Skip to main content
SpringerLink
Log in

Genetic tapestry of Capsicum fruit colors: a comparative analysis of four cultivated species

  • Original Article
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Key message

Genome-wide association study of color spaces across the four cultivated Capsicum spp. revealed a shared set of genes influencing fruit color, suggesting mechanisms and pathways across Capsicum species are conserved during the speciation. Notably, Cytochrome P450 of the carotenoid pathway, MYB transcription factor, and pentatricopeptide repeat-containing protein are the major genes responsible for fruit color variation across the Capsicum species.

Abstract

Peppers (Capsicum spp.) rank among the most widely consumed spices globally. Fruit color, serving as a determinant for use in food colorants and cosmeceuticals and an indicator of nutritional contents, significantly influences market quality and price. Cultivated Capsicum species display extensive phenotypic diversity, especially in fruit coloration. Our study leveraged the genetic variance within four Capsicum species (Capsicum baccatum, Capsicum chinense, Capsicum frutescens, and Capsicum annuum) to elucidate the genetic mechanisms driving color variation in peppers and related Solanaceae species. We analyzed color metrics and chromatic attributes (Red, Green, Blue, L*, a*, b*, Luminosity, Hue, and Chroma) on samples cultivated over six years (2015–2021). We resolved genomic regions associated with fruit color diversity through the sets of SNPs obtained from Genotyping by Sequencing (GBS) and genome-wide association study (GWAS) with a Multi-Locus Mixed Linear Model (MLMM). Significant SNPs with FDR correction were identified, within the Cytochrome P450, MYB-related genes, Pentatricopeptide repeat proteins, and ABC transporter family were the most common among the four species, indicating comparative evolution of fruit colors. We further validated the role of a pentatricopeptide repeat-containing protein (Chr01:31,205,460) and a cytochrome P450 enzyme (Chr08:45,351,919) via competitive allele-specific PCR (KASP) genotyping. Our findings advance the understanding of the genetic underpinnings of Capsicum fruit coloration, with developed KASP assays holding potential for applications in crop breeding and aligning with consumer preferences. This study provides a cornerstone for future research into exploiting Capsicum's diverse fruit color variation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Aguilar-Meléndez A, Morrell PL, Roose ML, Kim SC (2009) Genetic diversity and structure in semiwild and domesticated chiles (Capsicum annuum; Solanaceae) from Mexico. Am J Bot 96:1190–1202

    Article  PubMed  Google Scholar 

  • Aharoni A, De Vos CHR, Wein M, Sun ZK, Greco R, Kroon A, Mol JNM, O’Connell AP (2001) The strawberry FaMYB1 transcription factor suppresses anthocyanin and flavonol accumulation in transgenic tobacco. Plant J 28:319–332

    Article  CAS  PubMed  Google Scholar 

  • Ahmad N, Liu JY, Tian X, Noman M, Jameel A, Yao N, Dong YY, Wang N, Li XW, Wang FW, Liu XM, Li HY (2019) Overexpression of a novel cytochrome P450 promotes flavonoid biosynthesis and osmotic stress tolerance in transgenic arabidopsis. Genes. https://doi.org/10.3390/genes10100756

    Article  PubMed  PubMed Central  Google Scholar 

  • An JP, Wang XF, Li YY, Song LQ, Zhao LL, You CX, Hao YJ (2018) EIN3-LIKE1, MYB1, and ETHYLENE RESPONSE FACTOR3 act in a regulatory loop that synergistically modulates ethylene biosynthesis and anthocyanin accumulation. Plant Physiol 178:808–823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Azlan A, Sultana S, Huei CS, Razman MR (2022) Antioxidant, anti-obesity, nutritional and other beneficial effects of different chili pepper: a review. Molecules. https://doi.org/10.3390/molecules27030898

    Article  PubMed  PubMed Central  Google Scholar 

  • Ballester AR, Tikunov Y, Molthoff J, Grandillo S, Viquez-Zamora M, de Vos R, de Maagd RA, van Heusden S, Bovy AG (2016) Identification of loci affecting accumulation of secondary metabolites in tomato fruit of a Solanum lycopersicum × Solanum chmielewskii introgression line population. Front Plant Sci. https://doi.org/10.3389/fpls.2016.01428

    Article  PubMed  PubMed Central  Google Scholar 

  • Borevitz JO, Xia YJ, Blount J, Dixon RA, Lamb C (2000) Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell 12:2383–2393

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Borges RM (2015) Fruit and seed volatiles: multiple stage settings, actors and props in an evolutionary play. J Indian Inst Sci 95:93–104

    Google Scholar 

  • Borovsky Y, Oren-Shamir M, Ovadia R, De Jong W, Paran I (2004) The A locus that controls anthocyanin accumulation in pepper encodes a MYB transcription factor homologous to Anthocyanin2 of Petunia. Theor Appl Genet 109:23–29

    Article  CAS  PubMed  Google Scholar 

  • Borovsky Y, Paran I (2008) Chlorophyll breakdown during pepper fruit ripening in the chlorophyll retainer mutation is impaired at the homolog of the senescence-inducible stay-green gene. Theor Appl Genet 117:235–240

    Article  CAS  PubMed  Google Scholar 

  • Carrizo García C, Barfuss MH, Sehr EM, Barboza GE, Samuel R, Moscone EA, Ehrendorfer F (2016) Phylogenetic relationships, diversification and expansion of chili peppers (Capsicum, Solanaceae). Ann Bot 118:35–51

    Article  PubMed  PubMed Central  Google Scholar 

  • Chagne D, Kui LW, Espley RV, Volz RK, How NM, Rouse S, Brendolise C, Carlisle CM, Kumar S, De Silva N, Micheletti D, McGhie T, Crowhurst RN, Storey RD, Velasco R, Hellens RP, Gardiner SE, Allan AC (2013) An ancient duplication of apple MYB transcription factors is responsible for novel red fruit-flesh phenotypes. Plant Physiol 161:225–239

    Article  CAS  PubMed  Google Scholar 

  • Chen H, Ji H, Zhu S, Zhu K, Ye J, Deng X (2023) Carotenoid and transcriptome profiles of a novel citrus cultivar ‘Jinlegan’ reveal mechanisms of yellowish fruit formation. Hortic Adv 1:5

    Article  Google Scholar 

  • Chen ZJ, Yu L, Liu WJ, Zhang J, Wang N, Chen XS (2021) Research progress of fruit color development in apple (Malus domestica Borkh.). Plant Physiol Biochem 162:267–279

    Article  CAS  PubMed  Google Scholar 

  • Choudhury SR, Roy S, Nag A, Singh SK, Sengupta DN (2012) Characterization of an AGAMOUS-like MADS box protein, a probable constituent of flowering and fruit ripening regulatory system in banana. PLoS ONE. https://doi.org/10.1371/journal.pone.0044361

    Article  PubMed  PubMed Central  Google Scholar 

  • Christ B, Sussenbacher I, Moser S, Bichsel N, Egert A, Muller T, Krautler B, Hortensteiner S (2013) Cytochrome P450 CYP89A9 is involved in the formation of major chlorophyll catabolites during leaf senescence in arabidopsis. Plant Cell 25:1868–1880

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cingolani P (2022) Variant annotation and functional prediction: SnpEff. In: Ng C, Piscuoglio S (eds) Variant calling: methods and protocols. Springer US, New York, NY, pp 289–314

    Chapter  Google Scholar 

  • Coe KM, Ellison S, Senalik D, Dawson J, Simon P (2021) The influence of the Or and carotene hydroxylase genes on carotenoid accumulation in orange carrots Daucus carota (L.). Theor Appl Genet 134:3351–3362

    Article  CAS  PubMed  Google Scholar 

  • Craig KL, Tyers M (1999) The F-box: a new motif for ubiquitin dependent proteolysis in cell cycle regulation and signal transduction. Prog Biophys Mol Biol 72:299–328

    Article  CAS  PubMed  Google Scholar 

  • Darrigues A, Hall J, van der Knaap E, Francis DM, Dujmovic N, Gray S (2008) Tomato analyzer-color test: a new tool for efficient digital phenotyping. J Am Soc Hortic Sci 133:579–586

    Article  Google Scholar 

  • Deepa N, Kaur C, George B, Singh B, Kapoor HC (2007) Antioxidant constituents in some sweet pepper (Capsicum annuum L.) genotypes during maturity. Lwt-Food Sci Technol 40:121–129

    Article  CAS  Google Scholar 

  • Diao QN, Tian SB, Cao YY, Yao DW, Fan HW, Zhang YP (2023) Transcriptome analysis reveals association of carotenoid metabolism pathway with fruit color in melon. Sci Rep. https://doi.org/10.1038/s41598-023-31432-y

    Article  PubMed  PubMed Central  Google Scholar 

  • Docimo T, Francese G, Ruggiero A, Batelli G, De Palma M, Bassolino L, Toppino L, Rotino GL, Mennella G, Tucci M (2016) Phenylpropanoids accumulation in eggplant fruit: characterization of biosynthetic genes and regulation by a MYB transcription factor. Front Plant Sci 6:1233

    Article  PubMed  PubMed Central  Google Scholar 

  • Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SE (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE 6:e19379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eriksson EM, Bovy A, Manning K, Harrison L, Andrews J, De Silva J, Tucker GA, Seymour GB (2004) Effect of the colorless non-ripening mutation on cell wall biochemistry and gene expression during tomato fruit development and ripening. Plant Physiol 136:4184–4197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feder A, Burger J, Gao S, Lewinsohn E, Katzir N, Schaffer AA, Meir A, Davidovich-Rikanati R, Portnoy V, Gal-On A, Fei ZJ, Kashi Y, Tadmor Y (2015) A kelch domain-containing F-box coding gene negatively regulates flavonoid accumulation in muskmelon. Plant Physiol 169:1714–1726

    PubMed  PubMed Central  Google Scholar 

  • Ferik F, Ates D, Ercisli S, Erdogan A, Orhan E, Tanyolac MB (2022) Genome-wide association links candidate genes to fruit firmness, fruit flesh color, flowering time, and soluble solid content in apricot (Prunus armeniaca L.). Mol Biol Rep 49:5283–5291

    Article  CAS  PubMed  Google Scholar 

  • Fiol A, Garcia-Gomez BE, Jurado-Ruiz F, Alexiou K, Howad W, Aranzana MJ (2021) Characterization of japanese plum (Prunus salicina) PsMYB10 alleles reveals structural variation and polymorphisms correlating with fruit skin color. Front Plant Sci. https://doi.org/10.3389/fpls.2021.655267

    Article  PubMed  PubMed Central  Google Scholar 

  • Fournier-Level A, Le Cunff L, Gomez C, Doligez A, Ageorges A, Roux C, Bertrand Y, Souquet JM, Cheynier V, This P (2009) Quantitative genetic bases of anthocyanin variation in grape (Vitis vinifera L. ssp sativa) berry: a quantitative trait locus to quantitative trait nucleotide integrated study. Genetics 183:1127–1139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frank CA, Nelson RG, Simonne EH, Behe BK, Simonne AH (2001) Consumer preferences for color, price, and vitamin C content of bell peppers. HortScience 36:795–800

    Article  Google Scholar 

  • Galpaz N, Gonda I, Shem-Tov D, Barad O, Tzuri G, Lev S, Fei Z, Xu Y, Mao L, Jiao C (2018) Deciphering genetic factors that determine melon fruit-quality traits using RNA-Seq-based high-resolution QTL and eQTL mapping. Plant J 94:169–191

    Article  CAS  PubMed  Google Scholar 

  • Gonzali S, Perata P (2021) Fruit colour and novel mechanisms of genetic regulation of pigment production in tomato fruits. Horticulturae. https://doi.org/10.3390/horticulturae7080259

    Article  Google Scholar 

  • Han Z, Hu Y, Lv Y, Rose JK, Sun Y, Shen F, Wang Y, Zhang X, Xu X, Wu T (2018) Natural variation underlies differences in ETHYLENE RESPONSE FACTOR17 activity in fruit peel degreening. Plant Physiol 176:2292–2304

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He C, Holme J, Anthony J (2014) SNP genotyping: the KASP assay. In: Fleury D, Whitford R (eds) Crop breeding: methods and protocols. Springer New York, pp 75–86

    Chapter  Google Scholar 

  • He F, Mu L, Yan GL, Liang NN, Pan QH, Wang J, Reeves MJ, Duan CQ (2010) Biosynthesis of anthocyanins and their regulation in colored grapes. Molecules 15:9057–9091

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Howard LR, Talcott ST, Brenes CH, Villalon B (2000) Changes in phytochemical and antioxidant activity of selected pepper cultivars (Capsicum species) as influenced by maturity. J Agric Food Chem 48:1713–1720

    Article  CAS  PubMed  Google Scholar 

  • Hurtado-Hernandez H, Smith PG (1985) Inheritance of mature fruit color in Capsicum-ANNUUM-L. J Hered 76:211–213

    Article  Google Scholar 

  • Jang S-J, Jeong H-B, Jung A, Kang M-Y, Kim S, Ha S-H, Kwon J-K, Kang B-C (2020) Phytoene synthase 2 can compensate for the absence of PSY1 in the control of color in Capsicum fruit. J Exp Bot 71:3417–3427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jin HL, Martin C (1999) Multifunctionality and diversity within the plant MYB-gene family. Plant Mol Biol 41:577–585

    Article  CAS  PubMed  Google Scholar 

  • Kapoor L, Simkin AJ, Doss CGP, Siva R (2022a) Fruit ripening: dynamics and integrated analysis of carotenoids and anthocyanins. Bmc Plant Biol. https://doi.org/10.1186/s12870-021-03411-w

    Article  PubMed  PubMed Central  Google Scholar 

  • Kapoor L, Simkin AJ, Doss CGP, Siva R (2022b) Fruit ripening: dynamics and integrated analysis of carotenoids and anthocyanins. BMC Plant Biol 22:1–22

    Article  Google Scholar 

  • Kayesh E, Shangguan L, Korir NK, Sun X, Bilkish N, Zhang Y, Han J, Song C, Cheng Z-M, Fang J (2013) Fruit skin color and the role of anthocyanin. Acta Physiol Plant 35:2879–2890

    Article  CAS  Google Scholar 

  • Kiferle C, Fantini E, Bassolino L, Povero G, Spelt C, Buti S, Giuliano G, Quattrocchio F, Koes R, Perata P, Gonzali S (2015) Tomato R2R3-MYB proteins SlANT1 and SlAN2: same protein activity different roles. PLoS ONE. https://doi.org/10.1371/journal.pone.0136365

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim DS, Hwang BK (2014) An important role of the pepper phenylalanine ammonia-lyase gene (PAL1) in salicylic acid-dependent signalling of the defence response to microbial pathogens. J Exp Bot 65:2295–2306

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim S, Park J, Yeom SI, Kim YM, Seo E, Kim KT, Kim MS, Lee JM, Cheong K, Shin HS, Kim SB, Han K, Lee J, Park M, Lee HA, Lee HY, Lee Y, Oh S, Lee JH, Choi E, Lee SE, Jeon J, Kim H, Choi G, Song H, Lee SC, Kwon JK, Koo N, Hong Y, Kim RW, Kang WH, Huh JH, Kang BC, Yang TJ, Lee YH, Bennetzen JL, Choi D (2017) New reference genome sequences of hot pepper reveal the massive evolution of plant disease-resistance genes by retroduplication. Genome Biol. https://doi.org/10.1186/s13059-017-1341-9

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim S, Park M, Yeom SI, Kim YM, Lee JM, Lee HA, Seo E, Choi J, Cheong K, Kim KT, Jung K, Lee GW, Oh SK, Bae C, Kim SB, Lee HY, Kim SY, Kim MS, Kang BC, Jo YD, Yang HB, Jeong HJ, Kang WH, Kwon JK, Shin C, Lim JY, Park JH, Huh JH, Kim JS, Kim BD, Cohen O, Paran I, Suh MC, Lee SB, Kim YK, Shin Y, Noh SJ, Park J, Seo YS, Kwon SY, Kim HA, Park JM, Kim HJ, Choi SB, Bosland PW, Reeves G, Jo SH, Lee BW, Cho HT, Choi HS, Lee MS, Yu Y, Do Choi Y, Park BS, van Deynze A, Ashrafi H, Hill T, Kim WT, Pai HS, Ahn HK, Yeam I, Giovannoni JJ, Rose JKC, Sorensen I, Lee SJ, Kim RW, Choi IY, Choi BS, Lim JS, Lee YH, Choi D (2014) Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum species. Nat Genet 46:270

    Article  CAS  PubMed  Google Scholar 

  • Kraft KH, Brown CH, Nabhan GP, Luedeling E, Luna Ruiz JdJ, Coppens d’Eeckenbrugge G, Hijmans RJ, Gepts P (2014) Multiple lines of evidence for the origin of domesticated chili pepper, Capsicum annuum, in Mexico. Proc Natl Acad Sci 111:6165–6170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kui LW, Bolitho K, Grafton K, Kortstee A, Karunairetnam S, McGhie TK, Espley RV, Hellens RP, Allan AC (2010) An R2R3 MYB transcription factor associated with regulation of the anthocyanin biosynthetic pathway in Rosaceae. Bmc Plant Biol. https://doi.org/10.1186/1471-2229-10-50

    Article  Google Scholar 

  • Liu G-S, Li H-L, Grierson D, Fu D-Q (2022) NAC transcription factor family regulation of fruit ripening and quality: a review. Cells 11:525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu S, Zhang Q, Kollie L, Dong J, Liang Z (2023) Molecular networks of secondary metabolism accumulation in plants: current understanding and future challenges. Ind Crops Prod 201:116901

    Article  CAS  Google Scholar 

  • Mbanjo EGN, Kretzschmar T, Jones H, Ereful N, Blanchard C, Boyd LA, Sreenivasulu N (2020) The genetic basis and nutritional benefits of pigmented rice grain. Front Genet. https://doi.org/10.3389/fgene.2020.00229

    Article  PubMed  PubMed Central  Google Scholar 

  • McLeod L, Barchi L, Tumino G, Tripodi P, Salinier J, Gros C, Boyaci HF, Ozalp R, Borovsky Y, Schafleitner R, Barchenger D, Finkers R, Brouwer M, Stein N, Rabanus-Wallace MT, Giuliano G, Voorrips R, Paran I, Lefebvre V (2023) Multi-environment association study highlights candidate genes for robust agronomic quantitative trait loci in a novel worldwide Capsicum core collection. Plant J. https://doi.org/10.1111/tpj.16425

    Article  PubMed  Google Scholar 

  • Mendes ND, Goncalves E (2020) The role of bioactive components found in peppers. Trends Food Sci Technol 99:229–243

    Article  Google Scholar 

  • Meng X, Yang DY, Li XD, Zhao SY, Sui N, Meng QW (2015) Physiological changes in fruit ripening caused by overexpression of tomato SlAN2, an R2R3-MYB factor. Plant Physiol Biochem 89:24–30

    Article  CAS  PubMed  Google Scholar 

  • Moreno JC, Mi JN, Alagoz Y, Al-Babili S (2021) Plant apocarotenoids: from retrograde signaling to interspecific communication. Plant J 105:351–375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Munshell AH (1912) A pigment color system and notation. Am J Psychol 23:236–244

    Article  Google Scholar 

  • Nabi BG, Mukhtar K, Ahmed W, Manzoor MF, Ranjha MMAN, Kieliszek M, Bhat ZF, Aadil RM (2023) Natural pigments: anthocyanins, carotenoids, chlorophylls, and betalains as food colorants in food products. Food Biosci 52:102403

    Article  CAS  Google Scholar 

  • Nankar AN, Tringovska I, Grozeva S, Ganeva D, Kostova D (2020a) Tomato phenotypic diversity determined by combined approaches of conventional and high-throughput tomato analyzer phenotyping. Plants-Basel. https://doi.org/10.3390/plants9020197

    Article  PubMed  PubMed Central  Google Scholar 

  • Nankar AN, Tringovska I, Grozeva S, Todorova V, Kostova D (2020b) Application of high-throughput phenotyping tool Tomato Analyzer to characterize Balkan Capsicum fruit diversity. Sci Hortic. https://doi.org/10.1016/j.scienta.2019.108862

    Article  Google Scholar 

  • Natarajan P, Akinmoju TA, Nimmakayala P, Lopez-Ortiz C, Garcia-Lozano M, Thompson BJ, Stommel J, Reddy UK (2020) Integrated metabolomic and transcriptomic analysis to characterize cutin biosynthesis between low-and high-cutin genotypes of Capsicum chinense Jacq. Int J Mol Sci 21:1397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nimmakayala P, Lopez-Ortiz C, Shahi B, Abburi VL, Natarajan P, Kshetry AO, Shinde S, Davenport B, Stommel J, Reddy UK (2021) Exploration into natural variation for genes associated with fruit shape and size among Capsicum chinense collections. Genomics 113:3002–3014

    Article  CAS  PubMed  Google Scholar 

  • Park G, Shahwar D, Jang G, Shin J, Kwon G, Kim Y, Hong CO, Jin B, Kim H, Lee O, Park Y (2023) Identification of a novel locus C2 controlling canary yellow flesh color in watermelons. Front Genet. https://doi.org/10.3389/fgene.2023.1256627

    Article  PubMed  PubMed Central  Google Scholar 

  • Philippe F, Pelloux J, Rayon C (2017) Plant pectin acetylesterase structure and function: new insights from bioinformatic analysis. BMC Genomics. https://doi.org/10.1186/s12864-017-3833-0

    Article  PubMed  PubMed Central  Google Scholar 

  • Pickersgill B (1971) Relationships between weedy and cultivated forms in some species of chili peppers (genus Capsicum). Evolution 25:683–691

    PubMed  Google Scholar 

  • Qin C, Yu C, Shen Y, Fang X, Chen L, Min J, Cheng J, Zhao S, Xu M, Luo Y, Yang Y, Wu Z, Mao L, Wu H, Ling-Hu C, Zhou H, Lin H, Gonzalez-Morales S, Trejo-Saavedra DL, Tian H, Tang X, Zhao M, Huang Z, Zhou A, Yao X, Cui J, Li W, Chen Z, Feng Y, Niu Y, Bi S, Yang X, Li W, Cai H, Luo X, Montes-Hernandez S, Leyva-Gonzalez MA, Xiong Z, He X, Bai L, Tan S, Tang X, Liu D, Liu J, Zhang S, Chen M, Zhang L, Zhang L, Zhang Y, Liao W, Zhang Y, Wang M, Lv X, Wen B, Liu H, Luan H, Zhang Y, Yang S, Wang X, Xu J, Li X, Li S, Wang J, Palloix A, Bosland PW, Li Y, Krogh A, Rivera-Bustamante RF, Herrera-Estrella L, Yin Y, Yu J, Hu K, Zhang Z (2014) Whole-genome sequencing of cultivated and wild peppers provides insights into Capsicum domestication and specialization. Proc Natl Acad Sci USA 111:5135–5140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qin TF, Zhao P, Sun JL, Zhao YP, Zhang YX, Yang QY, Wang WP, Chen ZQ, Mai TF, Zou YY, Liu GX, Hao W (2021) Research progress of PPR proteins in RNA editing, stress response, plant growth and development. Front Genet. https://doi.org/10.3389/fgene.2021.765580

    Article  PubMed  PubMed Central  Google Scholar 

  • Robarts D, Wolfe A, Jourdan P (2012) Relationships among germplasm accessions of viola and phlox examined by analysis of flower color and morphology using tomato analyzer (TM) image analysis software. HortScience 47:S344–S344

    Google Scholar 

  • Rodriguez-Uribe L, Guzman I, Rajapakse W, Richins RD, O’Connell MA (2012) Carotenoid accumulation in orange-pigmented Capsicum annuum fruit, regulated at multiple levels. J Exp Bot 63:517–526

    Article  CAS  PubMed  Google Scholar 

  • Sathasivam R, Ki J-S (2018) A review of the biological activities of microalgal carotenoids and their potential use in healthcare and cosmetic industries. Mar Drugs 16:26

    Article  PubMed  PubMed Central  Google Scholar 

  • Schifferstein HNJ, Wehrle T, Carbon CC (2019) Consumer expectations for vegetables with typical and atypical colors: the case of carrots. Food Qual Prefer 72:98–108

    Article  Google Scholar 

  • Schreiber G, Reuveni M, Evenor D, Oren-Shamir M, Ovadia R, Sapir-Mir M, Bootbool-Man A, Nahon S, Shlomo H, Chen L, Levin I (2012) ANTHOCYANIN1 from Solanum chilense is more efficient in accumulating anthocyanin metabolites than its Solanum lycopersicum counterpart in association with the ANTHOCYANIN FRUIT phenotype of tomato. Theor Appl Genet 124:295–307

    Article  CAS  PubMed  Google Scholar 

  • Schulman BA, Carrano AC, Jeffrey PD, Bowen Z, Kinnucan ERE, Finnin MS, Elledge SJ, Harper JW, Pagano M, Pavietich NP (2000) Insights into SCF ubiquitin ligases from the structure of the Skp1-Skp2 complex. Nature 408:381–386

    Article  CAS  PubMed  Google Scholar 

  • Scossa F, Roda F, Tohge T, Georgiev MI, Fernie AR (2019) The hot and the colorful: understanding the metabolism, genetics and evolution of consumer preferred metabolic traits in pepper and related species. Crit Rev Plant Sci 38:339–381

    Article  CAS  Google Scholar 

  • Shibuya T, Nishiyama M, Kato K, Kanayama Y (2021) Characterization of the FLAVIN-BINDING, KELCH REPEAT, F-BOX 1 Homolog SlFKF1 in tomato as a model for plants with fleshy fruit. Int J Mol Sci. https://doi.org/10.3390/ijms22041735

    Article  PubMed  PubMed Central  Google Scholar 

  • Shumskaya M, Wurtzel ET (2013) The carotenoid biosynthetic pathway: thinking in all dimensions. Plant Sci 208:58–63

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sim SC, Durstewitz G, Plieske J, Wieseke R, Ganal MW, Van Deynze A, Hamilton JP, Buell CR, Causse M, Wijeratne S, Francis DM (2012) Development of a large SNP genotyping array and generation of high-density genetic maps in tomato. PLoS ONE 7:e40563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Soltabayeva A, Dauletova N, Serik S, Sandybek M, Omondi JO, Kurmanbayeva A, Srivastava S (2022) Receptor-like kinases (LRR-RLKs) in response of plants to biotic and abiotic stresses. Plants-Basel. https://doi.org/10.3390/plants11192660

    Article  PubMed  PubMed Central  Google Scholar 

  • Stommel JR, Dumm JM (2015) Coordinated regulation of biosynthetic and regulatory genes coincides with anthocyanin accumulation in developing eggplant fruit. J Am Soc Hortic Sci 140:129–135

    Article  CAS  Google Scholar 

  • Stommel JR, Lightbourn GJ, Winkel BS, Griesbach RJ (2009) transcription factor families regulate the anthocyanin biosynthetic pathway in Capsicum annuum. J Am Soc Hortic Sci 134:244–251

    Article  Google Scholar 

  • Subburaj S, Tu LH, Lee K, Park GS, Lee H, Chun JP, Lim YP, Park MW, McGregor C, Lee GJ (2020) A genome-wide analysis of the pentatricopeptide repeat (PPR) gene family and ppr-derived markers for flesh color in watermelon (Citrullus lanatus). Genes. https://doi.org/10.3390/genes11101125

    Article  PubMed  PubMed Central  Google Scholar 

  • Takos AM, Jaffe FW, Jacob SR, Bogs J, Robinson SP, Walker AR (2006) Light-induced expression of a MYB gene regulates anthocyanin biosynthesis in red apples. Plant Physiol 142:1216–1232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanaka Y, Brugliera F (2013) Flower colour and cytochromes P450. Philos Trans R Soc B-Biol Sci. https://doi.org/10.1098/rstb.2012.0432

    Article  Google Scholar 

  • Tong H, Nankar AN, Liu J, Todorova V, Ganeva D, Grozeva S, Tringovska I, Pasev G, Radeva-Ivanova V, Gechev T (2022) Genomic prediction of morphometric and colorimetric traits in solanaceous fruits. Hortic Res. https://doi.org/10.1093/hr/uhac072

    Article  PubMed  PubMed Central  Google Scholar 

  • Venkatesh J, Lee S-Y, Back S, Kim T-G, Kim GW, Kim J-M, Kwon J-K, Kang B-C (2023) Update on the genetic and molecular regulation of the biosynthetic pathways underlying pepper fruit color and pungency. Curr Plant Biol 35–36:100303

    Article  Google Scholar 

  • Villa-Rivera MG, Ochoa-Alejo N (2021) Transcriptional regulation of ripening in chili pepper fruits (Capsicum spp.). Int J Mol Sci. https://doi.org/10.3390/ijms222212151

    Article  PubMed  PubMed Central  Google Scholar 

  • Wahyuni Y, Ballester AR, Sudarmonowati E, Bino RJ, Bovy AG (2013) Secondary metabolites of Capsicum species and their importance in the human diet. J Nat Prod 76:783–793

    Article  CAS  PubMed  Google Scholar 

  • Walsh BM, Hoot SB (2001) Phylogenetic relationships of Capsicum (Solanaceae) using DNA sequences from two noncoding regions: the chloroplast atpB-rbcL spacer region and nuclear waxy introns. Int J Plant Sci 162:1409–1418

    Article  CAS  Google Scholar 

  • Wang L, Zhong Y, Liu J, Ma R, Miao Y, Chen W, Zheng J, Pang X, Wan H (2023) Pigment biosynthesis and molecular genetics of fruit color in pepper. Plants (basel). https://doi.org/10.3390/plants12112156

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang X, An Y, Xu P, Xiao J (2021a) Functioning of PPR proteins in organelle RNA metabolism and chloroplast biogenesis. Front Plant Sci 12:627501

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang XW, An YQ, Xu P, Xiao JW (2021b) Functioning of PPR proteins in organelle RNA metabolism and chloroplast biogenesis. Front Plant Sci. https://doi.org/10.3389/fpls.2021.627501

    Article  PubMed  PubMed Central  Google Scholar 

  • Weale ME (2010) Quality control for genome-wide association studies. In: Barnes MR, Breen G (eds) Genetic variation: methods and protocols. Springer, pp 341–372

    Chapter  Google Scholar 

  • Williams PM, Barkan A (2003) A chloroplast-localized PPR protein required for plastid ribosome accumulation. Plant J 36:675–686

    Article  CAS  PubMed  Google Scholar 

  • Wu B, Shen F, Chen CJ, Liu L, Wang X, Zheng WY, Deng Y, Wang T, Huang ZY, Xiao C, Zhou Q, Wang Y, Wu T, Xu XF, Han ZH, Zhang XZ (2021) Natural variations in a pectin acetylesterase gene, MdPAE10, contribute to prolonged apple fruit shelf life. Plant Genome. https://doi.org/10.1002/tpg2.20084

    Article  PubMed  Google Scholar 

  • Xiang Y, Yu Huang X, Zhao Y-W, Wang C-K, Sun Q, Hu D-G (2024) Role of an ATP binding cassette (ABC) transporter MdABCI17 in the anthocyanin accumulation of apple. Sci Hortic 323:112502

    Article  CAS  Google Scholar 

  • Xu J, Wang XY, Guo WZ (2015) The cytochrome P450 superfamily: key players in plant development and defense. J Integr Agric 14:1673–1686

    Article  CAS  Google Scholar 

  • Xu X, Zhang XB, Shi YF, Wang HM, Feng BH, Li XH, Huang QN, Song LX, Guo D, He Y, Wu JL (2016) A point mutation in an F-box domain-containing protein is responsible for brown hull phenotype in rice. Rice Sci 23:1–8

    Article  CAS  Google Scholar 

  • Zhou XS, Rao SM, Wrightstone E, Sun TH, Lui ACW, Welsch R, Li L (2022) Phytoene synthase: the key rate-limiting enzyme of carotenoid biosynthesis in plants. Front Plant Sci. https://doi.org/10.3389/fpls.2022.884720

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors thank Venkata Abburi and Alicia Talavera-Caro for field studies, technical assistance, and help with the analysis and compiling.

Funding

This study was supported by the National Institute of Food and Agriculture USDA-NIFA (grant no. 2019–38821-29064, 2023–38821-39807, and wvax-EA-Padma-2024) and the National Science Foundation: NSF Award Number 2318707.

Author information

Author notes

  1. Ambika Bhattarai and Padma Nimmakayala have contributed equally to this work.

Authors and Affiliations

  1. Gus R. Douglass Institute and Department of Biology, West Virginia State University, Institute, WV, USA

    Ambika Bhattarai, Padma Nimmakayala, Brittany Davenport, Purushothaman Natarajan, Krittika Tonapi, Sai Satish Kadiyala, Carlos Lopez-Ortiz, Lizbeth Ibarra-Muñoz & Umesh K. Reddy

  2. Laboratorio de Biorremediación, Facultad de Ciencias Biológicas, Universidad Autónoma de Coahuila, 27275, Torreon, Coahuila, Mexico

    Lizbeth Ibarra-Muñoz & Nagamani Balagurusamy

  3. Department of Biology, University of Texas Rio Grande Valley, Edinburg, TX, USA

    Manohar Chakrabarti

  4. Division of Plant & Soil Sciences, West Virginia University, Morgantown, WV, USA

    Vagner Benedito

  5. Lane Department of Computer Science and Electrical Engineering, West Virginia University, Morgantown, WV, 26506, USA

    Donald A. Adjeroh

Authors
  1. Ambika Bhattarai
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Padma Nimmakayala
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Brittany Davenport
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Purushothaman Natarajan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Krittika Tonapi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sai Satish Kadiyala
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Carlos Lopez-Ortiz
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Lizbeth Ibarra-Muñoz
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Manohar Chakrabarti
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Vagner Benedito
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Donald A. Adjeroh
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Nagamani Balagurusamy
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Umesh K. Reddy
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization, P.N., U.K.R., and N.B.; Data curation, A.B. and P. N.; Formal analysis, P.N., and A.B.; Funding acquisition, P.N., D.A., and U.K.R.; Investigation, A.B., B.D. and P.N.; Methodology, A.B., P.NA., K.T., C.L.-O., L.I.-M.; Project administration, P.N., and U.K.R.; Software, U.K.R, A.B., P.NA., S.S.K., and D.A.; Supervision, P.N., U.K.R. and N.B.; Validation, A.B., C.L.-O., L.I.-M.; Visualization, P.N., U.K.R.; Writing—original draft, A.B., C.L.-O., P.N., U.K.R., N.B., M.C., D.A., V.B.; Writing—review and editing, P.N., U.K.R., N.B., M.C., D.A., V.B.; All authors have read and agreed to the published version of the manuscript.

Corresponding authors

Correspondence to Padma Nimmakayala, Nagamani Balagurusamy or Umesh K. Reddy.

Ethics declarations

Conflicts of interest

The authors declare no conflict of interest.

Additional information

Communicated by Sanwen Huang.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 7100 KB)

Supplementary file2 (XLSX 130 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bhattarai, A., Nimmakayala, P., Davenport, B. et al. Genetic tapestry of Capsicum fruit colors: a comparative analysis of four cultivated species. Theor Appl Genet 137, 130 (2024). https://doi.org/10.1007/s00122-024-04635-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00122-024-04635-8

Search

Navigation