Sorry, you need to enable JavaScript to visit this website.

Targeted gene mutation in tetraploid potato through transient TALEN expression in protoplasts

TitleTargeted gene mutation in tetraploid potato through transient TALEN expression in protoplasts
Publication TypeArticolo su Rivista peer-reviewed
Year of Publication2015
AuthorsNicolia, A., Proux-Wéra E., Åhman I., Onkokesung N., Andersson M., Andreasson E., and Zhu L.-H.
JournalJournal of Biotechnology
Volume204
Pagination17 - 24
Date Published2015
ISBN Number01681656 (ISSN)
Keywordsacetolactate synthase, article, branched chain amino acid, callus (plant), gene deletion, Gene editing, Gene expression, gene function, gene mutation, gene targeting, Genes, genetic transfection, Mutagenesis, mutation rate, nonhuman, Plants (botany), potato, priority journal, Protoplast, shoot, Site directed mutagenesis, Site-directed mutagenesis, Solanum tuberosum, TALEN, tetraploidy, transcription activator like effector nuclease, Transient gene expression, Transient gene expressions, vegetable breeding
Abstract

Potato is the third largest food crop in the world, however, the high degree of heterozygosity, the tetrasomic inheritance and severe inbreeding depression are major difficulties for conventional potato breeding. The rapid development of modern breeding methods offers new possibilities to enhance breeding efficiency and precise improvement of desirable traits. New site-directed mutagenesis techniques that can directly edit the target genes without any integration of recombinant DNA are especially favorable. Here we present a successful pipeline for site-directed mutagenesis in tetraploid potato through transient TALEN expression in protoplasts. The transfection efficiency of protoplasts was 38-39% and the site-directed mutation frequency was 7-8% with a few base deletions as the predominant type of mutation. Among the protoplast-derived calli, 11-13% showed mutations and a similar frequency (10%) was observed in the regenerated shoots. Our results indicate that the site-directed mutagenesis technology could be used as a new breeding method in potato as well as for functional analysis of important genes to promote sustainable potato production. © 2015 Elsevier B.V.

Notes

Export Date: 26 August 2015CODEN: JBITDCorrespondence Address: Andreasson, E.; Department of Plant Breeding, Swedish University of Agricultural Sciences, SLU, Box 101, SwedenChemicals/CAS: acetolactate synthase, 9027-45-6References: Ahloowalia, B.S., Maluszynski, M., Nichterlein, K., Global impact of mutation-derived varieties (2004) Euphytica, 135, pp. 187-204;Ali, A., Alexandersson, E., Sandin, M., Resjö, S., Lenman, M., Hedley, P., Levander, F., Andreasson, E., Quantitative proteomics and transcriptomics of potato in response to Phytophthora infestans in compatible and incompatible interactions (2014) BMC Genom., 15, p. 497; Anjum, M., Effect of protoplast source and media on growth and regenerability of protoplast-derived calluses of Solarium tuberosum L. (1998) Acta Physiol. Plant., 20, pp. 129-133; Barrell, P.J., Meiyalaghan, S., Jacobs, J.M.E., Conner, A.J., Applications of biotechnology and genomics in potato improvement (2013) Plant Biotechnol. J., 11, pp. 907-920; Brooks, C., Nekrasov, V., Lippman, Z., Van Eck, J., Efficient gene editing in tomato in the first generation using the CRISPR/Cas9 system (2014) Plant Physiol.; Cardi, T., Puite, K., Ramulu, K., Plant regeneration from mesophyll protoplasts of Solanum commersoni (1990) Plant Sci., 70, pp. 215-221; Cermak, T., Doyle, E.L., Christian, M., Wang, L., Zhang, Y., Schmidt, C., Baller, J.A., Voytas, D.F., Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting (2011) Nucleic Acids Res., 39; Chen, K., Gao, C., Targeted genome modification technologies and their applications in crop improvements (2013) Plant Cell Rep.; Chiu, W., Niwa, Y., Zeng, W., Hirano, T., Kobayashi, H., Sheen, J., Engineered GFP as a vital reporter in plants (1996) Curr. Biol., 6, pp. 325-330; Christian, M., Cermak, T., Doyle, E.L., Schmidt, C., Zhang, F., Hummel, A., Bogdanove, A.J., Voytas, D.F., Targeting DNA double-strand breaks with TAL effector nucleases (2010) Genetics, 186, pp. 757-761; Craig, W., Gargano, D., Scotti, N., Nguyen, T.T., Lao, N.T., Kavanagh, T.A., Dix, P.J., Cardi, T., Direct gene transfer in potato: a comparison of particle bombardment of leaf explants and PEG-mediated transformation of protoplasts (2005) Plant Cell Rep., 24, pp. 603-611; Curtin, S.J., Voytas, D.F., Stupar, R.M., Genome engineering of crops with designer nucleases (2012) Plant Genome J., 5, p. 42; Curtin, S.J., Zhang, F., Sander, J.D., Haun, W.J., Starker, C., Baltes, N.J., Reyon, D., Stupar, R.M., Targeted mutagenesis of duplicated genes in soybean with zinc-finger nucleases (2011) Plant Physiol., 156, pp. 466-473; Edwards, K., Johnstone, C., Thompson, C., A simple and rapid method for the preparation of plant genomic DNA for PCR analysis (1991) Nucleic Acids Res., 19, p. 1349; Endo, M., Osakabe, K., Ichikawa, H., Toki, S., Molecular characterization of true and ectopic gene targeting events at the acetolactate synthase gene in Arabidopsis (2006) Plant Cell Physiol., 47, pp. 372-379; Fichtner, F., Urrea Castellanos, R., Ülker, B., Precision genetic modifications: a new era in molecular biology and crop improvement (2014) Planta; Fischer, R., Hain, R., Chapter 29: tobacco protoplast transformation and use for functional analysis of newly isolated genes and gene constructs (1995) Methods Cell Biol., 50, pp. 401-410; Foulger, D., Jones, M.G.K., Improved efficiency of genotype-dependent regeneration from protoplasts of important potato cultivars (1986) Plant Cell Rep., 5, pp. 72-76; Fu, L., Niu, B., Zhu, Z., Wu, S., Li, W., CD-HIT: accelerated for clustering the next-generation sequencing data (2012) Bioinformatics, 28, pp. 3150-3152; Gaj, T., Gersbach, C.A., Barbas, C.F., ZFN TALEN, and CRISPR/Cas-based methods for genome engineering (2013) Trends Biotechnol., pp. 1-9; Gurushidze, M., Hensel, G., Hiekel, S., Schedel, S., Valkov, V., Kumlehn, J., True-breeding targeted gene knock-out in barley using designer TALE-Nuclease in haploid cells (2014) PLOS ONE, 9; Halpin, C., Cooke, S.E., Barakate, A., El Amrani, A., Ryan, M.D., Self-processing 2A-polyproteins - a system for co-ordinate expression of multiple proteins in transgenic plants (1999) Plant J., 17, pp. 453-459; Hartung, F., Schiemann, J., Precise plant breeding using new genome editing techniques: opportunities, safety and regulation in the EU (2013) Plant J.; Haun, W., Coffman, A., Clasen, B.M., Demorest, Z.L., Lowy, A., Ray, E., Retterath, A., Zhang, F., Improved soybean oil quality by targeted mutagenesis of the fatty acid desaturase 2 gene family (2014) Plant Biotechnol. J., pp. 1-7; Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J.A., Charpentier, E., A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity (2012) Science; Jones, H., Ooms, G., Jones, M.G., Transient gene expression in electroporated Solanum protoplasts (1989) Plant Mol. Biol., 13, pp. 503-511; Karimi, M., Inzé, D., Depicker, A., GATEWAY™ vectors for Agrobacterium-mediated plant transformation (2002) Trends Plant Sci., 7, pp. 193-195; Kim, D., Pertea, G., Trapnell, C., Pimentel, H., Kelley, R., Salzberg, S.L., TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions (2013) Genome Biol., 14; Kim, H., Kim, J.-S., A guide to genome engineering with programmable nucleases (2014) Nat. Rev. Genet., 15, pp. 321-334; Larkin, P.J., Purification and viability determinations of plant protoplasts (1976) Planta, 128, pp. 213-216; Leucci, M.R., Di Sansebastiano, G.-P., Gigante, M., Dalessandro, G., Piro, G., Secretion marker proteins and cell-wall polysaccharides move through different secretory pathways (2007) Planta, 225, pp. 1001-1017; Li, T., Liu, B., Spalding, M.H., Weeks, D.P., Yang, B., High-efficiency TALEN-based gene editing produces disease-resistant rice (2012) Nat. Biotechnol., 30, pp. 390-392; Liang, Z., Zhang, K., Chen, K., Gao, C., Targeted mutagenesis in Zea mays using TALENs and the CRISPR/Cas system (2013) J. Genet. Genom., 41, pp. 63-68; Lindhout, P., Meijer, D., Schotte, T., Hutten, R.C.B., Visser, R.G.F., Eck, H.J., Towards F1 hybrid seed potato breeding (2011) Potato Res., 54, pp. 301-312; Lor, V.S., Starker, C.G., Voytas, D.F., Weiss, D., Olszewski, N.E., Targeted mutagenesis of the tomato PROCERA gene using TALENs (2014) Plant Physiol., 166, pp. 1288-1291; Mackay, G.R., (2003) Potato Breeding at SCRI During the Last Quarter of the 20th Century; Nguyen, H.P., Chakravarthy, S., Velásquez, A.C., McLane, H.L., Zeng, L., Nakayashiki, H., Park, D.-H., Martin, G.B., Methods to study PAMP-triggered immunity using tomato and Nicotiana benthamiana (2010) Mol. Plant Microbe Interact., 23, pp. 991-999; Podevin, N., Davies, H.V., Hartung, F., Nogué, F., Casacuberta, J.M., Site-directed nucleases: a paradigm shift in predictable, knowledge-based plant breeding (2013) Trends Biotechnol., 31, pp. 375-383; Quinlan, A.R., Hall, I.M., BEDTools: a flexible suite of utilities for comparing genomic features (2010) Bioinformatics, 26, pp. 841-842; Reyon, D., Tsai, S.Q., Khayter, C., Foden, J.A., Sander, J.D., Joung, J.K., FLASH assembly of TALENs for high-throughput genome editing (2012) Nat. Biotechnol., 30, pp. 460-465; Robinson, J.T., Thorvaldsdóttir, H., Winckler, W., Guttman, M., Lander, E.S., Getz, G., Mesirov, J.P., Integrative genomics viewer (2011) Nat. Biotechnol., 29, pp. 24-26; Sawai, S., Ohyama, K., Yasumoto, S., Seki, H., Sakuma, T., Yamamoto, T., Takebayashi, Y., Umemoto, N., Sterol side chain reductase 2 is a key enzyme in the biosynthesis of cholesterol, the common precursor of toxic steroidal glycoalkaloids in potato (2014) Plant Cell, 26, pp. 3763-3774; Shan, Q., Wang, Y., Chen, K., Liang, Z., Li, J., Zhang, Y., Zhang, K., Gao, C., Rapid and efficient gene modification in rice and brachypodium using TALENs (2013) Mol. Plant, pp. 1-4; Sharma, S., Sarkar, D., Pandey, S.K., Chandel, P., Tiwari, J.K., Stoloniferous shoot protoplast, an efficient cell system in potato for somatic cell genetic manipulations (2011) Sci. Hortic. (Amsterdam), 128, pp. 84-91; Sheen, J., Signal transduction in maize and arabidopsis mesophyll protoplasts (2001) Plant Physiol., 127, pp. 1466-1475; Shepard, J.F., Totren, R.E., Mesophyll cell protoplasts of potato isolation, proliferation, and plant regeneration (1977) Plant Physiol., 60, pp. 313-316; Shu, Q., Forster, B., Nakagawa, H., (2012) Plant Mutation Breeding and Biotechnology, , CAB International and FAO; Shukla, V.K., Doyon, Y., Miller, J.C., DeKelver, R.C., Moehle, E.A., Worden, S.E., Mitchell, J.C., Urnov, F.D., Precise genome modification in the crop species Zea mays using zinc-finger nucleases (2009) Nature, 459, pp. 437-441; Spooner, D.M., McLean, K., Ramsay, G., Waugh, R., Bryan, G.J., A single domestication for potato based on multilocus amplified fragment length polymorphism genotyping (2005) Proc. Natl. Acad. Sci. U. S. A., 102, pp. 14694-14699; Tan, S., Evans, R.R., Dahmer, M.L., Singh, B.K., Shaner, D.L., Imidazolinone-tolerant crops: history, current status and future (2005) Pest Manag. Sci., 61, pp. 246-257; Tavazza, R., Ancora, G., Plant regeneration from mesophyll protoplasts in commercial potato cultivars (Primura, Kennebec, Spunta Desirée) (1986) Plant Cell Rep., 5, pp. 243-246; Townsend, J.A., Wright, D.A., Winfrey, R.J., Fu, F., Maeder, M.L., Joung, J.K., Voytas, D.F., High-frequency modification of plant genes using engineered zinc-finger nucleases (2009) Nature, 459, pp. 442-445; Uitdewilligen, J.G.A.M.L., Wolters, A.-M.A., D’hoop, B.B., Borm, T.J.A., Visser, R.G.F., van Eck, H.J., A next-generation sequencing method for genotyping-by-sequencing of highly heterozygous autotetraploid potato (2013) PLOS ONE, 8; Valton, J., Dupuy, A., Daboussi, F., Thomas, S., Maréchal, A., Macmaster, R., Melliand, K., Duchateau, P., Overcoming transcription activator-like effector (TALE) DNA binding domain sensitivity to cytosine methylation (2012) J. Biol. Chem., 287, pp. 38427-38432; Wang, Y., Cheng, X., Shan, Q., Zhang, Y., Liu, J., Gao, C., Qiu, J.-L., Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew (2014) Nat. Biotechnol., pp. 1-6; Waugh, R., Leader, D.J., McCallum, N., Caldwell, D., Harvesting the potential of induced biological diversity (2006) Trends Plant Sci., 11, pp. 71-79; Wendt, T., Holm, P.B., Starker, C.G., Christian, M., Voytas, D.F., Brinch-Pedersen, H., Holme, I.B., TAL effector nucleases induce mutations at a pre-selected location in the genome of primary barley transformants (2013) Plant Mol. Biol., pp. 279-285; Wood, C.C., Petrie, J.R., Shrestha, P., Mansour, M.P., Nichols, P.D., Green, A.G., Singh, S.P., A leaf-based assay using interchangeable design principles to rapidly assemble multistep recombinant pathways (2009) Plant Biotechnol. J., 7, pp. 914-924; Yoo, S.-D., Cho, Y.-H., Sheen, J., Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis (2007) Nat. Protoc., 2, pp. 1565-1572; Zhang, H., Zhang, J., Wei, P., Zhang, B., Gou, F., Feng, Z., Mao, Y., Zhu, J.-K., The CRISPR/Cas9 system produces specific and homozygous targeted gene editing in rice in one generation (2014) Plant Biotechnol. J., pp. 1-11; Zhang, Y., Su, J., Duan, S., Ao, Y., Dai, J., Liu, J., Wang, P., Wang, H., A highly efficient rice green tissue protoplast system for transient gene expression and studying light/chloroplast-related processes (2011) Plant Methods, 7, p. 30; Zhang, Y., Zhang, F., Li, X., Baller, J.A., Qi, Y., Starker, C.G., Bogdanove, A.J., Voytas, D.F., Transcription activator-like effector nucleases enable efficient plant genome engineering (2013) Plant Physiol., 161, pp. 20-27; Zhou, H., Liu, B., Weeks, D.P., Spalding, M.H., Yang, B., Large chromosomal deletions and heritable small genetic changes induced by CRISPR/Cas9 in rice (2014) Nucleic Acids Res., pp. 1-12

URLhttp://www.scopus.com/inward/record.url?eid=2-s2.0-84927722975&partnerID=40&md5=369a93409188796846e1e057467810a2
Citation Key5414