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Plant gene editing through de novo induction of meristems
Open accessAbstract
Plant gene editing is typically performed by delivering reagents such as Cas9 and single guide RNAs to explants in culture. Edited cells are then induced to differentiate into whole plants by exposure to various hormones. The creation of edited plants through tissue culture is often inefficient, time-consuming, works for only limited species and genotypes, and causes unintended changes to the genome and epigenome. Here we report two methods to generate gene-edited dicotyledonous plants through de novo meristem induction. Developmental regulators and gene-editing reagents are delivered to somatic cells of whole plants. This induces meristems that produce shoots with targeted DNA modifications, and gene edits are transmitted to the next generation. The de novo induction of gene-edited meristems sidesteps the need for tissue culture and promises to overcome a bottleneck in plant gene editing.
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“Injection of Agrobacterium tumefaciens carrying the development regulators WUS2 and SHOOT MERISTEMLESS (STM) into tobacco seedlings led to the development of gene-edited shoots with heritable mutations (Maher et al., 2020).”
From Genetic resources and precise gene editing for targeted improvement of barley abiotic stress tolerance (2023) · cites this paper as Maher et al., 2020
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“De novo induction of geneedited meristems also avoids the tissue culture step and can be induced in aseptically grown seedlings and soil-grown plants (Maher et al., 2020).”
From Genetic resources and precise gene editing for targeted improvement of barley abiotic stress tolerance (2023) · cites this paper as Maher et al., 2020
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“In light of this new technique, the gene-edited somatic cells are reprogrammed into themeristematic cells by the co-expression of developmental regulators (DRs) with genome editingmachinery (Maher et al., 2020) that helps tomake genome editing faster and more straightforward.”
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“However, also in these respects novel techniques such as de novo induction of meristems might help one day to bypass such limitations, making all crops amenable to GE (Maher et al., 2020).”
BackgroundTargeted DNA insertion in plants
Dong, O. X., & Ronald, P. C. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2004834117 · Cited by 107
Genome Editing for Resistance to Insect Pests: An Emerging Tool for Crop Improvement
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“Gene editing through de novo induction of meristems (Maher et al., 2020) may, in future, allow for the direct transformation of soil-grown perennial species, which would help bypass the need for time-consuming, and often inefficient transformation techniques based on cultured cells.”
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“A similar approach has been used for gene-editing by inducing meristems in somatic cells by ectopically expressing DRs including BBM, WUS, SHOOT MERISTEMLESS (STM), and ISOPENTENYL TRANSFERASE (IPT) by Agrobacterium injection (Maher et al., 2020).”
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“When used together with a Cas9/gRNA plasmid, this novel approach produced gene-edited shoots without the use of tissue culture, offering great potential to speed up the breeding cycles for many plant species [59].”
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“Transgenic shoots in tomato, potato, and grapevine (Vitis vinifera) have been generated using the de novo induction of meristems (Maher et al., 2020).”
MethodAttaining the promise of plant gene editing at scale
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Self-citationPlastid Transformation: How Does it Work? Can it Be Applied to Crops? What Can it Offer?
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GRF-GIF Chimeras Boost Plant Regeneration
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“However, overexpression of morphogenic regulators such as Bbm and Wus2 has the potential not only to induce somatic embryogenesis in an expanded range of genotypes, but also to bypass or accelerate tissue culture via de novo meristem formation as demonstrated in eudicots (Maher et al., 2020).”
BackgroundExpanding the plant genome editing toolbox with recently developed CRISPR–Cas systems
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“Recently, strategies to overcome some of these conventional problems have been reported: plant gene editing through de novo induction of meristems (Maher et al., 2020), efficient gene targeting in Arabidopsis (Miki et al., 2018), and genome editing during haploid induction (Kelliher et al., 2019),…”
Biopolymeric Nanoparticles–Multifunctional Materials of the Future
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“…innovative gene-editing strategies, such as injecting WUS2 and IPT co-delivered with gene-editing reagents directly into dicot plants to induce meristem formation in somatic tissues, have opened new avenues for tissue culture-independent gene editing (Cody et al., 2023; Maher et al., 2020).”
A comprehensive review of in planta stable transformation strategies
Bélanger, J. G., Copley, T. R., Hoyos‐Villegas, V., Charron, J., & O’Donoughue, L. S. (2024) · Plant Methods · doi:10.1186/s13007-024-01200-8 · Cited by 79
“Maher et al. [175] demonstrated that this approach generates high transformation rates with tobacco/ Nicotiana benthamiana (i.e. gene editing efficiencies ranging from 30 to 95”
BackgroundMethodInfluentialCRISPR-Cas: A robust technology for enhancing consumer-preferred commercial traits in crops
Verma, V., Kumar, A., Partap, M., Thakur, M., & Bhargava, B. (2023) · Frontiers in Plant Science · doi:10.3389/fpls.2023.1122940 · Cited by 84
“Recently developed, gene editing method has simplified or eliminated tissue culture by reprogramming genome-edited somatic cells into meristems via coexpressing DRs and gene editing components, allowing direct regeneration of genome-edited plants from somatic cells (Maher et al., 2020).”
BackgroundThe mechanism of host-induced germination in root parasitic plants
Nelson, D. C. (2021) · PLANT PHYSIOLOGY · doi:10.1093/plphys/kiab043 · Cited by 77
Xia, X., Cheng, X., Li, R., Yao, J., Li, Z., & Cheng, Y. (2021) · Theoretical and Applied Genetics · doi:10.1007/s00122-021-03874-3 · Cited by 78
“2019) and the de novo induction of gene-edited meristems for avoiding time-consuming tissue culture (Maher et al. 2020), for characterizing gene function and crop improvement remains to be investigated in tomato.”
BackgroundAhmar, S., Hensel, G., & Gruszka, D. (2023) · Biotechnology Advances · doi:10.1016/j.biotechadv.2023.108248 · Cited by 79
Novel CRISPR/Cas applications in plants: from prime editing to chromosome engineering
Huang, T., & Puchta, H. (2021) · Transgenic Research · doi:10.1007/s11248-021-00238-x · Cited by 77
Highly efficient and genotype-independent barley gene editing based on anther culture
Han, Y., Broughton, S., Liu, L., Zhang, X.-Q., Zeng, J., He, X., & Li, C. (2021) · Plant Communications · doi:10.1016/j.xplc.2020.100082 · Cited by 73
“…sidestep difficulties in tissue culture and advance crop transformation; however, each tested plant genotype responded differently to the combination(s) of developmental regulators (Lowe et al., 2016; Maher et al., 2020), indicating the need to identify an optimal combination for each genotype.”
BackgroundMolecular evolution and functional modification of plant miRNAs with CRISPR
Deng, F., Zeng, F., Shen, Q., Abbas, A., Cheng, J., Jiang, W. J., Chen, G. J., Shah, A. N., Holford, P., Tanveer, M., et al. (2022) · Trends in Plant Science · doi:10.1016/j.tplants.2022.01.009 · Cited by 74
Plant Promoters and Terminators for High-Precision Bioengineering
Brooks, E., Elorriaga, E., Liu, Y., Duduit, J. R., Yuan, G., Tsai, C., Tuskan, G. A., Ranney, T. G., Yang, X., & Liu, W. (2023) · BioDesign Research · doi:10.34133/bdr.0013 · Cited by 72
“Since 2016, morphogenic regulators have been applied to transform recalcitrant cultivars, increase transformation efficiency, shorten the time for plant regeneration, and generate desirable phenotypes while bypassing the tissue culture process [173–175].”
BackgroundCody, J. P., Maher, M. F., Nasti, R. A., Starker, C. G., Chamness, J. C., & Voytas, D. F. (2022) · Nature Protocols · doi:10.1038/s41596-022-00749-9 · Cited by 71
“(6) Fully regenerated and genetically modified plants are transferred to soil.”
BackgroundSelf-citationThe Promising Nanovectors for Gene Delivery in Plant Genome Engineering
Zhi, H., Zhou, S., Pan, W., Shang, Y., Zeng, Z., & Zhang, H. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23158501 · Cited by 77
Tools and targets: the dual role of plant viruses in CRISPR–Cas genome editing
Uranga, M., & Daròs, J. (2023) · The Plant Genome · doi:10.1002/tpg2.20220 · Cited by 68
Efficient CRISPR-mediated base editing in Agrobacterium spp.
Rodrigues, S. D., Karimi, M., Impens, L., Lerberge, E. V., Coussens, G., Aesaert, S., Rombaut, D., Holtappels, D., Ibrahim, H. M. M., MONTAGU, M. V., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2013338118 · Cited by 66
Engineering Metabolism in Nicotiana Species: A Promising Future
Molina‐Hidalgo, F. J., Vázquez‐Vilar, M., D’Andrea, L., Demurtas, O. C., Fraser, P. D., Giuliano, G., Bock, R., Orzáez, D., & Goossens, A. (2020) · Trends in biotechnology · doi:10.1016/j.tibtech.2020.11.012 · Cited by 65
Gene-Editing Technologies and Applications in Legumes: Progress, Evolution, and Future Prospects
Baloğlu, M. C., Altunoğlu, Y. Ç., Baloglu, P., Yildiz, A. B., Türkölmez, N., & Çiftçi, Y. Ö. (2022) · Frontiers in Genetics · doi:10.3389/fgene.2022.859437 · Cited by 74
“CRISPR/Cas 9 Glyma14g04180 (late-embryogenesis abundant protein) Insertion and deletion mutations Di et al. (2019)”
BackgroundInfluentialNanoparticles for protein delivery in planta
Wang, J., Cunningham, F. J., Goh, N. S., Boozarpour, N. N., Pham, M., & Landry, M. P. (2021) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2021.102052 · Cited by 64
CRISPR/Cas9 Technique for Temperature, Drought, and Salinity Stress Responses
Li, X., Xu, S., Aoyagi, M., Yuan, S., Iwama, T., Kobayashi, M., & Miura, K. (2022) · Current Issues in Molecular Biology · doi:10.3390/cimb44060182 · Cited by 67
“This method achieves relatively high genome-editing efficiency in Nicotiana benthamiana [112].”
MethodPandey, A. K., Rubiales, D., Wang, Y., Fang, P., Sun, T., Liu, N., & Xu, P. (2021) · Theoretical and Applied Genetics · doi:10.1007/s00122-020-03751-5 · Cited by 62
Novel and emerging biotechnological crop protection approaches
Giudice, G., Moffa, L., Varotto, S., Cardone, M. F., Bergamini, C., Lorenzis, G. D., Velasco, R., Nerva, L., & Chitarra, W. (2021) · Plant Biotechnology Journal · doi:10.1111/pbi.13605 · Cited by 63
“Despite the great potential of such approach, the fact that gene sequences of morphogenic regulators are protected by patents from private companies (Lowe et al., 2016; Maher et al., 2020) might limit the application of this technological innovation.”
BackgroundHotter, drier, CRISPR: the latest edit on climate change
Massel, K., Lam, Y., Wong, A. C. S., Hickey, L. T., Borrell, A. K., & Godwin, I. D. (2021) · Theoretical and Applied Genetics · doi:10.1007/s00122-020-03764-0 · Cited by 65
An update on precision genome editing by homology-directed repair in plants
Chen, J., Li, S., He, Y., Li, J., & Xia, L. (2022) · PLANT PHYSIOLOGY · doi:10.1093/plphys/kiac037 · Cited by 67
Chennakesavulu, K., Singh, H., Trivedi, P. K., Jain, M., & Yadav, S. R. (2022) · Plant Cell Reports · doi:10.1007/s00299-021-02681-w · Cited by 60
Genome editing reagent delivery in plants
Ghogare, R., Ludwig, Y., Bueno, G. M., Slamet-Loedin, I. H., & Dhingra, A. (2021) · Transgenic Research · doi:10.1007/s11248-021-00239-w · Cited by 61
Wu, Y., Ren, Q., Zhong, Z., Liu, G., Han, Y., Bao, Y., Liu, L., Xiang, S., Liu, S., Tang, X., et al. (2022) · Plant Biotechnology Journal · doi:10.1111/pbi.13838 · Cited by 56
“We hypothesize that Phase II 328 somaclonal variation may be reduced by accelerating plant regeneration with the 329 expression of morphogenic or growth factors, as recently demonstrated in different plant 330 species[45-47].”
BackgroundPepper Crop Improvement Against Cucumber Mosaic Virus (CMV): A Review
Li, N., Yu, C., Yin, Y., Gao, S., Wang, F., Jiao, C., & Yao, M. (2020) · Frontiers in Plant Science · doi:10.3389/fpls.2020.598798 · Cited by 57
New Technologies and Strategies for Grapevine Breeding Through Genetic Transformation
Campos, G., Chialva, C., Miras, S. L., & Lijavetzky, D. (2021) · Frontiers in Plant Science · doi:10.3389/fpls.2021.767522 · Cited by 57
“Plant Cell Rep. 34, 1849–1856. doi: 10.1007/ s00299-015-1832-7 Maher, M. F., Nasti, R. A., Vollbrecht, M., Starker, C. G., Clark, M. D., and Voytas, D. F. (2020).”
InfluentialSpelling Changes and Fluorescent Tagging With Prime Editing Vectors for Plants
Wang, L., Kaya, H. B., Zhang, N., Rai, R., Willmann, M. R., Carpenter, S. C. D., Read, A. C., Martin, F., Fei, Z., Leach, J. E., et al. (2021) · Frontiers in Genome Editing · doi:10.3389/fgeed.2021.617553 · Cited by 57
“However, efficiencies are likely to be higher in stably transformed plants or with meristem transformation (Maher et al., 2020), and possibly with optimization of RT template and PBS length (Lin et al.”
BackgroundKocsisova, Z., & Coneva, V. (2023) · Frontiers in Genome Editing · doi:10.3389/fgeed.2023.1209586 · Cited by 59
Auxin signaling, transport, and regulation during adventitious root formation
Adem, M., Sharma, L., Shekhawat, G. S., Šafránek, M., & Jásik, J. (2024) · Current Plant Biology · doi:10.1016/j.cpb.2024.100385 · Cited by 55
Genes and genome editing tools for breeding desirable phenotypes in ornamentals
Giovannini, A., Laura, M., Nesi, B., Savona, M. R., & Cardi, T. (2021) · Plant Cell Reports · doi:10.1007/s00299-020-02632-x · Cited by 55
Crop bioengineering via gene editing: reshaping the future of agriculture
Atia, M. A. M., Jiang, W., Sedeek, K., Butt, H., & Mahfouz, M. M. (2024) · Plant Cell Reports · doi:10.1007/s00299-024-03183-1 · Cited by 59
“According to Maher et al. (2020), it is possible to regenerate genome-altered shoots from soil-grown tobacco without the need for a tissue-culture stage.”
BackgroundMethod
Metadata
- Authors
- Maher, M. F., Nasti, R. A., Vollbrecht, M., Starker, C. G., Clark, M. D., & Voytas, D. F.
- Affiliations
- University of Minnesota (US)
- Corresponding author
- Voytas, Daniel F.
- ORCID
- Venue
- Nature Biotechnology
- Published
- 2019-12-16
- Volume
- 38
- Issue
- 1
- Pages
- 84-89
- ISSN
- 0733-222X (ISSN-L)
- 1087-0156
- 1546-1696
- PMC
- PMC6954279
- OpenAlex
- W2995711654
- Cited by
- 541
- References
- 27
- Citations by year
- 2026: 64 · 2025: 86 · 2024: 68 · 2023: 78 · 2022: 94 · 2021: 93 · 2020: 55 · 2019: 2
- FWCI
- 20.08
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature Biotechnology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- U.S. Department of Health & Human Services | NIH | National Institute of General Medical Sciences (T32-GM008347)
- Hackett Fund of the University of Minnesota TechAccel
- TechAccel
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › CRISPR and Genetic Engineering
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant tissue culture and regeneration
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
- Keywords
- Cas9, single guide RNA, somatic cells, dicotyledonous plants, transgenerational inheritance, developmental regulators, epigenome, genome editing
- MeSH terms
- Gene Editing, CRISPR-Associated Protein 9, Base Sequence, Mutation, Plant Proteins, Soil, Nicotiana, Meristem, Plant Shoots, Transgenes, Plants, Genetically Modified, Seedlings
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