Genome-Wide Analysis of Fruit Color and Carotenoid Content in Capsicum Core Collection
Abstract
:1. Introduction
2. Results
2.1. Fruit Colors and Carotenoid Content Variations
2.2. Correlation and Principal Components Analysis
2.3. Genome-Wide Association Analysis
3. Discussion
4. Materials and Methods
4.1. Chemicals and Plant Material
4.2. Pepper Fruit Color Assessment and Analysis of Carotenoids
4.3. Genomic DNA (gDNA) Extraction
4.4. Library Preparation for Genotyping-by-Sequencing (GBS)
4.5. SNP Calling, Filtering, and Sequence Preprocessing
4.6. Genome-Wide Association Study (GWAS)
4.7. Statistical Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
- Tripodi, P.; Kumar, S. The Capsicum Crop: An Introduction. In The Capsicum Genome; Ramchiary, N., Kole, C., Eds.; Compendium of Plant Genomes; Springer International Publishing: Cham, Switzerland, 2019; pp. 1–8. ISBN 978-3-319-97216-9. [Google Scholar]
- Pereira-Dias, L.; Vilanova, S.; Fita, A.; Prohens, J.; Rodríguez-Burruezo, A. Genetic Diversity, Population Structure, and Relationships in a Collection of Pepper (Capsicum spp.) Landraces from the Spanish Centre of Diversity Revealed by Genotyping-by-Sequencing (GBS). Hortic. Res. 2019, 6, 54. [Google Scholar] [CrossRef] [PubMed]
- Sun, T.; Yuan, H.; Cao, H.; Yazdani, M.; Tadmor, Y.; Li, L. Carotenoid Metabolism in Plants: The Role of Plastids. Mol. Plant 2018, 11, 58–74. [Google Scholar] [CrossRef] [PubMed]
- Antonio, A.S.; Wiedemann, L.S.M.; Veiga Junior, V.F. The Genus Capsicum: A Phytochemical Review of Bioactive Secondary Metabolites. RSC Adv. 2018, 8, 25767–25784. [Google Scholar] [CrossRef] [PubMed]
- Baenas, N.; Belović, M.; Ilic, N.; Moreno, D.A.; García-Viguera, C. Industrial Use of Pepper (Capsicum annum L.) Derived Products: Technological Benefits and Biological Advantages. Food Chem. 2019, 274, 872–885. [Google Scholar] [CrossRef]
- Borovsky, Y.; Tadmor, Y.; Bar, E.; Meir, A.; Lewinsohn, E.; Paran, I. Induced Mutation in β-CAROTENE HYDROXYLASE Results in Accumulation of β-Carotene and Conversion of Red to Orange Color in Pepper Fruit. Theor. Appl. Genet. 2013, 126, 557–565. [Google Scholar] [CrossRef]
- Tian, S.-L.; Li, L.; Shah, S.N.M.; Gong, Z.-H. The Relationship between Red Fruit Colour Formation and Key Genes of Capsanthin Biosynthesis Pathway in Capsicum annuum. Biol. Plant 2015, 59, 507–513. [Google Scholar] [CrossRef]
- Venkatesh, J.; Lee, S.-Y.; Back, S.; Kim, T.-G.; Kim, G.W.; Kim, J.-M.; Kwon, J.-K.; Kang, B.-C. Update on the Genetic and Molecular Regulation of the Biosynthetic Pathways Underlying Pepper Fruit Color and Pungency. Curr. Plant Biol. 2023, 35–36, 100303. [Google Scholar] [CrossRef]
- Guzman, I.; Hamby, S.; Romero, J.; Bosland, P.W.; O’Connell, M.A. Variability of Carotenoid Biosynthesis in Orange Colored Capsicum spp. Plant Sci. 2010, 179, 49–59. [Google Scholar] [CrossRef]
- De Azevedo-Meleiro, C.H.; Rodriguez-Amaya, D.B. Qualitative and Quantitative Differences in the Carotenoid Composition of Yellow and Red Peppers Determined by HPLC-DAD-MS. J. Sep. Sci. 2009, 32, 3652–3658. [Google Scholar] [CrossRef]
- Liu, Y. The Impacts of Artificial Intelligence on Design. Landsc. Archit. Front. 2018, 6, 52. [Google Scholar] [CrossRef]
- Borovsky, Y.; Oren-Shamir, M.; Ovadia, R.; De Jong, W.; Paran, I. The A Locus That Controls Anthocyanin Accumulation in Pepper Encodes a MYB Transcription Factor Homologous to Anthocyanin2 of Petunia. Theor. Appl. Genet. 2004, 109, 23–29. [Google Scholar] [CrossRef] [PubMed]
- Lightbourn, G.J.; Griesbach, R.J.; Novotny, J.A.; Clevidence, B.A.; Rao, D.D.; Stommel, J.R. Effects of Anthocyanin and Carotenoid Combinations on Foliage and Immature Fruit Color of Capsicum annuum L. J. Hered. 2008, 99, 105–111. [Google Scholar] [CrossRef] [PubMed]
- Berry, H.M.; Rickett, D.V.; Baxter, C.J.; Enfissi, E.M.A.; Fraser, P.D. Carotenoid Biosynthesis and Sequestration in Red Chilli Pepper Fruit and Its Impact on Colour Intensity Traits. J. Exp. Bot. 2019, 70, 2637–2650. [Google Scholar] [CrossRef] [PubMed]
- Krinsky, N.I.; Johnson, E.J. Carotenoid Actions and Their Relation to Health and Disease. Mol. Asp. Med. 2005, 26, 459–516. [Google Scholar] [CrossRef]
- Tanumihardjo, S.A.; Russell, R.M.; Stephensen, C.B.; Gannon, B.M.; Craft, N.E.; Haskell, M.J.; Lietz, G.; Schulze, K.; Raiten, D.J. Biomarkers of Nutrition for Development (BOND)—Vitamin A Review. J. Nutr. 2016, 146, 1816S–1848S. [Google Scholar] [CrossRef]
- Buscemi, S.; Corleo, D.; Di Pace, F.; Petroni, M.L.; Satriano, A.; Marchesini, G. The Effect of Lutein on Eye and Extra-Eye Health. Nutrients 2018, 10, 1321. [Google Scholar] [CrossRef]
- Story, E.N.; Kopec, R.E.; Schwartz, S.J.; Harris, G.K. An Update on the Health Effects of Tomato Lycopene. Annu. Rev. Food Sci. Technol. 2010, 1, 189–210. [Google Scholar] [CrossRef]
- Kotake-Nara, E.; Miyashita, K.; Nagao, A.; Kushiro, M.; Zhang, H.; Sugawara, T. Carotenoids Affect Proliferation of Human Prostate Cancer Cells. J. Nutr. 2001, 131, 3303–3306. [Google Scholar] [CrossRef]
- Arimboor, R.; Natarajan, R.B.; Menon, K.R.; Chandrasekhar, L.P.; Moorkoth, V. Red Pepper (Capsicum annuum) Carotenoids as a Source of Natural Food Colors: Analysis and Stability—A Review. J. Food Sci. Technol. 2015, 52, 1258–1271. [Google Scholar] [CrossRef]
- Fayos, O.; Ochoa-Alejo, N.; De La Vega, O.M.; Savirón, M.; Orduna, J.; Mallor, C.; Barbero, G.F.; Garcés-Claver, A. Assessment of Capsaicinoid and Capsinoid Accumulation Patterns during Fruit Development in Three Chili Pepper Genotypes (Capsicum spp.) Carrying Pun1 and pAMT Alleles Related to Pungency. J. Agric. Food Chem. 2019, 67, 12219–12227. [Google Scholar] [CrossRef]
- Carvalho, A.V.; De Andrade Mattietto, R.; De Oliveira Rios, A.; De Almeida Maciel, R.; Moresco, K.S.; De Souza Oliveira, T.C. Bioactive Compounds and Antioxidant Activity of Pepper (Capsicum sp.) Genotypes. J. Food Sci. Technol. 2015, 52, 7457–7464. [Google Scholar] [CrossRef]
- Lefebvre, V.; Kuntz, M.; Camara, B.; Palloix, A. The Capsanthin-Capsorubin Synthase Gene: A Candidate Gene for the y Locus Controlling the Red Fruit Colour in Pepper. Plant Mol. Biol. 1998, 36, 785–789. [Google Scholar] [CrossRef] [PubMed]
- Huh, J.H.; Kang, B.C.; Nahm, S.H.; Kim, S.; Ha, K.S.; Lee, M.H.; Kim, B.D. A Candidate Gene Approach Identified Phytoene Synthase as the Locus for Mature Fruit Color in Red Pepper (Capsicum spp.). Theor. Appl. Genet. 2001, 102, 524–530. [Google Scholar] [CrossRef]
- Lang, Y.-Q.; Yanagawa, S.; Sasanuma, T.; Sasakuma, T. Orange Fruit Color in Capsicum Due to Deletion of Capsanthin-Capsorubin Synthesis Gene. Breed. Sci. 2004, 54, 33–39. [Google Scholar] [CrossRef]
- Hong, M.; Chi, Z.-H.; Wang, Y.-Q.; Tang, Y.-M.; Deng, Q.-X.; He, M.-Y.; Wang, R.-K.; He, Y.-Z. Expression of a Chromoplast-Specific Lycopene β-Cyclase Gene (CYC-B) is Implicated in Carotenoid Accumulation and Coloration in the Loquat. Biomolecules 2019, 9, 874. [Google Scholar] [CrossRef]
- Han, K.; Jeong, H.-J.; Yang, H.-B.; Kang, S.-M.; Kwon, J.-K.; Kim, S.; Choi, D.; Kang, B.-C. An Ultra-High-Density Bin Map Facilitates High-Throughput QTL Mapping of Horticultural Traits in Pepper (Capsicum annuum). DNA Res. 2016, 23, 81–91. [Google Scholar] [CrossRef]
- Nimmakayala, P.; Abburi, V.L.; Saminathan, T.; Alaparthi, S.B.; Almeida, A.; Davenport, B.; Nadimi, M.; Davidson, J.; Tonapi, K.; Yadav, L.; et al. Genome-Wide Diversity and Association Mapping for Capsaicinoids and Fruit Weight in Capsicum annuum L. Sci. Rep. 2016, 6, 38081. [Google Scholar] [CrossRef]
- Wu, L.; Wang, P.; Wang, Y.; Cheng, Q.; Lu, Q.; Liu, J.; Li, T.; Ai, Y.; Yang, W.; Sun, L.; et al. Genome-Wide Correlation of 36 Agronomic Traits in the 287 Pepper (Capsicum) Accessions Obtained from the SLAF-Seq-Based GWAS. Int. J. Mol. Sci. 2019, 20, 5675. [Google Scholar] [CrossRef]
- Fu, G.; Yu, S.; Wu, K.; Yang, M.; Altaf, M.A.; Wu, Z.; Deng, Q.; Lu, X.; Fu, H.; Wang, Z.; et al. Genome-Wide Association Study and Candidate Gene Identification for Agronomic Traits in 182 Upward-Growing Fruits of C. frutescens and C. annuum. Sci. Rep. 2024, 14, 14691. [Google Scholar] [CrossRef]
- Huang, X.; Wei, X.; Sang, T.; Zhao, Q.; Feng, Q.; Zhao, Y.; Li, C.; Zhu, C.; Lu, T.; Zhang, Z.; et al. Genome-Wide Association Studies of 14 Agronomic Traits in Rice Landraces. Nat. Genet. 2010, 42, 961–967. [Google Scholar] [CrossRef]
- Zhao, K.; Tung, C.-W.; Eizenga, G.C.; Wright, M.H.; Ali, M.L.; Price, A.H.; Norton, G.J.; Islam, M.R.; Reynolds, A.; Mezey, J.; et al. Genome-Wide Association Mapping Reveals a Rich Genetic Architecture of Complex Traits in Oryza Sativa. Nat. Commun. 2011, 2, 467. [Google Scholar] [CrossRef] [PubMed]
- Li, H.; Peng, Z.; Yang, X.; Wang, W.; Fu, J.; Wang, J.; Han, Y.; Chai, Y.; Guo, T.; Yang, N.; et al. Genome-Wide Association Study Dissects the Genetic Architecture of Oil Biosynthesis in Maize Kernels. Nat. Genet. 2013, 45, 43–50. [Google Scholar] [CrossRef] [PubMed]
- Liu, J.; He, Z.; Rasheed, A.; Wen, W.; Yan, J.; Zhang, P.; Wan, Y.; Zhang, Y.; Xie, C.; Xia, X. Genome-Wide Association Mapping of Black Point Reaction in Common Wheat (Triticum aestivum L.). BMC Plant Biol. 2017, 17, 220. [Google Scholar] [CrossRef] [PubMed]
- Tian, S.-L.; Li, L.; Chai, W.-G.; Shah, S.N.M.; Gong, Z.-H. Effects of Silencing Key Genes in the Capsanthin Biosynthetic Pathway on Fruit Color of Detached Pepper Fruits. BMC Plant Biol. 2014, 14, 314. [Google Scholar] [CrossRef]
- Sharoni, Y.; Linnewiel-Hermoni, K.; Khanin, M.; Salman, H.; Veprik, A.; Danilenko, M.; Levy, J. Carotenoids and Apocarotenoids in Cellular Signaling Related to Cancer: A Review. Mol. Nutr. Food Res. 2012, 56, 259–269. [Google Scholar] [CrossRef]
- Sporn, M.B.; Liby, K.T. Is Lycopene an Effective Agent for Preventing Prostate Cancer? Cancer Prev. Res. 2013, 6, 384–386. [Google Scholar] [CrossRef]
- Jeong, H.-B.; Jang, S.-J.; Kang, M.-Y.; Kim, S.; Kwon, J.-K.; Kang, B.-C. Candidate Gene Analysis Reveals That the Fruit Color Locus C1 Corresponds to PRR2 in Pepper (Capsicum frutescens). Front. Plant Sci. 2020, 11, 399. [Google Scholar] [CrossRef]
- Kahlau, S.; Bock, R. Plastid Transcriptomics and Translatomics of Tomato Fruit Development and Chloroplast-to-Chromoplast Differentiation: Chromoplast Gene Expression Largely Serves the Production of a Single Protein. Plant Cell 2008, 20, 856–874. [Google Scholar] [CrossRef]
- Egea, I.; Barsan, C.; Bian, W.; Purgatto, E.; Latche, A.; Chervin, C.; Bouzayen, M.; Pech, J.-C. Chromoplast Differentiation: Current Status and Perspectives. Plant Cell Physiol. 2010, 51, 1601–1611. [Google Scholar] [CrossRef]
- Barsan, C.; Zouine, M.; Maza, E.; Bian, W.; Egea, I.; Rossignol, M.; Bouyssie, D.; Pichereaux, C.; Purgatto, E.; Bouzayen, M.; et al. Proteomic Analysis of Chloroplast-to-Chromoplast Transition in Tomato Reveals Metabolic Shifts Coupled with Disrupted Thylakoid Biogenesis Machinery and Elevated Energy-Production Components. Plant Physiol. 2012, 160, 708–725. [Google Scholar] [CrossRef]
- Suzuki, M.; Takahashi, S.; Kondo, T.; Dohra, H.; Ito, Y.; Kiriiwa, Y.; Hayashi, M.; Kamiya, S.; Kato, M.; Fujiwara, M.; et al. Plastid Proteomic Analysis in Tomato Fruit Development. PLoS ONE 2015, 10, e0137266. [Google Scholar] [CrossRef] [PubMed]
- Haile, M.; Ro, N.; Ko, H.-C.; Oh, H.; Lee, G.-A. A Comprehensive Genome-Wide Association Study of Carotenoid and Capsaicinoid Contents in Capsicum chinense Germplasm. Int. J. Mol. Sci. 2023, 24, 13885. [Google Scholar] [CrossRef] [PubMed]
- Ko, H.-C.; Haile, M.; Lee, S.; Hwang, A.; Lee, G.-A.; Choi, Y.-M.; Hahn, B.-S.; Ro, N. Correlation of Carotenoids Content and ASTA Values of Pepper (Capsicum chinense) Genetic Resources. Horticulturae 2022, 8, 486. [Google Scholar] [CrossRef]
- Rodríguez-Rodríguez, E.; Sánchez-Prieto, M.; Olmedilla-Alonso, B. Assessment of Carotenoid Concentrations in Red Peppers (Capsicum annuum) under Domestic Refrigeration for Three Weeks as Determined by HPLC-DAD. Food Chem. X 2020, 6, 100092. [Google Scholar] [CrossRef] [PubMed]
- Bosland, P.W. Capsicums: Innovative Uses of an Ancient Crop. In Progress in New Crops; Janick, J., Ed.; ASHS Press: Arlington, TA, USA, 1996; pp. 479–487. [Google Scholar]
- Fernández-García, E.; Carvajal-Lérida, I.; Pérez-Gálvez, A. Carotenoids Exclusively Synthesized in Red Pepper (Capsanthin and Capsorubin) Protect Human Dermal Fibroblasts against UVB Induced DNA Damage. Photochem. Photobiol. Sci. 2016, 15, 1204–1211. [Google Scholar] [CrossRef] [PubMed]
- Jo, S.J.; Kim, J.W.; Choi, H.O.; Kim, J.H.; Kim, H.J.; Woo, S.H.; Han, B.H. Capsanthin Inhibits Both Adipogenesis in 3T3-L1 Preadipocytes and Weight Gain in High-Fat Diet-Induced Obese Mice. Biomol. Ther. 2017, 25, 329–336. [Google Scholar] [CrossRef]
- Mohd Hassan, N.; Yusof, N.A.; Yahaya, A.F.; Mohd Rozali, N.N.; Othman, R. Carotenoids of Capsicum Fruits: Pigment Profile and Health-Promoting Functional Attributes. Antioxidants 2019, 8, 469. [Google Scholar] [CrossRef]
- Subburaj, S.; Tu, L.; Lee, K.; Park, G.-S.; Lee, H.; Chun, J.-P.; Lim, Y.-P.; Park, M.-W.; McGregor, C.; Lee, G.-J. A Genome-Wide Analysis of the Pentatricopeptide Repeat (PPR) Gene Family and PPR-Derived Markers for Flesh Color in Watermelon (Citrullus lanatus). Genes 2020, 11, 1125. [Google Scholar] [CrossRef]
- Park, G.; Shahwar, D.; Jang, G.; Shin, J.; Kwon, G.; Kim, Y.; Hong, C.O.; Jin, B.; Kim, H.; Lee, O.; et al. Identification of a Novel Locus C2 Controlling Canary Yellow Flesh Color in Watermelons. Front. Genet. 2023, 14, 1256627. [Google Scholar] [CrossRef]
- Galpaz, N.; Gonda, I.; Shem-Tov, D.; Barad, O.; Tzuri, G.; Lev, S.; Fei, Z.; Xu, Y.; Mao, L.; Jiao, C.; et al. Deciphering Genetic Factors That Determine Melon Fruit-quality Traits Using RNA -Seq-based High-resolution QTL and eQTL Mapping. Plant J. 2018, 94, 169–191. [Google Scholar] [CrossRef]
- Eriksson, E.M.; Bovy, A.; Manning, K.; Harrison, L.; Andrews, J.; De Silva, J.; Tucker, G.A.; Seymour, G.B. Effect of the Colorless Non-Ripening Mutation on Cell Wall Biochemistry and Gene Expression during Tomato Fruit Development and Ripening. Plant Physiol. 2004, 136, 4184–4197. [Google Scholar] [CrossRef] [PubMed]
- Williams, P.M.; Barkan, A. A Chloroplast-localized PPR Protein Required for Plastid Ribosome Accumulation. Plant J. 2003, 36, 675–686. [Google Scholar] [CrossRef] [PubMed]
- Wang, X.; An, Y.; Xu, P.; Xiao, J. Functioning of PPR Proteins in Organelle RNA Metabolism and Chloroplast Biogenesis. Front. Plant Sci. 2021, 12, 627501. [Google Scholar] [CrossRef]
- Qin, T.; Zhao, P.; Sun, J.; Zhao, Y.; Zhang, Y.; Yang, Q.; Wang, W.; Chen, Z.; Mai, T.; Zou, Y.; et al. Research Progress of PPR Proteins in RNA Editing, Stress Response, Plant Growth and Development. Front. Genet. 2021, 12, 765580. [Google Scholar] [CrossRef] [PubMed]
- Bhattarai, A.; Nimmakayala, P.; Davenport, B.; Natarajan, P.; Tonapi, K.; Kadiyala, S.S.; Lopez-Ortiz, C.; Ibarra-Muñoz, L.; Chakrabarti, M.; Benedito, V.; et al. Genetic Tapestry of Capsicum Fruit Colors: A Comparative Analysis of Four Cultivated Species. Theor. Appl. Genet. 2024, 137, 130. [Google Scholar] [CrossRef] [PubMed]
- Mol, J.; Grotewold, E.; Koes, R. How Genes Paint Flowers and Seeds. Trends Plant Sci. 1998, 3, 212–217. [Google Scholar] [CrossRef]
- Chalker-Scott, L. Environmental Significance of Anthocyanins in Plant Stress Responses. Photochem. Photobiol. 1999, 70, 1–9. [Google Scholar] [CrossRef]
- Mink, P.J.; Scrafford, C.G.; Barraj, L.M.; Harnack, L.; Hong, C.-P.; Nettleton, J.A.; Jacobs, D.R. Flavonoid Intake and Cardiovascular Disease Mortality: A Prospective Study in Postmenopausal Women. Am. J. Clin. Nutr. 2007, 85, 895–909. [Google Scholar] [CrossRef]
- Koes, R.; Verweij, W.; Quattrocchio, F. Flavonoids: A Colorful Model for the Regulation and Evolution of Biochemical Pathways. Trends Plant Sci. 2005, 10, 236–242. [Google Scholar] [CrossRef]
- Hichri, I.; Barrieu, F.; Bogs, J.; Kappel, C.; Delrot, S.; Lauvergeat, V. Recent Advances in the Transcriptional Regulation of the Flavonoid Biosynthetic Pathway. J. Exp. Bot. 2011, 62, 2465–2483. [Google Scholar] [CrossRef]
- Kitamura, S.; Shikazono, N.; Tanaka, A. TRANSPARENT TESTA 19 Is Involved in the Accumulation of Both Anthocyanins and Proanthocyanidins in Arabidopsis. Plant J. 2004, 37, 104–114. [Google Scholar] [CrossRef] [PubMed]
- Marrs, K.A.; Alfenito, M.R.; Lloyd, A.M.; Walbot, V. A Glutathione S-Transferase Involved in Vacuolar Transfer Encoded by the Maize Gene Bronze-2. Nature 1995, 375, 397–400. [Google Scholar] [CrossRef] [PubMed]
- Alfenito, M.R.; Souer, E.; Goodman, C.D.; Buell, R.; Mol, J.; Koes, R.; Walbot, V. Functional Complementation of Anthocyanin Sequestration in the Vacuole by Widely Divergent Glutathione S-Transferases. Plant Cell 1998, 10, 1135–1149. [Google Scholar] [CrossRef] [PubMed]
- Sun, Y.; Li, H.; Huang, J.-R. Arabidopsis TT19 Functions as a Carrier to Transport Anthocyanin from the Cytosol to Tonoplasts. Mol. Plant 2012, 5, 387–400. [Google Scholar] [CrossRef]
- Zhao, J. Flavonoid Transport Mechanisms: How to Go, and with Whom. Trends Plant Sci. 2015, 20, 576–585. [Google Scholar] [CrossRef]
- Hu, B.; Zhao, J.; Lai, B.; Qin, Y.; Wang, H.; Hu, G. LcGST4 Is an Anthocyanin-Related Glutathione S-Transferase Gene in Litchi Chinensis Sonn. Plant Cell Rep. 2016, 35, 831–843. [Google Scholar] [CrossRef]
- Pérez-Díaz, R.; Madrid-Espinoza, J.; Salinas-Cornejo, J.; González-Villanueva, E.; Ruiz-Lara, S. Differential Roles for VviGST1, VviGST3, and VviGST4 in Proanthocyanidin and Anthocyanin Transport in Vitis Vinífera. Front. Plant Sci. 2016, 7, 1166. [Google Scholar] [CrossRef]
- Luo, H.; Dai, C.; Li, Y.; Feng, J.; Liu, Z.; Kang, C. Reduced Anthocyanins in Petioles Codes for a GST Anthocyanin Transporter That Is Essential for the Foliage and Fruit Coloration in Strawberry. J. Exp. Bot. 2018, 69, 2595–2608. [Google Scholar] [CrossRef]
- Jiang, S.; Chen, M.; He, N.; Chen, X.; Wang, N.; Sun, Q.; Zhang, T.; Xu, H.; Fang, H.; Wang, Y.; et al. MdGSTF6, Activated by MdMYB1, Plays an Essential Role in Anthocyanin Accumulation in Apple. Hortic. Res. 2019, 6, 40. [Google Scholar] [CrossRef]
- Welsch, R.; Maass, D.; Voegel, T.; DellaPenna, D.; Beyer, P. Transcription Factor RAP2.2 and Its Interacting Partner SINAT2: Stable Elements in the Carotenogenesis of Arabidopsis Leaves. Plant Physiol. 2007, 145, 1073–1085. [Google Scholar] [CrossRef]
- Xie, Q.; Guo, H.-S.; Dallman, G.; Fang, S.; Weissman, A.M.; Chua, N.-H. SINAT5 Promotes Ubiquitin-Related Degradation of NAC1 to Attenuate Auxin Signals. Nature 2002, 419, 167–170. [Google Scholar] [CrossRef] [PubMed]
- Park, B.S.; Sang, W.G.; Yeu, S.Y.; Choi, Y.D.; Paek, N.-C.; Kim, M.C.; Song, J.T.; Seo, H.S. Post-Translational Regulation of FLC Is Mediated by an E3 Ubiquitin Ligase Activity of SINAT5 in Arabidopsis. Plant Sci. 2007, 173, 269–275. [Google Scholar] [CrossRef]
- Park, B.S.; Eo, H.J.; Jang, I.-C.; Kang, H.-G.; Song, J.T.; Seo, H.S. Ubiquitination of LHY by SINAT5 Regulates Flowering Time and Is Inhibited by DET1. Biochem. Biophys. Res. Commun. 2010, 398, 242–246. [Google Scholar] [CrossRef] [PubMed]
- Nolan, T.M.; Brennan, B.; Yang, M.; Chen, J.; Zhang, M.; Li, Z.; Wang, X.; Bassham, D.C.; Walley, J.; Yin, Y. Selective Autophagy of BES1 Mediated by DSK2 Balances Plant Growth and Survival. Dev. Cell 2017, 41, 33–46.e7. [Google Scholar] [CrossRef] [PubMed]
- Wang, W.; Fan, Y.; Niu, X.; Miao, M.; Kud, J.; Zhou, B.; Zeng, L.; Liu, Y.; Xiao, F. Functional Analysis of the Seven in Absentia Ubiquitin Ligase Family in Tomato. Plant Cell Environ. 2018, 41, 689–703. [Google Scholar] [CrossRef]
- Qi, H.; Xia, F.-N.; Xie, L.-J.; Yu, L.-J.; Chen, Q.-F.; Zhuang, X.-H.; Wang, Q.; Li, F.; Jiang, L.; Xie, Q.; et al. TRAF Family Proteins Regulate Autophagy Dynamics by Modulating AUTOPHAGY PROTEIN6 Stability in Arabidopsis. Plant Cell 2017, 29, 890–911. [Google Scholar] [CrossRef]
- Zhang, C.; Hao, Z.; Ning, Y.; Wang, G.-L. SINA E3 Ubiquitin Ligases: Versatile Moderators of Plant Growth and Stress Response. Mol. Plant 2019, 12, 610–612. [Google Scholar] [CrossRef]
- Fu, J.; Wu, Q.; Wang, X.; Sun, J.; Liao, L.; Li, L.; Xu, Q. A Novel Histone Methyltransferase Gene CgSDG40 Positively Regulates Carotenoid Biosynthesis during Citrus Fruit Ripening1. J. Integr. Agric. 2024, 23, 2633–2648. [Google Scholar] [CrossRef]
- Cazzonelli, C.I.; Cuttriss, A.J.; Cossetto, S.B.; Pye, W.; Crisp, P.; Whelan, J.; Finnegan, E.J.; Turnbull, C.; Pogson, B.J. Regulation of Carotenoid Composition and Shoot Branching in Arabidopsis by a Chromatin Modifying Histone Methyltransferase, SDG8. Plant Cell 2009, 21, 39–53. [Google Scholar] [CrossRef]
- Liu, S.; Liu, M.; Cao, Y.; Xu, Y.; Liu, H.; Zhu, Q.; Zhang, X.; Luan, F. Identification of Chromosome Region and Candidate Genes for Canary-Yellow Flesh (Cyf) Locus in Watermelon (Citrullus lanatus). Plant Sci. 2023, 329, 111594. [Google Scholar] [CrossRef]
- Zhang, J.; Sun, H.; Guo, S.; Ren, Y.; Li, M.; Wang, J.; Yu, Y.; Zhang, H.; Gong, G.; He, H.; et al. ClZISO Mutation Leads to Photosensitive Flesh in Watermelon. Theor. Appl. Genet. 2022, 135, 1565–1578. [Google Scholar] [CrossRef] [PubMed]
- Kim, J.K.; Lee, S.Y.; Chu, S.M.; Lim, S.H.; Suh, S.-C.; Lee, Y.-T.; Cho, H.S.; Ha, S.-H. Variation and Correlation Analysis of Flavonoids and Carotenoids in Korean Pigmented Rice (Oryza sativa L.) Cultivars. J. Agric. Food Chem. 2010, 58, 12804–12809. [Google Scholar] [CrossRef] [PubMed]
- Lee, H.-Y.; Ro, N.-Y.; Jeong, H.-J.; Kwon, J.-K.; Jo, J.; Ha, Y.; Jung, A.; Han, J.-W.; Venkatesh, J.; Kang, B.-C. Genetic Diversity and Population Structure Analysis to Construct a Core Collection from a Large Capsicum Germplasm. BMC Genet. 2016, 17, 142. [Google Scholar] [CrossRef] [PubMed]
- Elshire, R.J.; Glaubitz, J.C.; Sun, Q.; Poland, J.A.; Kawamoto, K.; Buckler, E.S.; Mitchell, S.E. A Robust, Simple Genotyping-by-Sequencing (GBS) Approach for High Diversity Species. PLoS ONE 2011, 6, e19379. [Google Scholar] [CrossRef] [PubMed]
- De Donato, M.; Peters, S.O.; Mitchell, S.E.; Hussain, T.; Imumorin, I.G. Genotyping-by-Sequencing (GBS): A Novel, Efficient and Cost-Effective Genotyping Method for Cattle Using Next-Generation Sequencing. PLoS ONE 2013, 8, e62137. [Google Scholar] [CrossRef]
- Catchen, J.; Hohenlohe, P.A.; Bassham, S.; Amores, A.; Cresko, W.A. Stacks: An Analysis Tool Set for Population Genomics. Mol. Ecol. 2013, 22, 3124–3140. [Google Scholar] [CrossRef]
- Andrews, S. A Quality Control Tool for High Throughput Sequence Data. 2010. Available online: http://www.bioinformatics.babraham.ac.uk/projects/fastqc/ (accessed on 8 July 2019).
- Martin, M. Cutadapt Removes Adapter Sequences from High-Throughput Sequencing Reads. EMBnet J. 2011, 17, 10. [Google Scholar] [CrossRef]
- Bradbury, P.J.; Zhang, Z.; Kroon, D.E.; Casstevens, T.M.; Ramdoss, Y.; Buckler, E.S. TASSEL: Software for Association Mapping of Complex Traits in Diverse Samples. Bioinformatics 2007, 23, 2633–2635. [Google Scholar] [CrossRef]
Carotenoid | Mean | SE | SD | Minimum | Maximum | No. of Accessions with Measurable Pigment |
---|---|---|---|---|---|---|
α-carotene | 3.49 | 0.42 | 7.36 | 0 | 86.94 | 294 |
Antheraxanthin | 1.71 | 0.29 | 5.04 | 0 | 53.56 | 66 |
β-carotene | 36.62 | 2.22 | 38.88 | 0 | 272.15 | 304 |
β-cryptoxanthin | 63.7 | 3.66 | 64.06 | 0 | 476.23 | 296 |
Capsanthin | 239.12 | 11.79 | 206.22 | 0 | 1348.53 | 291 |
Capsorubin | 25.8 | 1.75 | 30.57 | 0 | 265.99 | 289 |
Lutein | 1.63 | 0.58 | 10.1 | 0 | 113.92 | 12 |
Violaxanthin | 3.76 | 1.1 | 19.17 | 0 | 182.58 | 106 |
Zeaxanthin | 63.25 | 3.36 | 58.76 | 0 | 352.25 | 284 |
Total Carotenoid | 439.06 | 19.75 | 345.52 | 7.09 | 2566.67 | 306 |
Chromosome | Genic | Intergenic | Number of SNPs |
---|---|---|---|
1 | 2 | 6 | 8 |
2 | 2 | 1 | 3 |
3 | 4 | 2 | 6 |
4 | 2 | 4 | 6 |
5 | 6 | 4 | 10 |
6 | 12 | 1 | 13 |
7 | 7 | 6 | 13 |
8 | 5 | 1 | 6 |
9 | 4 | 5 | 9 |
10 | 2 | 0 | 2 |
11 | 2 | 1 | 3 |
12 | 10 | 2 | 12 |
Total | 58 | 33 | 91 |
Trait | Chr. | Pos. | −log (p-Value) | Ref. | Alt | SNP Type | Protein | Minor Allele | Major Allele |
---|---|---|---|---|---|---|---|---|---|
Fruit color at mature stage | 2 | 167079497 | 6.66 | T | C | Genic | RING-type domain-containing protein | C | T |
3 | 137561221 | 6.00 | G | T | Intergenic | Intergenic | T | G | |
3 | 137561156 | 6.04 | A | G | Intergenic | Intergenic | G | A | |
6 | 200892457 | 7.20 | A | T | Genic | Pentatricopeptide repeat-containing protein | T | A | |
6 | 25789177 | 6.64 | G | A | Genic | PITH domain-containing protein | A | G | |
6 | 200623395 | 6.03 | C | T | Intergenic | Intergenic | T | C | |
7 | 250212419 | 6.13 | G | A | Intergenic | Intergenic | A | G | |
9 | 46177512 | 6.48 | T | A | Genic | Tropinone reductase 2 | A | T | |
9 | 41391568 | 6.18 | T | C | Genic | Beta carbonic anhydrase 5, chloroplastic | C | T | |
9 | 37619422 | 6.02 | C | T | Intergenic | Intergenic | T | C | |
9 | 51246107 | 6.04 | C | T | Genic | Putative glutathione S-transferase | T | C | |
12 | 243316298 | 6.58 | T | G | Genic | Mitochondrial proton/calcium exchanger protein | G | T | |
12 | 243316322 | 6.58 | T | G | Genic | Mitochondrial proton/calcium exchanger protein | G | T | |
12 | 243316335 | 6.58 | G | A | Genic | Mitochondrial proton/calcium exchanger protein | A | G | |
12 | 36410086 | 6.28 | A | C | Genic | Gamete expressed protein 1 | C | A |
Traits | Chr. | Pos. | −log (p-Value) | Ref. | Alt | SNP Type | Protein Feature |
---|---|---|---|---|---|---|---|
α-carotene | 1 | 69188981 | 6.32 | A | G | Genic | E3 ubiquitin-protein ligase SINAT2 |
2 | 139769588 | 6.64 | C | T | Genic | Protein SCAR1 (AtSCAR1) | |
3 | 257691563 | 7.83 | C | T | Genic | Sucrose synthase 6 (AtSUS6) | |
3 | 278759458 | 8.02 | T | G | Genic | DENN domain and WD repeat-containing protein SCD1 | |
3 | 282407208 | 10.25 | G | A | Genic | Hexokinase-1 | |
5 | 1431693 | 7.96 | C | A | Genic | Putative disease resistance protein RGA1 | |
5 | 212795785 | 6.16 | G | A | Genic | Ribosomal biogenesis protein LAS1L | |
6 | 7784015 | 7.98 | A | G | Genic | 3-oxoacyl-[acyl-carrier-protein] synthase, mitochondrial | |
6 | 152007017 | 7.93 | G | A | Genic | Molybdenum cofactor sulfurase (MCS) | |
6 | 236907247 | 9.77 | A | T | Genic | U-box domain-containing protein 13 | |
7 | 193979854 | 6.07 | A | G | Genic | Thymidylate kinase (AtTMPK) | |
8 | 90513554 | 7.77 | C | T | Genic | Mitochondrial carrier protein CoAc1 | |
8 | 139507673 | 9.86 | T | C | Genic | Ribosome biogenesis protein bms1 | |
9 | 151061309 | 9.84 | G | A | Genic | Protein SPA1-RELATED 3 | |
10 | 232860589 | 9.92 | C | T | Genic | Disease resistance protein At4g27190,2 | |
11 | 253614532 | 9.84 | C | A | Genic | Putative disease resistance RPP13-like protein 1 | |
12 | 37631709 | 9.79 | A | T | Genic | Pentatricopeptide repeat-containing protein, chloroplastic | |
Antheraxanthin | 1 | 1790608 | 7.04 | G | A | Genic | Transcription termination factor MTEF18, mitochondrial |
1 | 13687346 | 6.76 | A | T | Genic | tRNA N(3)-methylcytidine methyltransferase | |
1 | 105823683 | 6.02 | G | A | Genic | 1:Probable methyltransferase PMT2 | |
4 | 1032836 | 5.97 | C | T | Genic | Phosphatidylinositol 4-kinase alpha 1 | |
6 | 235401244 | 6.17 | G | A | Genic | Protein disulfide isomerase-like 1–4 | |
6 | 235401309 | 6.16 | G | A | Genic | Protein disulfide isomerase-like 1–4 | |
7 | 1570608 | 10.06 | C | G | Genic | CA.PGAv.1.6.scaffold1357.17 | |
7 | 15180043 | 6.72 | G | A | Genic | Chaperone protein DnaJ 2 | |
7 | 215963930 | 7.84 | G | T | Genic | Probable NADH dehydrogenase [ubiquinone] | |
8 | 139306996 | 6.65 | C | A | Genic | Peptide-N(4)-(N-acetyl-beta-glucosaminyl)asparagine amidase | |
10 | 980949 | 7.44 | G | A | Genic | Septin and tuftelin-interacting protein 1 homolog 1 | |
11 | 251812831 | 6.06 | G | A | Genic | Beta-glucosidase BoGH3B | |
12 | 242740510 | 8.09 | G | T | Genic | Disease resistance protein Roq1 | |
12 | 242740511 | 8.08 | C | T | Genic | Disease resistance protein Roq1 | |
β-carotene | 6 | 125911050 | 6.61 | A | G | Genic | Probably inactive leucine-rich repeat receptor-like protein kinase |
7 | 210903829 | 6.00 | G | A | Genic | Probable beta-1,3-galactosyltransferase 2 | |
β-cryptoxanthin | 1 | 69188981 | 6.94 | A | G | Genic | E3 ubiquitin-protein ligase SINAT2 |
3 | 260332995 | 7.65 | T | C | Genic | Chaperone protein dnaJ 49 | |
5 | 228154657 | 8.18 | C | A | Genic | Protein-tyrosine-phosphatase MKP1 | |
6 | 92442789 | 7.99 | C | T | Genic | Stamen-specific protein FIL1 | |
7 | 63490717 | 7.81 | A | G | Genic | Rop guanine nucleotide exchange factor 14 | |
8 | 124720627 | 7.89 | C | T | Genic | DEAD-box ATP-dependent RNA helicase 8 | |
12 | 160178786 | 7.87 | G | A | Genic | Protein MHF1 homolog (AtMHF1) | |
Capsanthin | 5 | 17846748 | 6.56 | T | C | Genic | Lignin-forming anionic peroxidase |
5 | 32192112 | 6.08 | G | C | Genic | Tobamovirus multiplication protein 3 | |
5 | 228154657 | 8.01 | C | A | Genic | Protein-tyrosine-phosphatase MKP1 | |
6 | 92442789 | 6.10 | C | T | Genic | Stamen-specific protein FIL1 | |
7 | 63490717 | 6.63 | A | G | Genic | Rop guanine nucleotide exchange factor 14 | |
8 | 124720627 | 6.10 | C | T | Genic | DEAD-box ATP-dependent RNA helicase 8 | |
12 | 160178786 | 6.24 | G | A | Genic | Protein MHF1 homolog | |
Capsorubin | 1 | 253857646 | 5.99 | C | T | Genic | Alanine--tRNA ligase |
4 | 2341870 | 6.15 | C | A | Genic | Receptor-like protein 19 | |
Zeaxanthin | 12 | 17593725 | 6.11 | C | T | Genic | Pleiotropic drug resistance protein 2 |
Total Carotenoid | 6 | 97491774 | 6.13 | G | C | Genic | Acid phosphatase 1 |
6 | 184116834 | 6.10 | C | T | Genic | Histone–lysine N-methyltransferase |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Ro, N.; Oh, H.; Ko, H.-C.; Yi, J.; Na, Y.-W.; Haile, M. Genome-Wide Analysis of Fruit Color and Carotenoid Content in Capsicum Core Collection. Plants 2024, 13, 2562. https://doi.org/10.3390/plants13182562
Ro N, Oh H, Ko H-C, Yi J, Na Y-W, Haile M. Genome-Wide Analysis of Fruit Color and Carotenoid Content in Capsicum Core Collection. Plants. 2024; 13(18):2562. https://doi.org/10.3390/plants13182562
Chicago/Turabian StyleRo, Nayoung, Hyeonseok Oh, Ho-Cheol Ko, Jungyoon Yi, Young-Wang Na, and Mesfin Haile. 2024. "Genome-Wide Analysis of Fruit Color and Carotenoid Content in Capsicum Core Collection" Plants 13, no. 18: 2562. https://doi.org/10.3390/plants13182562