VvEPFL9-1 knock-out via CRISPR/Cas9 reduces stomatal density in grapevine
Open accessAbstract
Epidermal Patterning Factor Like 9 (EPFL9), also known as STOMAGEN, is a cysteine-rich peptide that induces stomata formation in vascular plants, acting antagonistically to other epidermal patterning factors (EPF1, EPF2). In grapevine there are two EPFL9 genes, EPFL9-1 and EPFL9-2 sharing 82% identity at protein level in the mature functional C-terminal domain. In this study, CRISPR/Cas9 system was applied to functionally characterize VvEPFL9-1 in ‘Sugraone’, a highly transformable genotype. A set of plants, regenerated after gene transfer in embryogenic calli via Agrobacterium tumefaciens, were selected for evaluation. For many lines, the editing profile in the target site displayed a range of mutations mainly causing frameshift in the coding sequence or affecting the second cysteine residue. The analysis of stomata density revealed that in edited plants the number of stomata was significantly reduced compared to control, demonstrating for the first time the role of EPFL9 in a perennial fruit crop. Three edited lines were then assessed for growth, photosynthesis, stomatal conductance, and water use efficiency in experiments carried out at different environmental conditions. Intrinsic water-use efficiency was improved in edited lines compared to control, indicating possible advantages in reducing stomatal density under future environmental drier scenarios. Our results show the potential of manipulating stomatal density for optimizing grapevine adaptation under changing climate conditions.
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Regulating stomatal density by editing VvEPFL9-1 in grapevines results in improved water conservation and higher WUE under drought conditions.
“In grapevines, regulating stomatal density by editing genes like VvEPFL9-1 has resulted in improved water conservation and higher WUE under drought conditions (Clemens et al., 2022).”
From Emerging applications of gene editing technologies for the development of climate-resilient crops (2025) · cites this paper as Clemens et al., 2022
The Discussion (page unavailable) reports lower transpiration in edited grapevines than in wild type under moderate water stress, supporting water conservation in that condition. But the water-stress Results (page unavailable) say intrinsic water-use efficiency (iWUE) was not significantly different between edited and wild-type plants. The claim overstates the evidence by saying editing resulted in higher WUE under drought conditions. (LLM, conf=0.90)
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Cites
MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms
Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018) · Molecular Biology and Evolution · doi:10.1093/molbev/msy096 · Cited by 37,683 · see citing works
A Programmable Dual-RNA–Guided DNA Endonuclease in Adaptive Bacterial Immunity
Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J. A., & Charpentier, E. (2012) · Science · doi:10.1126/science.1225829 · Cited by 17,116 · see citing works
Search-and-replace genome editing without double-strand breaks or donor DNA
Anzalone, A. V., Randolph, P. B., Davis, J. R., Sousa, A. A., Koblan, L. W., Levy, J. M., Chen, P. J., Wilson, C., Newby, G. A., Raguram, A., et al. (2019) · Nature · doi:10.1038/s41586-019-1711-4 · Cited by 4,767 · see citing works
SignalP 5.0 improves signal peptide predictions using deep neural networks
Armenteros, J. J. A., Tsirigos, K. D., Sønderby, C. K., Petersen, T. N., Winther, O., Brunak, S., von HEIJNE, G., & Nielsen, H. (2019) · Nature Biotechnology · doi:10.1038/s41587-019-0036-z · Cited by 4,206 · see citing works
Unipro UGENE: a unified bioinformatics toolkit
Okonechnikov, K., Golosova, O., Fursov, M., & the UGENE team (2012) · Bioinformatics · doi:10.1093/bioinformatics/bts091 · Cited by 3,181 · see citing works
CRISPR/Cas Genome Editing and Precision Plant Breeding in Agriculture
Chen, K., Wang, Y., Zhang, R., Zhang, H., & Gao, C. (2019) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-050718-100049 · Cited by 1,643 · see citing works
CRISPResso2 provides accurate and rapid genome editing sequence analysis
Clement, K., Rees, H. A., Canver, M. C., Gehrke, J. M., Farouni, R., Hsu, J. Y., Cole, M. A., Liu, D. R., Joung, J. K., Bauer, D. E., et al. (2019) · Nature Biotechnology · doi:10.1038/s41587-019-0032-3 · Cited by 1,632 · see citing works
Climate Change and Global Wine Quality
Jones, G. V., White, M. A., Cooper, O. R., & Storchmann, K. (2005) · Climatic Change · doi:10.1007/s10584-005-4704-2 · Cited by 1,207 · see citing works
Stomatal Size, Speed, and Responsiveness Impact on Photosynthesis and Water Use Efficiency1[C]
Lawson, T., & Blatt, M. (2014) · Plant Physiology · doi:10.1104/pp.114.237107 · Cited by 1,046 · see citing works
Maximum leaf conductance driven by CO 2 effects on stomatal size and density over geologic time
Franks, P. J., & Beerling, D. J. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0904209106 · Cited by 966 · see citing works
DNA-Free Genetically Edited Grapevine and Apple Protoplast Using CRISPR/Cas9 Ribonucleoproteins
Malnoy, M., Viola, R., Jung, M., Koo, O. J., Kim, S., Kim, J., Velasco, R., & Kanchiswamy, C. N. (2016) · Frontiers in Plant Science · doi:10.3389/fpls.2016.01904 · Cited by 766 · see citing works
Self-citationImpact of stomatal density and morphology on water-use efficiency in a changing world
Bertolino, L. T., Caine, R. S., & Gray, J. E. (2019) · Frontiers in Plant Science · doi:10.3389/fpls.2019.00225 · Cited by 706 · see citing works
Plantecophys - An R Package for Analysing and Modelling Leaf Gas Exchange Data
Duursma, R. A. (2015) · PLoS ONE · doi:10.1371/journal.pone.0143346 · Cited by 645 · see citing works
Schultz, H. R. (2003) · Plant Cell & Environment · doi:10.1046/j.1365-3040.2003.01064.x · Cited by 621 · see citing works
Sherwood, S. C., & Fu, Q. (2014) · Science · doi:10.1126/science.1247620 · Cited by 596 · see citing works
Easy Leaf Area: Automated digital image analysis for rapid and accurate measurement of leaf area
Easlon, H. M., & Bloom, A. J. (2014) · Applications in Plant Sciences · doi:10.3732/apps.1400033 · Cited by 586 · see citing works
Caine, R. S., Yin, X., Sloan, J., Harrison, E. L., Mohammed, U., Fulton, T., Biswal, A. K., Dionora, J., Chater, C., Coe, R. A., et al. (2018) · New Phytologist · doi:10.1111/nph.15344 · Cited by 569 · see citing works
Termination of asymmetric cell division and differentiation of stomata
Pillitteri, L. J., Sloan, D. B., Bogenschutz, N. L., & Torii, K. U. (2006) · Nature · doi:10.1038/nature05467 · Cited by 562 · see citing works
Stomagen positively regulates stomatal density in Arabidopsis
Sugano, S. S., Shimada, T., Imai, Y., Okawa, K., Tamai, A., Mori, M., & Hara‐Nishimura, I. (2009) · Nature · doi:10.1038/nature08682 · Cited by 477 · see citing works
An Update on the Impact of Climate Change in Viticulture and Potential Adaptations
van Leeuwen, C., Destrac-Irvine, A., Dubernet, M., Duchêne, É., Gowdy, M., Marguerit, E., Pieri, P., Parker, A. K., de Rességuier, L., & Ollat, N. (2019) · Agronomy · doi:10.3390/agronomy9090514 · Cited by 476 · see citing works
SCHULTZ, H. (2000) · Australian Journal of Grape and Wine Research · doi:10.1111/j.1755-0238.2000.tb00156.x · Cited by 435 · see citing works
Lovisolo, C., Perrone, I., Carra, A. M., Ferrandino, A., Flexas, J., Medrano, H., & Schubert, A. (2010) · Functional Plant Biology · doi:10.1071/fp09191 · Cited by 426 · see citing works
Gambetta, G. A., Herrera, J., Dayer, S., Feng, Q., Hochberg, U., & Castellarin, S. D. (2020) · Journal of Experimental Botany · doi:10.1093/jxb/eraa245 · Cited by 416 · see citing works
Reducing Stomatal Density in Barley Improves Drought Tolerance without Impacting on Yield
Hughes, J., Hepworth, C., Dutton, C., Dunn, J. A., Hunt, L., Stephens, J., Waugh, R., Cameron, D. D., & Gray, J. E. (2017) · PLANT PHYSIOLOGY · doi:10.1104/pp.16.01844 · Cited by 409 · see citing works
Hara, K., Yokoo, T., Kajita, R., Onishi, T., Yahata, S., Peterson, K. M., Torii, K. U., & Kakimoto, T. (2009) · Plant and Cell Physiology · doi:10.1093/pcp/pcp068 · Cited by 397 · see citing works
Stomatal closure is induced by hydraulic signals and maintained by ABA in drought-stressed grapevine
Tombesi, S., Nardini, A., Frioni, T., Soccolini, M., Zadra, C., Farinelli, D., Poni, S., & Palliotti, A. (2015) · Scientific Reports · doi:10.1038/srep12449 · Cited by 395 · see citing works
Increasing water‐use efficiency directly through genetic manipulation of stomatal density
Franks, P. J., Doheny‐Adams, T., Britton‐Harper, Z. J., & Gray, J. E. (2015) · New Phytologist · doi:10.1111/nph.13347 · Cited by 391 · see citing works
Doheny‐Adams, T., Hunt, L., Franks, P. J., Beerling, D. J., & Gray, J. E. (2012) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2011.0272 · Cited by 368 · see citing works
Berry ripening: recently heard through the grapevine
Kühn, N., Guan, L., Dai, Z., Wu, B., Lauvergeat, V., Gomès, É., Li, S., Godoy, F., Arce‐Johnson, P., & Delrot, S. (2013) · Journal of Experimental Botany · doi:10.1093/jxb/ert395 · Cited by 365 · see citing works
Palliotti, A., Tombesi, S., Silvestroni, O., Lanari, V., Gatti, M., & Poni, S. (2014) · Scientia Horticulturae · doi:10.1016/j.scienta.2014.07.039 · Cited by 320 · see citing works
The influence of stomatal morphology and distribution on photosynthetic gas exchange
Harrison, E. L., Cubas, L. A., Gray, J. E., & Hepworth, C. (2019) · The Plant Journal · doi:10.1111/tpj.14560 · Cited by 296 · see citing works
Competitive binding of antagonistic peptides fine-tunes stomatal patterning
Lee, J. S., Hnilova, M., Maes, M., Lin, Y.-C. L., Putarjunan, A., Han, S., Ávila-Pacheco, J., & Torii, K. U. (2015) · Nature · doi:10.1038/nature14561 · Cited by 288 · see citing works
Grapevine Responses to Heat Stress and Global Warming
Venios, X., Korkas, E., Nisiotou, A. A., & Banilas, G. (2020) · Plants · doi:10.3390/plants9121754 · Cited by 249 · see citing works
Reduced stomatal density in bread wheat leads to increased water-use efficiency
Dunn, J. A., Hunt, L., Afsharinafar, M., Meselmani, M. A. A., Mitchell, A., Howells, R. M., Wallington, E. J., Fleming, A. J., & Gray, J. E. (2019) · Journal of Experimental Botany · doi:10.1093/jxb/erz248 · Cited by 248 · see citing works
Tomasi, D., Jones, G. V., Giust, M., Lovat, L., & Gaiotti, F. (2011) · American Journal of Enology and Viticulture · doi:10.5344/ajev.2011.10108 · Cited by 247 · see citing works
Rienth, M., Vigneron, N., Darriet, P., Sweetman, C., Burbidge, C. A., Bonghi, C., Walker, R. P., Famiani, F., & Castellarin, S. D. (2021) · Frontiers in Plant Science · doi:10.3389/fpls.2021.643258 · Cited by 245 · see citing works
Wan, D., Guo, Y., Cheng, Y., Hu, Y., Xiao, S., Wang, Y., & Wen, Y. (2020) · Horticulture Research · doi:10.1038/s41438-020-0339-8 · Cited by 237 · see citing works
Methods and Applications of CRISPR-Mediated Base Editing in Eukaryotic Genomes
Hess, G. T., Tycko, J., Yao, D., & Bassik, M. C. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.09.029 · Cited by 234 · see citing works
CRISPR-Cas9 and CRISPR-Cpf1 mediated targeting of a stomatal developmental gene EPFL9 in rice
Yin, X., Biswal, A. K., Dionora, J., Perdigon, K. M., Balahadia, C. P., Mazumdar, S., Chater, C., Lin, H., Coe, R. A., Kretzschmar, T., et al. (2017) · Plant Cell Reports · doi:10.1007/s00299-017-2118-z · Cited by 230 · see citing works
Stomatal Density is Controlled by a Mesophyll-Derived Signaling Molecule
Kondo, T., Kajita, R., Miyazaki, A., Hokoyama, M., Nakamura-Miura, T., Mizuno, S., Masuda, Y., Irie, K., Tanaka, Y., Takada, S., et al. (2009) · Plant and Cell Physiology · doi:10.1093/pcp/pcp180 · Cited by 222 · see citing works
Site-directed nucleases: a paradigm shift in predictable, knowledge-based plant breeding
Podevin, N., Davies, H. V., Hartung, F., Nogué, F., & Casacuberta, J. M. (2013) · Trends in biotechnology · doi:10.1016/j.tibtech.2013.03.004 · Cited by 214 · see citing works
Marshall, E., Costa, L. M., & Gutièrrez‐Marcos, J. F. (2011) · Journal of Experimental Botany · doi:10.1093/jxb/err002 · Cited by 206 · see citing works
Hepworth, C., Doheny‐Adams, T., Hunt, L., Cameron, D. D., & Gray, J. E. (2015) · New Phytologist · doi:10.1111/nph.13598 · Cited by 203 · see citing works
The signalling peptide EPFL9 is a positive regulator of stomatal development
Hunt, L., Bailey, K. J., & Gray, J. E. (2010) · New Phytologist · doi:10.1111/j.1469-8137.2010.03200.x · Cited by 184 · see citing works
Future Climate Change Impacts on European Viticulture: A Review on Recent Scientific Advances
Droulia, F. E., & Charalampopoulos, I. (2021) · Atmosphere · doi:10.3390/atmos12040495 · Cited by 178 · see citing works
Bota, J., Tomás, M., Flexas, J., Medrano, H., & Escalona, J. M. (2015) · Agricultural Water Management · doi:10.1016/j.agwat.2015.07.016 · Cited by 171 · see citing works
Climate change impacts and adaptive strategies: lessons from the grapevine
Mosedale, J. R., Abernethy, K., Smart, R., Wilson, R. J., & Maclean, I. M. D. (2016) · Global Change Biology · doi:10.1111/gcb.13406 · Cited by 170 · see citing works
Exploiting natural variation and genetic manipulation of stomatal conductance for crop improvement
Faralli, M., Matthews, J. S. A., & Lawson, T. (2019) · Current opinion in plant biology · doi:10.1016/j.pbi.2019.01.003 · Cited by 158 · see citing works
Self-citationWhat is the expected impact of climate change on wine aroma compounds and their precursors in grape?
Pons, A., Allamy, L., Schüttler, A., Rauhut, D., Thibon, C., & Darriet, P. (2017) · OENO One · doi:10.20870/oeno-one.2016.0.0.1868 · Cited by 148 · see citing works
SOAR, C. J., Dry, P. R., & LOVEYS, B. R. (2006) · Australian Journal of Grape and Wine Research · doi:10.1111/j.1755-0238.2006.tb00047.x · Cited by 147 · see citing works
Wang, Z., Wong, D. C. J., Wang, Y., Xu, G., Ren, C., Liu, Y., Kuang, Y., Fan, P., Li, S., Xin, H., et al. (2021) · PLANT PHYSIOLOGY · doi:10.1093/plphys/kiab142 · Cited by 147 · see citing works
Li, M.-Y., Jiao, Y., Wang, Y., Zhang, N., Wang, B., Liu, R., Yin, X., Xu, Y., & Liu, G. (2020) · Horticulture Research · doi:10.1038/s41438-020-00371-4 · Cited by 142 · see citing works
Life History Variation as a Model for Understanding Trade-Offs in Plant–Environment Interactions
Lundgren, M. R., & Marais, D. L. D. (2020) · Current Biology · doi:10.1016/j.cub.2020.01.003 · Cited by 141 · see citing works
Stomatal development: focusing on the grasses
Hepworth, C., Caine, R. S., Harrison, E. L., Sloan, J., & Gray, J. E. (2017) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2017.07.009 · Cited by 132 · see citing works
Atauri, I. G. D. C., Duchêne, É., Destrac-Irvine, A., Barbeau, G., de Rességuier, L., Lacombe, T., Parker, A. K., Saurin, N., & van Leeuwen, C. (2017) · OENO One · doi:10.20870/oeno-one.2016.0.0.1622 · Cited by 128 · see citing works
Lavoie‐Lamoureux, A., Sacco, D., Risse, P., & Lovisolo, C. (2016) · Physiologia Plantarum · doi:10.1111/ppl.12530 · Cited by 124 · see citing works
Ohki, S., Takeuchi, M., & Mori, M. (2011) · Nature Communications · doi:10.1038/ncomms1520 · Cited by 123 · see citing works
Climate change decouples drought from early wine grape harvests in France
Cook, B. I., & Wolkovich, E. M. (2016) · Nature Climate Change · doi:10.1038/nclimate2960 · Cited by 123 · see citing works
Function genomics of abiotic stress tolerance in plants: a CRISPR approach
Jain, M. (2015) · Frontiers in Plant Science · doi:10.3389/fpls.2015.00375 · Cited by 118 · see citing works
Molecular control of stomatal development
Zoulias, N., Harrison, E. L., Casson, S. A., & Gray, J. E. (2018) · Biochemical Journal · doi:10.1042/bcj20170413 · Cited by 116 · see citing works
Advances and perspectives on the use of CRISPR/Cas9 systems in plant genomics research
Liu, D., Hu, R., Palla, K. J., Tuskan, G. A., & Yang, X. (2016) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2016.01.007 · Cited by 115 · see citing works
Dayer, S., Herrera, J., Dai, Z., Burlett, R., Lamarque, L. J., Delzon, S., Bortolami, G., Cochard, H., & Gambetta, G. A. (2020) · Journal of Experimental Botany · doi:10.1093/jxb/eraa186 · Cited by 114 · see citing works
Deficit Irrigation Alters Grapevine Growth, Physiology, and Fruit Microclimate
Keller, M., Romero, P., Gohil, H. L., Smithyman, R. P., Riley, W. R., Casassa, L. F., & Harbertson, J. F. (2016) · American Journal of Enology and Viticulture · doi:10.5344/ajev.2016.16032 · Cited by 105 · see citing works
Bobeica, N., Poni, S., Hilbert, G., Renaud, C., Gomès, É., Delrot, S., & Dai, Z. (2015) · Frontiers in Plant Science · doi:10.3389/fpls.2015.00382 · Cited by 100 · see citing works
The impact of climate change on grapevine phenology and the influence of altitude: A regional study
Alikadic, A., Pertot, I., Eccel, E., Dolci, C., Zarbo, C., Caffarra, A., de Filippi, R., & Furlanello, C. (2019) · Agricultural and Forest Meteorology · doi:10.1016/j.agrformet.2019.02.030 · Cited by 95 · see citing works
Mohammed, U., Caine, R. S., Atkinson, J. A., Harrison, E. L., Wells, D. M., Chater, C., Gray, J. E., Swarup, R., & Murchie, E. H. (2019) · Scientific Reports · doi:10.1038/s41598-019-41922-7 · Cited by 92 · see citing works
Positive and negative peptide signals control stomatal density
Shimada, T., Sugano, S. S., & Hara‐Nishimura, I. (2011) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-011-0685-7 · Cited by 88 · see citing works
Genetic and Genomic Approaches for Adaptation of Grapevine to Climate Change
Delrot, S., Grimplet, J., Carbonell‐Bejerano, P., Schwandner, A., Bert, P., Bavaresco, L., Costa, L. D., Gaspero, G. D., Duchêne, É., Hausmann, L., et al. (2020) · Springer eBooks · doi:10.1007/978-3-319-97946-5_7 · Cited by 82 · see citing works
Self-citationClimate change risks and adaptation: new indicators for Mediterranean viticulture
Santillán, D., Garrote, L., Iglesias, A., & Sotés, V. (2019) · Mitigation and Adaptation Strategies for Global Change · doi:10.1007/s11027-019-09899-w · Cited by 73 · see citing works
Costa, L. D., Piazza, S., Pompili, V., Salvagnin, U., Cestaro, A., Moffa, L., Vittani, L., Moser, C., & Malnoy, M. (2020) · Scientific Reports · doi:10.1038/s41598-020-77110-1 · Cited by 72 · see citing works
Self-citationHomologous genes of epidermal patterning factor regulate stomatal development in rice
Lu, J., He, J., Zhou, X., Zhong, J., Li, J., & Liang, Y. (2019) · Journal of Plant Physiology · doi:10.1016/j.jplph.2019.01.010 · Cited by 66 · see citing works
Regeneration of non-chimeric plants from DNA-free edited grapevine protoplasts
Scintilla, S., Salvagnin, U., Giacomelli, L., Zeilmaker, T., Malnoy, M., van der Voort, J. R., & Moser, C. (2022) · Frontiers in Plant Science · doi:10.3389/fpls.2022.1078931 · Cited by 64 · see citing works
Self-citationMorales-Navarro, S., Pérez-Díaz, R., Ortega, A., de Marcos, A., Mena, M., Fenoll, C., González-Villanueva, E., & Ruíz-Lara, S. (2018) · Frontiers in Plant Science · doi:10.3389/fpls.2018.00940 · Cited by 63 · see citing works
Molitor, D., & Junk, J. (2019) · OENO One · doi:10.20870/oeno-one.2019.53.3.2329 · Cited by 62 · see citing works
Pores for Thought: Can Genetic Manipulation of Stomatal Density Protect Future Rice Yields?
Buckley, C. R., Caine, R. S., & Gray, J. E. (2020) · Frontiers in Plant Science · doi:10.3389/fpls.2019.01783 · Cited by 62 · see citing works
Parker, A. K., Atauri, I. G. D. C., Trought, M. C. T., Destrac, A., Agnew, R. H., Sturman, A. P., & van Leeuwen, C. (2020) · OENO One · doi:10.20870/oeno-one.2020.54.4.3861 · Cited by 50 · see citing works
Faralli, M., Bontempo, L., Bianchedi, P. L., Moser, C., Bertamini, M., Lawson, T., Camin, F., Stefanini, M., & Varotto, C. (2021) · Journal of Experimental Botany · doi:10.1093/jxb/erab552 · Cited by 44 · see citing works
Self-citationSPEECHLESS Speaks Loudly in Stomatal Development
Chen, L., Wu, Z., & Hou, S. (2020) · Frontiers in Plant Science · doi:10.3389/fpls.2020.00114 · Cited by 43 · see citing works
Edwards, E. J., Unwin, D., Kilmister, R. L., & Treeby, M. T. (2017) · OENO One · doi:10.20870/oeno-one.2016.0.0.1586 · Cited by 35 · see citing works
Villalobos-González, L., Muñoz-Araya, M., Franck, N., & Pastenes, C. (2019) · Frontiers in Plant Science · doi:10.3389/fpls.2019.01522 · Cited by 34 · see citing works
Chen, T., Peng, J., Yin, X., Li, M., Xiang, G., Wang, Y., Lei, Y., & Xu, Y. (2021) · Horticulture Research · doi:10.1038/s41438-021-00482-6 · Cited by 30 · see citing works
Evolutionary trade‐offs in stomatal spacing
Lawson, T., & McElwain, J. C. (2016) · New Phytologist · doi:10.1111/nph.13972 · Cited by 28 · see citing works
Modified grape composition under climate change conditions requires adaptations in the vineyard
van Leeuwen, C., & Destrac-Irvine, A. (2017) · OENO One · doi:10.20870/oeno-one.2016.0.0.1647 · Cited by 28 · see citing works
Costa, L. D., Vaccari, I., Mandolini, M., & Martinelli, L. (2009) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf802740m · Cited by 25 · see citing works
Regeneration of Plants from DNA-free Edited Grapevine ProtoplastsPreprint
Scintilla, S., Salvagnin, U., Giacomelli, L., Zeilmaker, T., Malnoy, M., van der Voort, J. R., & Moser, C. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.07.16.452503 · Cited by 22 · see citing works
Self-citationPrats-Llinàs, M. T., Nieto, H., DeJong, T. M., Girona, J., & Marsal, J. (2019) · Scientia Horticulturae · doi:10.1016/j.scienta.2019.109065 · Cited by 20 · see citing works
Jones, G. V. (2013) · Springer eBooks · doi:10.1007/978-94-007-6925-0_30 · Cited by 20 · see citing works
Generation of mildew-resistant grapevine clones via genome editing
Giacomelli, L., Zeilmaker, T., Malnoy, M., van der Voort, J. R., & Moser, C. (2019) · Acta Horticulturae · doi:10.17660/actahortic.2019.1248.28 · Cited by 15 · see citing works
Self-citationArrizabalaga-Arriazu, M., Morales, F., Irigoyen, J. J., Hilbert, G., & Pascual, I. (2021) · Australian Journal of Grape and Wine Research · doi:10.1111/ajgw.12494 · Cited by 14 · see citing works
Costa, L. D., Vinciguerra, D., Giacomelli, L., Salvagnin, U., Piazza, S., Spinella, K., Malnoy, M., Moser, C., & Marchesi, U. (2021) · European Food Research and Technology · doi:10.1007/s00217-021-03881-0 · Cited by 9 · see citing works
Self-citationTrait-based responses of seven annual crops to elevated CO2and water limitation
McGranahan, D. A., & Poling, B. (2018) · Renewable Agriculture and Food Systems · doi:10.1017/s1742170517000692 · Cited by 8 · see citing works
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- Delrot S. Grimplet J. Carbonell-bejerano P. Schwandner A. Bert P. Bavaresco L.. (2020). “ Genomic Designing of Climate-Smart Fruit Crops” in Genomic Designing of Climate-Smart Fruit Crops. ed. Kole C. (Switzerland: Springer International Publishing), 157– 270.
- INTEGRAPE Workshop (2021). In XIth International Symposium on Grapevine Physiology and Biotechnology. Stellenbosch, South Africa.
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- Authors
- Clemens, M., Faralli, M., Lagreze, J., Bontempo, L., Piazza, S., Varotto, C., Malnoy, M., Oechel, W., Rizzoli, A., & Dalla Costa, L.
- Affiliations
- Fondazione Edmund Mach (IT)
- University of Exeter (GB)
- Corresponding author
- Faralli, Michele
- Venue
- Frontiers in Plant Science
- Publisher
- Frontiers Media SA
- Published
- 2022-05-17
- Volume
- 13
- Pages
- 878001-878001
- ISSN
- 1664-462X (ISSN-L)
- PMC
- PMC9152544
- OpenAlex
- W4280600624
- Cited by
- 57
- References
- 91
- Citations by year
- 2026: 9 · 2025: 16 · 2024: 15 · 2023: 15 · 2022: 2
- FWCI
- 6.61
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Frontiers in Plant Science (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Iris (University of Trento) (submittedVersion, cc-by)
- CINECA IRIS Institutional Research Information System (Fondazione Edmund Mach) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Autonomous Province of Trento
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › CRISPR and Genetic Engineering
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Horticultural and Viticultural Research
- Keywords
- stomatal density, grapevine, cysteine-rich peptides, gene knockout, CRISPR/Cas9 genome editing, water use efficiency, stomatal conductance, photosynthesis, climate change adaptation
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