyz using Agrobacterium rhizogenes without selection. Ind Crops Prod 89:356–362. https://doi.org/10.1016/j.indcrop.2016.05.029
Igarashi M, Hatsuyama Y, Harada T, Fukasawa-Akada T (2016) Biotechnology and apple breeding in Japan. Breed Sci 66:18–33. https://doi.org/10.1270/jsbbs.66.18
Irish BM, Goenaga R, Zhang D et al (2010) Microsatellite fingerprinting of the USDA-ARS tropical agriculture research station cacao (Theobroma cacao L.) germplasm collection. Crop Sci 50:656–667
Ito Y, Nishizawa-Yokoi A, Endo M et al (2015) CRISPR/Cas9-mediated mutagenesis of the RIN locus that regulates tomato fruit ripening. Biochem Biophys Res Commun 467:76–82. https://doi.org/10.1016/j.bbrc.2015.09.117
Ito Y, Nishizawa-Yokoi A, Endo M et al (2017) Re-evaluation of the rin mutation and the role of RIN in the induction of tomato ripening. Nat Plants 3:866–874. https://doi.org/10.1038/s41477-017-0041-5
Ito Y, Sekiyama Y, Nakayama H et al (2020) Allelic mutations in the ripening-inhibitor locus generate extensive variation in tomato ripening. Plant Physiol 183:80–95. https://doi.org/10.1104/pp.20.00020
Jaganathan D, Ramasamy K, Sellamuthu G et al (2018) CRISPR for crop improvement: an update review. Front Plant Sci 9:1–17. https://doi.org/10.3389/fpls.2018.00985
Jia H, Wang N (2014) Targeted genome editing of sweet orange using Cas9/sgRNA. PLoS ONE. https://doi.org/10.1371/journal.pone.0093806
Jia H, Orbovic V, Jones JB, Wang N (2016) Modification of the PthA4 effector binding elements in Type I CsLOB1 promoter using Cas9/sgRNA to produce transgenic Duncan grapefruit alleviating XccΔpthA4: DCsLOB1.3 infection. Plant Biotechnol J 14:1291–1301. https://doi.org/10.1111/pbi.12495
Jia H, Orbović V, Wang N (2019) CRISPR-LbCas12a-mediated modification of citrus. Plant Biotechnol J 17:1928–1937. https://doi.org/10.1111/pbi.13109
Jia H, Wang N (2020) Generation of homozygous canker-resistant citrus in the T0 generation using CRISPR-SpCas9p. Plant Biotechnol J. https://doi.org/10.1111/pbi.13375
Jia H, Zhang Y, Orbović V et al (2017) Genome editing of the disease susceptibility gene CsLOB1 in citrus confers resistance to citrus canker. Plant Biotechnol J 15:817–823. https://doi.org/10.1111/pbi.12677
Joint FAO IAEA Division of Nuclear Techniques in Food and Agriculture (1999) Mutation breeding review
Kaiser N, Douches D, Dhingra A et al (2020) The role of conventional plant breeding in ensuring safe levels of naturally occurring toxins in food crops. Trends Food Sci Technol 100:51–66. https://doi.org/10.1016/j.tifs.2020.03.042
Kaur N, Alok A, Kaur N et al (2018) CRISPR/Cas9-mediated efficient editing in phytoene desaturase (PDS) demonstrates precise manipulation in banana cv. Rasthali genome. Funct Integr Genomics 18:89–99
Kaur N, Alok A, Kumar P et al (2020) CRISPR/Cas9 directed editing of lycopene epsilon-cyclase modulates metabolic flux for β-carotene biosynthesis in banana fruit. Metab Eng 59:76–86
Kazama T, Okuno M, Watari Y, Yanase S, Koizuka C, Tsuruta Y, Sugaya H, Toyoda A, Itoh T, Tsutsumi N, Toriyama K, Koizuka N, Arimura S (2019) Curing cytoplasmic male sterility via TALEN-mediated mitochondrial genome editing. Nat Plants 5(7):722–730. https://doi.org/10.1038/s41477-019-0459-z
Kishi-Kaboshi M, Aida R, Sasaki K (2017) Generation of gene-edited Chrysanthemum morifolium using multicopy transgenes as targets and markers. Plant Cell Physiol 58:216–226. https://doi.org/10.1093/pcp/pcw222
Klap C, Yeshayahou E, Bolger AM, Arazi T, Gupta SK, Shabtai S, Usadel B, Salts Y, Barg R (2017) Tomato facultative parthenocarpy results from SlAGAMOUS-LIKE 6 loss of function. Plant Biotechnol J 15:634–647. https://doi.org/10.1111/pbi.12662
Klopper A (2018) You say tomato. Nat Phys 14:872. https://doi.org/10.1038/s41567-018-0284-8
Kui L, Chen H, Zhang W et al (2017) Building a genetic manipulation tool box for orchid biology: identification of constitutive promoters and application of CRISPR/Cas9 in the orchid, Dendrobium officinale. Front Plant Sci 7:2036. https://doi.org/10.3389/fpls.2016.02036
Kwon C-T, Heo J, Lemmon ZH, Capua Y, Hutton SF, Van Eck J, Park SJ, Lippman ZB (2020) Rapid customization of Solanaceae fruit crops for urban agriculture. Nat Biotechnol 38(2):182–188
Lee J, Han S, Lee HHY, Jeong B, Heo T-Y, Hyun TK, Kim K, Je BI, Lee H, Shim D, Park SJ, Ryu H (2019) Brassinosteroids facilitate xylem differentiation and wood formation in tomato. Planta 249(5):1391–1403. https://doi.org/10.1007/s00425-019-03094-6
Lemmon ZH, Reem NT, Dalrymple J, Soyk S, Swartwood KE, Rodriguez-Leal D, Van Eck J, Lippman ZB (2018) Rapid improvement of domestication traits in an orphan crop by genome editing. Nat Plants 4(10):766–770. https://doi.org/10.1038/s41477-018-0259-x
Li C, Unver T, Zhang B (2017) A high-efficiency CRISPR/Cas9 system for targeted mutagenesis in Cotton (Gossypium hirsutum L.). Sci Rep. https://doi.org/10.1038/srep43902
Li R, Li R, Li X et al (2018a) Multiplexed CRISPR/Cas9-mediated metabolic engineering of γ-aminobutyric acid levels in Solanum lycopersicum. Plant Biotechnol J 16:415–427. https://doi.org/10.1111/pbi.12781
Li R, Liu C, Zhao R et al (2019) CRISPR/Cas9-mediated SlNPR1 mutagenesis reduces tomato plant drought tolerance. BMC Plant Biol 19:1–13. https://doi.org/10.1186/s12870-018-1627-4
Li R, Zhang L, Wang L et al (2018b) Reduction of tomato-plant chilling tolerance by CRISPR-Cas9-mediated SlCBF1 mutagenesis. J Agric Food Chem 66:9042–9051. https://doi.org/10.1021/acs.jafc.8b02177
Li S, Zhu B, Pirrello J et al (2020) Roles of RIN and ethylene in tomato fruit ripening and ripening-associated traits. New Phytol 226:460–475. https://doi.org/10.1111/nph.16362
Li T, Yang X, Yu Y et al (2018c) Domestication of wild tomato is accelerated by genome editing. Nat Biotechnol. https://doi.org/10.1038/nbt.4273
Liu Y, Merrick P, Zhang Z et al (2018) Targeted mutagenesis in tetraploid switchgrass (Panicum virgatum L.) using CRISPR/Cas9. Plant Biotechnol J 16:381–393. https://doi.org/10.1111/pbi.12778
Liu Y, Du M, Deng L, Shen J, Fang M, Chen Q, Lu Y, Wang Q, Li C, Zhai Q (2019) MYC2 regulates the termination of jasmonate signaling via an autoregulatory negative feedback loop. Plant Cell 31(1):106–127. https://doi.org/10.1105/tpc.18.00405
Liu X, Zhang Q, Yang G, Zhang C, Dong H, Liu Y, Yin R, Lin L (2020) Pivotal roles of Tomato photoreceptor SlUVR8 in seedling development and UV-B stress tolerance. Biochem Biophys Res Commun 522(1):177-183
Lor VS, Starker CG, Voytas DF et al (2014) Targeted mutagenesis of the tomato PROCERA gene using transcription activator-like effector nucleases. Plant Physiol 166:1288–1291. https://doi.org/10.1104/pp.114.247593
Lu H, Klocko AL, Dow M, Ma C, Amarasinghe V, Strauss SH (2016) Low frequency of zinc-finger nuclease-induced mutagenesis in Populus. Mol Breed. https://doi.org/10.1007/s11032-016-0546-z
Ma X, Zhang X, Liu H, Li Z (2020) Highly efficient DNA-free plant genome editing using virally delivered CRISPR-Cas9. Nat Plants 6:773–779
Maher MF, Nasti RA, Vollbrecht M et al (2020) Plant gene editing through de novo induction of meristems. Nat Biotechnol 38:84–89. https://doi.org/10.1038/s41587-019-0337-2
Mao Y, Botella JR, Liu Y, Zhu JK (2019) Gene editing in plants: progress and challenges. Natl Sci Rev 6:421–437. https://doi.org/10.1093/nsr/nwz005
Martín-Pizarro C, Triviño JC, Posé D (2019) Functional analysis of the TM6 MADS-box gene in the octoploid strawberry by CRISPR/Cas9-directed mutagenesis. J Exp Bot 70:885–895
Mikulic-Petkovsek M, Ivancic A, Schmitzer V et al (2016) Comparison of major taste compounds and antioxidative properties of fruits and flowers of different Sambucus species and interspecific hybrids. Food Chem 200:134–140. https://doi.org/10.1016/j.foodchem.2016.01.044
Moose SP, Mumm RH (2008) Molecular plant breeding as the foundation for 21st century crop improvement. Plant Physiol 147:969–977. https://doi.org/10.1104/pp.108.118232
Nageswara-Rao M, Soneji JR, Kwit C et al (2013) Advances in biotechnology and genomics of switchgrass
Naim F, Dugdale B, Kleidon J et al (2018) Gene editing the phytoene desaturase alleles of Cavendish banana using CRISPR/Cas9. Transgenic Res 27:451–460
Nakajima I, Ban Y, Azuma A et al (2017) CRISPR/Cas9-mediated targeted mutagenesis in grape. PLoS ONE 12:1–16. https://doi.org/10.1371/journal.pone.0177966
Nekrasov V, Wang C, Win J et al (2017) Rapid generation of a transgene-free powdery mildew resistant tomato by genome deletion. Sci Rep 7:1–6. https://doi.org/10.1038/s41598-017-00578-x
Nguyen THT, Park S, Jeong J, Shin YS, Sim SJ, Jin ES (2020) Enhancing lipid productivity by modulating lipid catabolism using the CRISPR-Cas9 system in Chlamydomonas. J Appl Phycol 32(5):2829–2840. https://doi.org/10.1007/s10811-020-02172-7
Nishihara M, Higuchi A, Watanabe A, Tasaki K (2018) Application of the CRISPR/Cas9 system for modification of flower color in Torenia fournieri. BMC Plant Biol 18:331. https://doi.org/10.1186/s12870-018-1539-3
Nishihara M, Nakatsuka T (2011) Genetic engineering of flavonoid pigments to modify flower color in floricultural plants. Biotechnol Lett 33:433–441. https://doi.org/10.1007/s10529-010-0461-z
Nishitani C, Hirai N, Komori S et al (2016) Efficient genome editing in apple. Sci Rep 6:31481. https://doi.org/10.1038/srep31481
Nonaka S, Arai C, Takayama M, Matsukura C, Ezura H (2017) Efficient increase of Γ aminobutyric acid (GABA) content in tomato fruits by targeted mutagenesis. Sci Rep. https://doi.org/10.1038/s41598-017-06400-y
Ntui VO, Tripathi JN, Tripathi L (2020) Robust CRISPR/Cas9 mediated genome editing tool for banana and plantain (Musa spp.). Curr Plant Biol 21:100128
Omura M, Shimada T (2016) Citrus breeding, genetics and genomics in Japan. Breed Sci 66:3–17. https://doi.org/10.1270/jsbbs.66.3
Ortigosa A, Gimenez-Ibanez S, Leonhardt N, Solano R (2019) Design of a bacterial speck resistant tomato by CRISPR/Cas9-mediated editing of SlJAZ2. Plant Biotechnol J 17:665–673. https://doi.org/10.1111/pbi.13006
Pal L, Lucia L (2019) Renaissance of industrial hemp: a miracle crop for a multitude of products. BioResources 14:2460–2464
Pan C, Ye L, Qin L et al (2016) CRISPR/Cas9-mediated efficient and heritable targeted mutagenesis in tomato plants in the first and later generations. Sci Rep 6:2–10. https://doi.org/10.1038/srep24765
Park J-J, Yoo CG, Flanagan A et al (2017) Defined tetra-allelic gene disruption of the 4-coumarate:coenzyme A ligase 1 (Pv4CL1) gene by CRISPR/Cas9 in switchgrass results in lignin reduction and improved sugar release. Biotechnol Biofuels 10:284. https://doi.org/10.1186/s13068-017-0972-0
Peer R, Rivlin G, Golobovitch S et al (2015) Targeted mutagenesis using zinc-finger nucleases in perennial fruit trees. Planta 241:941–951. https://doi.org/10.1007/s00425-014-2224-x
Peng A, Chen S, Lei T et al (2017) Engineering canker-resistant plants through CRISPR/Cas9-targeted editing of the susceptibility gene Cs LOB 1 promoter in citrus. Plant Biotechnol J 15:1509–1519
Pompili V, Dalla Costa L, Piazza S et al (2020) Reduced fire blight susceptibility in apple cultivars using a high-efficiency CRISPR/Cas9-FLP/FRT-based gene editing system. Plant Biotechnol J 18:845–858. https://doi.org/10.1111/pbi.13253
Qin X, Li W, Liu Y, Tan M, Ganal M, Chetelat RT (2018) A farnesyl pyrophosphate synthase gene expressed in pollen functions in S-RNase-independent unilateral incompatibility. Plant J 93(3):417–430. https://doi.org/10.1111/tpj.13796
Qiu Z, Wang H, Li D, Yu B, Hui Q, Yan S, Huang Z, Cui X, Cao B (2019) Identification of candidate HY5-dependent and -independent regulators of anthocyanin biosynthesis in tomato. Plant Cell Physiol 60(3):643–656. https://doi.org/10.1093/pcp/pcy236
Radha T, Mathew L (2007) Fruit crops, vol 3. New India Publishing
Rao X, Chen X, Shen H et al (2019) Gene regulatory networks for lignin biosynthesis in switchgrass (Panicum virgatum ). Plant Biotechnol J 17:580–593. https://doi.org/10.1111/pbi.13000
Ren C, Liu X, Zhang Z et al (2016) CRISPR/Cas9-mediated efficient targeted mutagenesis in Chardonnay (Vitis vinifera L.). Sci Rep 6:1–9. https://doi.org/10.1038/srep32289
Ren F, Ren C, Zhang Z et al (2019) Efficiency optimization of CRISPR/CAS9-mediated targeted mutagenesis in grape. Front Plant Sci 10:1–9. https://doi.org/10.3389/fpls.2019.00612
Rodríguez-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
Sawettalake N, Bunnag S, Wang Y et al (2017) DOAP1 promotes flowering in the orchid dendrobium chao praya smile. Front Plant Sci 8:400. https://doi.org/10.3389/fpls.2017.00400
Schubert R, Dobritzsch S, Gruber C, Hause G, Athmer B, Schreiber T, Marillonnet S, Okabe Y, Ezura H, Acosta IF, Tarkowska D, Hause B (2019) Tomato myb21 acts in ovules to mediate jasmonate-regulated fertility. Plant Cell 31(5):1043–1062. https://doi.org/10.1105/tpc.18.00978
Scorza R, Callahan A, Ravelonandro M, Braverman M (2012) Development and regulation of the plum pox virus resistant transgenic plum `HoneySweet’. In: Wozniak CA, McHughen A (eds) Regulation of agricultural biotechnology: The United States and Canada. Springer, Dordrecht, pp 269–280
Shao X, Wu S, Dou T et al (2020) Using CRISPR/Cas9 genome editing system to create MaGA20ox2 gene-modified semi-dwarf banana. Plant Biotechnol J 18:17–19
Shew AM, Nalley LL, Snell HA et al (2018) CRISPR versus GMOs: public acceptance and valuation. Glob Food Sec 19:71–80
Shibuya K, Watanabe K, Ono M (2018) CRISPR/Cas9-mediated mutagenesis of the EPHEMERAL1 locus that regulates petal senescence in Japanese morning glory. Plant Physiol Biochem 131:53–57. https://doi.org/10.1016/j.plaphy.2018.04.036
Shu P, Li ZZ, Min D, Zhang X, Ai W, Li J, Zhou J, Li Z, Li F, Li X (2020) CRISPR/Cas9-Mediated SlMYC2 mutagenesis adverse to tomato plant growth and MeJA-induced fruit resistance to Botrytis cinerea. J Agric Food Chem 68(20):5529–5538. https://doi.org/10.1021/acs.jafc.9b08069
Shulga OA, Mitiouchkina TY, Shchennikova AV et al (2011) Overexpression of AP1-like genes from Asteraceae induces early-flowering in transgenic Chrysanthemum plants. Vitr Cell Dev Biol - Plant 47:553–560. https://doi.org/10.1007/s11627-011-9393-0
Souza LM, Francisco FR, Gonçalves PS et al (2019) Genomic selection in rubber tree breeding: a comparison of models and methods for managing G×E interactions. Front Plant Sci 10:1353. https://doi.org/10.3389/fpls.2019.01353
Soyk S, Müller NA, Park SJ, Schmalenbach I, Jiang K, Hayama R, Zhang L, Van Eck J, Jiménez-Gómez JM, Lippman ZB (2017) Variation in the flowering gene SELF PRUNING 5G promotes day-neutrality and early yield in tomato. Nat Genet 49(1):162–168. https://doi.org/10.1038/ng.3733
Sreedharan S, Shekhawat UKS, Ganapathi TR (2013) Transgenic banana plants overexpressing a native plasma membrane aquaporin MusaPIP1;2 display high tolerance levels to different abiotic stresses. Plant Biotechnol J 11:942–952. https://doi.org/10.1111/pbi.12086
Subburaj S, Chung SJ, Lee C et al (2016a) Site-directed mutagenesis in Petunia × hybrida protoplast system using direct delivery of purified recombinant Cas9 ribonucleoproteins. Plant Cell Rep 35:1535–1544. https://doi.org/10.1007/s00299-016-1937-7
Subburaj S, Chung SJ, Lee C et al (2016b) Site-directed mutagenesis in Petunia× hybrida protoplast system using direct delivery of purified recombinant Cas9 ribonucleoproteins. Plant Cell Rep 35:1535–1544
Sun L, Kao T (2018) CRISPR/Cas9-mediated knockout of PiSSK1 reveals essential role of S-locus F-box protein-containing SCF complexes in recognition of non-self S-RNases during cross-compatible pollination in self-incompatible Petunia inflata. Plant Reprod 31:129–143. https://doi.org/10.1007/s00497-017-0314-1
Sunitha S, Rock CD (2020) CRISPR/Cas9-mediated targeted mutagenesis of TAS4 and MYBA7 loci in grapevine rootstock 101-14. Transgenic Res 29:355–367. https://doi.org/10.1007/s11248-020-00196-w
Takahashi K, Ide Y, Hayakawa J, Yoshimitsu Y, Fukuhara I, Abe J, Kasai Y, Harayama S (2018) Lipid productivity in TALEN-induced starchless mutants of the unicellular green alga Coccomyxa sp. strain Obi. Algal Res 32:300–307. https://doi.org/10.1016/j.algal.2018.04.020
Tian S, Jiang L, Cui X et al (2018) Engineering herbicide-resistant watermelon variety through CRISPR/Cas9-mediated base-editing. Plant Cell Rep 37:1353–1356. https://doi.org/10.1007/s00299-018-2299-0
Tian S, Jiang L, Gao Q et al (2017) Efficient CRISPR/Cas9-based gene knockout in watermelon. Plant Cell Rep 36:399–406. https://doi.org/10.1007/s00299-016-2089-5
Tomlinson L, Yang Y, Emenecker R, Smoker M, Taylor J, Perkins S, Smith J, MacLean D, Olszewski NE, Jones JDG (2019) Using CRISPR/Cas9 genome editing in tomato to create a gibberellin-responsive dominant dwarf DELLA allele. Plant Biotechnol J 17(1):132–140. https://doi.org/10.1111/pbi.12952
Tong C-G, Wu F-H, Yuan Y-H et al (2020) High-efficiency CRISPR/Cas-based editing of Phalaenopsis orchid MADS genes. Plant Biotechnol J 18:889–891. https://doi.org/10.1111/pbi.13264
Tripathi JN, Ntui VO, Ron M et al (2019a) CRISPR/Cas9 editing of endogenous banana streak virus in the B genome of Musa spp. overcomes a major challenge in banana breeding. Commun Biol 2:1–11
Tripathi L, Ntui VO, Tripathi JN (2019b) Application of genetic modification and genome editing for developing climate-smart banana. Food Energy Secur 8:e00168
Ueta R, Abe C, Watanabe T, Sugano SS, Ishihara R, Ezura H, Osakabe Y, Osakabe K (2017) Rapid breeding of parthenocarpic tomato plants using CRISPR/Cas9. Sci Rep. https://doi.org/10.1038/s41598-017-00501-4
van Bakel H, Stout JM, Cote AG et al (2011) The draft genome and transcriptome of Cannabis sativa. Genome Biol. https://doi.org/10.1186/gb-2011-12-10-r102
Van Beilen JB, Poirier Y (2007) Prospects for biopolymer production in plants. Adv Biochem Eng/Biotechnol 107:133–151. https://doi.org/10.1007/10_2007_056
Veillet F, Perrot L, Chauvin L et al (2019) Transgene-free genome editing in tomato and potato plants using agrobacterium-mediated delivery of a CRISPR/Cas9 cytidine base editor. Int J Mol Sci 20:1–10. https://doi.org/10.3390/ijms20020402
Veillet F, Perrot L, Guyon-Debast A, Kermarrec M-P, Chauvin L, Chauvin J-E, Gallois J-L, Mazier M, Nogué F (2020) Expanding the CRISPR toolbox in P. Patens using SpCas9-NG variant and application for gene and base editing in solanaceae crops. Int J Mol Sci. https://doi.org/10.3390/ijms21031024
Voytas DF, Gao C (2014) Precision genome engineering and agriculture: opportunities and regulatory challenges. PLoS Biol 12:e1001877. https://doi.org/10.1371/journal.pbio.1001877
Van TV, Sivankalyani V, Kim EJ et al (2020) Highly efficient homology-directed repair using CRISPR/Cpf1-geminiviral replicon in tomato. Plant Biotechnol J. https://doi.org/10.1111/pbi.13373
Wang D, Samsulrizal NH, Yan C et al (2019a) Characterization of CRISPR mutants targeting genes modulating pectin degradation in ripening tomato 1[OPEN]. Plant Physiol 179:544–557. https://doi.org/10.1104/pp.18.01187
Wang L, Chen L, Li R et al (2017a) Reduced drought tolerance by CRISPR/Cas9-mediated SlMAPK3 mutagenesis in tomato plants. J Agric Food Chem 65:8674–8682. https://doi.org/10.1021/acs.jafc.7b02745
Wang L, Chen S, Peng A et al (2019b) CRISPR/Cas9-mediated editing of CsWRKY22 reduces susceptibility to Xanthomonas citri subsp. citri in Wanjincheng orange (Citrus sinensis (L.) Osbeck). Plant Biotechnol Rep 13:501–510. https://doi.org/10.1007/s11816-019-00556-x
Wang L, Wang L, Tan Q et al (2016a) Efficient inactivation of symbiotic nitrogen fixation related genes in Lotus japonicus Using CRISPR-Cas9. Front Plant Sci 7:1333
Wang M, Mao Y, Lu Y et al (2017b) Multiplex gene editing in rice using the CRISPR-Cpf1 system. Mol Plant 10:1011–1013. https://doi.org/10.1016/j.molp.2017.03.001
Wang X, Tu M, Wang D et al (2018a) CRISPR/Cas9-mediated efficient targeted mutagenesis in grape in the first generation. Plant Biotechnol J 16:844–855. https://doi.org/10.1111/pbi.12832
Wang Y, Liu X, Ren C et al (2016b) Identification of genomic sites for CRISPR/Cas9-based genome editing in the Vitis vinifera genome. BMC Plant Biol 16:3–9. https://doi.org/10.1186/s12870-016-0787-3
Wang Z-P, Xing H-L, Dong L et al (2015) Egg cell-specific promoter-controlled CRISPR/Cas9 efficiently generates homozygous mutants for multiple target genes in Arabidopsis in a single generation. Genome Biol 16:144
Wang Z, Wang S, Li D et al (2018b) Optimized paired-sgRNA/Cas9 cloning and expression cassette triggers high-efficiency multiplex genome editing in kiwifruit. Plant Biotechnol J 16:1424–1433. https://doi.org/10.1111/pbi.12884
Watanabe K, Breier U, Hensel G et al (2016) Stable gene replacement in barley by targeted double-strand break induction. J Exp Bot 67:1433–1445
Watanabe K, Kobayashi A, Endo M et al (2017) CRISPR/Cas9-mediated mutagenesis of the dihydroflavonol-4-reductase-B (DFR-B) locus in the Japanese morning glory Ipomoea (Pharbitis) nil. Sci Rep 7:1–9. https://doi.org/10.1038/s41598-017-10715-1
Watanabe K, Oda-Yamamizo C, Sage-Ono K et al (2018) Alteration of flower colour in Ipomoea nil through CRISPR/Cas9-mediated mutagenesis of carotenoid cleavage dioxygenase 4. Transgenic Res 27:25–38. https://doi.org/10.1007/s11248-017-0051-0
Wilson FM, Harrison K, Armitage AD et al (2019) CRISPR/Cas9-mediated mutagenesis of phytoene desaturase in diploid and octoploid strawberry. Plant Methods 15:1–13. https://doi.org/10.1186/s13007-019-0428-6
Wolabu TW, Cong L, Park J-J, Bao Q, Chen M, Sun J, Xu B, Ge Y, Chai, M, Liu Z, Wang Z-Y (2020) Development of a highly efficient multiplex genome editing system in outcrossing tetraploid alfalfa (Medicago sativa). Front Plant Sci. https://doi.org/10.3389/fpls.2020.01063
Wolter F, Klemm J, Puchta H (2018) Efficient in planta gene targeting in Arabidopsis using egg cell-specific expression of the Cas9 nuclease of Staphylococcus aureus. Plant J 94:735–746. https://doi.org/10.1111/tpj.13893
Wu S, Zhu H, Liu J et al (2020) Establishment of a PEG-mediated protoplast transformation system based on DNA and CRISPR/Cas9 ribonucleoprotein complexes for banana
Xiao Y, Kang B, Li M, Xiao L, Xiao H, Shen H, Yang W (2020) Transcription of lncRNA ACoS-AS1 is essential to trans-splicing between SlPsy1 and ACoS-AS1 that causes yellow fruit in tomato. RNA Biol 17(4):596-607. https://doi.org/10.1080/15476286.2020.1721095
Xing S, Jia M, Wei L et al (2018) CRISPR/Cas9-introduced single and multiple mutagenesis in strawberry. J Genet Genomics 45:685–687. https://doi.org/10.1016/j.jgg.2018.04.006
Xiong J-S, Ding J, Li Y (2015) Genome-editing technologies and their potential application in horticultural crop breeding. Hortic Res 2:15019. https://doi.org/10.1038/hortres.2015.19
Xiong X, Liu W, Jiang J, Xu L, Huang L, Cao J (2019) Efficient genome editing of Brassica campestris based on the CRISPR/Cas9 system. Mol Genet Genomics 294(5):1251–1261. https://doi.org/10.1007/s00438-019-01564-w
Xu K (2013) An overview of arctic apples: basic facts and characteristics. N Y State Hortic Soc 21:8–10
Xu C, Park SJ, Van Eck J, Lippman ZB (2016) Control of inflorescence architecture in tomato by BTB/POZ transcriptional regulators. Genes Dev 30 (18):2048–2061. https://doi.org/10.1101/gad.288415.116
Xu J, Kang BC, Naing AH et al (2020) CRISPR/Cas9-mediated editing of 1-aminocyclopropane-1-carboxylate oxidase1 enhances Petunia flower longevity. Plant Biotechnol J 18:287–297. https://doi.org/10.1111/pbi.13197
Yabor L, Pérez L, Gómez D et al (2020) Histological evaluation of pineapple transgenic plants following 8 years of field growth. Euphytica. https://doi.org/10.1007/s10681-020-2555-6
Yan R, Wang Z, Ren Y et al (2019) Establishment of efficient genetic transformation systems and application of CRISPR/Cas9 genome editing technology in Lilium pumilum DC. Fisch. and Lilium longiflorum white heaven. Int J Mol Sci 20:2920. https://doi.org/10.3390/ijms20122920
Yan S, Chen N, Huang Z, Li D, Zhi J, Yu B, Liu X, Cao B, Qiu Z (2020) Anthocyanin fruit encodes an R2R3-MYB transcription factor, SlAN2-like, activating the transcription of SlMYBATV to fine-tune anthocyanin content in tomato fruit. New Phytol 225:2048–2063. https://doi.org/10.1111/nph.16272
Yang T, Deng L, Zhao W et al (2019) Rapid breeding of pink-fruited tomato hybrids using the CRISPR/Cas9 system. J Genet Genomics 46:505–508. https://doi.org/10.1016/j.jgg.2019.10.002
Ye S, Chen G, Kohnen MV, Wang W, Cai C, Ding W, Wu C, Gu L, Zheng Y, Ma X, Lin C, Zhu Q (2020) Robust CRISPR/Cas9 mediated genome editing and its application in manipulating plant height in the first generation of hexaploid Ma bamboo (Dendrocalamus latiflorus Munro). Plant Biotechnol J 18(7):1501–1503. https://doi.org/10.1111/pbi.13320
Young TR, Firoozabady E (2010) U.S. Patent No. 7,663,021. U.S. Patent and Trademark Office, Washington, DC
Yu Q, Powles SB (2014) Resistance to AHAS inhibitor herbicides: current understanding. Pest Manag Sci 70:1340–1350. https://doi.org/10.1002/ps.3710
Yu QH, Wang B, Li N et al (2017) CRISPR/Cas9-induced targeted mutagenesis and gene replacement to generate long-shelf life tomato lines. Sci Rep 7:1–9. https://doi.org/10.1038/s41598-017-12262-1
Yu W, Wang L, Zhao R, Sheng J, Zhang S, Li R, Shen L (2019a) Knockout of SlMAPK3 enhances tolerance to heat stress involving ROS homeostasis in tomato plants. BMC Plant Biol 19:1–13. https://doi.org/10.1186/s12870-019-1939-z
Yu T, Tzeng DTW, Li R, Chen J, Zhong S, Fu D, Zhu B, Luo Y, Zhu H (2019b) Genome-wide identification of long non-coding RNA targets of the tomato MADS box transcription factor RIN and function analysis. Ann Bot 123(3):469–482. https://doi.org/10.1093/aob/mcy178
Yuan X, Wang H, Cai J et al (2019) NAC transcription factors in plant immunity. Phytopathol Res 1:1–13. https://doi.org/10.1186/s42483-018-0008-0
Yuste-Lisbona FJ, Fernández-Lozano A, Pineda B, Bretones S, Ortíz-Atienza A, García-Sogo B, Müller NA, Angosto T, Capel J, Moreno V, Jiménez-Gómez JM, Lozano R (2020) ENO regulates tomato fruit size through the floral meristem development network. Proc Natl Acad Sci U S A 117(14):8187–8195. https://doi.org/10.1073/pnas.1913688117
Zhang B, Yang X, Yang C et al (2016) Exploiting the CRISPR/Cas9 system for targeted genome mutagenesis in Petunia. Sci Rep 6:1–8. https://doi.org/10.1038/srep20315
Zhang F, LeBlanc C, Irish VF, Jacob Y (2017) Rapid and efficient CRISPR/Cas9 gene editing in Citrus using the YAO promoter. Plant Cell Rep 36:1883–1887. https://doi.org/10.1007/s00299-017-2202-4
Zhang N, Roberts HM, Van Eck J, Martin GB (2020) Generation and molecular characterization of CRISPR/Cas9-induced mutations in 63 immunity-associated genes in tomato reveals specificity and a range of gene modifications. Front Plant Sci 11:1–13. https://doi.org/10.3389/fpls.2020.00010
Zhao P, You Q, Lei M (2019) A CRISPR/Cas9 deletion into the phosphate transporter SlPHO1;1 reveals its role in phosphate nutrition of tomato seedlings. Physiol Plant 167(4):556–563. https://doi.org/10.1111/ppl.12897
Zhi J, Liu X, Li D, Huang Y, Yan S, Cao B, Qiu Z (2020) CRISPR/Cas9-mediated SlAN2 mutants reveal various regulatory models of anthocyanin biosynthesis in tomato plant. Plant Cell Rep 39(6):799–809. https://doi.org/10.1007/s00299-020-02531-1
Zhong M, Wang Y, Hou K, Shu S, Sun J, Guo S (2019) TGase positively regulates photosynthesis via activation of Calvin cycle enzymes in tomato. Hortic Res. https://doi.org/10.1038/s41438-019-0173-z
Zhou J, Wang G, Liu Z (2018) Efficient genome editing of wild strawberry genes, vector development and validation. Plant Biotechnol J 16:1868–1877. https://doi.org/10.1111/pbi.12922
Zhou P, Jia R, Chen S et al (2017) Cloning and expression analysis of four citrus WRKY genes responding to Xanthomon asaxonopodis pv. citri. Acta Hortic Sin 44:452–462. https://doi.org/10.16420/j.issn.0513-353x.2016-0577
Zsögön A, Čermák T, Naves ER, Notini MM, Edel KH, Weinl S, Freschi L, Voytas DF, Kudla J, Peres LEP (2018) De novo domestication of wild tomato using genome editing. Nat Biotechnol 36(12):1211–1216. https://doi.org/10.1038/nbt.4272
Acknowledgments
The authors would like to acknowledge funding from MINECO, Spain (PGC2018-097655-B-I00 to P Christou), Generalitat de Catalunya Grant 2017 SGR 828 to the Agricultural Biotechnology and Bioeconomy Unit (ABBU). Work in the Dhingra lab in crop improvement is supported in part by Washington State University Agriculture Research Center Hatch grant WNP00011. ES and FR acknowledge the support received from the Department of Horticulture, BW was supported in part by a Research Assistantship from the Washington State University Graduate School. The authors would also like to thank Drs A. McHughen and H. Quemada for input and clarifications on US genome editing regulations. We would also like to thank the anonymous reviewers for their insightful comments.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Ramirez-Torres, F., Ghogare, R., Stowe, E. et al. Genome editing in fruit, ornamental, and industrial crops. Transgenic Res 30, 499–528 (2021). https://doi.org/10.1007/s11248-021-00240-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11248-021-00240-3