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Beyond green and red: unlocking the genetic orchestration of tomato fruit color and pigmentation

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Abstract

Fruit color is a genetic trait and a key factor for consumer acceptability and is therefore receiving increasing importance in several breeding programs. Plant pigments offer plants with a variety of colored organs that attract animals for pollination, favoring seed dispersers and conservation of species. The pigments inside plant cells not only play a light-harvesting role but also provide protection against light damage and exhibit nutritional and ecological value for health and visual pleasure in humans. Tomato (Solanum lycopersicum) is a leading vegetable crop; its fruit color formation is associated with the accumulation of several natural pigments, which include carotenoids in the pericarp, flavonoids in the peel, as well as the breakdown of chlorophyll during fruit ripening. To improve tomato fruit quality, several techniques, such as genetic engineering and genome editing, have been used to alter fruit color and regulate the accumulation of secondary metabolites in related pathways. Recently, clustered regularly interspaced short palindromic repeat (CRISPR)-based systems have been extensively used for genome editing in many crops, including tomatoes, and promising results have been achieved using modified CRISPR systems, including CAS9 (CRISPR/CRISPR-associated-protein) and CRISPR/Cas12a systems. These advanced tools in biotechnology and whole genome sequencing of various tomato species will certainly advance the breeding of tomato fruit color with a high degree of precision. Here, we attempt to summarize the current advancement and effective application of genetic engineering techniques that provide further flexibility for fruit color formation. Furthermore, we have also discussed the challenges and opportunities of genetic engineering and genome editing to improve tomato fruit color.

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References

  • Abdallah NA, Prakash CS, McHughen AG (2015) Genome editing for crop improvement: challenges and opportunities. GM Crops Food 6:183–205

    PubMed  Google Scholar 

  • Adato A, Mandel T, Mintz-Oron S, Venger I, Levy D, Yativ M, Domínguez E, Wang Z, De Vos RC, Jetter R (2009) Fruit-surface flavonoid accumulation in tomato is controlled by a SlMYB12-regulated transcriptional network. PLoS Genet 5:e1000777

    PubMed  PubMed Central  Google Scholar 

  • Ariizumi T, Kishimoto S, Kakami R, Maoka T, Hirakawa H, Suzuki Y, Ozeki Y, Shirasawa K, Bernillon S, Okabe Y (2014) 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 79:453–465

    CAS  PubMed  Google Scholar 

  • Arnao M, Hernández-Ruiz J (2020) Melatonin in flowering, fruit set and fruit ripening. Plant Reprod 33:77–87

    CAS  PubMed  Google Scholar 

  • Balbuena MS, Broadhead GT, Dahake A, Barnett E, Vergara M, Skogen KA, Jogesh T, Raguso RA (2022) Mutualism has its limits: consequences of asymmetric interactions between a well-defended plant and its herbivorous pollinator. Philos Trans R Soc B 377:20210166

    Google Scholar 

  • Ballester A-R, Molthoff J, de Vos R, BtL H, Orzaez D, Fernandez-Moreno J-P, Tripodi P, Grandillo S, Martin C, Heldens J (2010) Biochemical and molecular analysis of pink tomatoes: deregulated expression of the gene encoding transcription factor SlMYB12 leads to pink tomato fruit color. Plant Physiol 152:71–84

    CAS  PubMed  PubMed Central  Google Scholar 

  • Barton KA, Binns AN, Matzke AJ, Chilton M-D (1983) Regeneration of intact tobacco plants containing full length copies of genetically engineered T-DNA, and transmission of T-DNA to R1 progeny. Cell 32:1033–1043

    CAS  PubMed  Google Scholar 

  • Bate NJ, Orr J, Ni W, Meromi A, Nadler-Hassar T, Doerner PW, Dixon RA, Lamb CJ, Elkind Y (1994) Quantitative relationship between phenylalanine ammonia-lyase levels and phenylpropanoid accumulation in transgenic tobacco identifies a rate-determining step in natural product synthesis. Proc Natl Acad Sci 91:7608–7612

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bergougnoux V (2014) The history of tomato: from domestication to biopharming. Biotechnol Adv 32:170–189

    CAS  PubMed  Google Scholar 

  • Bornman JF, Barnes PW, Robson TM, Robinson SA, Jansen MA, Ballare CL, Flint SD (2019) Linkages between stratospheric ozone, UV radiation and climate change and their implications for terrestrial ecosystems. Photochem Photobiol Sci 18:681–716

    CAS  PubMed  Google Scholar 

  • Bovy A, de Vos R, Kemper M, Schijlen E, Almenar Pertejo M, Muir S, Collins G, Robinson S, Verhoeyen M, Hughes S (2002) High-flavonol tomatoes resulting from the heterologous expression of the maize transcription factor genes LC and C1. Plant Cell 14:2509–2526

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brooks C, Nekrasov V, Lippman ZB, Van Eck J (2014) Efficient gene editing in tomato in the first generation using the clustered regularly interspaced short palindromic repeats/CRISPR-associated9 system. Plant Physiol 166:1292–1297

    PubMed  PubMed Central  Google Scholar 

  • Broun P (2004) Transcription factors as tools for metabolic engineering in plants. Curr Opin Plant Biol 7:202–209

    CAS  PubMed  Google Scholar 

  • Busi MV, Bustamante C, D'angelo C, Hidalgo-Cuevas M, Boggio SB, Valle EM, Zabaleta E (2003) MADS-box genes expressed during tomato seed and fruit development. Plant Mol Biol 52:801–815

    CAS  PubMed  Google Scholar 

  • Butelli E, Titta L, Giorgio M, Mock H-P, Matros A, Peterek S, Schijlen EG, Hall RD, Bovy AG, Luo J (2008) Enrichment of tomato fruit with health-promoting anthocyanins by expression of select transcription factors. Nature biotechnology 26:1301–1308

    CAS  PubMed  Google Scholar 

  • Cai CQ, Doyon Y, Ainley WM, Miller JC, DeKelver RC, Moehle EA, Rock JM, Lee Y-L, Garrison R, Schulenberg L (2009) Targeted transgene integration in plant cells using designed zinc finger nucleases. Plant Mol Biol 69:699–709

    CAS  PubMed  Google Scholar 

  • Cao X, Qiu Z, Wang X, Van Giang T, Liu X, Wang J, Wang X, Gao J, Guo Y, Du Y (2017) A putative R3 MYB repressor is the candidate gene underlying atroviolacium, a locus for anthocyanin pigmentation in tomato fruit. J Exp Bot 68:5745–5758

    CAS  PubMed  PubMed Central  Google Scholar 

  • Carrera E, Ruiz-Rivero O, Peres LEP, Atares A, Garcia-Martinez JL (2012) Characterization of the procera tomato mutant shows novel functions of the SlDELLA protein in the control of flower morphology, cell division and expansion, and the auxin-signaling pathway during fruit-set and development. Plant Physiol 160:1581–1596

    CAS  PubMed  PubMed Central  Google Scholar 

  • Čermák T, Baltes NJ, Čegan R, Zhang Y, Voytas DF (2015) High-frequency, precise modification of the tomato genome. Genome Biol 16:1–15

    Google Scholar 

  • Chalukova M, Manuelyan H (1991) Breeding for carotenoid pigments in tomato genetic improvement of tomato. Springer, pp 179–195

    Google Scholar 

  • Chattopadhyay T, Hazra P, Akhtar S, Maurya D, Mukherjee A, Roy S (2021) Skin colour, carotenogenesis and chlorophyll degradation mutant alleles: genetic orchestration behind the fruit colour variation in tomato. Plant Cell Rep 40:767–782

    CAS  PubMed  Google Scholar 

  • Chen L, Stacewicz-Sapuntzakis M, Duncan C, Sharifi R, Ghosh L, Rv B, Ashton D, Bowen PE (2001) Oxidative DNA damage in prostate cancer patients consuming tomato sauce-based entrees as a whole-food intervention. J Natl Cancer Inst 93:1872–1879

    CAS  PubMed  Google Scholar 

  • Cheng M, Cui Y, Yan X, Zhang R, Wang J, Wang X (2022) Effect of dual-modified cassava starches on intelligent packaging films containing red cabbage extracts. Food Hydrocoll 124:107225

    CAS  Google Scholar 

  • Chung M-Y, Nath UK, Vrebalov J, Gapper N, Lee JM, Lee D-J, Kim CK, Giovannoni J (2020) Ectopic expression of miRNA172 in tomato (Solanum lycopersicum) reveals novel function in fruit development through regulation of an AP2 transcription factor. BMC Plant Biol 20:1–15

    Google Scholar 

  • Colanero S, Perata P, Gonzali S (2020) What’s behind purple tomatoes? Insight into the mechanisms of anthocyanin synthesis in tomato fruits. Plant Physiol 182:1841–1853

    CAS  PubMed  PubMed Central  Google Scholar 

  • Davuluri GR, Van Tuinen A, Fraser PD, Manfredonia A, Newman R, Burgess D, Brummell DA, King SR, Palys J, Uhlig J (2005) Fruit-specific RNAi-mediated suppression of DET1 enhances carotenoid and flavonoid content in tomatoes. Nat Biotechnol 23:890–895

    CAS  PubMed  Google Scholar 

  • Deng L, Wang H, Sun C, Li Q, Jiang H, Du M, Li C-B, Li C (2018) Efficient generation of pink-fruited tomatoes using CRISPR/Cas9 system. J Genet Genom= Yi chuan xue bao 45:51–54

    CAS  Google Scholar 

  • Dhar MK, Sharma R, Koul A, Kaul S (2015) Development of fruit color in Solanaceae: a story of two biosynthetic pathways. Brief Funct Genomics 14:199–212

    CAS  PubMed  Google Scholar 

  • Egea I, Barsan C, Bian W, Purgatto E, Latché A, Chervin C, Bouzayen M, Pech J-C (2010) Chromoplast differentiation: current status and perspectives. Plant and Cell Physiol 51:1601–1611

    CAS  Google Scholar 

  • Egea I, Bian W, Barsan C, Jauneau A, Pech J-C, Latché A, Li Z, Chervin C (2011) Chloroplast to chromoplast transition in tomato fruit: spectral confocal microscopy analyses of carotenoids and chlorophylls in isolated plastids and time-lapse recording on intact live tissue. Ann Bot 108:291–297

    CAS  PubMed  PubMed Central  Google Scholar 

  • Elmeer KES (2013) Factors regulating somatic embryogenesis in plants. Somatic embryogenesis and gene expression. Narosa Publishing House, New Delhi, pp 56–81

    Google Scholar 

  • Farinha T, Zsögön A, Peres LEP (2009) Breeding the tomato Micro-Tom model system for ornamental ValueXXIII international eucarpia symposium. Section Ornamentals: Colourful Breed Genet 836:215–220

    Google Scholar 

  • Fenn MA, Giovannoni JJ (2021) Phytohormones in fruit development and maturation. Plant J 105:446–458

    CAS  PubMed  Google Scholar 

  • Fraser P, Bramley P, Seymour G (2001) Effect of the Cnr mutation on carotenoid formation during tomato fruit ripening. Phytochemistry 58:75–79

    CAS  PubMed  Google Scholar 

  • Fujisawa M, Nakano T, Shima Y, Ito Y (2013) A large-scale identification of direct targets of the tomato MADS box transcription factor RIPENING INHIBITOR reveals the regulation of fruit ripening. Plant Cell 25:371–386

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fujisawa M, Shima Y, Higuchi N, Nakano T, Koyama Y, Kasumi T, Ito Y (2012) Direct targets of the tomato-ripening regulator RIN identified by transcriptome and chromatin immunoprecipitation analyses. Planta 235:1107–1122

    CAS  PubMed  Google Scholar 

  • Gao L, Zhao W, Qu H, Wang Q, Zhao L (2016) The yellow-fruited tomato 1 (yft1) mutant has altered fruit carotenoid accumulation and reduced ethylene production as a result of a genetic lesion in ETHYLENE INSENSITIVE2. Theor Appl Genet 129:717–728

    CAS  PubMed  Google Scholar 

  • Gent MP (2007) Effect of degree and duration of shade on quality of greenhouse tomato. HortScience 42:514–520

    Google Scholar 

  • Giovannoni JJ (2007) Fruit ripening mutants yield insights into ripening control. Curr Opin Plant Biol 10:283–289

    CAS  PubMed  Google Scholar 

  • Gonzali S, Mazzucato A, Perata P (2009) Purple as a tomato: towards high anthocyanin tomatoes. Trends Plant Sci 14:237–241

    CAS  PubMed  Google Scholar 

  • Gonzali S, Perata P (2021) Fruit colour and novel mechanisms of genetic regulation of pigment production in tomato fruits. Horticulturae 7:259

    Google Scholar 

  • Gould WA (2013) Tomato production, processing and technology. Elsevier

    Google Scholar 

  • Grandillo S, Ku H, Tanksley S (1999) Identifying the loci responsible for natural variation in fruit size and shape in tomato. Theor Appl Genet 99:978–987

    CAS  Google Scholar 

  • Hiei Y, Ohta S, Komari T, Kumashiro T (1994) Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J 6:271–282

    CAS  PubMed  Google Scholar 

  • Howitt CA, Pogson BJ (2006) Carotenoid accumulation and function in seeds and non-green tissues. Plant Cell Environ 29:435–445

    CAS  PubMed  Google Scholar 

  • Jaakola L, Poole M, Jones MO, Kämäräinen-Karppinen T, Koskimäki JJ, Hohtola A, Häggman H, Fraser PD, Manning K, King GJ (2010) A SQUAMOSA MADS box gene involved in the regulation of anthocyanin accumulation in bilberry fruits. Plant Physiol 153:1619–1629

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jan R, Asaf S, Numan M, Kim K-M (2021) Plant secondary metabolite biosynthesis and transcriptional regulation in response to biotic and abiotic stress conditions. Agronomy 11:968

    CAS  Google Scholar 

  • Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E (2012) A programmable dual-RNA–guided DNA endonuclease in adaptive bacterial immunity. Science 337:816–821

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jones C, Mes P, Myers J (2003) Characterization and inheritance of the Anthocyanin fruit (Aft) tomato. J Hered 94:449–456

    CAS  PubMed  Google Scholar 

  • Kachanovsky DE, Filler S, Isaacson T, Hirschberg J (2012) Epistasis in tomato color mutations involves regulation of phytoene synthase 1 expression by cis-carotenoids. Proc Natl Acad Sci 109:19021–19026

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kang B, Gu Q, Tian P, Xiao L, Cao H, Yang W (2014) A chimeric transcript containing Psy1 and a potential mRNA is associated with yellow flesh color in tomato accession PI 114490. Planta 240:1011–1021

    CAS  PubMed  Google Scholar 

  • Karlova R, Rosin FM, Busscher-Lange J, Parapunova V, Do PT, Fernie AR, Fraser PD, Baxter C, Angenent GC, de Maagd RA (2011) Transcriptome and metabolite profiling show that APETALA2a is a major regulator of tomato fruit ripening. Plant Cell 23:923–941

    CAS  PubMed  PubMed Central  Google Scholar 

  • Khandagale K, Nadaf A (2016) Genome editing for targeted improvement of plants. Plant Biotechnol Rep 10:327–343

    Google Scholar 

  • Khudairi AK (1972) The ripening of tomatoes: a molecular ecological approach to the physiology of fruit ripening. Am Sci 60:696–707

    CAS  Google Scholar 

  • Kiferle C, Fantini E, Bassolino L, Povero G, Spelt C, Buti S, Giuliano G, Quattrocchio F, Koes R, Perata P (2015) Tomato R2R3-MYB proteins SlANT1 and SlAN2: same protein activity, different roles. PLoS ONE 10:e0136365

    PubMed  PubMed Central  Google Scholar 

  • Knapp S (2002) Tobacco to tomatoes: a phylogenetic perspective on fruit diversity in the Solanaceae. J Exp Bot 53:2001–2022

    CAS  PubMed  Google Scholar 

  • Kramer MG, Redenbaugh K (1994) Commercialization of a tomato with an antisense polygalacturonase gene: The FLAVR SAVR™ tomato story. Euphytica 79:293–297

    Google Scholar 

  • Krikorian A (1982) Cloning higher plants from aseptically cultured tissues and cells. Biol Rev 57:151–218

    Google Scholar 

  • Kumar N, Reddy M (2011) In vitro plant propagation: a review. J For Environ Sci 27:61–72

    Google Scholar 

  • Kumari C, Sharma M, Kumar V, Sharma R, Sharma P, Kumar P, Irfan M (2022) Genome editing technology for genetic amelioration of fruits and vegetables for alleviating post-harvest loss. Bioengineering 9:176

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li C, Brant E, Budak H, Zhang B (2021) CRISPR/Cas: a Nobel Prize award-winning precise genome editing technology for gene therapy and crop improvement. J Zhejiang Un-Sci B 22:253–284

    CAS  Google Scholar 

  • Li M, Xia Q, Lv S, Tong J, Wang Z, Nie Q, Yang J (2022) Enhanced CO 2 capture for photosynthetic lycopene production in engineered Rhodopseudomonas palustris, a purple nonsulfur bacterium. Green Chem 24:7500–7518

    CAS  Google Scholar 

  • Li W, Zhang J, Sun H, Wang S, Chen K, Liu Y, Li H, Ma Y, Zhang Z (2018) FveRGA1, encoding a DELLA protein, negatively regulates runner production in Fragaria vesca. Planta 247:941–951

    CAS  PubMed  Google Scholar 

  • Lin Z, Hong Y, Yin M, Li C, Zhang K, Grierson D (2008) A tomato HD-Zip homeobox protein, LeHB-1, plays an important role in floral organogenesis and ripening. Plant J 55:301–310

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu YS, Gur A, Ronen G, Causse M, Damidaux R, Buret M, Hirschberg J, Zamir D (2003) There is more to tomato fruit colour than candidate carotenoid genes. Plant Biotechnol J 1:195–207

    CAS  PubMed  Google Scholar 

  • Lor VS, Starker CG, Voytas DF, Weiss D, Olszewski NE (2014) Targeted mutagenesis of the tomato PROCERA gene using transcription activator-like effector nucleases. Plant Physiol 166:1288–1291

    PubMed  PubMed Central  Google Scholar 

  • Luo J, Butelli E, Hill L, Parr A, Niggeweg R, Bailey P, Weisshaar B, Martin C (2008) AtMYB12 regulates caffeoyl quinic acid and flavonol synthesis in tomato: expression in fruit results in very high levels of both types of polyphenol. Plant J 56:316–326

    CAS  PubMed  Google Scholar 

  • Ma J-J, Chen X, Song Y-T, Zhang G-F, Zhou X-Q, Que S-P, Mao F, Pervaiz T, Lin J-X, Li Y (2021) MADS-box transcription factors MADS11 and DAL1 interact to mediate the vegetative-to-reproductive transition in pine. Plant Physiol 187:247–262

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ma X, Liu Y (2016) CRISPR/Cas9-based genome editing systems and the analysis of targeted genome mutations in plants. Yi Chuan=. Hereditas 38:118–125

    CAS  PubMed  Google Scholar 

  • Manning K, Tör M, Poole M, Hong Y, Thompson AJ, King GJ, Giovannoni JJ, Seymour GB (2006) A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat Genet 38:948–952

    CAS  PubMed  Google Scholar 

  • Martín-Pizarro C, Posé D (2018) Genome editing as a tool for fruit ripening manipulation. Front Plant Sci 9:1415

    PubMed  PubMed Central  Google Scholar 

  • Massa S, Pagliarello R, Cemmi A, Di Sarcina I, Bombarely A, Demurtas OC, Diretto G, Paolini F, Petzold HE, Bliek M (2022) Modifying anthocyanins biosynthesis in tomato hairy roots: a test bed for plant resistance to ionizing radiation and antioxidant properties in space. Front Plant Sci 13

  • Mathews H, Clendennen SK, Caldwell CG, Liu XL, Connors K, Matheis N, Schuster DK, Menasco D, Wagoner W, Lightner J (2003) Activation tagging in tomato identifies a transcriptional regulator of anthocyanin biosynthesis, modification, and transport. Plant Cell 15:1689–1703

    CAS  PubMed  PubMed Central  Google Scholar 

  • McCormick S, Niedermeyer J, Fry J, Barnason A, Horsch R, Fraley R (1986) Leaf disc transformation of cultivated tomato (L. esculentum) using Agrobacterium tumefaciens. Plant Cell Rep 5:81–84

    CAS  PubMed  Google Scholar 

  • Mooney M, Desnos T, Harrison K, Jones J, Carpenter R, Coen E (1995) Altered regulation of tomato and tobacco pigmentation genes caused by the delila gene of Antirrhinum. Plant J 7:333–339

    CAS  Google Scholar 

  • Muir SR, Collins GJ, Robinson S, Hughes S, Bovy A, Ric De Vos CHV, van Tunen AJ, Verhoeyen ME (2001) Overexpression of petunia chalcone isomerase in tomato results in fruit containing increased levels of flavonols. Nat Biotechnol 19:470–474

    CAS  PubMed  Google Scholar 

  • Munné-Bosch S, Vincent C (2019) Physiological mechanisms underlying fruit sunburn. Crit Rev Plant Sci 38:140–157

    Google Scholar 

  • Naing AH, Ai TN, Lim KB, Lee IJ, Kim CK (2018) Overexpression of Rosea1 from snapdragon enhances anthocyanin accumulation and abiotic stress tolerance in transgenic tobacco. Front Plant Sci 9:1070

    PubMed  PubMed Central  Google Scholar 

  • Namitha L, Gangaprasad A (2020) Exotic edible fruit trees conserved in the Thiruvanan-Thapuram Napier Museum and Zoological Park garden. Plant Arch 20:715–719

    Google Scholar 

  • Orsi B, Sestari I, Preczenhak AP, Tessmer MA, da Silva Souza MA, Hassimotto NMA, Kluge RA (2021) Allelic variations in the tomato carotenoid pathway lead to pleiotropic effects on fruit ripening and nutritional quality. Postharvest Biol Technol 181:111632

    CAS  Google Scholar 

  • Öztürk Hİ (2022) Morphological and molecular characterization of some tomato (Solanum lycopersicum L.) genotypes collected from Erzincan Province of Turkey. Mol Biol Rep 49:7111–7121

    PubMed  Google Scholar 

  • Pan IL, McQuinn R, Giovannoni JJ, Irish VF (2010) Functional diversification of AGAMOUS lineage genes in regulating tomato flower and fruit development. J Exp Bot 61:1795–1806

    CAS  PubMed  PubMed Central  Google Scholar 

  • Panchuk II, Volkov RA, Schöffl F (2002) Heat stress-and heat shock transcription factor-dependent expression and activity of ascorbate peroxidase in Arabidopsis. Plant Physiol 129:838–853

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pandit SS, Kulkarni RS, Chidley HG, Giri AP, Pujari KH, Köllner TG, Degenhardt J, Gershenzon J, Gupta VS (2009) Changes in volatile composition during fruit development and ripening of ‘Alphonso’mango. J Sci Food Agric 89:2071–2081

    CAS  Google Scholar 

  • Pankratov I, McQuinn R, Schwartz J, Bar E, Fei Z, Lewinsohn E, Zamir D, Giovannoni JJ, Hirschberg J (2016) Fruit carotenoid-deficient mutants in tomato reveal a function of the plastidial isopentenyl diphosphate isomerase (IDI 1) in carotenoid biosynthesis. Plant J 88:82–94

    CAS  PubMed  Google Scholar 

  • Petroni K, Tonelli C (2011) Recent advances on the regulation of anthocyanin synthesis in reproductive organs. Plant Sci 181:219–229

    CAS  PubMed  Google Scholar 

  • Polturak G, Aharoni A (2019) Advances and future directions in betalain metabolic engineering. New Phytologist 224:1472–1478

    PubMed  Google Scholar 

  • Povero G, Gonzali S, Bassolino L, Mazzucato A, Perata P (2011) Transcriptional analysis in high-anthocyanin tomatoes reveals synergistic effect of Aft and atv genes. J Plant Physiol 168:270–279

    CAS  PubMed  Google Scholar 

  • Qiu Z, Wang X, Gao J, Guo Y, Huang Z, Du Y (2016) The tomato Hoffman’s anthocyaninless gene encodes a bHLH transcription factor involved in anthocyanin biosynthesis that is developmentally regulated and induced by low temperatures. PLoS ONE 11:e0151067

    PubMed  PubMed Central  Google Scholar 

  • Racsko J, Schrader L (2012) Sunburn of apple fruit: historical background, recent advances and future perspectives. Crit Rev Plant Sci 31:455–504

    Google Scholar 

  • Rai MK, Shekhawat N (2014) Recent advances in genetic engineering for improvement of fruit crops. Plant Cell. Tissue Organ Culture (PCTOC) 116:1–15

    CAS  Google Scholar 

  • Ron M, Kajala K, Pauluzzi G, Wang D, Reynoso MA, Zumstein K, Garcha J, Winte S, Masson H, Inagaki S (2014) 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 166:455–469

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ronen G, Carmel-Goren L, Zamir D, Hirschberg J (2000) An alternative pathway to β-carotene formation in plant chromoplasts discovered by map-based cloning of Beta and old-gold color mutations in tomato. Proc Natl Acad Sci 97:11102–11107

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rosati C, Aquilani R, Dharmapuri S, Pallara P, Marusic C, Tavazza R, Bouvier F, Camara B, Giuliano G (2000) Metabolic engineering of beta-carotene and lycopene content in tomato fruit. Plant J 24:413–420

    CAS  PubMed  Google Scholar 

  • Rothan C, Diouf I, Causse M (2019) Trait discovery and editing in tomato. Plant J 97:73–90

    CAS  PubMed  Google Scholar 

  • Sangeetha J, Sarim KM, Thangadurai D, Gupta A, Mundaragi A, Sheth BP, Wani SA, Baqual MF, Habib H (2019) Nanoparticle-mediated plant gene transfer for precision farming and sustainable agricultureNanotechnology for agriculture. Springer, pp 263–284

    Google Scholar 

  • Scarano A, Butelli E, De Santis S, Cavalcanti E, Hill L, De Angelis M, Giovinazzo G, Chieppa M, Martin C, Santino A (2018) Combined dietary anthocyanins, flavonols, and stilbenoids alleviate inflammatory bowel disease symptoms in mice. Front Nutr 4:75

    PubMed  PubMed Central  Google Scholar 

  • Schwinn K, Venail J, Shang Y, Mackay S, Alm V, Butelli E, Oyama R, Bailey P, Davies K, Martin C (2006) A small family of MYB-regulatory genes controls floral pigmentation intensity and patterning in the genus Antirrhinum. Plant Cell 18:831–851

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shrawat AK, Armstrong CL (2018) Development and application of genetic engineering for wheat improvement. Crit Rev Plant Sci 37:335–421

    Google Scholar 

  • Singh P, Goyal G (2008) Dietary lycopene: its properties and anticarcinogenic effects. Compr Rev Food Sci Food Saf 7:255–270

    CAS  PubMed  Google Scholar 

  • Sinnott-Armstrong MA, Donoghue MJ, Jetz W (2021) Dispersers and environment drive global variation in fruit colour syndromes. Ecol Lett 24:1387–1399

    PubMed  Google Scholar 

  • Smita S, Rajwanshi R, Lenka SK, Katiyar A, Chinnusamy V, Bansal KC (2013) Expression profile of genes coding for carotenoid biosynthetic pathway during ripening and their association with accumulation of lycopene in tomato fruits. J Genet 92:363–368

    CAS  PubMed  Google Scholar 

  • Stanley L, Yuan Y-W (2019) Transcriptional regulation of carotenoid biosynthesis in plants: so many regulators, so little consensus. Front Plant Sci 10:1017

    PubMed  PubMed Central  Google Scholar 

  • Steyn W (2008) Prevalence and functions of anthocyanins in fruits. Anthocyanins:86–105

  • Steyn WJ, Wand S, Holcroft D, Jacobs G (2002) Anthocyanins in vegetative tissues: a proposed unified function in photoprotection. New Phytol 155:349–361

    CAS  PubMed  Google Scholar 

  • Steyn WJ, Wand SJ, Jacobs G, Rosecrance RC, Roberts SC (2009) Evidence for a photoprotective function of low-temperature-induced anthocyanin accumulation in apple and pear peel. Physiol Plant 136:461–472

    CAS  PubMed  Google Scholar 

  • Stommel JR (2007) Genetic enhancement of tomato fruit nutritive value. Genet Improve Solanaceous Crops 2:193–238

    CAS  Google Scholar 

  • Sun C, Deng L, Du M, Zhao J, Chen Q, Huang T, Jiang H, Li C-B, Li C (2020) A transcriptional network promotes anthocyanin biosynthesis in tomato flesh. Mol Plant 13:42–58

    CAS  PubMed  Google Scholar 

  • Sun H-J, Uchii S, Watanabe S, Ezura H (2006) A highly efficient transformation protocol for Micro-Tom, a model cultivar for tomato functional genomics. Plant Cell Physiol 47:426–431

    CAS  PubMed  Google Scholar 

  • Sun N, Zhao H (2013) Transcription activator-like effector nucleases (TALENs): a highly efficient and versatile tool for genome editing. Biotechnol Bioeng 110:1811–1821

    CAS  PubMed  Google Scholar 

  • Tadmor Y, King S, Levi A, Davis A, Meir A, Wasserman B, Hirschberg J, Lewinsohn E (2005) Comparative fruit colouration in watermelon and tomato. Food Res Int 38:837–841

    CAS  Google Scholar 

  • Tanaka Y, Sasaki N, Ohmiya A (2008) Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids. Plant J 54:733–749

    CAS  PubMed  Google Scholar 

  • Teixido AL, Fuzessy LF, Souza CS, Gomes IN, Kaminski LA, Oliveira PC, Maruyama PK (2022) Anthropogenic impacts on plant-animal mutualisms: a global synthesis for pollination and seed dispersal. Biol Conserv:266, 109461

  • Tominaga-Wada R, Nukumizu Y, Wada T (2013) Tomato (Solanum lycopersicum) homologs of TRIPTYCHON (SlTRY) and GLABRA3 (SlGL3) are involved in anthocyanin accumulation. Plant Signal Behav 8:e24575

    PubMed  PubMed Central  Google Scholar 

  • Traveset A, Heleno R, Nogales M (2014) The ecology of seed dispersal seeds: the ecology of regeneration in plant communities. CABI Wallingford UK, pp 62–93

    Google Scholar 

  • Valenta K, Nevo O (2020) The dispersal syndrome hypothesis: how animals shaped fruit traits, and how they did not. Funct Ecol 34:1158–1169

    Google Scholar 

  • Verhoeyen M, Bovy A, Collins G, Muir S, Robinson S, De Vos C, Colliver S (2002) Increasing antioxidant levels in tomatoes through modification of the flavonoid biosynthetic pathway. J Exp Bot 53:2099–2106

    CAS  PubMed  Google Scholar 

  • Voytas DF, Gao C (2014) Precision genome engineering and agriculture: opportunities and regulatory challenges. PLoS Biol 12:e1001877

    PubMed  PubMed Central  Google Scholar 

  • Wallace TC, Bailey RL, Blumberg JB, Burton-Freeman B, Chen CO, Crowe-White KM, Drewnowski A, Hooshmand S, Johnson E, Lewis R (2020) Fruits, vegetables, and health: a comprehensive narrative, umbrella review of the science and recommendations for enhanced public policy to improve intake. Crit Rev Food Sci Nutr 60:2174–2211

    CAS  PubMed  Google Scholar 

  • Walter MH, Strack D (2011) Carotenoids and their cleavage products: biosynthesis and functions. Nat Prod Rep 28:663–692

    CAS  PubMed  Google Scholar 

  • Willson MF, Whelan CJ (1990) The evolution of fruit color in fleshy-fruited plants. Am Nat 136:790–809

    Google Scholar 

  • Xie K, Yang Y (2019) A multiplexed CRISPR/Cas9 editing system based on the endogenous tRNA processing plant genome editing witH CRISPR systems. Springer, pp 63–73

    Google Scholar 

  • Xie Y, Zhang T, Huang X, Xu C (2022) A two-in-one breeding strategy boosts rapid utilization of wild species and elite cultivars. Plant Biotechnol J 20:800–802

    PubMed  PubMed Central  Google Scholar 

  • Yamamoto T, Kashojiya S, Kamimura S, Kameyama T, Ariizumi T, Ezura H, Miura K (2018) Application and development of genome editing technologies to the Solanaceae plants. Plant Physiol Biochem 131:37–46

    CAS  PubMed  Google Scholar 

  • Yang T, Ali M, Lin L, Li P, He H, Zhu Q, Sun C, Wu N, Zhang X, Huang T (2023) Recoloring tomato fruit by CRISPR/Cas9-mediated multiplex gene editing. Hortic Res 10(1):uhac214

    PubMed  Google Scholar 

  • Yang T, Deng L, Zhao W, Zhang R, Jiang H, Ye Z, Li C-B, Li C (2019) Rapid breeding of pink-fruited tomato hybrids using the CRISPR/Cas9 system. J Genet Genomics= Yi chuan xue bao 46:505-508

  • Yuan D, Chen J, Shen H, Yang W (2008) Genetics of flesh color and nucleotide sequence analysis of phytoene synthase gene 1 in a yellow-fruited tomato accession PI114490. Sci Hortic 118:20–24

    CAS  Google Scholar 

  • Zhang H, Zhang J, Lang Z, Botella JR, Zhu J-K (2017) Genome editing—principles and applications for functional genomics research and crop improvement. Crit Rev Plant Sci 36:291–309

    Google Scholar 

  • Zhang LJ, Buatois LA, Mángano MG (2022) Potential and problems in evaluating secular changes in the diversity of animal-substrate interactions at ichnospecies rank. Terra Nova 34:433–440

    Google Scholar 

  • Zhang Q (2021) Purple tomatoes, black rice and food security. Nat Rev Genet 22:414–414

    CAS  PubMed  Google Scholar 

  • Zhang Y, Butelli E, Alseekh S, Tohge T, Rallapalli G, Luo J, Kawar PG, Hill L, Santino A, Fernie AR (2015) Multi-level engineering facilitates the production of phenylpropanoid compounds in tomato. Nat Commun 6:1–11

    Google Scholar 

  • Zhang Y, Stommel JR (1999) 049 Development of molecular markers linked to high pigment (hp) and dark green (dg) loci in tomato. HortScience 34:449D–449

    Google Scholar 

  • Zhang Z-L, Shin M, Zou X, Huang J, T-hD H, Shen QJ (2009) A negative regulator encoded by a rice WRKY gene represses both abscisic acid and gibberellins signaling in aleurone cells. Plant Mol Biol 70:139–151

    CAS  PubMed  Google Scholar 

  • Zhao W, Gao L, Li Y, Wang M, Zhang L, Zhao L (2020) Yellow-fruited phenotype is caused by 573 bp insertion at 5'UTR of YFT1 allele in yft1 mutant tomato. Plant Sci 300:110637

    CAS  PubMed  Google Scholar 

  • Zhao W, Li Y, Fan S, Wen T, Wang M, Zhang L, Zhao L (2021) The transcription factor WRKY32 affects tomato fruit colour by regulating YELLOW FRUITED-TOMATO 1, a core component of ethylene signal transduction. J Exp Bot 72:4269–4282

    CAS  PubMed  Google Scholar 

  • Zhou M, Deng L, Guo S, Yuan G, Li C, Li C (2022) Alternative transcription and feedback regulation suggest that SlIDI1 is involved in tomato carotenoid synthesis in a complex way. Hortic Res 9. https://doi.org/10.1093/hr/uhab045

  • Zhu G, Wang S, Huang Z, Zhang S, Liao Q, Zhang C, Lin T, Qin M, Peng M, Yang C (2018) Rewiring of the fruit metabolome in tomato breeding. Cell 172(249-261):e212

    Google Scholar 

  • Zuluaga DL, Gonzali S, Loreti E, Pucciariello C, Degl’ Innocenti E, Guidi L, Alpi A, Perata P (2008) Arabidopsis thaliana MYB75/PAP1 transcription factor induces anthocyanin production in transgenic tomato plants. Funct Plant Biol 35:606–618

    CAS  PubMed  Google Scholar 

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Acknowledgements

We would like to express our gratitude to two anonymous reviewers for thoroughly reviewing our manuscript. Owing the space limitations, we sincerely regret individuals whose work we were unable to cite.

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M.N. drafted the manuscript. W.Z. and N.A. reviewed and helped in editing of the manuscript. L.Z. reviewed and supervised the manuscript. All authors have read and approved the final version of the manuscript.

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Correspondence to Lingxia Zhao.

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Naeem, M., Zhao, W., Ahmad, N. et al. Beyond green and red: unlocking the genetic orchestration of tomato fruit color and pigmentation. Funct Integr Genomics 23, 243 (2023). https://doi.org/10.1007/s10142-023-01162-5

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