Application of Genome Editing in Tomato Breeding: Mechanisms, Advances, and Prospects

. 2021 Jan 12 ; 22 (2) : . [epub] 20210112

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid33445555

Plants regularly face the changing climatic conditions that cause biotic and abiotic stress responses. The abiotic stresses are the primary constraints affecting crop yield and nutritional quality in many crop plants. The advances in genome sequencing and high-throughput approaches have enabled the researchers to use genome editing tools for the functional characterization of many genes useful for crop improvement. The present review focuses on the genome editing tools for improving many traits such as disease resistance, abiotic stress tolerance, yield, quality, and nutritional aspects of tomato. Many candidate genes conferring tolerance to abiotic stresses such as heat, cold, drought, and salinity stress have been successfully manipulated by gene modification and editing techniques such as RNA interference, insertional mutagenesis, and clustered regularly interspaced short palindromic repeat (CRISPR/Cas9). In this regard, the genome editing tools such as CRISPR/Cas9, which is a fast and efficient technology that can be exploited to explore the genetic resources for the improvement of tomato and other crop plants in terms of stress tolerance and nutritional quality. The review presents examples of gene editing responsible for conferring both biotic and abiotic stresses in tomato simultaneously. The literature on using this powerful technology to improve fruit quality, yield, and nutritional aspects in tomato is highlighted. Finally, the prospects and challenges of genome editing, public and political acceptance in tomato are discussed.

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Razifard H., Ramos A., Della Valle A.L., Bodary C., Goetz E., Manser E.J., Li X., Zhang L., Visa S., Tieman D. Genomic evidence for complex domestication history of the cultivated tomato in Latin America. Mol. Biol. Evol. 2020;37:1118–1132. doi: 10.1093/molbev/msz297. PubMed DOI PMC

Meyer R.S., Purugganan M.D. Evolution of crop species: Genetics of domestication and diversification. Nat. Rev. Genet. 2013;14:840–852. doi: 10.1038/nrg3605. PubMed DOI

Parmar N., Singh K.H., Sharma D., Singh L., Kumar P., Nanjundan J., Khan Y.J., Chauhan D.K., Thakur A.K. Genetic engineering strategies for biotic and abiotic stress tolerance and quality enhancement in horticultural crops: A comprehensive review. 3 Biotech. 2017;7:239. doi: 10.1007/s13205-017-0870-y. PubMed DOI PMC

Bawa A., Anilakumar K. Genetically modified foods: Safety, risks and public concerns—A review. J. Food Sci. Technol. 2013;50:1035–1046. doi: 10.1007/s13197-012-0899-1. PubMed DOI PMC

Gascuel Q., Diretto G., Monforte A.J., Fortes A.M., Granell A. Use of natural diversity and biotechnology to increase the quality and nutritional content of tomato and grape. Front. Plant Sci. 2017;8:652. doi: 10.3389/fpls.2017.00652. PubMed DOI PMC

Labate J.A., Grandillo S., Fulton T., Muños S., Caicedo A.L., Peralta I., Ji Y., Shetelat R.T., Scott J.W., Gonzalo M.J. Genome Mapping and Molecular Breeding in Plants. Volume 5 Springer; Berlin/Heidelberg, Germany: New York, NY, USA: 2007. Tomato.

Just D., Garcia V., Fernandez L., Bres C., Mauxion J.-P., Petit J., Jorly J., Assali J., Bournonville C., Ferrand C. Micro-Tom mutants for functional analysis of target genes and discovery of new alleles in tomato. Plant Biotechnol. 2013;30 doi: 10.5511/plantbiotechnology.13.0622a. DOI

Meissner R., Chague V., Zhu Q., Emmanuel E., Elkind Y., Levy A.A. A high throughput system for transposon tagging and promoter trapping in tomato. Plant J. 2000;22:265–274. doi: 10.1046/j.1365-313x.2000.00735.x. PubMed DOI

Menda N., Semel Y., Peled D., Eshed Y., Zamir D. In silico screening of a saturated mutation library of tomato. Plant J. 2004;38:861–872. doi: 10.1111/j.1365-313X.2004.02088.x. PubMed DOI

Rothan C., Diouf I., Causse M. Trait discovery and editing in tomato. Plant J. 2019;97:73–90. doi: 10.1111/tpj.14152. PubMed DOI

Ariizumi T., Kishimoto S., Kakami R., Maoka T., Hirakawa H., Suzuki Y., Ozeki Y., Shirasawa K., Bernillon S., Okabe Y. Identification of the carotenoid modifying gene PALE YELLOW PETAL 1 as an essential factor in xanthophyll esterification and yellow flower pigmentation in tomato (S olanum lycopersicum) Plant J. 2014;79:453–465. doi: 10.1111/tpj.12570. PubMed DOI

Chaudhary J., Alisha A., Bhatt V., Chandanshive S., Kumar N., Mir Z., Kumar A., Yadav S.K., Shivaraj S., Sonah H. Mutation breeding in tomato: Advances, applicability and challenges. Plants. 2019;8:128. doi: 10.3390/plants8050128. PubMed DOI PMC

Hao S., Ariizumi T., Ezura H. SEXUAL STERILITY is essential for both male and female gametogenesis in tomato. Plant Cell Physiol. 2017;58:22–34. PubMed

Isaacson T., Ronen G., Zamir D., Hirschberg J. Cloning of tangerine from tomato reveals a carotenoid isomerase essential for the production of β-carotene and xanthophylls in plants. Plant Cell. 2002;14:333–342. doi: 10.1105/tpc.010303. PubMed DOI PMC

Minoia S., Petrozza A., D’Onofrio O., Piron F., Mosca G., Sozio G., Cellini F., Bendahmane A., Carriero F. A new mutant genetic resource for tomato crop improvement by TILLING technology. BMC Res. Notes. 2010;3:69. doi: 10.1186/1756-0500-3-69. PubMed DOI PMC

Okabe Y., Asamizu E., Saito T., Matsukura C., Ariizumi T., Brès C., Rothan C., Mizoguchi T., Ezura H. Tomato TILLING technology: Development of a reverse genetics tool for the efficient isolation of mutants from Micro-Tom mutant libraries. Plant Cell Physiol. 2011;52:1994–2005. doi: 10.1093/pcp/pcr134. PubMed DOI PMC

Park S.J., Jiang K., Tal L., Yichie Y., Gar O., Zamir D., Eshed Y., Lippman Z.B. Optimization of crop productivity in tomato using induced mutations in the florigen pathway. Nat. Genet. 2014;46:1337–1342. doi: 10.1038/ng.3131. PubMed DOI

Petit J., Bres C., Just D., Garcia V., Mauxion J.-P., Marion D., Bakan B., Joubès J., Domergue F., Rothan C. Analyses of tomato fruit brightness mutants uncover both cutin-deficient and cutin-abundant mutants and a new hypomorphic allele of GDSL lipase. Plant Physiol. 2014;164:888–906. doi: 10.1104/pp.113.232645. PubMed DOI PMC

Petit J., Bres C., Mauxion J.-P., Tai F.W.J., Martin L.B., Fich E.A., Joubès J., Rose J.K., Domergue F., Rothan C. The glycerol-3-phosphate acyltransferase GPAT6 from tomato plays a central role in fruit cutin biosynthesis. Plant Physiol. 2016;171:894–913. doi: 10.1104/pp.16.00409. PubMed DOI PMC

Pulungan S.I., Yano R., Okabe Y., Ichino T., Kojima M., Takebayashi Y., Sakakibara H., Ariizumi T., Ezura H. SlLAX1 is required for normal leaf development mediated by balanced adaxial and abaxial pavement cell growth in tomato. Plant Cell Physiol. 2018;59:1170–1186. doi: 10.1093/pcp/pcy052. PubMed DOI

Shi J.X., Adato A., Alkan N., He Y., Lashbrooke J., Matas A.J., Meir S., Malitsky S., Isaacson T., Prusky D. The tomato S l SHINE 3 transcription factor regulates fruit cuticle formation and epidermal patterning. New Phytol. 2013;197:468–480. doi: 10.1111/nph.12032. PubMed DOI

Xu J., Wolters-Arts M., Mariani C., Huber H., Rieu I. Heat stress affects vegetative and reproductive performance and trait correlations in tomato (Solanum lycopersicum) Euphytica. 2017;213:156. doi: 10.1007/s10681-017-1949-6. DOI

Yeats T.H., Buda G.J., Wang Z., Chehanovsky N., Moyle L.C., Jetter R., Schaffer A.A., Rose J.K. The fruit cuticles of wild tomato species exhibit architectural and chemical diversity, providing a new model for studying the evolution of cuticle function. Plant J. 2012;69:655–666. doi: 10.1111/j.1365-313X.2011.04820.x. PubMed DOI PMC

Bai Y., Kissoudis C., Yan Z., Visser R.G., van der Linden G. Plant behaviour under combined stress: Tomato responses to combined salinity and pathogen stress. Plant J. 2018;93:781–793. doi: 10.1111/tpj.13800. PubMed DOI

Foolad M., Lin G., Chen F. Comparison of QTLs for seed germination under non-stress, cold stress and salt stress in tomato. Plant Breed. 1999;118:167–173. doi: 10.1046/j.1439-0523.1999.118002167.x. DOI

Wen J., Jiang F., Weng Y., Sun M., Shi X., Zhou Y., Yu L., Wu Z. Identification of heat-tolerance QTLs and high-temperature stress-responsive genes through conventional QTL mapping, QTL-seq and RNA-seq in tomato. BMC Plant Biol. 2019;19:398. doi: 10.1186/s12870-019-2008-3. PubMed DOI PMC

Causse M., Duffe P., Gomez M., Buret M., Damidaux R., Zamir D., Gur A., Chevalier C., Lemaire-Chamley M., Rothan C. A genetic map of candidate genes and QTLs involved in tomato fruit size and composition. J. Exp. Bot. 2004;55:1671–1685. doi: 10.1093/jxb/erh207. PubMed DOI

Liu Y.S., Gur A., Ronen G., Causse M., Damidaux R., Buret M., Hirschberg J., Zamir D. There is more to tomato fruit colour than candidate carotenoid genes. Plant Biotechnol. J. 2003;1:195–207. doi: 10.1046/j.1467-7652.2003.00018.x. PubMed DOI

Stevens R., Page D., Gouble B., Garchery C., Zamir D., Causse M. Tomato fruit ascorbic acid content is linked with monodehydroascorbate reductase activity and tolerance to chilling stress. Plant Cell Environ. 2008;31:1086–1096. doi: 10.1111/j.1365-3040.2008.01824.x. PubMed DOI

Bauchet G., Grenier S., Samson N., Bonnet J., Grivet L., Causse M. Use of modern tomato breeding germplasm for deciphering the genetic control of agronomical traits by Genome Wide Association study. Theor. Appl. Genet. 2017;130:875–889. doi: 10.1007/s00122-017-2857-9. PubMed DOI

Shirasawa K., Fukuoka H., Matsunaga H., Kobayashi Y., Kobayashi I., Hirakawa H., Isobe S., Tabata S. Genome-wide association studies using single nucleotide polymorphism markers developed by re-sequencing of the genomes of cultivated tomato. DNA Res. 2013;20:593–603. doi: 10.1093/dnares/dst033. PubMed DOI PMC

Tieman D., Zhu G., Resende M.F., Lin T., Nguyen C., Bies D., Rambla J.L., Beltran K.S.O., Taylor M., Zhang B. A chemical genetic roadmap to improved tomato flavor. Science. 2017;355:391–394. doi: 10.1126/science.aal1556. PubMed DOI

Sauvage C., Segura V., Bauchet G., Stevens R., Do P.T., Nikoloski Z., Fernie A.R., Causse M. Genome-wide association in tomato reveals 44 candidate loci for fruit metabolic traits. Plant Physiol. 2014;165:1120–1132. doi: 10.1104/pp.114.241521. PubMed DOI PMC

Zhang J., Zhao J., Xu Y., Liang J., Chang P., Yan F., Li M., Liang Y., Zou Z. Genome-wide association mapping for tomato volatiles positively contributing to tomato flavor. Front. Plant Sci. 2015;6:1042. doi: 10.3389/fpls.2015.01042. PubMed DOI PMC

Zhao J., Sauvage C., Zhao J., Bitton F., Bauchet G., Liu D., Huang S., Tieman D.M., Klee H.J., Causse M. Meta-analysis of genome-wide association studies provides insights into genetic control of tomato flavor. Nat. Commun. 2019;10:1–12. doi: 10.1038/s41467-019-09462-w. PubMed DOI PMC

Sun Y., Liang Y., Wu J., Li Y., Cui X., Qin L. Dynamic QTL analysis for fruit lycopene content and total soluble solid content in a Solanum lycopersicum x S. pimpinellifolium cross. Genet. Mol. Res. 2012;11:3696–3710. doi: 10.4238/2012.August.17.8. PubMed DOI

Bolger A., Scossa F., Bolger M.E., Lanz C., Maumus F., Tohge T., Quesneville H., Alseekh S., Sørensen I., Lichtenstein G. The genome of the stress-tolerant wild tomato species Solanum pennellii. Nat. Genet. 2014;46:1034–1038. doi: 10.1038/ng.3046. PubMed DOI PMC

Consortium T.G. The tomato genome sequence provides insights into fleshy fruit evolution. Nature. 2012;485:635. doi: 10.1038/nature11119. PubMed DOI PMC

Consortium T.G.S., Aflitos S., Schijlen E., de Jong H., de Ridder D., Smit S., Finkers R., Wang J., Zhang G., Li N. Exploring genetic variation in the tomato (Solanum section Lycopersicon) clade by whole-genome sequencing. Plant J. 2014;80:136–148. PubMed

Gao L., Gonda I., Sun H., Ma Q., Bao K., Tieman D.M., Burzynski-Chang E.A., Fish T.L., Stromberg K.A., Sacks G.L. The tomato pan-genome uncovers new genes and a rare allele regulating fruit flavor. Nat. Genet. 2019;51:1044–1051. doi: 10.1038/s41588-019-0410-2. PubMed DOI

Fernandez-Pozo N., Menda N., Edwards J.D., Saha S., Tecle I.Y., Strickler S.R., Bombarely A., Fisher-York T., Pujar A., Foerster H. The Sol Genomics Network (SGN)—From genotype to phenotype to breeding. Nucleic Acids Res. 2015;43:D1036–D1041. doi: 10.1093/nar/gku1195. PubMed DOI PMC

Lin T., Zhu G., Zhang J., Xu X., Yu Q., Zheng Z., Zhang Z., Lun Y., Li S., Wang X. Genomic analyses provide insights into the history of tomato breeding. Nat. Genet. 2014;46:1220–1226. doi: 10.1038/ng.3117. PubMed DOI

Razali R., Bougouffa S., Morton M.J., Lightfoot D.J., Alam I., Essack M., Arold S.T., Kamau A.A., Schmöckel S.M., Pailles Y. The genome sequence of the wild tomato Solanum pimpinellifolium provides insights into salinity tolerance. Front. Plant Sci. 2018;9:1402. doi: 10.3389/fpls.2018.01402. PubMed DOI PMC

Zhu G., Wang S., Huang Z., Zhang S., Liao Q., Zhang C., Lin T., Qin M., Peng M., Yang C. Rewiring of the fruit metabolome in tomato breeding. Cell. 2018;172:249–261.e212. doi: 10.1016/j.cell.2017.12.019. PubMed DOI

Mondini L., Noorani A., Pagnotta M.A. Assessing plant genetic diversity by molecular tools. Diversity. 2009;1:19–35. doi: 10.3390/d1010019. DOI

Wenzel G. Molecular plant breeding: Achievements in green biotechnology and future perspectives. Appl. Microbiol. Biotechnol. 2006;70:642–650. doi: 10.1007/s00253-006-0375-9. PubMed DOI

Hidema J., Teranishi M., Iwamatsu Y., Hirouchi T., Ueda T., Sato T., Burr B., Sutherland B.M., Yamamoto K., Kumagai T. Spontaneously occurring mutations in the cyclobutane pyrimidine dimer photolyase gene cause different sensitivities to ultraviolet-B in rice. Plant J. 2005;43:57–67. doi: 10.1111/j.1365-313X.2005.02428.x. PubMed DOI

Manova V., Gruszka D. DNA damage and repair in plants—From models to crops. Front. Plant Sci. 2015;6:885. doi: 10.3389/fpls.2015.00885. PubMed DOI PMC

Brock R. The role of induced mutations in plant improvement. Radiat. Bot. 1971;11:181–196. doi: 10.1016/S0033-7560(71)90273-0. DOI

Brock R. Genetic Diversity in Plants. Springer; Boston, MA, USA: 1977. Prospects and perspectives in mutation breeding; pp. 117–132. PubMed

Veillet F., Perrot L., Chauvin L., Kermarrec M.-P., Guyon-Debast A., Chauvin J.-E., Nogué F., Mazier M. Transgene-free genome editing in tomato and potato plants using agrobacterium-mediated delivery of a CRISPR/Cas9 cytidine base editor. Int. J. Mol. Sci. 2019;20:402. doi: 10.3390/ijms20020402. PubMed DOI PMC

Puchta H. Applying CRISPR/Cas for genome engineering in plants: The best is yet to come. Curr. Opin. Plant Biol. 2017;36:1–8. doi: 10.1016/j.pbi.2016.11.011. PubMed DOI

Tang X., Lowder L.G., Zhang T., Malzahn A.A., Zheng X., Voytas D.F., Zhong Z., Chen Y., Ren Q., Li Q. A CRISPR–Cpf1 system for efficient genome editing and transcriptional repression in plants. Nat. Plants. 2017;3:1–5. PubMed

Vats S., Kumawat S., Kumar V., Patil G.B., Joshi T., Sonah H., Sharma T.R., Deshmukh R. Genome editing in plants: Exploration of technological advancements and challenges. Cells. 2019;8:1386. doi: 10.3390/cells8111386. PubMed DOI PMC

Yoder J.I. Rapid proliferation of the maize transposable element Activator in transgenic tomato. Plant Cell. 1990;2:723–730. PubMed PMC

Liu Y., Schiff M., Dinesh-Kumar S. Virus-induced gene silencing in tomato. Plant J. 2002;31:777–786. doi: 10.1046/j.1365-313X.2002.01394.x. PubMed DOI

Čermák T., Baltes N.J., Čegan R., Zhang Y., Voytas D.F. High-frequency, precise modification of the tomato genome. Genome Biol. 2015;16:232. doi: 10.1186/s13059-015-0796-9. PubMed DOI PMC

Gupta P., Reddaiah B., Salava H., Upadhyaya P., Tyagi K., Sarma S., Datta S., Malhotra B., Thomas S., Sunkum A. Next-generation sequencing (NGS)-based identification of induced mutations in a doubly mutagenized tomato (Solanum lycopersicum) population. Plant J. 2017;92:495–508. doi: 10.1111/tpj.13654. PubMed DOI

David-Schwartz R., Badani H., Smadar W., Levy A.A., Galili G., Kapulnik Y. Identification of a novel genetically controlled step in mycorrhizal colonization: Plant resistance to infection by fungal spores but not extra-radical hyphae. Plant J. 2001;27:561–569. doi: 10.1046/j.1365-313X.2001.01113.x. PubMed DOI

Negi S., Santisree P., Kharshiing E.V., Sharma R. Inhibition of the ubiquitin—Proteasome pathway alters cellular levels of nitric oxide in tomato seedlings. Mol. Plant. 2010;3:854–869. doi: 10.1093/mp/ssq033. PubMed DOI

Brooks C., Nekrasov V., Lippman Z.B., Van Eck J. Efficient gene editing in tomato in the first generation using the clustered regularly interspaced short palindromic repeats/CRISPR-associated9 system. Plant Physiol. 2014;166:1292–1297. doi: 10.1104/pp.114.247577. PubMed DOI PMC

Liu R., How-Kit A., Stammitti L., Teyssier E., Rolin D., Mortain-Bertrand A., Halle S., Liu M., Kong J., Wu C. A DEMETER-like DNA demethylase governs tomato fruit ripening. Proc. Natl. Acad. Sci. USA. 2015;112:10804–10809. doi: 10.1073/pnas.1503362112. PubMed DOI PMC

Stadler L.J. Genetic effects of X-rays in maize. Proc. Natl. Acad. Sci. USA. 1928;14:69. doi: 10.1073/pnas.14.1.69. PubMed DOI PMC

Smith H.H. Radiation in the production of useful mutations. Bot. Rev. 1958;24:1–24. doi: 10.1007/BF02872515. DOI

Naito K., Kusaba M., Shikazono N., Takano T., Tanaka A., Tanisaka T., Nishimura M. Transmissible and nontransmissible mutations induced by irradiating Arabidopsis thaliana pollen with γ-rays and carbon ions. Genetics. 2005;169:881–889. doi: 10.1534/genetics.104.033654. PubMed DOI PMC

Okamura M., Yasuno N., Ohtsuka M., Tanaka A., Shikazono N., Hase Y. Wide variety of flower-color and -shape mutants regenerated from leaf cultures irradiated with ion beams. Nucl. Instrum. Methods Phys. Res. Sect. B Beam Interact. Mater. At. 2003;206:574–578. doi: 10.1016/S0168-583X(03)00835-8. DOI

Shikazono N., Suzuki C., Kitamura S., Watanabe H., Tano S., Tanaka A. Analysis of mutations induced by carbon ions in Arabidopsis thaliana. J. Exp. Bot. 2005;56:587–596. doi: 10.1093/jxb/eri047. PubMed DOI

Abe T., Ryuto H., Fukunishi N. Ion beam radiation mutagenesis. Plant Mutat. Breed. Biotechnol. 2012:99–106. doi: 10.1079/9781780640853.0099. DOI

Magori S., Tanaka A., Kawaguchi M. The Handbook of Plant Mutation Screening. WILEY-VCH Verlag; Weinheim, Germany: 2010. Physically induced mutation: Ion beam mutagenesis; pp. 3–16.

Tanaka A., Shikazono N., Hase Y. Studies on biological effects of ion beams on lethality, molecular nature of mutation, mutation rate, and spectrum of mutation phenotype for mutation breeding in higher plants. J. Radiat. Res. 2010;51:223–233. doi: 10.1269/jrr.09143. PubMed DOI

Mba C. Induced mutations unleash the potentials of plant genetic resources for food and agriculture. Agronomy. 2013;3:200–231. doi: 10.3390/agronomy3010200. DOI

Kazama Y., Hirano T., Nishihara K., Ohbu S., Shirakawa Y., Abe T. Effect of high-LET Fe-ion beam irradiation on mutation induction in Arabidopsis thaliana. Genes Genet. Syst. 2013;88:189–197. doi: 10.1266/ggs.88.189. PubMed DOI

Kazama Y., Hirano T., Saito H., Liu Y., Ohbu S., Hayashi Y., Abe T. Characterization of highly efficient heavy-ion mutagenesis in Arabidopsis thaliana. BMC Plant Biol. 2011;11:161. doi: 10.1186/1471-2229-11-161. PubMed DOI PMC

Kazama Y., Ishii K., Hirano T., Wakana T., Yamada M., Ohbu S., Abe T. Different mutational function of low-and high-linear energy transfer heavy-ion irradiation demonstrated by whole-genome resequencing of Arabidopsis mutants. Plant J. 2017;92:1020–1030. doi: 10.1111/tpj.13738. PubMed DOI

Kazama Y., Ma L., Hirano T., Ohbu S., Shirakawa Y., Hatakeyama S., Tanaka S., Abe T. Rapid evaluation of effective linear energy transfer in heavy-ion mutagenesis of Arabidopsis thaliana. Plant Biotechnol. 2012;29:441–445. doi: 10.5511/plantbiotechnology.12.0921a. DOI

Cheema A.A., Atta B.M. Radiosensitivity studies in basmati rice. Pak. J. Bot. 2003;35:197–207.

Sato Y., Shirasawa K., Takahashi Y., Nishimura M., Nishio T. Mutant selection from progeny of gamma-ray-irradiated rice by DNA heteroduplex cleavage using Brassica petiole extract. Breed. Sci. 2006;56:179–183. doi: 10.1270/jsbbs.56.179. DOI

Matsukura C., Yamaguchi I., Inamura M., Ban Y., Kobayashi Y., Yin Y.-G., Saito T., Kuwata C., Imanishi S., Nishimura S. Generation of gamma irradiation-induced mutant lines of the miniature tomato (Solanum lycopersicum L.) cultivar ‘Micro-Tom’. Plant Biotechnol. 2007;24:39–44. doi: 10.5511/plantbiotechnology.24.39. DOI

Melamed S. Chemical and Physical Mutagenesis in the Tomato Cultivar Micro-Tom. Hebrew University of Jerusalem; Jerusalem, Israel: 1999.

Leitão J. Chemical mutagenesis. In: Shu Q.Y., Forster B.P., Nakagawa H., editors. Plant Mutat. Breed. Biotechnol. CABI Publishing; Wallingford, UK: 2012. pp. 135–158.

Heslot H. Manual on Mutation Breeding. Iaea Vienna Second; IAEA, Vienna: 1977. Review of main mutagenic compounds; pp. 51–58. (Technical Report Series).

Saito T., Ariizumi T., Okabe Y., Asamizu E., Hiwasa-Tanase K., Fukuda N., Mizoguchi T., Yamazaki Y., Aoki K., Ezura H. TOMATOMA: A novel tomato mutant database distributing Micro-Tom mutant collections. Plant Cell Physiol. 2011;52:283–296. doi: 10.1093/pcp/pcr004. PubMed DOI PMC

Van Harten A.M. Mutation Breeding: Theory and Practical Applications. Cambridge University Press; Cambridge, UK: 1998. p. 353.

Till B.J., Cooper J., Tai T.H., Colowit P., Greene E.A., Henikoff S., Comai L. Discovery of chemically induced mutations in rice by TILLING. BMC Plant Biol. 2007;7:19. doi: 10.1186/1471-2229-7-19. PubMed DOI PMC

Szarejko I., Maluszynski M. Translocations and inversions in barley induced by fast neutrons and N-nitroso-N-methylurea (MNUA)[Mutagenesis] Barley Genet. Newsl. 1980;10:67–69.

Maluszynski M., Szarejko I., Maluszynska J. Encyclopedia of Applied Plant Sciences. Academic Press; New York, NY, USA: 2003. pp. 186–201.

Wienholds E., Van Eeden F., Kosters M., Mudde J., Plasterk R.H., Cuppen E. Efficient target-selected mutagenesis in zebrafish. Genome Res. 2003;13:2700–2707. doi: 10.1101/gr.1725103. PubMed DOI PMC

Wisman E., Koornneef M., Chase T., Lifshytz E., Ramanna M., Zabel P. Genetic and molecular characterization of an Adh-1 null mutant in tomato. Mol. Gen. Genet. MGG. 1991;226:120–128. doi: 10.1007/BF00273595. PubMed DOI

Piron F., Nicolaï M., Minoïa S., Piednoir E., Moretti A., Salgues A., Zamir D., Caranta C., Bendahmane A. An induced mutation in tomato eIF4E leads to immunity to two potyviruses. PLoS ONE. 2010;5:e11313. doi: 10.1371/journal.pone.0011313. PubMed DOI PMC

Kostov K., Batchvarova R., Slavov S. Application of chemical mutagenesis to increase the resistance of tomato to Orobanche ramosa L. Bulg. J. Agric. Sci. 2007;13:505–513.

Mazzucato A., Cellini F., Bouzayen M., Zouine M., Mila I., Minoia S., Petrozza A., Picarella M.E., Ruiu F., Carriero F. A TILLING allele of the tomato Aux/IAA9 gene offers new insights into fruit set mechanisms and perspectives for breeding seedless tomatoes. Mol. Breed. 2015;35:22. doi: 10.1007/s11032-015-0222-8. DOI

Maghuly F., Jankowicz-Cieslak J., Till B.J., Laimer M. Jatropha, Challenges for a New Energy Crop. Springer; New York, NY, USA: 2013. The Use of Ecotilling for the Genetic Improvement of Jatropha curcas L. pp. 335–349.

Maghuly F., Laimer M. The Jatropha Genome. Springer; Cham, Switzerland: 2017. Forward and reverse genetics for the improvement of Jatropha; pp. 131–148.

Greene E.A., Codomo C.A., Taylor N.E., Henikoff J.G., Till B.J., Reynolds S.H., Enns L.C., Burtner C., Johnson J.E., Odden A.R. Spectrum of chemically induced mutations from a large-scale reverse-genetic screen in Arabidopsis. Genetics. 2003;164:731–740. PubMed PMC

Till B.J., Reynolds S.H., Weil C., Springer N., Burtner C., Young K., Bowers E., Codomo C.A., Enns L.C., Odden A.R. Discovery of induced point mutations in maize genes by TILLING. BMC Plant Biol. 2004;4:12. doi: 10.1186/1471-2229-4-12. PubMed DOI PMC

Caldwell D.G., McCallum N., Shaw P., Muehlbauer G.J., Marshall D.F., Waugh R. A structured mutant population for forward and reverse genetics in Barley (Hordeum vulgare L.) Plant J. 2004;40:143–150. doi: 10.1111/j.1365-313X.2004.02190.x. PubMed DOI

Slade A.J., Fuerstenberg S.I., Loeffler D., Steine M.N., Facciotti D. A reverse genetic, nontransgenic approach to wheat crop improvement by TILLING. Nat. Biotechnol. 2005;23:75–81. doi: 10.1038/nbt1043. PubMed DOI

Perry J.A., Wang T.L., Welham T.J., Gardner S., Pike J.M., Yoshida S., Parniske M. A TILLING reverse genetics tool and a web-accessible collection of mutants of the legume Lotus japonicus. Plant Physiol. 2003;131:866–871. doi: 10.1104/pp.102.017384. PubMed DOI PMC

Marroni F., Pinosio S., Di Centa E., Jurman I., Boerjan W., Felice N., Cattonaro F., Morgante M. Large-scale detection of rare variants via pooled multiplexed next-generation sequencing: Towards next-generation Ecotilling. Plant J. 2011;67:736–745. doi: 10.1111/j.1365-313X.2011.04627.x. PubMed DOI

Rigola D., van Oeveren J., Janssen A., Bonné A., Schneiders H., van der Poel H.J., van Orsouw N.J., Hogers R.C., de Both M.T., van Eijk M.J. High-throughput detection of induced mutations and natural variation using KeyPoint™ technology. PLoS ONE. 2009;4:e4761. doi: 10.1371/journal.pone.0004761. PubMed DOI PMC

Tsai H., Howell T., Nitcher R., Missirian V., Watson B., Ngo K.J., Lieberman M., Fass J., Uauy C., Tran R.K. Discovery of rare mutations in populations: TILLING by sequencing. Plant Physiol. 2011;156:1257–1268. doi: 10.1104/pp.110.169748. PubMed DOI PMC

Zhu Q., Smith S.M., Ayele M., Yang L., Jogi A., Chaluvadi S.R., Bennetzen J.L. High-throughput discovery of mutations in tef semi-dwarfing genes by next-generation sequencing analysis. Genetics. 2012;192:819–829. doi: 10.1534/genetics.112.144436. PubMed DOI PMC

Bado S. Ph.D. Thesis. University of Natural Resources and Life Sciences; Vienna, Austria: 2015. Advances in Plant Mutation Breeding.

Sauer N.J., Mozoruk J., Miller R.B., Warburg Z.J., Walker K.A., Beetham P.R., Schöpke C.R., Gocal G.F. Oligonucleotide-directed mutagenesis for precision gene editing. Plant Biotechnol. J. 2016;14:496–502. doi: 10.1111/pbi.12496. PubMed DOI PMC

Gocal G.F., Schöpke C., Beetham P.R. Advances in New Technology for Targeted Modification of Plant Genomes. Springer; New York, NY, USA: 2015. Oligo-mediated targeted gene editing; pp. 73–89.

Cole-Strauss A., Yoon K., Xiang Y., Byrne B.C., Rice M.C., Gryn J., Holloman W.K., Kmiec E.B. Correction of the mutation responsible for sickle cell anemia by an RNA-DNA oligonucleotide. Science. 1996;273:1386–1389. doi: 10.1126/science.273.5280.1386. PubMed DOI

Yoon K., Cole-Strauss A., Kmiec E.B. Targeted gene correction of episomal DNA in mammalian cells mediated by a chimeric RNA. DNA oligonucleotide. Proc. Natl. Acad. Sci. USA. 1996;93:2071–2076. doi: 10.1073/pnas.93.5.2071. PubMed DOI PMC

Beetham P.R., Kipp P.B., Sawycky X.L., Arntzen C.J., May G.D. A tool for functional plant genomics: Chimeric RNA/DNA oligonucleotides cause in vivo gene-specific mutations. Proc. Natl. Acad. Sci. USA. 1999;96:8774–8778. doi: 10.1073/pnas.96.15.8774. PubMed DOI PMC

Zhu T., Peterson D.J., Tagliani L., Clair G.S., Baszczynski C.L., Bowen B. Targeted manipulation of maize genes in vivo using chimeric RNA/DNA oligonucleotides. Proc. Natl. Acad. Sci. USA. 1999;96:8768–8773. doi: 10.1073/pnas.96.15.8768. PubMed DOI PMC

Kochevenko A., Willmitzer L. Chimeric RNA/DNA oligonucleotide-based site-specific modification of the tobacco acetolactate syntase gene. Plant Physiol. 2003;132:174–184. doi: 10.1104/pp.102.016857. PubMed DOI PMC

Okuzaki A., Toriyama K. Chimeric RNA/DNA oligonucleotide-directed gene targeting in rice. Plant Cell Rep. 2004;22:509–512. doi: 10.1007/s00299-003-0698-2. PubMed DOI

Dong C., Beetham P., Vincent K., Sharp P. Oligonucleotide-directed gene repair in wheat using a transient plasmid gene repair assay system. Plant Cell Rep. 2006;25:457–465. doi: 10.1007/s00299-005-0098-x. PubMed DOI

Chinnusamy V., Zhu J.-K. RNA-directed DNA methylation and demethylation in plants. Sci. China Ser. C Life Sci. 2009;52:331–343. doi: 10.1007/s11427-009-0052-1. PubMed DOI PMC

Zhang H., Lang Z., Zhu J.-K. Dynamics and function of DNA methylation in plants. Nat. Rev. Mol. Cell Biol. 2018;19:489–506. doi: 10.1038/s41580-018-0016-z. PubMed DOI

Gallego-Bartolomé J., Liu W., Kuo P.H., Feng S., Ghoshal B., Gardiner J., Zhao J.M.-C., Park S.Y., Chory J., Jacobsen S.E. Co-targeting RNA polymerases IV and V promotes efficient de novo DNA methylation in Arabidopsis. Cell. 2019;176:1068–1082.e19. doi: 10.1016/j.cell.2019.01.029. PubMed DOI PMC

Greenberg M.V., Deleris A., Hale C.J., Liu A., Feng S., Jacobsen S.E. Interplay between active chromatin marks and RNA-directed DNA methylation in Arabidopsis thaliana. PLoS Genet. 2013;9:e1003946. doi: 10.1371/journal.pgen.1003946. PubMed DOI PMC

Zhong X., Du J., Hale C.J., Gallego-Bartolome J., Feng S., Vashisht A.A., Chory J., Wohlschlegel J.A., Patel D.J., Jacobsen S.E. Molecular mechanism of action of plant DRM de novo DNA methyltransferases. Cell. 2014;157:1050–1060. doi: 10.1016/j.cell.2014.03.056. PubMed DOI PMC

Xie M., Yu B. siRNA-directed DNA methylation in plants. Curr. Genom. 2015;16:23–31. doi: 10.2174/1389202915666141128002211. PubMed DOI PMC

Cuerda-Gil D., Slotkin R.K. Non-canonical RNA-directed DNA methylation. Nat. Plants. 2016;2:1–8. doi: 10.1038/nplants.2016.163. PubMed DOI

Haag J.R., Ream T.S., Marasco M., Nicora C.D., Norbeck A.D., Pasa-Tolic L., Pikaard C.S. In vitro transcription activities of Pol IV, Pol V, and RDR2 reveal coupling of Pol IV and RDR2 for dsRNA synthesis in plant RNA silencing. Mol. Cell. 2012;48:811–818. doi: 10.1016/j.molcel.2012.09.027. PubMed DOI PMC

Xie Z., Johansen L.K., Gustafson A.M., Kasschau K.D., Lellis A.D., Zilberman D., Jacobsen S.E., Carrington J.C. Genetic and functional diversification of small RNA pathways in plants. PLoS Biol. 2004;2:e104. doi: 10.1371/journal.pbio.0020104. PubMed DOI PMC

Pikaard C. Cell biology of the Arabidopsis nuclear siRNA pathway for RNA-directed chromatin modification. Cold Spring Harb. Symp. Quant. Biol. 2006;71:473–480. doi: 10.1101/sqb.2006.71.046. PubMed DOI

Brocklehurst S., Watson M., Carr I.M., Out S., Heidmann I., Meyer P. Induction of epigenetic variation in Arabidopsis by over-expression of DNA METHYLTRANSFERASE1 (MET1) PLoS ONE. 2018;13:e0192170. doi: 10.1371/journal.pone.0192170. PubMed DOI PMC

Habu Y. Epigenetic silencing of endogenous repetitive sequences by MORPHEUS’MOLECULE1 in Arabidopsis thaliana. Epigenetics. 2010;5:562–565. doi: 10.4161/epi.5.7.12518. PubMed DOI

Ji L., Jordan W.T., Shi X., Hu L., He C., Schmitz R.J. TET-mediated epimutagenesis of the Arabidopsis thaliana methylome. Nat. Commun. 2018;9:1–9. doi: 10.1038/s41467-018-03289-7. PubMed DOI PMC

Saze H., Kakutani T. Heritable epigenetic mutation of a transposon-flanked Arabidopsis gene due to lack of the chromatin-remodeling factor DDM1. EMBO J. 2007;26:3641–3652. doi: 10.1038/sj.emboj.7601788. PubMed DOI PMC

Slotkin R.K., Vaughn M., Borges F., Tanurdžić M., Becker J.D., Feijó J.A., Martienssen R.A. Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell. 2009;136:461–472. doi: 10.1016/j.cell.2008.12.038. PubMed DOI PMC

Otagaki S., Kawai M., Masuta C., Kanazawa A. Size and positional effects of promoter RNA segments on virus-induced RNA-directed DNA methylation and transcriptional gene silencing. Epigenetics. 2011;6:681–691. doi: 10.4161/epi.6.6.16214. PubMed DOI PMC

Li Q., Eichten S.R., Hermanson P.J., Zaunbrecher V.M., Song J., Wendt J., Rosenbaum H., Madzima T.F., Sloan A.E., Huang J. Genetic perturbation of the maize methylome. Plant Cell. 2014;26:4602–4616. doi: 10.1105/tpc.114.133140. PubMed DOI PMC

Kasai A., Bai S., Hojo H., Harada T. Epigenome editing of potato by grafting using transgenic tobacco as siRNA donor. PLoS ONE. 2016;11:e0161729. doi: 10.1371/journal.pone.0161729. PubMed DOI PMC

Hu L., Li N., Xu C., Zhong S., Lin X., Yang J., Zhou T., Yuliang A., Wu Y., Chen Y.-R. Mutation of a major CG methylase in rice causes genome-wide hypomethylation, dysregulated genome expression, and seedling lethality. Proc. Natl. Acad. Sci. USA. 2014;111:10642–10647. doi: 10.1073/pnas.1410761111. PubMed DOI PMC

Manning K., Tör M., Poole M., Hong Y., Thompson A.J., King G.J., Giovannoni J.J., Seymour G.B. A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat. Genet. 2006;38:948–952. doi: 10.1038/ng1841. PubMed DOI

Zhong S., Fei Z., Chen Y.-R., Zheng Y., Huang M., Vrebalov J., McQuinn R., Gapper N., Liu B., Xiang J. Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening. Nat. Biotechnol. 2013;31:154–159. doi: 10.1038/nbt.2462. PubMed DOI

Zhou L., Tian S., Qin G. RNA methylomes reveal the m 6 A-mediated regulation of DNA demethylase gene SlDML2 in tomato fruit ripening. Genome Biol. 2019;20:1–23. doi: 10.1186/s13059-019-1771-7. PubMed DOI PMC

Trewick S.C., Henshaw T.F., Hausinger R.P., Lindahl T., Sedgwick B. Oxidative demethylation by Escherichia coli AlkB directly reverts DNA base damage. Nature. 2002;419:174–178. doi: 10.1038/nature00908. PubMed DOI

Rossi M., Iusem N.D. Tomato (Lycopersicon esculentum) genomic clone homologous to a gene encoding an abscisic acid-induced protein. Plant Physiol. 1994;104:1073. doi: 10.1104/pp.104.3.1073. PubMed DOI PMC

Frankel N., Hasson E., Iusem N.D., Rossi M.S. Adaptive evolution of the water stress-induced gene Asr2 in Lycopersicon species dwelling in arid habitats. Mol. Biol. Evol. 2003;20:1955–1962. doi: 10.1093/molbev/msg214. PubMed DOI

González R.M., Ricardi M.M., Iusem N.D. Epigenetic marks in an adaptive water stress-responsive gene in tomato roots under normal and drought conditions. Epigenetics. 2013;8:864–872. doi: 10.4161/epi.25524. PubMed DOI PMC

Voinnet O. RNA silencing as a plant immune system against viruses. Trends Genet. 2001;17:449–459. doi: 10.1016/S0168-9525(01)02367-8. PubMed DOI

Fire A., Xu S., Montgomery M.K., Kostas S.A., Driver S.E., Mello C.C. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature. 1998;391:806–811. doi: 10.1038/35888. PubMed DOI

Kørner C.J., Pitzalis N., Peña E.J., Erhardt M., Vazquez F., Heinlein M. Crosstalk between PTGS and TGS pathways in natural antiviral immunity and disease recovery. Nat. Plants. 2018;4:157–164. doi: 10.1038/s41477-018-0117-x. PubMed DOI

Sijen T., Vijn I., Rebocho A., van Blokland R., Roelofs D., Mol J.N., Kooter J.M. Transcriptional and posttranscriptional gene silencing are mechanistically related. Curr. Biol. 2001;11:436–440. doi: 10.1016/S0960-9822(01)00116-6. PubMed DOI

Baulcombe D.C., English J.J. Ectopic pairing of homologous DNA and post-transcriptional gene silencing in transgenic plants. Curr. Opin. Biotechnol. 1996;7:173–180. doi: 10.1016/S0958-1669(96)80009-7. DOI

Chuang C.-F., Meyerowitz E.M. Specific and heritable genetic interference by double-stranded RNA in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA. 2000;97:4985–4990. doi: 10.1073/pnas.060034297. PubMed DOI PMC

Waterhouse P.M., Graham M.W., Wang M.-B. Virus resistance and gene silencing in plants can be induced by simultaneous expression of sense and antisense RNA. Proc. Natl. Acad. Sci. USA. 1998;95:13959–13964. doi: 10.1073/pnas.95.23.13959. PubMed DOI PMC

Baulcombe D. 100 Years of Virology. Springer; Vienna, Austria: 1999. Viruses and gene silencing in plants; pp. 189–201. PubMed

Burch-Smith T.M., Schiff M., Liu Y., Dinesh-Kumar S.P. Efficient virus-induced gene silencing in Arabidopsis. Plant Physiol. 2006;142:21–27. doi: 10.1104/pp.106.084624. PubMed DOI PMC

Lange M., Yellina A.L., Orashakova S., Becker A. Advanced Structural Safety Studies. Volume 975. Springer Science and Business Media LLC.; Berlin/Heidelberg, Germany: 2013. Virus-Induced Gene Silencing (VIGS) in Plants: An Overview of Target Species and the Virus-Derived Vector Systems; pp. 1–14. PubMed

Lu R., Martin-Hernandez A.M., Peart J.R., Malcuit I., Baulcombe D.C. Virus-induced gene silencing in plants. Methods. 2003;30:296–303. doi: 10.1016/S1046-2023(03)00037-9. PubMed DOI

Van Kammen A. Virus-induced gene silencing in infected and transgenic plants. Trends Plant Sci. 1997;2:409–411. doi: 10.1016/S1360-1385(97)01128-X. DOI

Bernstein E., Caudy A.A., Hammond S.M., Hannon G.J. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature. 2001;409:363–366. doi: 10.1038/35053110. PubMed DOI

Hutvágner G., Zamore P.D. A microRNA in a multiple-turnover RNAi enzyme complex. Science. 2002;297:2056–2060. doi: 10.1126/science.1073827. PubMed DOI

Kawamata T., Tomari Y. Making risc. Trends Biochem. Sci. 2010;35:368–376. doi: 10.1016/j.tibs.2010.03.009. PubMed DOI

Pratt A.J., MacRae I.J. The RNA-induced silencing complex: A versatile gene-silencing machine. J. Biol. Chem. 2009;284:17897–17901. doi: 10.1074/jbc.R900012200. PubMed DOI PMC

Kumagai M.H., Donson J., Della-Cioppa G., Harvey D., Hanley K., Grill L. Cytoplasmic inhibition of carotenoid biosynthesis with virus-derived RNA. Proc. Natl. Acad. Sci. USA. 1995;92:1679–1683. doi: 10.1073/pnas.92.5.1679. PubMed DOI PMC

Liu Y., Schiff M., Marathe R., Dinesh-Kumar S. Tobacco Rar1, EDS1 and NPR1/NIM1 like genes are required for N-mediated resistance to tobacco mosaic virus. Plant J. 2002;30:415–429. doi: 10.1046/j.1365-313X.2002.01297.x. PubMed DOI

Ratcliff F., Martin-Hernandez A.M., Baulcombe D.C. Technical advance: Tobacco rattle virus as a vector for analysis of gene function by silencing. Plant J. 2001;25:237–245. doi: 10.1046/j.0960-7412.2000.00942.x. PubMed DOI

Burch-Smith T.M., Anderson J.C., Martin G.B., Dinesh-Kumar S.P. Applications and advantages of virus-induced gene silencing for gene function studies in plants. Plant J. 2004;39:734–746. doi: 10.1111/j.1365-313X.2004.02158.x. PubMed DOI

Ekengren S.K., Liu Y., Schiff M., Dinesh-Kumar S., Martin G.B. Two MAPK cascades, NPR1, and TGA transcription factors play a role in Pto-mediated disease resistance in tomato. Plant J. 2003;36:905–917. doi: 10.1046/j.1365-313X.2003.01944.x. PubMed DOI

Ramegowda V., Mysore K.S., Senthil-Kumar M. Virus-induced gene silencing is a versatile tool for unraveling the functional relevance of multiple abiotic-stress-responsive genes in crop plants. Front. Plant Sci. 2014;5:323. doi: 10.3389/fpls.2014.00323. PubMed DOI PMC

McClintock B. The origin and behavior of mutable loci in maize. Proc. Natl. Acad. Sci. USA. 1950;36:344–355. doi: 10.1073/pnas.36.6.344. PubMed DOI PMC

Iida S., Terada R. Modification of endogenous natural genes by gene targeting in rice and other higher plants. Plant Mol. Biol. 2005;59:205–219. doi: 10.1007/s11103-005-2162-x. PubMed DOI

Pereira J.F., Ryan P.R. The role of transposable elements in the evolution of aluminium resistance in plants. J. Exp. Bot. 2019;70:41–54. doi: 10.1093/jxb/ery357. PubMed DOI

Flavell A.J., Pearce S.R., Kumar A. Plant transposable elements and the genome. Curr. Opin. Genet. Dev. 1994;4:838–844. doi: 10.1016/0959-437X(94)90068-X. PubMed DOI

Seidl M.F., Thomma B.P. Transposable elements direct the coevolution between plants and microbes. Trends Genet. 2017;33:842–851. doi: 10.1016/j.tig.2017.07.003. PubMed DOI

Gray Y.H. It takes two transposons to tango: Transposable-element-mediated chromosomal rearrangements. Trends Genet. 2000;16:461–468. doi: 10.1016/S0168-9525(00)02104-1. PubMed DOI

Thieme M., Bucher E. Transposable Elements as Tool for Crop Improvement. Adv. Bota. Res. 2018;88:165–202. doi: 10.1016/bs.abr.2018.09.001. DOI

McClintock B. Carnegie Inst. Wash. Year Book. 1948;47:155–169. PubMed

McClintock B. Nobel lecture. The significance of response of the genome to challenge. Science. 1984;226:792–801. doi: 10.1126/science.15739260. PubMed DOI

Ito H., Yoshida T., Tsukahara S., Kawabe A. Evolution of the ONSEN retrotransposon family activated upon heat stress in Brassicaceae. Gene. 2013;518:256–261. doi: 10.1016/j.gene.2013.01.034. PubMed DOI

Wicker T., Sabot F., Hua-Van A., Bennetzen J.L., Capy P., Chalhoub B., Flavell A., Leroy P., Morgante M., Panaud O. A unified classification system for eukaryotic transposable elements. Nat. Rev. Genet. 2007;8:973–982. doi: 10.1038/nrg2165. PubMed DOI

Grzebelus D. The Functional Impact of Transposable Elements on the Diversity of Plant Genomes. Diversity. 2018;10:18. doi: 10.3390/d10020018. DOI

Sangwan R.S., Ochatt S., Nava-Saucedo J.-E., Sangwan-Norreel B. T-DNA insertion mutagenesis. In: Shu Q.Y., Forster B.P., Nakagawa H., editors. Plant Mutat. Breed. Biotechnol. CABI Publishing; Wallingford, UK: 2012. pp. 489–506.

Belzile F., Yoder J.I. Pattern of somatic transposition in a high copy Ac tomato line. Plant J. 1992;2:173–179. PubMed

Briza J., Carroll B.J., Klimyuk V.I., Thomas C.M., Jones D.A., Jones J. Distribution of unlinked transpositions of a Ds element from a T-DNA locus on tomato chromosome 4. Genetics. 1995;141:383–390. PubMed PMC

Goldsbrough A.P., Lastrella C.N., Yoder J.I. Transposition mediated re–positioning and subsequent elimination of marker genes from transgenic tomato. Bio/technology. 1993;11:1286–1292. doi: 10.1038/nbt1193-1286. DOI

Osborne B.I., Corr C.A., Prince J.P., Hehl R., Tanksley S.D., McCormick S., Baker B. Ac transposition from a T-DNA can generate linked and unlinked clusters of insertions in the tomato genome. Genetics. 1991;129:833–844. PubMed PMC

Peterson P.W., Yoder J.I. Amplification of Ac in tomato is correlated with high Ac transposition activity. Genome. 1995;38:265–276. doi: 10.1139/g95-033. PubMed DOI

Cooley M.B., Yoder J., Goldsbrough A., Still D. Site-selected insertional mutagenesis of tomato with maizeAc andDs elements. Mol. Gen. Genet. MGG. 1996;252:184–194. doi: 10.1007/BF02173219. PubMed DOI

Atarés A., Moyano E., Morales B., Schleicher P., García-Abellán J.O., Antón T., García-Sogo B., Perez-Martin F., Lozano R., Flores F.B. An insertional mutagenesis programme with an enhancer trap for the identification and tagging of genes involved in abiotic stress tolerance in the tomato wild-related species Solanum pennellii. Plant Cell Rep. 2011;30:1865. doi: 10.1007/s00299-011-1094-y. PubMed DOI PMC

Van der Biezen E.A., Brandwagt B.F., van Leeuwen W., Nijkamp H.J.J., Hille J. Identification and isolation of theFEEBLY gene from tomato by transposon tagging. Mol. Gen. Genet. MGG. 1996;251:267–280. doi: 10.1007/BF02172517. PubMed DOI

Bibikova M., Golic M., Golic K.G., Carroll D. Targeted chromosomal cleavage and mutagenesis in Drosophila using zinc-finger nucleases. Genetics. 2002;161:1169–1175. PubMed PMC

Osakabe K., Osakabe Y., Toki S. Site-directed mutagenesis in Arabidopsis using custom-designed zinc finger nucleases. Proc. Natl. Acad. Sci. USA. 2010;107:12034–12039. doi: 10.1073/pnas.1000234107. PubMed DOI PMC

Shukla V.K., Doyon Y., Miller J.C., DeKelver R.C., Moehle E.A., Worden S.E., Mitchell J.C., Arnold N.L., Gopalan S., Meng X. Precise genome modification in the crop species Zea mays using zinc-finger nucleases. Nature. 2009;459:437–441. doi: 10.1038/nature07992. PubMed DOI

Persikov A.V., Wetzel J.L., Rowland E.F., Oakes B.L., Xu D.J., Singh M., Noyes M.B. A systematic survey of the Cys2His2 zinc finger DNA-binding landscape. Nucleic Acids Res. 2015;43:1965–1984. doi: 10.1093/nar/gku1395. PubMed DOI PMC

Bitinaite J., Wah D.A., Aggarwal A.K., Schildkraut I. FokI dimerization is required for DNA cleavage. Proc. Natl. Acad. Sci. USA. 1998;95:10570–10575. doi: 10.1073/pnas.95.18.10570. PubMed DOI PMC

Hiroyuki S., Susumu K. New restriction endonucleases from Flavobacterium okeanokoites (FokI) and Micrococcus luteus (MluI) Gene. 1981;16:73–78. doi: 10.1016/0378-1119(81)90062-7. PubMed DOI

Carroll D. Genome engineering with zinc-finger nucleases. Genetics. 2011;188:773–782. doi: 10.1534/genetics.111.131433. PubMed DOI PMC

Petolino J.F. Genome editing in plants via designed zinc finger nucleases. Vitr. Cell. Dev. Biol. Plant. 2015;51:1–8. doi: 10.1007/s11627-015-9663-3. PubMed DOI PMC

Mohanta T.K., Bashir T., Hashem A., Abd_Allah E.F., Bae H. Genome editing tools in plants. Genes. 2017;8:399. doi: 10.3390/genes8120399. PubMed DOI PMC

Kim Y.-G., Cha J., Chandrasegaran S. Hybrid restriction enzymes: Zinc finger fusions to Fok I cleavage domain. Proc. Natl. Acad. Sci. USA. 1996;93:1156–1160. doi: 10.1073/pnas.93.3.1156. PubMed DOI PMC

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. Nature. 2009;459:442–445. doi: 10.1038/nature07845. PubMed DOI PMC

Zhang F., Maeder M.L., Unger-Wallace E., Hoshaw J.P., Reyon D., Christian M., Li X., Pierick C.J., Dobbs D., Peterson T. High frequency targeted mutagenesis in Arabidopsis thaliana using zinc finger nucleases. Proc. Natl. Acad. Sci. USA. 2010;107:12028–12033. doi: 10.1073/pnas.0914991107. PubMed DOI PMC

Curtin S.J., Zhang F., Sander J.D., Haun W.J., Starker C., Baltes N.J., Reyon D., Dahlborg E.J., Goodwin M.J., Coffman A.P. Targeted mutagenesis of duplicated genes in soybean with zinc-finger nucleases. Plant Physiol. 2011;156:466–473. doi: 10.1104/pp.111.172981. PubMed DOI PMC

Mushtaq M., Bhat J.A., Mir Z.A., Sakina A., Ali S., Singh A.K., Tyagi A., Salgotra R.K., Dar A.A., Bhat R. CRISPR/Cas approach: A new way of looking at plant-abiotic interactions. J. Plant Physiol. 2018;224:156–162. doi: 10.1016/j.jplph.2018.04.001. PubMed DOI

Gaj T., Sirk S.J., Shui S.-l., Liu J. Genome-editing technologies: Principles and applications. Cold Spring Harb. Perspect. Biol. 2016;8:a023754. doi: 10.1101/cshperspect.a023754. PubMed DOI PMC

Gupta R.M., Musunuru K. Expanding the genetic editing tool kit: ZFNs, TALENs, and CRISPR-Cas9. J. Clin. Investig. 2014;124:4154–4161. doi: 10.1172/JCI72992. PubMed DOI PMC

Ramirez C.L., Foley J.E., Wright D.A., Müller-Lerch F., Rahman S.H., Cornu T.I., Winfrey R.J., Sander J.D., Fu F., Townsend J.A. Unexpected failure rates for modular assembly of engineered zinc fingers. Nat. Methods. 2008;5:374–375. doi: 10.1038/nmeth0508-374. PubMed DOI PMC

Sun N., Zhao H. Transcription activator-like effector nucleases (TALENs): A highly efficient and versatile tool for genome editing. Biotechnol. Bioeng. 2013;110:1811–1821. doi: 10.1002/bit.24890. PubMed DOI

Boch J., Scholze H., Schornack S., Landgraf A., Hahn S., Kay S., Lahaye T., Nickstadt A., Bonas U. Breaking the code of DNA binding specificity of TAL-type III effectors. Science. 2009;326:1509–1512. doi: 10.1126/science.1178811. PubMed DOI

Moscou M.J., Bogdanove A.J. A simple cipher governs DNA recognition by TAL effectors. Science. 2009;326:1501. doi: 10.1126/science.1178817. PubMed DOI

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. Genetics. 2010;186:757–761. doi: 10.1534/genetics.110.120717. PubMed DOI PMC

Ding Q., Regan S.N., Xia Y., Oostrom L.A., Cowan C.A., Musunuru K. Enhanced efficiency of human pluripotent stem cell genome editing through replacing TALENs with CRISPRs. Cell Stem Cell. 2013;12:393. doi: 10.1016/j.stem.2013.03.006. PubMed DOI PMC

Mussolino C., Morbitzer R., Lütge F., Dannemann N., Lahaye T., Cathomen T. A novel TALE nuclease scaffold enables high genome editing activity in combination with low toxicity. Nucleic Acids Res. 2011;39:9283–9293. doi: 10.1093/nar/gkr597. PubMed DOI PMC

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. Nat. Biotechnol. 2012;30:460. doi: 10.1038/nbt.2170. PubMed DOI PMC

Cermak T., Doyle E.L., Christian M., Wang L., Zhang Y., Schmidt C., Baller J.A., Somia N.V., Bogdanove A.J., Voytas D.F. Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res. 2011;39:e82. doi: 10.1093/nar/gkr218. PubMed DOI PMC

Christian M., Qi Y., Zhang Y., Voytas D.F. Targeted mutagenesis of Arabidopsis thaliana using engineered TAL effector nucleases. G3 Genes Genomes Genet. 2013;3:1697–1705. PubMed PMC

Mahfouz M.M., Li L., Shamimuzzaman M., Wibowo A., Fang X., Zhu J.-K. De novo-engineered transcription activator-like effector (TALE) hybrid nuclease with novel DNA binding specificity creates double-strand breaks. Proc. Natl. Acad. Sci. USA. 2011;108:2623–2628. doi: 10.1073/pnas.1019533108. PubMed DOI PMC

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. Plant Physiol. 2013;161:20–27. doi: 10.1104/pp.112.205179. PubMed DOI PMC

Li T., Liu B., Spalding M.H., Weeks D.P., Yang B. High-efficiency TALEN-based gene editing produces disease-resistant rice. Nat. Biotechnol. 2012;30:390. doi: 10.1038/nbt.2199. PubMed DOI

Shah S.A., Erdmann S., Mojica F.J., Garrett R.A. Protospacer recognition motifs: Mixed identities and functional diversity. RNA Biol. 2013;10:891–899. doi: 10.4161/rna.23764. PubMed DOI PMC

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. Plant Mol. Biol. 2013;83:279–285. doi: 10.1007/s11103-013-0078-4. PubMed DOI PMC

Shan Q., Wang Y., Chen K., Liang Z., Li J., Zhang Y., Zhang K., Liu J., Voytas D.F., Zheng X. Rapid and efficient gene modification in rice and Brachypodium using TALENs. Mol. Plant. 2013;6:1365–1368. doi: 10.1093/mp/sss162. PubMed DOI PMC

Jinek M., Chylinski K., Fonfara I., Hauer M., Doudna J.A., Charpentier E. A programmable dual-RNA–guided DNA endonuclease in adaptive bacterial immunity. Science. 2012;337:816–821. doi: 10.1126/science.1225829. PubMed DOI PMC

Wang J., Li J., Zhao H., Sheng G., Wang M., Yin M., Wang Y. Structural and mechanistic basis of PAM-dependent spacer acquisition in CRISPR-Cas systems. Cell. 2015;163:840–853. doi: 10.1016/j.cell.2015.10.008. PubMed DOI

Pennisi E. The CRISPR craze. Science. 2013;341:833–836. doi: 10.1126/science.341.6148.833. PubMed DOI

Segal D.J., Meckler J.F. Genome engineering at the dawn of the golden age. Annu. Rev. Genom. Hum. Genet. 2013;14:135–158. doi: 10.1146/annurev-genom-091212-153435. PubMed DOI

Barrangou R., Fremaux C., Deveau H., Richards M., Boyaval P., Moineau S., Romero D.A., Horvath P. CRISPR provides acquired resistance against viruses in prokaryotes. Science. 2007;315:1709–1712. doi: 10.1126/science.1138140. PubMed DOI

Horvath P., Barrangou R. CRISPR/Cas, the immune system of bacteria and archaea. Science. 2010;327:167–170. doi: 10.1126/science.1179555. PubMed DOI

Jinek M., Jiang F., Taylor D.W., Sternberg S.H., Kaya E., Ma E., Anders C., Hauer M., Zhou K., Lin S. Structures of Cas9 endonucleases reveal RNA-mediated conformational activation. Science. 2014;343:1247997. doi: 10.1126/science.1247997. PubMed DOI PMC

Belhaj K., Chaparro-Garcia A., Kamoun S., Patron N.J., Nekrasov V. Editing plant genomes with CRISPR/Cas9. Curr. Opin. Biotechnol. 2015;32:76–84. doi: 10.1016/j.copbio.2014.11.007. PubMed DOI

Dagdas Y.S., Chen J.S., Sternberg S.H., Doudna J.A., Yildiz A. A conformational checkpoint between DNA binding and cleavage by CRISPR-Cas9. Sci. Adv. 2017;3:eaao0027. doi: 10.1126/sciadv.aao0027. PubMed DOI PMC

Jiang F., Doudna J.A. CRISPR–Cas9 structures and mechanisms. Annu. Rev. Biophys. 2017;46:505–529. doi: 10.1146/annurev-biophys-062215-010822. PubMed DOI

Koonin E.V., Makarova K.S., Zhang F. Diversity, classification and evolution of CRISPR-Cas systems. Curr. Opin. Microbiol. 2017;37:67–78. doi: 10.1016/j.mib.2017.05.008. PubMed DOI PMC

Chen K., Wang Y., Zhang R., Zhang H., Gao C. CRISPR/Cas genome editing and precision plant breeding in agriculture. Annu. Rev. Plant Biol. 2019;70:667–697. doi: 10.1146/annurev-arplant-050718-100049. PubMed DOI

Knott G.J., Doudna J.A. CRISPR-Cas guides the future of genetic engineering. Science. 2018;361:866–869. doi: 10.1126/science.aat5011. PubMed DOI PMC

Freudhofmaier M. Master’s Thesis. University of Natural Resources and Life Sciences (BOKU); Vienna, Austria: 2018. Gene Editing of Commercially Important Genes of Jatropha curcas L. CRISPR/Cas9 Mediated Gene Knock-Out.

Peterson B.A., Haak D.C., Nishimura M.T., Teixeira P.J., James S.R., Dangl J.L., Nimchuk Z.L. Genome-wide assessment of efficiency and specificity in CRISPR/Cas9 mediated multiple site targeting in Arabidopsis. PLoS ONE. 2016;11:e0162169. doi: 10.1371/journal.pone.0162169. PubMed DOI PMC

Mali P., Esvelt K.M., Church G.M. Cas9 as a versatile tool for engineering biology. Nat. Methods. 2013;10:957–963. doi: 10.1038/nmeth.2649. PubMed DOI PMC

Mojica F.J., Díez-Villaseñor C., García-Martínez J., Almendros C. Short motif sequences determine the targets of the prokaryotic CRISPR defence system. Microbiology. 2009;155:733–740. doi: 10.1099/mic.0.023960-0. PubMed DOI

Karvelis T., Gasiunas G., Young J., Bigelyte G., Silanskas A., Cigan M., Siksnys V. Rapid characterization of CRISPR-Cas9 protospacer adjacent motif sequence elements. Genome Biol. 2015;16:1–13. doi: 10.1186/s13059-015-0818-7. PubMed DOI PMC

Lee C.M., Cradick T.J., Bao G. The Neisseria meningitidis CRISPR-Cas9 system enables specific genome editing in mammalian cells. Mol. Ther. 2016;24:645–654. doi: 10.1038/mt.2016.8. PubMed DOI PMC

Müller M., Lee C.M., Gasiunas G., Davis T.H., Cradick T.J., Siksnys V., Bao G., Cathomen T., Mussolino C. Streptococcus thermophilus CRISPR-Cas9 systems enable specific editing of the human genome. Mol. Ther. 2016;24:636–644. doi: 10.1038/mt.2015.218. PubMed DOI PMC

Ran F.A., Cong L., Yan W.X., Scott D.A., Gootenberg J.S., Kriz A.J., Zetsche B., Shalem O., Wu X., Makarova K.S. In vivo genome editing using Staphylococcus aureus Cas9. Nature. 2015;520:186–191. doi: 10.1038/nature14299. PubMed DOI PMC

Abudayyeh O.O., Gootenberg J.S., Konermann S., Joung J., Slaymaker I.M., Cox D.B., Shmakov S., Makarova K.S., Semenova E., Minakhin L. C2c2 is a single-component programmable RNA-guided RNA-targeting CRISPR effector. Science. 2016;353:aaf5573. doi: 10.1126/science.aaf5573. PubMed DOI PMC

East-Seletsky A., O’Connell M.R., Knight S.C., Burstein D., Cate J.H., Tjian R., Doudna J.A. Two distinct RNase activities of CRISPR-C2c2 enable guide-RNA processing and RNA detection. Nature. 2016;538:270–273. doi: 10.1038/nature19802. PubMed DOI PMC

Jaganathan D., Ramasamy K., Sellamuthu G., Jayabalan S., Venkataraman G. CRISPR for crop improvement: An update review. Front. Plant Sci. 2018;9:985. doi: 10.3389/fpls.2018.00985. PubMed DOI PMC

Damalas C.A., Eleftherohorinos I.G. Pesticide exposure, safety issues, and risk assessment indicators. Int. J. Environ. Res. Public Health. 2011;8:1402–1419. doi: 10.3390/ijerph8051402. PubMed DOI PMC

Tilman D., Cassman K.G., Matson P.A., Naylor R., Polasky S. Agricultural sustainability and intensive production practices. Nature. 2002;418:671–677. doi: 10.1038/nature01014. PubMed DOI

Dunwell J.M. Transgenic approaches to crop improvement. J. Exp. Bot. 2000;51:487–496. doi: 10.1093/jexbot/51.suppl_1.487. PubMed DOI

Yin K., Qiu J.-L. Genome editing for plant disease resistance: Applications and perspectives. Philos. Trans. R. Soc. B. 2019;374:20180322. doi: 10.1098/rstb.2018.0322. PubMed DOI PMC

Buxdorf K., Rubinsky G., Barda O., Burdman S., Aharoni A., Levy M. The transcription factor SlSHINE3 modulates defense responses in tomato plants. Plant Mol. Biol. 2014;84:37–47. doi: 10.1007/s11103-013-0117-1. PubMed DOI

Yang L., Huang W., Xiong F., Xian Z., Su D., Ren M., Li Z. Silencing of Sl PL, which encodes a pectate lyase in tomato, confers enhanced fruit firmness, prolonged shelf-life and reduced susceptibility to grey mould. Plant Biotechnol. J. 2017;15:1544–1555. doi: 10.1111/pbi.12737. PubMed DOI PMC

Ye J., Liu G., Chen W., Zhang F., Li H., Ye Z., Zhang Y. Knockdown of SlNL33 accumulates ascorbate, enhances disease and oxidative stress tolerance in tomato (Solanum lycopersicum) Plant Growth Regul. 2019;89:49–58. doi: 10.1007/s10725-019-00512-3. DOI

Di Pietro A., García-Maceira F.I., Méglecz E., Roncero M.I.G. A MAP kinase of the vascular wilt fungus Fusarium oxysporum is essential for root penetration and pathogenesis. Mol. Microbiol. 2001;39:1140–1152. doi: 10.1111/j.1365-2958.2001.02307.x. PubMed DOI

Pareek M., Rajam M.V. RNAi-mediated silencing of MAP kinase signalling genes (Fmk1, Hog1, and Pbs2) in Fusarium oxysporum reduces pathogenesis on tomato plants. Fungal Biol. 2017;121:775–784. doi: 10.1016/j.funbio.2017.05.005. PubMed DOI

Zhang S., Wang L., Zhao R., Yu W., Li R., Li Y., Sheng J., Shen L. Knockout of SlMAPK3 reduced disease resistance to Botrytis cinerea in tomato plants. J. Agric. Food Chem. 2018;66:8949–8956. doi: 10.1021/acs.jafc.8b02191. PubMed DOI

Prihatna C., Barbetti M.J., Barker S.J. A novel tomato fusarium wilt tolerance gene. Front. Microbiol. 2018;9:1226. doi: 10.3389/fmicb.2018.01226. PubMed DOI PMC

Nekrasov V., Wang C., Win J., Lanz C., Weigel D., Kamoun S. Rapid generation of a transgene-free powdery mildew resistant tomato by genome deletion. Sci. Rep. 2017;7:1–6. doi: 10.1038/s41598-017-00578-x. PubMed DOI PMC

Koseoglou E. Master’s Thesis. Wageningen University and Research; Wageningen, The Netherlands: 2017. The Study of SlPMR4 CRISPR/Cas9-Mediated Tomato Allelic Series for Resistance Against Powdery Mildew.

Huibers R.P., Loonen A.E., Gao D., Van den Ackerveken G., Visser R.G., Bai Y. Powdery mildew resistance in tomato by impairment of SlPMR4 and SlDMR1. PLoS ONE. 2013;8:e67467. doi: 10.1371/journal.pone.0067467. PubMed DOI PMC

Tashkandi M., Ali Z., Aljedaani F., Shami A., Mahfouz M.M. Engineering resistance against Tomato yellow leaf curl virus via the CRISPR/Cas9 system in tomato. Plant Signal. Behav. 2018;13:e1525996. doi: 10.1080/15592324.2018.1525996. PubMed DOI PMC

Fuentes A., Ramos P.L., Fiallo E., Callard D., Sánchez Y., Peral R., Rodríguez R., Pujol M. Intron–hairpin RNA derived from replication associated protein C1 gene confers immunity to Tomato yellow leaf curl virus infection in transgenic tomato plants. Transgenic Res. 2006;15:291–304. doi: 10.1007/s11248-005-5238-0. PubMed DOI

Ramesh S., Mishra A., Praveen S. Hairpin RNA-mediated strategies for silencing of tomato leaf curl virus AC1 and AC4 genes for effective resistance in plants. Oligonucleotides. 2007;17:251–257. doi: 10.1089/oli.2006.0063. PubMed DOI

Praveen S., Mishra A.K., Dasgupta A. Antisense suppression of replicase gene expression recovers tomato plants from leaf curl virus infection. Plant Sci. 2005;168:1011–1014. doi: 10.1016/j.plantsci.2004.12.008. DOI

Ortigosa A., Gimenez-Ibanez S., Leonhardt N., Solano R. Design of a bacterial speck resistant tomato by CRISPR/Cas9-mediated editing of Sl JAZ 2. Plant Biotechnol. J. 2019;17:665–673. doi: 10.1111/pbi.13006. PubMed DOI PMC

Almirón M., Link A.J., Furlong D., Kolter R. A novel DNA-binding protein with regulatory and protective roles in starved Escherichia coli. Genes Dev. 1992;6:2646–2654. doi: 10.1101/gad.6.12b.2646. PubMed DOI

Ceci P., Ilari A., Falvo E., Chiancone E. The Dps Protein of Agrobacterium tumefaciens Does Not Bind to DNA but Protects It toward Oxidative Cleavage X-RAY crystal structure, iron binding, and hydroxyl-radical scavenging properties. J. Biol. Chem. 2003;278:20319–20326. doi: 10.1074/jbc.M302114200. PubMed DOI

Choi S.H., Baumler D.J., Kaspar C.W. Contribution of dps to acid stress tolerance and oxidative stress tolerance in Escherichia coli O157: H7. Appl. Environ. Microbiol. 2000;66:3911–3916. doi: 10.1128/AEM.66.9.3911-3916.2000. PubMed DOI PMC

Halsey T.A., Vazquez-Torres A., Gravdahl D.J., Fang F.C., Libby S.J. The ferritin-like Dps protein is required for Salmonella enterica serovar Typhimurium oxidative stress resistance and virulence. Infect. Immun. 2004;72:1155–1158. doi: 10.1128/IAI.72.2.1155-1158.2004. PubMed DOI PMC

Martinez A., Kolter R. Protection of DNA during oxidative stress by the nonspecific DNA-binding protein Dps. J. Bacteriol. 1997;179:5188–5194. doi: 10.1128/JB.179.16.5188-5194.1997. PubMed DOI PMC

Nair S., Finkel S.E. Dps protects cells against multiple stresses during stationary phase. J. Bacteriol. 2004;186:4192–4198. doi: 10.1128/JB.186.13.4192-4198.2004. PubMed DOI PMC

Saumaa S., Tover A., Tark M., Tegova R., Kivisaar M. Oxidative DNA damage defense systems in avoidance of stationary-phase mutagenesis in Pseudomonas putida. J. Bacteriol. 2007;189:5504–5514. doi: 10.1128/JB.00518-07. PubMed DOI PMC

Colburn-Clifford J.M., Scherf J.M., Allen C. Ralstonia solanacearum Dps contributes to oxidative stress tolerance and to colonization of and virulence on tomato plants. Appl. Environ. Microbiol. 2010;76:7392–7399. doi: 10.1128/AEM.01742-10. PubMed DOI PMC

Hu T., Ye J., Tao P., Li H., Zhang J., Zhang Y., Ye Z. The tomato HD-Zip I transcription factor Sl HZ 24 modulates ascorbate accumulation through positive regulation of the d-mannose/l-galactose pathway. Plant J. 2016;85:16–29. doi: 10.1111/tpj.13085. PubMed DOI

De Toledo Thomazella D.P., Brail Q., Dahlbeck D., Staskawicz B. CRISPR-Cas9 mediated mutagenesis of a DMR6 ortholog in tomato confers broad-spectrum disease resistance. BioRxiv. 2016:064824. doi: 10.1101/064824. PubMed DOI PMC

Shu P., Li Z., Min D., Zhang X., Ai W., Li J., Zhou J., Li Z., Li F., Li X. CRISPR/Cas9-Mediated SlMYC2 Mutagenesis Adverse to Tomato Plant Growth and MeJA-Induced Fruit Resistance to Botrytis cinerea. J. Agric. Food Chem. 2020;68:5529–5538. doi: 10.1021/acs.jafc.9b08069. PubMed DOI

Liu L., Zhang J., Xu J., Li Y., Guo L., Wang Z., Zhang X., Zhao B., Guo Y.-D., Zhang N. CRISPR/Cas9 targeted mutagenesis of SlLBD40, a Lateral Organ Boundaries Domain transcription factor, enhances drought tolerance in tomato. Plant Sci. 2020;301:110683. doi: 10.1016/j.plantsci.2020.110683. PubMed DOI

Martínez M.I.S., Bracuto V., Koseoglou E., Appiano M., Jacobsen E., Visser R.G., Wolters A.-M.A., Bai Y. CRISPR/Cas9-targeted mutagenesis of the tomato susceptibility gene PMR4 for resistance against powdery mildew. BMC Plant Biol. 2020;20:284. PubMed PMC

Song L.X., Xu X.C., Wang F.N., Wang Y., Xia X.J., Shi K., Zhou Y.H., Zhou J., Yu J.Q. Brassinosteroids act as a positive regulator for resistance against root-knot nematode involving RESPIRATORY BURST OXIDASE HOMOLOG-dependent activation of MAPKs in tomato. Plant Cell Environ. 2018;41:1113–1125. doi: 10.1111/pce.12952. PubMed DOI

Reddy K., Rajam M. Targeting chitinase gene of Helicoverpa armigera by host-induced RNA interference confers insect resistance in tobacco and tomato. Plant Mol. Biol. 2016;90:281–292. PubMed

Wang T., Deng Z., Zhang X., Wang H., Wang Y., Liu X., Liu S., Xu F., Li T., Fu D. Tomato DCL2b is required for the biosynthesis of 22-nt small RNAs, the resulting secondary siRNAs, and the host defense against ToMV. Hortic. Res. 2018;5:1–14. doi: 10.1038/s41438-018-0073-7. PubMed DOI PMC

Wang Z., Hardcastle T.J., Pastor A.C., Yip W.H., Tang S., Baulcombe D.C. A novel DCL2-dependent miRNA pathway in tomato affects susceptibility to RNA viruses. Genes Dev. 2018;32:1155–1160. doi: 10.1101/gad.313601.118. PubMed DOI PMC

Schwind N., Zwiebel M., Itaya A., Ding B., WANG M.B., Krczal G., Wassenegger M. RNAi-mediated resistance to Potato spindle tuber viroid in transgenic tomato expressing a viroid hairpin RNA construct. Mol. Plant Pathol. 2009;10:459–469. doi: 10.1111/j.1364-3703.2009.00546.x. PubMed DOI PMC

Li Y., Qin L., Zhao J., Muhammad T., Cao H., Li H., Zhang Y., Liang Y. SlMAPK3 enhances tolerance to tomato yellow leaf curl virus (TYLCV) by regulating salicylic acid and jasmonic acid signaling in tomato (Solanum lycopersicum) PLoS ONE. 2017;12:e0172466. doi: 10.1371/journal.pone.0172466. PubMed DOI PMC

Srivastava R., Kumar R. The expanding roles of APETALA2/Ethylene Responsive Factors and their potential applications in crop improvement. Brief. Funct. Genom. 2019;18:240–254. doi: 10.1093/bfgp/elz001. PubMed DOI

Fowler S., Thomashow M.F. Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell. 2002;14:1675–1690. doi: 10.1105/tpc.003483. PubMed DOI PMC

Zhang Z., Zhang H., Quan R., Wang X.-C., Huang R. Transcriptional regulation of the ethylene response factor LeERF2 in the expression of ethylene biosynthesis genes controls ethylene production in tomato and tobacco. Plant Physiol. 2009;150:365–377. doi: 10.1104/pp.109.135830. PubMed DOI PMC

Zhang Z., Huang R. Enhanced tolerance to freezing in tobacco and tomato overexpressing transcription factor TERF2/LeERF2 is modulated by ethylene biosynthesis. Plant Mol. Biol. 2010;73:241–249. doi: 10.1007/s11103-010-9609-4. PubMed DOI

Jang J.-C., Sheen J. Sugar sensing in higher plants. Plant Cell. 1994;6:1665–1679. PubMed PMC

Rolland F., Baena-Gonzalez E., Sheen J. Sugar sensing and signaling in plants: Conserved and novel mechanisms. Annu. Rev. Plant Biol. 2006;57:675–709. doi: 10.1146/annurev.arplant.57.032905.105441. PubMed DOI

Smeekens S. Sugar-induced signal transduction in plants. Annu. Rev. Plant Biol. 2000;51:49–81. doi: 10.1146/annurev.arplant.51.1.49. PubMed DOI

Smeekens S., Rook F. Sugar sensing and sugar-mediated signal transduction in plants. Plant Physiol. 1997;115:7. doi: 10.1104/pp.115.1.7. PubMed DOI PMC

Xu X.-X., Hu Q., Yang W.-N., Jin Y. The roles of cell wall invertase inhibitor in regulating chilling tolerance in tomato. BMC Plant Biol. 2017;17:195. doi: 10.1186/s12870-017-1145-9. PubMed DOI PMC

Cai B., Li Q., Xu Y., Yang L., Bi H., Ai X. Genome-wide analysis of the fructose 1, 6-bisphosphate aldolase (FBA) gene family and functional characterization of FBA7 in tomato. Plant Physiol. Biochem. 2016;108:251–265. doi: 10.1016/j.plaphy.2016.07.019. PubMed DOI

Michelis R., Gepstein S. Identification and characterization of a heat-induced isoform of aldolase in oat chloroplast. Plant Mol. Biol. 2000;44:487–498. doi: 10.1023/A:1026528319769. PubMed DOI

Purev M., Kim M.K., Samdan N., Yang D.-C. Isolation of a novel fructose-1, 6-bisphosphate aldolase gene from Codonopsis lanceolata and analysis of the response of this gene to abiotic stresses. Mol. Biol. 2008;42:179. doi: 10.1134/S0026893308020027. PubMed DOI

Cai B., Li Q., Liu F., Bi H., Ai X. Decreasing fructose-1, 6-bisphosphate aldolase activity reduces plant growth and tolerance to chilling stress in tomato seedlings. Physiol. Plant. 2018;163:247–258. doi: 10.1111/ppl.12682. PubMed DOI

Tubiello F.N., Soussana J.-F., Howden S.M. Crop and pasture response to climate change. Proc. Natl. Acad. Sci. USA. 2007;104:19686–19690. doi: 10.1073/pnas.0701728104. PubMed DOI PMC

Link V., Sinha A.K., Vashista P., Hofmann M.G., Proels R.K., Ehness R., Roitsch T. A heat-activated MAP kinase in tomato: A possible regulator of the heat stress response. FEBS Lett. 2002;531:179–183. doi: 10.1016/S0014-5793(02)03498-1. PubMed DOI

Evrard A., Kumar M., Lecourieux D., Lucks J., von Koskull-Döring P., Hirt H. Regulation of the heat stress response in Arabidopsis by MPK6-targeted phosphorylation of the heat stress factor HsfA2. PeerJ. 2013;1:e59. doi: 10.7717/peerj.59. PubMed DOI PMC

Ding H., He J., Wu Y., Wu X., Ge C., Wang Y., Zhong S., Peiter E., Liang J., Xu W. The tomato mitogen-activated protein kinase slmpk1 is as a negative regulator of the high-temperature stress response. Plant Physiol. 2018;177:633–651. doi: 10.1104/pp.18.00067. PubMed DOI PMC

Mishra S.K., Tripp J., Winkelhaus S., Tschiersch B., Theres K., Nover L., Scharf K.-D. In the complex family of heat stress transcription factors, HsfA1 has a unique role as master regulator of thermotolerance in tomato. Genes Dev. 2002;16:1555–1567. doi: 10.1101/gad.228802. PubMed DOI PMC

Liu D., Kumar R., Claus L.A., Johnson A.J., Siao W., Vanhoutte I., Wang P., Bender K.W., Yperman K., Martins S. Endocytosis of BRASSINOSTEROID INSENSITIVE1 Is Partly Driven by a Canonical Tyr-Based Motif. Plant Cell. 2020;32:3598–3612. doi: 10.1105/tpc.20.00384. PubMed DOI PMC

Divi U.K., Krishna P. Brassinosteroid: A biotechnological target for enhancing crop yield and stress tolerance. New Biotechnol. 2009;26:131–136. doi: 10.1016/j.nbt.2009.07.006. PubMed DOI

Kagale S., Divi U.K., Krochko J.E., Keller W.A., Krishna P. Brassinosteroid confers tolerance in Arabidopsis thaliana and Brassica napus to a range of abiotic stresses. Planta. 2007;225:353–364. doi: 10.1007/s00425-006-0361-6. PubMed DOI

Nakashita H., Yasuda M., Nitta T., Asami T., Fujioka S., Arai Y., Sekimata K., Takatsuto S., Yamaguchi I., Yoshida S. Brassinosteroid functions in a broad range of disease resistance in tobacco and rice. Plant J. 2003;33:887–898. doi: 10.1046/j.1365-313X.2003.01675.x. PubMed DOI

Yin Y., Qin K., Song X., Zhang Q., Zhou Y., Xia X., Yu J. BZR1 transcription factor regulates heat stress tolerance through FERONIA receptor-like kinase-mediated reactive oxygen species signaling in tomato. Plant Cell Physiol. 2018;59:2239–2254. doi: 10.1093/pcp/pcy146. PubMed DOI

Priest D.M., Ambrose S.J., Vaistij F.E., Elias L., Higgins G.S., Ross A.R., Abrams S.R., Bowles D.J. Use of the glucosyltransferase UGT71B6 to disturb abscisic acid homeostasis in Arabidopsis thaliana. Plant J. 2006;46:492–502. doi: 10.1111/j.1365-313X.2006.02701.x. PubMed DOI

Sun Y., Ji K., Liang B., Du Y., Jiang L., Wang J., Kai W., Zhang Y., Zhai X., Chen P. Suppressing ABA uridine diphosphate glucosyltransferase (Sl UGT 75C1) alters fruit ripening and the stress response in tomato. Plant J. 2017;91:574–589. doi: 10.1111/tpj.13588. PubMed DOI

Jakoby M., Weisshaar B., Dröge-Laser W., Vicente-Carbajosa J., Tiedemann J., Kroj T., Parcy F. bZIP transcription factors in Arabidopsis. Trends Plant Sci. 2002;7:106–111. doi: 10.1016/S1360-1385(01)02223-3. PubMed DOI

Umezawa T., Nakashima K., Miyakawa T., Kuromori T., Tanokura M., Shinozaki K., Yamaguchi-Shinozaki K. Molecular basis of the core regulatory network in ABA responses: Sensing, signaling and transport. Plant Cell Physiol. 2010;51:1821–1839. doi: 10.1093/pcp/pcq156. PubMed DOI PMC

Zhu M., Meng X., Cai J., Li G., Dong T., Li Z. Basic leucine zipper transcription factor SlbZIP1 mediates salt and drought stress tolerance in tomato. BMC Plant Biol. 2018;18:83. doi: 10.1186/s12870-018-1299-0. PubMed DOI PMC

Guo X., Chen G., Naeem M., Yu X., Tang B., Li A., Hu Z. The MADS-box gene SlMBP11 regulates plant architecture and affects reproductive development in tomato plants. Plant Sci. 2017;258:90–101. doi: 10.1016/j.plantsci.2017.02.005. PubMed DOI

Yin W., Hu Z., Cui B., Guo X., Hu J., Zhu Z., Chen G. Suppression of the MADS-box gene SlMBP8 accelerates fruit ripening of tomato (Solanum lycopersicum) Plant Physiol. Biochem. 2017;118:235–244. doi: 10.1016/j.plaphy.2017.06.019. PubMed DOI

Li Y., Chu Z., Luo J., Zhou Y., Cai Y., Lu Y., Xia J., Kuang H., Ye Z., Ouyang B. The C2H2 zinc-finger protein Sl ZF 3 regulates AsA synthesis and salt tolerance by interacting with CSN 5B. Plant Biotechnol. J. 2018;16:1201–1213. doi: 10.1111/pbi.12863. PubMed DOI PMC

Bao H., Chen X., Lv S., Jiang P., Feng J., Fan P., Nie L., Li Y. Virus-induced gene silencing reveals control of reactive oxygen species accumulation and salt tolerance in tomato by γ-aminobutyric acid metabolic pathway. Plantcell Environ. 2015;38:600–613. doi: 10.1111/pce.12419. PubMed DOI

Hohmann S. Osmotic stress signaling and osmoadaptation in yeasts. Microbiol. Mol. Biol. Rev. 2002;66:300–372. doi: 10.1128/MMBR.66.2.300-372.2002. PubMed DOI PMC

Sharma P., Jha A.B., Dubey R.S., Pessarakli M. Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J. Bot. 2012;2012 doi: 10.1155/2012/217037. DOI

Yang Y., Tang N., Xian Z., Li Z. Two SnRK2 protein kinases genes play a negative regulatory role in the osmotic stress response in tomato. Plant Cell Tissue Organ Cult. PCTOC. 2015;122:421–434. doi: 10.1007/s11240-015-0779-2. DOI

Borsani O., Cuartero J., Valpuesta V., Botella M.A. Tomato tos1 mutation identifies a gene essential for osmotic tolerance and abscisic acid sensitivity. Plant J. 2002;32:905–914. doi: 10.1046/j.1365-313X.2002.01475.x. PubMed DOI

Li R., Zhang L., Wang L., Chen L., Zhao R., Sheng J., Shen L. Reduction of tomato-plant chilling tolerance by CRISPR–Cas9-mediated SlCBF1 mutagenesis. J. Agric. Food Chem. 2018;66:9042–9051. doi: 10.1021/acs.jafc.8b02177. PubMed DOI

Hu T., Wang Y., Wang Q., Dang N., Wang L., Liu C., Zhu J., Zhan X. The tomato 2-oxoglutarate-dependent dioxygenase gene SlF3HL is critical for chilling stress tolerance. Hortic. Res. 2019;6:1–12. doi: 10.1038/s41438-019-0127-5. PubMed DOI PMC

Zhang L., Guo X., Qin Y., Feng B., Wu Y., He Y., Wang A., Zhu J. The chilling tolerance divergence 1 protein confers cold stress tolerance in processing tomato. Plant Physiol. Biochem. 2020;151:34–46. doi: 10.1016/j.plaphy.2020.03.007. PubMed DOI

Zhuang K., Kong F., Zhang S., Meng C., Yang M., Liu Z., Wang Y., Ma N., Meng Q. Whirly1 enhances tolerance to chilling stress in tomato via protection of photosystem II and regulation of starch degradation. New Phytol. 2019;221:1998–2012. doi: 10.1111/nph.15532. PubMed DOI

Zhuang K., Wang J., Jiao B., Chen C., Zhang J., Ma N., Meng Q. SlWHIRLY1 maintains leaf photosynthetic capacity in tomato by regulating the expression of SlRbcS1 under chilling stress. J. Exp. Bot. 2020;71:3653–3663. doi: 10.1093/jxb/eraa145. PubMed DOI

Liu Y., Shi Y., Zhu N., Zhong S., Bouzayen M., Li Z. SlGRAS4 mediates a novel regulatory pathway promoting chilling tolerance in tomato. Plant Biotechnol. J. 2020;18:1620–1633. doi: 10.1111/pbi.13328. PubMed DOI PMC

Li H., Jiang X., Lv X., Ahammed G.J., Guo Z., Qi Z., Yu J., Zhou Y. Tomato GLR3. 3 and GLR3. 5 mediate cold acclimation-induced chilling tolerance by regulating apoplastic H2O2 production and redox homeostasis. Plantcell Environ. 2019;42:3326–3339. PubMed

Guo X., Li J., Zhang L., Zhang Z., He P., Wang W., Wang M., Wang A., Zhu J. Heterotrimeric G-protein α subunit (LeGPA1) confers cold stress tolerance to processing tomato plants (Lycopersicon esculentum Mill) BMC Plant Biol. 2020;20:394. doi: 10.1186/s12870-020-02615-w. PubMed DOI PMC

Wang L., Chen L., Li R., Zhao R., Yang M., Sheng J., Shen L. Reduced drought tolerance by CRISPR/Cas9-mediated SlMAPK3 mutagenesis in tomato plants. J. Agric. Food Chem. 2017;65:8674–8682. doi: 10.1021/acs.jafc.7b02745. PubMed DOI

Li R., Liu C., Zhao R., Wang L., Chen L., Yu W., Zhang S., Sheng J., Shen L. CRISPR/Cas9-Mediated SlNPR1 mutagenesis reduces tomato plant drought tolerance. BMC Plant Biol. 2019;19:38. PubMed PMC

Zhang Y., Li H., Shu W., Zhang C., Zhang W., Ye Z. Suppressed expression of ascorbate oxidase gene promotes ascorbic acid accumulation in tomato fruit. Plant Mol. Biol. Report. 2011;29:638–645. doi: 10.1007/s11105-010-0271-4. DOI

Ewas M., Gao Y., Wang S., Liu X., Zhang H., Nishawy E.M., Ali F., Shahzad R., Ziaf K., Subthain H. Manipulation of SlMXl for enhanced carotenoids accumulation and drought resistance in tomato. Sci. Bull. 2016;61:1413–1418. doi: 10.1007/s11434-016-1108-9. DOI

Song J., Xing Y., Munir S., Yu C., Song L., Li H., Wang T., Ye Z. An ATL78-Like RING-H2 finger protein confers abiotic stress tolerance through interacting with RAV2 and CSN5B in tomato. Front. Plant Sci. 2016;7:1305. doi: 10.3389/fpls.2016.01305. PubMed DOI PMC

Zhang Y., Li Q., Jiang L., Kai W., Liang B., Wang J., Du Y., Zhai X., Wang J., Zhang Y. Suppressing type 2C protein phosphatases alters fruit ripening and the stress response in tomato. Plant Cell Physiol. 2018;59:142–154. doi: 10.1093/pcp/pcx169. PubMed DOI

Zhu T., Zou L., Li Y., Yao X., Xu F., Deng X., Zhang D., Lin H. Mitochondrial alternative oxidase-dependent autophagy involved in ethylene-mediated drought tolerance in Solanum lycopersicum. Plant Biotechnol. J. 2018;16:2063–2076. doi: 10.1111/pbi.12939. PubMed DOI PMC

Li J., Chen C., Wei J., Pan Y., Su C., Zhang X. SpPKE1, a Multiple Stress-Responsive Gene Confers Salt Tolerance in Tomato and Tobacco. Int. J. Mol. Sci. 2019;20:2478. doi: 10.3390/ijms20102478. PubMed DOI PMC

Thirumalaikumar V.P., Devkar V., Mehterov N., Ali S., Ozgur R., Turkan I., Mueller-Roeber B., Balazadeh S. NAC transcription factor JUNGBRUNNEN 1 enhances drought tolerance in tomato. Plant Biotechnol. J. 2018;16:354–366. doi: 10.1111/pbi.12776. PubMed DOI PMC

Klap C., Yeshayahou E., Bolger A.M., Arazi T., Gupta S.K., Shabtai S., Usadel B., Salts Y., Barg R. Tomato facultative parthenocarpy results from Sl AGAMOUS-LIKE 6 loss of function. Plant Biotechnol. J. 2017;15:634–647. doi: 10.1111/pbi.12662. PubMed DOI PMC

Spicher L., Almeida J., Gutbrod K., Pipitone R., Dörmann P., Glauser G., Rossi M., Kessler F. Essential role for phytol kinase and tocopherol in tolerance to combined light and temperature stress in tomato. J. Exp. Bot. 2017;68:5845–5856. doi: 10.1093/jxb/erx356. PubMed DOI PMC

Zhang S., Wang S., Lv J., Liu Z., Wang Y., Ma N., Meng Q. SUMO E3 ligase SlSIZ1 facilitates heat tolerance in tomato. Plant Cell Physiol. 2018;59:58–71. doi: 10.1093/pcp/pcx160. PubMed DOI

Zhuang K., Gao Y., Liu Z., Diao P., Sui N., Meng Q., Meng C., Kong F. WHIRLY1 regulates HSP21. 5A expression to promote thermotolerance in tomato. Plant Cell Physiol. 2020;61:169–177. doi: 10.1093/pcp/pcz189. PubMed DOI

Olias R., Eljakaoui Z., Li J., DE MORALES P.A., MARÍN-MANZANO M.C., Pardo J.M., Belver A. The plasma membrane Na+/H+ antiporter SOS1 is essential for salt tolerance in tomato and affects the partitioning of Na+ between plant organs. Plant Cell Environ. 2009;32:904–916. doi: 10.1111/j.1365-3040.2009.01971.x. PubMed DOI

Cai X., Zhang C., Shu W., Ye Z., Li H., Zhang Y. The transcription factor SlDof22 involved in ascorbate accumulation and salinity stress in tomato. Biochem. Biophys. Res. Commun. 2016;474:736–741. doi: 10.1016/j.bbrc.2016.04.148. PubMed DOI

Wang L., Hu Z., Zhu M., Zhu Z., Hu J., Qanmber G., Chen G. The abiotic stress-responsive NAC transcription factor SlNAC11 is involved in drought and salt response in tomato (Solanum lycopersicum L.) Plant Celltissue Organ Cult. (PCTOC) 2017;129:161–174. doi: 10.1007/s11240-017-1167-x. DOI

Campos J.F., Cara B., Pérez-Martín F., Pineda B., Egea I., Flores F.B., Fernandez-Garcia N., Capel J., Moreno V., Angosto T. The tomato mutant ars1 (altered response to salt stress 1) identifies an R1-type MYB transcription factor involved in stomatal closure under salt acclimation. Plant Biotechnol. J. 2016;14:1345–1356. doi: 10.1111/pbi.12498. PubMed DOI PMC

Liu B., Ouyang Z., Zhang Y., Li X., Hong Y., Huang L., Liu S., Zhang H., Li D., Song F. Tomato NAC transcription factor SlSRN1 positively regulates defense response against biotic stress but negatively regulates abiotic stress response. PLoS ONE. 2014;9:e102067. doi: 10.1371/journal.pone.0102067. PubMed DOI PMC

Vick B.A., Zimmerman D.C. Biosynthesis of jasmonic acid by several plant species. Plant Physiol. 1984;75:458–461. doi: 10.1104/pp.75.2.458. PubMed DOI PMC

Heitz T., Bergey D.R., Ryan C.A. A gene encoding a chloroplast-targeted lipoxygenase in tomato leaves is transiently induced by wounding, systemin, and methyl jasmonate. Plant Physiol. 1997;114:1085–1093. doi: 10.1104/pp.114.3.1085. PubMed DOI PMC

Hu T., Hu Z., Zeng H., Qv X., Chen G. Tomato lipoxygenase D involved in the biosynthesis of jasmonic acid and tolerance to abiotic and biotic stress in tomato. Plant Biotechnol. Rep. 2015;9:37–45. doi: 10.1007/s11816-015-0341-z. DOI

AbuQamar S., Luo H., Laluk K., Mickelbart M.V., Mengiste T. Crosstalk between biotic and abiotic stress responses in tomato is mediated by the AIM1 transcription factor. Plant J. 2009;58:347–360. doi: 10.1111/j.1365-313X.2008.03783.x. PubMed DOI

Du L., Ali G.S., Simons K.A., Hou J., Yang T., Reddy A., Poovaiah B. Ca 2+/calmodulin regulates salicylic-acid-mediated plant immunity. Nature. 2009;457:1154–1158. doi: 10.1038/nature07612. PubMed DOI

Galon Y., Nave R., Boyce J.M., Nachmias D., Knight M.R., Fromm H. Calmodulin-binding transcription activator (CAMTA) 3 mediates biotic defense responses in Arabidopsis. FEBS Lett. 2008;582:943–948. doi: 10.1016/j.febslet.2008.02.037. PubMed DOI

Laluk K., Prasad K., Savchenko T., Celesnik H., Dehesh K., Levy M., Mitchell-Olds T., Reddy A. The calmodulin-binding transcription factor SIGNAL RESPONSIVE1 is a novel regulator of glucosinolate metabolism and herbivory tolerance in Arabidopsis. Plant Cell Physiol. 2012;53:2008–2015. doi: 10.1093/pcp/pcs143. PubMed DOI PMC

Nie H., Zhao C., Wu G., Wu Y., Chen Y., Tang D. SR1, a calmodulin-binding transcription factor, modulates plant defense and ethylene-induced senescence by directly regulating NDR1 and EIN3. Plant Physiol. 2012;158:1847–1859. doi: 10.1104/pp.111.192310. PubMed DOI PMC

Qiu Y., Xi J., Du L., Suttle J.C., Poovaiah B. Coupling calcium/calmodulin-mediated signaling and herbivore-induced plant response through calmodulin-binding transcription factor AtSR1/CAMTA3. Plant Mol. Biol. 2012;79:89–99. doi: 10.1007/s11103-012-9896-z. PubMed DOI

Doherty C.J., Van Buskirk H.A., Myers S.J., Thomashow M.F. Roles for Arabidopsis CAMTA transcription factors in cold-regulated gene expression and freezing tolerance. Plant Cell. 2009;21:972–984. doi: 10.1105/tpc.108.063958. PubMed DOI PMC

Kim Y., Park S., Gilmour S.J., Thomashow M.F. Roles of CAMTA transcription factors and salicylic acid in configuring the low-temperature transcriptome and freezing tolerance of A rabidopsis. Plant J. 2013;75:364–376. doi: 10.1111/tpj.12205. PubMed DOI

Pandey N., Ranjan A., Pant P., Tripathi R.K., Ateek F., Pandey H.P., Patre U.V., Sawant S.V. CAMTA 1 regulates drought responses in Arabidopsis thaliana. BMC Genom. 2013;14:216. doi: 10.1186/1471-2164-14-216. PubMed DOI PMC

Yang T., Peng H., Whitaker B.D., Jurick W.M. Differential expression of calcium/calmodulin-regulated SlSRs in response to abiotic and biotic stresses in tomato fruit. Physiol. Plant. 2013;148:445–455. doi: 10.1111/ppl.12027. PubMed DOI

Yang T., Peng H., Whitaker B.D., Conway W.S. Characterization of a calcium/calmodulin-regulated SR/CAMTA gene family during tomato fruit development and ripening. BMC Plant Biol. 2012;12:19. doi: 10.1186/1471-2229-12-19. PubMed DOI PMC

Li X., Huang L., Zhang Y., Ouyang Z., Hong Y., Zhang H., Li D., Song F. Tomato SR/CAMTA transcription factors SlSR1 and SlSR3L negatively regulate disease resistance response and SlSR1L positively modulates drought stress tolerance. BMC Plant Biol. 2014;14:286. doi: 10.1186/s12870-014-0286-3. PubMed DOI PMC

Priyanka B., Sekhar K., Reddy V.D., Rao K.V. Expression of pigeonpea hybrid-proline-rich protein encoding gene (CcHyPRP) in yeast and Arabidopsis affords multiple abiotic stress tolerance. Plant Biotechnol. J. 2010;8:76–87. doi: 10.1111/j.1467-7652.2009.00467.x. PubMed DOI

Tan J., Zhuo C., Guo Z. Nitric oxide mediates cold-and dehydration-induced expression of a novel MfHyPRP that confers tolerance to abiotic stress. Physiol. Plant. 2013;149:310–320. PubMed

Xu D., Huang X., Xu Z.-Q., Schläppi M. The HyPRP gene EARLI1 has an auxiliary role for germinability and early seedling development under low temperature and salt stress conditions in Arabidopsis thaliana. Planta. 2011;234:565–577. doi: 10.1007/s00425-011-1425-9. PubMed DOI

Yeom S.I., Seo E., Oh S.K., Kim K.W., Choi D. A common plant cell-wall protein HyPRP1 has dual roles as a positive regulator of cell death and a negative regulator of basal defense against pathogens. Plant J. 2012;69:755–768. doi: 10.1111/j.1365-313X.2011.04828.x. PubMed DOI

Zhang Y., Schläppi M. Cold responsive EARLI1 type HyPRPs improve freezing survival of yeast cells and form higher order complexes in plants. Planta. 2007;227:233–243. doi: 10.1007/s00425-007-0611-2. PubMed DOI

Li J., Ouyang B., Wang T., Luo Z., Yang C., Li H., Sima W., Zhang J., Ye Z. HyPRP1 gene suppressed by multiple stresses plays a negative role in abiotic stress tolerance in tomato. Front. Plant Sci. 2016;7:967. doi: 10.3389/fpls.2016.00967. PubMed DOI PMC

Chakravarthy S., Tuori R.P., D’Ascenzo M.D., Fobert P.R., Després C., Martin G.B. The tomato transcription factor Pti4 regulates defense-related gene expression via GCC box and non-GCC box cis elements. Plant Cell. 2003;15:3033–3050. doi: 10.1105/tpc.017574. PubMed DOI PMC

Gu Y.-Q., Wildermuth M.C., Chakravarthy S., Loh Y.-T., Yang C., He X., Han Y., Martin G.B. Tomato transcription factors Pti4, Pti5, and Pti6 activate defense responses when expressed in Arabidopsis. Plant Cell. 2002;14:817–831. doi: 10.1105/tpc.000794. PubMed DOI PMC

Mysore K.S., Crasta O.R., Tuori R.P., Folkerts O., Swirsky P.B., Martin G.B. Comprehensive transcript profiling of Pto-and Prf-mediated host defense responses to infection by Pseudomonas syringae pv. tomato. Plant J. 2002;32:299–315. doi: 10.1046/j.1365-313X.2002.01424.x. PubMed DOI

Sun Y., Liang B., Wang J., Kai W., Chen P., Jiang L., Du Y., Leng P. SlPti4 affects regulation of fruit ripening, seed germination and stress responses by modulating ABA signaling in tomato. Plant Cell Physiol. 2018;59:1956–1965. doi: 10.1093/pcp/pcy111. PubMed DOI

Xu C., Liberatore K.L., MacAlister C.A., Huang Z., Chu Y.-H., Jiang K., Brooks C., Ogawa-Ohnishi M., Xiong G., Pauly M. A cascade of arabinosyltransferases controls shoot meristem size in tomato. Nat. Genet. 2015;47:784–792. doi: 10.1038/ng.3309. PubMed DOI

Rodríguez-Leal D., Lemmon Z.H., Man J., Bartlett M.E., Lippman Z.B. Engineering quantitative trait variation for crop improvement by genome editing. Cell. 2017;171:470–480.e478. doi: 10.1016/j.cell.2017.08.030. PubMed DOI

Soyk S., Müller N.A., Park S.J., Schmalenbach I., Jiang K., Hayama R., Zhang L., Van Eck J., Jiménez-Gómez J.M., Lippman Z.B. Variation in the flowering gene SELF PRUNING 5G promotes day-neutrality and early yield in tomato. Nat. Genet. 2017;49:162–168. doi: 10.1038/ng.3733. PubMed DOI

Li T., Yang X., Yu Y., Si X., Zhai X., Zhang H., Dong W., Gao C., Xu C. Domestication of wild tomato is accelerated by genome editing. Nat. Biotechnol. 2018;36:1160–1163. doi: 10.1038/nbt.4273. PubMed DOI

Zsögön A., Čermák T., Naves E.R., Notini M.M., Edel K.H., Weinl S., Freschi L., Voytas D.F., Kudla J., Peres L.E.P. De novo domestication of wild tomato using genome editing. Nat. Biotechnol. 2018;36:1211–1216. doi: 10.1038/nbt.4272. PubMed DOI

Ito Y., Nishizawa-Yokoi A., Endo M., Mikami M., Toki S. CRISPR/Cas9-mediated mutagenesis of the RIN locus that regulates tomato fruit ripening. Biochem. Biophys. Res. Commun. 2015;467:76–82. doi: 10.1016/j.bbrc.2015.09.117. PubMed DOI

Ito Y., Nishizawa-Yokoi A., Endo M., Mikami M., Shima Y., Nakamura N., Kotake-Nara E., Kawasaki S., Toki S. Re-evaluation of the rin mutation and the role of RIN in the induction of tomato ripening. Nat. Plants. 2017;3:866–874. doi: 10.1038/s41477-017-0041-5. PubMed DOI

Ito Y., Sekiyama Y., Nakayama H., Nishizawa-Yokoi A., Endo M., Shima Y., Nakamura N., Kotake-Nara E., Kawasaki S., Hirose S. Allelic Mutations in the Ripening-Inhibitor Locus Generate Extensive Variation in Tomato Ripening. Plant Physiol. 2020;183:80–95. doi: 10.1104/pp.20.00020. PubMed DOI PMC

Yang Y., Zhu G., Li R., Yan S., Fu D., Zhu B., Tian H., Luo Y., Zhu H. The RNA editing factor SlORRM4 is required for normal fruit ripening in tomato. Plant Physiol. 2017;175:1690–1702. doi: 10.1104/pp.17.01265. PubMed DOI PMC

Yu Q.-h., Wang B., Li N., Tang Y., Yang S., Yang T., Xu J., Guo C., Yan P., Wang Q. CRISPR/Cas9-induced targeted mutagenesis and gene replacement to generate long-shelf life tomato lines. Sci. Rep. 2017;7:1–9. doi: 10.1038/s41598-017-12262-1. PubMed DOI PMC

Sravankumar T., Naik N., Kumar R. A ripening-induced SlGH3-2 gene regulates fruit ripening via adjusting auxin-ethylene levels in tomato (Solanum lycopersicum L.) Plant Mol. Biol. 2018;98:455–469. doi: 10.1007/s11103-018-0790-1. PubMed DOI

Ueta R., Abe C., Watanabe T., Sugano S.S., Ishihara R., Ezura H., Osakabe Y., Osakabe K. Rapid breeding of parthenocarpic tomato plants using CRISPR/Cas9. Sci. Rep. 2017;7:1–8. doi: 10.1038/s41598-017-00501-4. PubMed DOI PMC

Li X., Wang Y., Chen S., Tian H., Fu D., Zhu B., Luo Y., Zhu H. Lycopene is enriched in tomato fruit by CRISPR/Cas9-mediated multiplex genome editing. Front. Plant Sci. 2018;9:559. doi: 10.3389/fpls.2018.00559. PubMed DOI PMC

Gago C., Drosou V., Paschalidis K., Guerreiro A., Miguel G., Antunes D., Hilioti Z. Targeted gene disruption coupled with metabolic screen approach to uncover the LEAFY COTYLEDON1-LIKE4 (L1L4) function in tomato fruit metabolism. Plant Cell Rep. 2017;36:1065–1082. doi: 10.1007/s00299-017-2137-9. PubMed DOI

Hilioti Z., Ganopoulos I., Ajith S., Bossis I., Tsaftaris A. A novel arrangement of zinc finger nuclease system for in vivo targeted genome engineering: The tomato LEC1-LIKE4 gene case. Plant Cell Rep. 2016;35:2241–2255. doi: 10.1007/s00299-016-2031-x. PubMed DOI

Li R., Li R., Li X., Fu D., Zhu B., Tian H., Luo Y., Zhu H. Multiplexed CRISPR/Cas9-mediated metabolic engineering of γ-aminobutyric acid levels in Solanum lycopersicum. Plant Biotechnol. J. 2018;16:415–427. doi: 10.1111/pbi.12781. PubMed DOI PMC

Shimatani Z., Kashojiya S., Takayama M., Terada R., Arazoe T., Ishii H., Teramura H., Yamamoto T., Komatsu H., Miura K. Targeted base editing in rice and tomato using a CRISPR-Cas9 cytidine deaminase fusion. Nat. Biotechnol. 2017;35:441–443. doi: 10.1038/nbt.3833. PubMed DOI

Xu C., Park S.J., Van Eck J., Lippman Z.B. Control of inflorescence architecture in tomato by BTB/POZ transcriptional regulators. Genes Dev. 2016;30:2048–2061. doi: 10.1101/gad.288415.116. PubMed DOI PMC

Pan C., Ye L., Qin L., Liu X., He Y., Wang J., Chen L., Lu G. CRISPR/Cas9-mediated efficient and heritable targeted mutagenesis in tomato plants in the first and later generations. Sci. Rep. 2016;6:24765. doi: 10.1038/srep24765. PubMed DOI PMC

Keddie J.S., Carroll B., Jones J., Gruissem W. The DCL gene of tomato is required for chloroplast development and palisade cell morphogenesis in leaves. EMBO J. 1996;15:4208–4217. doi: 10.1002/j.1460-2075.1996.tb00795.x. PubMed DOI PMC

Ron M., Kajala K., Pauluzzi G., Wang D., Reynoso M.A., Zumstein K., Garcha J., Winte S., Masson H., Inagaki S. Hairy root transformation using Agrobacterium rhizogenes as a tool for exploring cell type-specific gene expression and function using tomato as a model. Plant Physiol. 2014;166:455–469. doi: 10.1104/pp.114.239392. PubMed DOI PMC

Lor V.S., Starker C.G., Voytas D.F., Weiss D., Olszewski N.E. Targeted mutagenesis of the tomato PROCERA gene using transcription activator-like effector nucleases. Plant Physiol. 2014;166:1288–1291. doi: 10.1104/pp.114.247593. PubMed DOI PMC

Hayut S.F., Bessudo C.M., Levy A.A. Targeted recombination between homologous chromosomes for precise breeding in tomato. Nat. Commun. 2017;8:1–9. PubMed PMC

Xie K., Zhang J., Yang Y. Genome-wide prediction of highly specific guide RNA spacers for CRISPR–Cas9-mediated genome editing in model plants and major crops. Mol. Plant. 2014;7:923–926. doi: 10.1093/mp/ssu009. PubMed DOI

Zaidi S.S.A., Mahfouz M.M., Mansoor S. CRISPR-Cpf1: A new tool for plant genome editing. Trends Plant Sci. 2017;22:550–553. doi: 10.1016/j.tplants.2017.05.001. PubMed DOI

Zetsche B., Gootenberg J.S., Abudayyeh O.O., Slaymaker I.M., Makarova K.S., Essletzbichler P., Volz S.E., Joung J., Van Der Oost J., Regev A. Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell. 2015;163:759–771. doi: 10.1016/j.cell.2015.09.038. PubMed DOI PMC

Hua K., Zhang J., Botella J.R., Ma C., Kong F., Liu B., Zhu J.-K. Perspectives on the application of genome-editing technologies in crop breeding. Mol. Plant. 2019;12:1047–1059. doi: 10.1016/j.molp.2019.06.009. PubMed DOI

Clarke J.L., Zhang P. Plant biotechnology for food security and bioeconomy. Plant Mol. Biol. 2013;83:1–3. doi: 10.1007/s11103-013-0097-1. PubMed DOI

Bhargava A., Srivastava S. Participatory Plant Breeding: Concept and Applications. Springer; Singapore: 2019.

Mann C.C. Genetic engineers aim to soup up crop photosynthesis. Science. 1999;283:314–316. doi: 10.1126/science.283.5400.314. PubMed DOI

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