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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

CaPSY1 gene plays likely the key role in carotenoid metabolism of pepper (Capsicum annuum) at ripening

Xiaochun Wei A B , Chunyang Meng A B , Yuxiang Yuan A , Ujjal Kumar Nath C , Yanyan Zhao A , Zhiyong Wang A , Shuangjuan Yang A , Lin Li A , Liujing Niu A , Qiuju Yao A , Fang Wei B D and Xiaowei Zhang https://orcid.org/0000-0003-0796-9247 A B D
+ Author Affiliations
- Author Affiliations

A Institute of Horticulture, Henan Academy of Agricultural Sciences, Postgraduate T&R Base of Zhengzhou University, Zhengzhou, 450002, China.

B School of Agricultural Sciences, Zhengzhou University, Zhengzhou, 450001, China.

C Department of Genetics and Plant Breeding, Bangladesh Agricultural University, Mymensingh 2202, Bangladesh.

D Corresponding authors. Email: fangwei@zzu.edu.cn; xiaowei5737@163.com

Functional Plant Biology 48(2) 141-155 https://doi.org/10.1071/FP19287
Submitted: 7 October 2019  Accepted: 11 August 2020   Published: 15 September 2020

Abstract

Phytoene synthase (PSY) is the first committed enzyme in carotenoid biosynthesis, which plays important role in ripen fruit colour. However, the roles of CaPSY genes are not explained detail in ripen pepper fruit colour. In this study, three CaPSY genes (CaPSY1, CaPSY2 and CaPSY3) were identified through basic local alignment search tool (BLAST) in pepper genome. Among them, CaPSY1 was predicted as putative candidate based on relative expression values using five developmental stages of fruit in Zunla-1 cultivar and also in ripen fruits of five contrasting pepper lines. The CaPSY1 was characterised functionally through virus-induced gene silencing (VIGS) in ripen fruits and overexpression in Arabidopsis thaliana (L.) Heynh. Silencing of CaPSY1 gene altered colour with increased lutein and decreased zeaxanthin content in pepper fruits. The transgenic Arabidopsis line CaPSY1 gene showed higher expression of PSY1 gene compared with WT and dwarf phenotype due to reduction of GA3 (gibberellic acid) and higher abscisic acid (ABA) content. Our results confirmed that CaPSY1 gene involved in carotenoid metabolism in ripen pepper fruit and provide clue to develop bright red coloured pepper lines through breeding.

Additional keywords: Capsicum spp., carotenoids, fruit ripening, gene silencing, gene expression.


References

Ahrazem O, Diretto G, Argandoña Picazo J, Fiore A, Rubio-Moraga Á, Rial C, Varela RM, Macías FA, Castillo R, Romano E, Gómez-Gómez L (2019) The specialized roles in carotenogenesis and apocarotenogenesis of the Phytoene Synthase gene family in saffron. Frontiers in Plant Science 10, 249-265
The specialized roles in carotenogenesis and apocarotenogenesis of the Phytoene Synthase gene family in saffron.Crossref | GoogleScholarGoogle Scholar | 30886624PubMed |

Aluru M, Xu Y, Guo R, Wang Z, Li S, White W, Wang K, Rodermel S (2008) Generation of transgenic maize with enhanced provitamin A content. Journal of Experimental Botany 59, 3551–3562.
Generation of transgenic maize with enhanced provitamin A content.Crossref | GoogleScholarGoogle Scholar | 18723758PubMed |

Ampomah-Dwamena C, Driedonks N, Lewis D, Shumskaya M, Chen X, Wurtzel ET, Espley RV, Allan AC (2015) The Phytoene Synthase gene family of apple (Malus × domestica) and its role in controlling fruit carotenoid content. BMC Plant Biology 15, 185
The Phytoene Synthase gene family of apple (Malus × domestica) and its role in controlling fruit carotenoid content.Crossref | GoogleScholarGoogle Scholar | 26215656PubMed |

Arango J, Wüst F, Beyer P, Welsch R (2010) Characterization of phytoene synthases from cassava and their involvement in abiotic stress-mediated responses. Planta 232, 1251–1262.
Characterization of phytoene synthases from cassava and their involvement in abiotic stress-mediated responses.Crossref | GoogleScholarGoogle Scholar | 20737168PubMed |

Armstrong GA (1997) Genetics of eubacterial carotenoid biosynthesis: a colorful tale. Annual Review of Microbiology 51, 629–659.
Genetics of eubacterial carotenoid biosynthesis: a colorful tale.Crossref | GoogleScholarGoogle Scholar | 9343362PubMed |

Bartley GE, Scolnik P (1993) cDNA cloning, expression during development, and genome mapping of PSY2, a second tomato gene encoding phytoene synthase. Journal of Biological Chemistry 268, 25718–25721.

Bent A (2006) Arabidopsis thaliana floral dip transformation method. In ‘Agrobacterium protocols’. pp. 87–104. (Humana Press: Totowa, NJ, USA)

Berry HM, Rickett DV, Baxter CJ, Enfissi EM, Fraser PD (2019) Carotenoid biosynthesis and sequestration in red chilli pepper fruit and its impact on colour intensity traits. Journal of Experimental Botany 70, 2637–2650.
Carotenoid biosynthesis and sequestration in red chilli pepper fruit and its impact on colour intensity traits.Crossref | GoogleScholarGoogle Scholar | 30820539PubMed |

Bjellqvist B, Basse B, Olsen E, Celis JE (1994) Reference points for comparisons of two-dimensional maps of proteins from different human cell types defined in a pH scale where isoelectric points correlate with polypeptide compositions. Electrophoresis 15, 529–539.
Reference points for comparisons of two-dimensional maps of proteins from different human cell types defined in a pH scale where isoelectric points correlate with polypeptide compositions.Crossref | GoogleScholarGoogle Scholar | 8055880PubMed |

Busch M, Seuter A, Hain R (2002) Functional analysis of the early steps of carotenoid biosynthesis in tobacco. Plant Physiology 128, 439–453.
Functional analysis of the early steps of carotenoid biosynthesis in tobacco.Crossref | GoogleScholarGoogle Scholar | 11842148PubMed |

Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020) TBtools, an integrative toolkit developed for interactive analyses of big biological data. Molecular Plant 13, 1194–1202.
TBtools, an integrative toolkit developed for interactive analyses of big biological data.Crossref | GoogleScholarGoogle Scholar | 32585190PubMed |

Chettry U, Chrungoo NK, Kulkarni K (2019) Comparative transcriptomics approach in elucidation of carotenoid biosynthesis regulation in grains of rice (Oryza sativa L.). Scientific Reports 9, 1631
Comparative transcriptomics approach in elucidation of carotenoid biosynthesis regulation in grains of rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 30733556PubMed |

Clotault J, Peltier D, Berruyer R, Thomas M, Briard M, Geoffriau E (2008) Expression of carotenoid biosynthesis genes during carrot root development. Journal of Experimental Botany 59, 3563–3573.
Expression of carotenoid biosynthesis genes during carrot root development.Crossref | GoogleScholarGoogle Scholar | 18757491PubMed |

Cunningham FX, Gantt E (1998) Genes and enzymes of carotenoid biosynthesis in plants. Annual Review of Plant physiology and Plant Molecular Biology 49, 557–583.
Genes and enzymes of carotenoid biosynthesis in plants.Crossref | GoogleScholarGoogle Scholar | 15012246PubMed |

Deng W, Wang Y, Liu Z, Cheng H, Xue Y (2014) HemI: a toolkit for illustrating heatmaps. PLoS One 9, e111988
HemI: a toolkit for illustrating heatmaps.Crossref | GoogleScholarGoogle Scholar | 25551554PubMed |

Dibari B, Murat F, Chosson A, Gautier V, Poncet C, Lecomte P, Mercier I, Bergès H, Pont C, Blanco A (2012) Deciphering the genomic structure, function and evolution of carotenogenesis related phytoene synthases in grasses. BMC Genomics 13, 221
Deciphering the genomic structure, function and evolution of carotenogenesis related phytoene synthases in grasses.Crossref | GoogleScholarGoogle Scholar | 22672222PubMed |

El-Gebali S, Mistry J, Bateman A, Eddy SR, Luciani A, Potter SC, Qureshi M, Richardson LJ, Salazar GA, Smart A (2019) The Pfam protein families database in 2019. Nucleic Acids Research 47, D427–D432.
The Pfam protein families database in 2019.Crossref | GoogleScholarGoogle Scholar | 30357350PubMed |

Fang J, Chai C, Qian Q, Li C, Tang J, Sun L, Huang Z, Guo X, Sun C, Liu M (2008) Mutations of genes in synthesis of the carotenoid precursors of ABA lead to pre‐harvest sprouting and photo‐oxidation in rice. The Plant Journal 54, 177–189.
Mutations of genes in synthesis of the carotenoid precursors of ABA lead to pre‐harvest sprouting and photo‐oxidation in rice.Crossref | GoogleScholarGoogle Scholar | 18208525PubMed |

Fantini E, Falcone G, Frusciante S, Giliberto L, Giuliano G (2013) Dissection of tomato lycopene biosynthesis through virus-induced gene silencing. Plant Physiology 163, 986–998.
Dissection of tomato lycopene biosynthesis through virus-induced gene silencing.Crossref | GoogleScholarGoogle Scholar | 24014574PubMed |

Fraser PD, Schuch W, Bramley PM (2000) Phytoene synthase from tomato (Lycopersicon esculentum) chloroplasts – partial purification and biochemical properties. Planta 211, 361–369.
Phytoene synthase from tomato (Lycopersicon esculentum) chloroplasts – partial purification and biochemical properties.Crossref | GoogleScholarGoogle Scholar | 10987554PubMed |

Fray RG, Wallace A, Fraser PD, Valero D, Hedden P, Bramley PM, Grierson D (1995) Constitutive expression of a fruit phytoene synthase gene in transgenic tomatoes causes dwarfism by redirecting metabolites from the gibberellin pathway. The Plant Journal 8, 693–701.
Constitutive expression of a fruit phytoene synthase gene in transgenic tomatoes causes dwarfism by redirecting metabolites from the gibberellin pathway.Crossref | GoogleScholarGoogle Scholar |

Gady AL, Vriezen WH, Van de Wal MH, Huang P, Bovy AG, Visser RG, Bachem CW (2012) Induced point mutations in the Phytoene Synthase 1 gene cause differences in carotenoid content during tomato fruit ripening. Molecular Breeding 29, 801–812.
Induced point mutations in the Phytoene Synthase 1 gene cause differences in carotenoid content during tomato fruit ripening.Crossref | GoogleScholarGoogle Scholar | 22408384PubMed |

Gallagher CE, Matthews PD, Li F, Wurtzel ET (2004) Gene duplication in the carotenoid biosynthetic pathway preceded evolution of the grasses. Plant Physiology 135, 1776–1783.
Gene duplication in the carotenoid biosynthetic pathway preceded evolution of the grasses.Crossref | GoogleScholarGoogle Scholar | 15247400PubMed |

Gasteiger E, Hoogland C, Gattiker A, Wilkins MR, Appel RD, Bairoch A (2005) Protein identification and analysis tools on the ExPASy server. In ‘The proteomics protocols handbook’. pp. 571–607. (Springer: Dordrecht, Netherlands)

Giuliano G (2017) Provitamin A biofortification of crop plants: a gold rush with many miners. Current Opinion in Biotechnology 44, 169–180.

Gómez-García MDR, Ochoa-Alejo N (2013) Biochemistry and molecular biology of carotenoid biosynthesis in chili peppers (Capsicum spp.). International Journal of Molecular Sciences 14, 19025–19053.
Biochemistry and molecular biology of carotenoid biosynthesis in chili peppers (Capsicum spp.).Crossref | GoogleScholarGoogle Scholar |

Ha S-H, Kim J-B, Park J-S, Lee S-W, Cho K-J (2007) A comparison of the carotenoid accumulation in capsicum varieties that show different ripening colours: deletion of the capsanthin-capsorubin synthase gene is not a prerequisite for the formation of a yellow pepper. Journal of Experimental Botany 58, 3135–3144.
A comparison of the carotenoid accumulation in capsicum varieties that show different ripening colours: deletion of the capsanthin-capsorubin synthase gene is not a prerequisite for the formation of a yellow pepper.Crossref | GoogleScholarGoogle Scholar | 17728301PubMed |

Hedden P (1993) Modern methods for the quantitative analysis of plant hormones. Annual Review of Plant Biology 44, 107–129.
Modern methods for the quantitative analysis of plant hormones.Crossref | GoogleScholarGoogle Scholar |

Hirschberg J (2001) Carotenoid biosynthesis in flowering plants. Current Opinion in Plant Biology 4, 210–218.
Carotenoid biosynthesis in flowering plants.Crossref | GoogleScholarGoogle Scholar | 11312131PubMed |

Hu B, Jin J, Guo A-Y, Zhang H, Luo J, Gao G (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31, 1296–1297.
GSDS 2.0: an upgraded gene feature visualization server.Crossref | GoogleScholarGoogle Scholar | 25504850PubMed |

Huang J-C, Zhong Y-J, Liu J, Sandmann G, Chen F (2013) Metabolic engineering of tomato for high-yield production of astaxanthin. Metabolic Engineering 17, 59–67.
Metabolic engineering of tomato for high-yield production of astaxanthin.Crossref | GoogleScholarGoogle Scholar | 23511430PubMed |

Huh J, Kang B, Nahm S, Kim S, Ha K, Lee M, Kim B (2001) A candidate gene approach identified phytoene synthase as the locus for mature fruit color in red pepper (Capsicum spp.). Theoretical and Applied Genetics 102, 524–530.
A candidate gene approach identified phytoene synthase as the locus for mature fruit color in red pepper (Capsicum spp.).Crossref | GoogleScholarGoogle Scholar |

Jeong HB, Kang MY, Jung A, Han K, Lee JH, Jo J, Lee HY, An JW, Kim S, Kang BC (2019) Single‐molecule real‐time sequencing reveals diverse allelic variations in carotenoid biosynthetic genes in pepper (Capsicum spp.). Plant Biotechnology Journal 17, 1081–1093.
Single‐molecule real‐time sequencing reveals diverse allelic variations in carotenoid biosynthetic genes in pepper (Capsicum spp.).Crossref | GoogleScholarGoogle Scholar | 30467964PubMed |

Ji K, Kai W, Zhao B, Sun Y, Yuan B, Dai S, Li Q, Chen P, Wang Y, Pei Y (2014) SlNCED1 and SlCYP707A2: key genes involved in ABA metabolism during tomato fruit ripening. Journal of Experimental Botany 65, 5243–5255.
SlNCED1 and SlCYP707A2: key genes involved in ABA metabolism during tomato fruit ripening.Crossref | GoogleScholarGoogle Scholar | 25039074PubMed |

Kachanovsky DE, Filler S, Isaacson T, Hirschberg J (2012) Epistasis in tomato color mutations involves regulation of Phytoene Synthase 1 expression by cis-carotenoids. Proceedings of the National Academy of Sciences of the United States of America 109, 19021–19026.
Epistasis in tomato color mutations involves regulation of Phytoene Synthase 1 expression by cis-carotenoids.Crossref | GoogleScholarGoogle Scholar | 23112190PubMed |

Kato M, Ikoma Y, Matsumoto H, Sugiura M, Hyodo H, Yano M (2004) Accumulation of carotenoids and expression of carotenoid biosynthetic genes during maturation in citrus fruit. Plant Physiology 134, 824–837.
Accumulation of carotenoids and expression of carotenoid biosynthetic genes during maturation in citrus fruit.Crossref | GoogleScholarGoogle Scholar | 14739348PubMed |

Kaur N, Pandey A, Kumar P, Pandey P, Kesarwani AK, Mantri SS, Awasthi P, Tiwari S (2017) Regulation of banana Phytoene Synthase (MaPSY) expression, characterization and their modulation under various abiotic stress conditions. Frontiers in Plant Science 8, 462
Regulation of banana Phytoene Synthase (MaPSY) expression, characterization and their modulation under various abiotic stress conditions.Crossref | GoogleScholarGoogle Scholar | 28421096PubMed |

Kim S, Park M, Yeom S-I, Kim Y-M, Lee JM, Lee H-A, Seo E, Choi J, Cheong K, Kim K-T, Jung K, Lee G-W, Oh S-K, Bae C, Kim S-B, Lee H-Y, Kim S-Y, Kim M-S, Kang B-C, Jo YD, Yang H-B, Jeong H-J, Kang W-H, Kwon J-K, Shin C, Lim JY, Park JH, Huh JH, Kim J-S, Kim B-D, Cohen O, Paran I, Suh MC, Lee SB, Kim Y-K, Shin Y, Noh S-J, Park J, Seo YS, Kwon S-Y, Kim HA, Park JM, Kim H-J, Choi S-B, Bosland PW, Reeves G, Jo S-H, Lee B-W, Cho H-T, Choi H-S, Lee M-S, Yu Y, Do Choi Y, Park B-S, van Deynze A, Ashrafi H, Hill T, Kim WT, Pai H-S, Ahn HK, Yeam I, Giovannoni JJ, Rose JKC, Sørensen I, Lee S-J, Kim RW, Choi I-Y, Choi B-S, Lim J-S, Lee Y-H, Choi D (2014) Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum species. Nature Genetics 46, 270–278.
Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum species.Crossref | GoogleScholarGoogle Scholar | 24441736PubMed |

Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for Bigger Datasets. Molecular Biology and Evolution 33, 1870–1874.
MEGA7: Molecular evolutionary genetics analysis version 7.0 for Bigger Datasets.Crossref | GoogleScholarGoogle Scholar | 27004904PubMed |

Lado J, Zacarías L, Rodrigo MJ (2016) Regulation of carotenoid biosynthesis during fruit development. In ‘Carotenoids in nature.’ pp. 161–198. (Springer: Cham, Switzerland)

Lalitha S (2000) Primer premier 5. Biotech Software & Internet Report 1, 270–272.
Primer premier 5.Crossref | GoogleScholarGoogle Scholar |

Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Research 30, 325–327.
PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences.Crossref | GoogleScholarGoogle Scholar | 11752327PubMed |

Li L, Yuan H (2013) Chromoplast biogenesis and carotenoid accumulation. Archives of Biochemistry and Biophysics 539, 102–109.
Chromoplast biogenesis and carotenoid accumulation.Crossref | GoogleScholarGoogle Scholar | 23851381PubMed | 23851381PubMed |

Li F, Tsfadia O, Wurtzel ET (2009) The phytoene synthase gene family in the grasses: subfunctionalization provides tissue-specific control of carotenogenesis. Plant Signaling & Behavior 4, 208–211.
The phytoene synthase gene family in the grasses: subfunctionalization provides tissue-specific control of carotenogenesis.Crossref | GoogleScholarGoogle Scholar |

Li Z, Wang S, Gui X-L, Chang X-B, Gong Z-H (2013) A further analysis of the relationship between yellow ripe-fruit color and the Capsanthin-Capsorubin Synthase gene in pepper (Capsicum sp.) indicated a new mutant variant in C. annuum and a tandem repeat structure in promoter region. PLoS One 8, e61996
A further analysis of the relationship between yellow ripe-fruit color and the Capsanthin-Capsorubin Synthase gene in pepper (Capsicum sp.) indicated a new mutant variant in C. annuum and a tandem repeat structure in promoter region.Crossref | GoogleScholarGoogle Scholar | 24391994PubMed | 24391994PubMed |

Lightbourn GJ, Griesbach RJ, Novotny JA, Clevidence BA, Rao DD, Stommel JR (2008) Effects of anthocyanin and carotenoid combinations on foliage and immature fruit color of Capsicum annuum L. Journal of Heredity 99, 105–111.
Effects of anthocyanin and carotenoid combinations on foliage and immature fruit color of Capsicum annuum L.Crossref | GoogleScholarGoogle Scholar | 18222931PubMed | 18222931PubMed |

Liu J-X, Chiou C-Y, Shen C-H, Chen P-J, Liu Y-C, Jian C-D, Shen X-L, Shen F-Q, Yeh K-W (2014) RNA interference-based gene silencing of phytoene synthase impairs growth, carotenoids, and plastid phenotype in Oncidium hybrid orchid. SpringerPlus 3, 478
RNA interference-based gene silencing of phytoene synthase impairs growth, carotenoids, and plastid phenotype in Oncidium hybrid orchid.Crossref | GoogleScholarGoogle Scholar | 25221736PubMed | 25221736PubMed |

Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method. Methods 25, 402–408.
Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method.Crossref | GoogleScholarGoogle Scholar | 11846609PubMed | 11846609PubMed |

Meier S, Tzfadia O, Vallabhaneni R, Gehring C, Wurtzel ET (2011) A transcriptional analysis of carotenoid, chlorophyll and plastidial isoprenoid biosynthesis genes during development and osmotic stress responses in Arabidopsis thaliana. BMC Systems Biology 5, 77
A transcriptional analysis of carotenoid, chlorophyll and plastidial isoprenoid biosynthesis genes during development and osmotic stress responses in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 21595952PubMed | 21595952PubMed |

Pandurangaiah S, Ravishankar KV, Shivashankar KS, Sadashiva AT, Pillakenchappa K, Narayanan SK (2016) Differential expression of carotenoid biosynthetic pathway genes in two contrasting tomato genotypes for lycopene content. Journal of Biosciences 41, 257–264.
Differential expression of carotenoid biosynthetic pathway genes in two contrasting tomato genotypes for lycopene content.Crossref | GoogleScholarGoogle Scholar | 27240986PubMed | 27240986PubMed |

Prado-Cabrero A, Beatty S, Howard A, Stack J, Bettin P, Nolan JM (2016) Assessment of lutein, zeaxanthin and meso-zeaxanthin concentrations in dietary supplements by chiral high-performance liquid chromatography. European Food Research and Technology 242, 599–608.
Assessment of lutein, zeaxanthin and meso-zeaxanthin concentrations in dietary supplements by chiral high-performance liquid chromatography.Crossref | GoogleScholarGoogle Scholar | 27069419PubMed | 27069419PubMed |

Qados AMA (2015) Effects of salicylic acid on growth, yield and chemical contents of pepper (Capsicum annuum L) plants grown under salt stress conditions. International Journal of Agriculture and Crop Sciences 8, 107–113.

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, González-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-Hernández S, Leyva-González 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 (2014a) Whole-genome sequencing of cultivated and wild peppers provides insights into Capsicum domestication and specialization. Proceedings of the National Academy of Sciences of the United States of America 111, 5135–5140.
Whole-genome sequencing of cultivated and wild peppers provides insights into Capsicum domestication and specialization.Crossref | GoogleScholarGoogle Scholar | 24591624PubMed | 24591624PubMed |

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, González-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-Hernández S, Leyva-González 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 (2014b) Whole-genome sequencing of cultivated and wild peppers provides insights into capsicum domestication and specialization. Proceedings of the National Academy of Sciences of the United States of America 111, 5135–5140.
Whole-genome sequencing of cultivated and wild peppers provides insights into capsicum domestication and specialization.Crossref | GoogleScholarGoogle Scholar | 24591624PubMed | 24591624PubMed |

Rodríguez‐Villalón A, Gas E, Rodríguez‐Concepción M (2009) Phytoene synthase activity controls the biosynthesis of carotenoids and the supply of their metabolic precursors in dark‐grown Arabidopsis seedlings. The Plant Journal 60, 424–435.
Phytoene synthase activity controls the biosynthesis of carotenoids and the supply of their metabolic precursors in dark‐grown Arabidopsis seedlings.Crossref | GoogleScholarGoogle Scholar | 19594711PubMed | 19594711PubMed |

Rozewicki J, Li S, Amada KM, Standley DM, Katoh K (2019) MAFFT-DASH: integrated protein sequence and structural alignment. Nucleic Acids Research 47, W5–W10.
MAFFT-DASH: integrated protein sequence and structural alignment.Crossref | GoogleScholarGoogle Scholar | 31062021PubMed | 31062021PubMed |

Shinozaki Y, Nicolas P, Fernandez-Pozo N, Ma Q, Evanich DJ, Shi Y, Xu Y, Zheng Y, Snyder SI, Martin LB (2018) High-resolution spatiotemporal transcriptome mapping of tomato fruit development and ripening. Nature Communications 9, 364
High-resolution spatiotemporal transcriptome mapping of tomato fruit development and ripening.Crossref | GoogleScholarGoogle Scholar | 29371663PubMed | 29371663PubMed |

Shumskaya M, Bradbury LMT, Monaco RR, Wurtzel ET (2012) Plastid localization of the key carotenoid enzyme phytoene synthase is altered by isozyme, allelic variation, and activity. The Plant Cell 24, 3725–3741.
Plastid localization of the key carotenoid enzyme phytoene synthase is altered by isozyme, allelic variation, and activity.Crossref | GoogleScholarGoogle Scholar | 23023170PubMed | 23023170PubMed |

Sieiro C, Poza M, De Miguel T, Villa T (2003) Genetic basis of microbial carotenogenesis. International Microbiology 6, 11–16.
Genetic basis of microbial carotenogenesis.Crossref | GoogleScholarGoogle Scholar | 12730708PubMed | 12730708PubMed |

Story EN, Kopec RE, Schwartz SJ, Harris GK (2010) An update on the health effects of tomato lycopene. Annual Review of Food Science and Technology 1, 189–210.
An update on the health effects of tomato lycopene.Crossref | GoogleScholarGoogle Scholar | 22129335PubMed | 22129335PubMed |

Sun T, Yuan H, Cao H, Yazdani M, Tadmor Y, Li L (2018) Carotenoid metabolism in plants: the role of plastids. Molecular Plant 11, 58–74.
Carotenoid metabolism in plants: the role of plastids.Crossref | GoogleScholarGoogle Scholar | 28958604PubMed | 28958604PubMed |

Tanaka Y, Sasaki N, Ohmiya A (2008) Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids. The Plant Journal 54, 733–749.
Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids.Crossref | GoogleScholarGoogle Scholar | 18476875PubMed | 18476875PubMed |

The Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485, 635–641.
The tomato genome sequence provides insights into fleshy fruit evolution.Crossref | GoogleScholarGoogle Scholar | 22660326PubMed | 22660326PubMed |

Tian S-L, Li L, Chai W-G, Shah SNM, Gong Z-H (2014) Effects of silencing key genes in the capsanthin biosynthetic pathway on fruit color of detached pepper fruits. BMC Plant Biology 14, 314
Effects of silencing key genes in the capsanthin biosynthetic pathway on fruit color of detached pepper fruits.Crossref | GoogleScholarGoogle Scholar | 25403855PubMed | 25403855PubMed |

Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar SK, Troggio M, Pruss D (2010) The genome of the domesticated apple (Malus× domestica Borkh.). Nature Genetics 42, 833–839.
The genome of the domesticated apple (Malus× domestica Borkh.).Crossref | GoogleScholarGoogle Scholar | 20802477PubMed | 20802477PubMed |

Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. Journal of Plant Physiology 144, 307–313.
The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution.Crossref | GoogleScholarGoogle Scholar |

Welsch R, Wüst F, Bär C, Al-Babili S, Beyer P (2008) A third phytoene synthase is devoted to abiotic stress-induced abscisic acid formation in rice and defines functional diversification of Phytoene Synthase genes. Plant Physiology 147, 367–380.
A third phytoene synthase is devoted to abiotic stress-induced abscisic acid formation in rice and defines functional diversification of Phytoene Synthase genes.Crossref | GoogleScholarGoogle Scholar | 18326788PubMed | 18326788PubMed |

Wurtzel ET (2019) Changing form and function through carotenoids and synthetic biology. Plant Physiology 179, 830–843.
Changing form and function through carotenoids and synthetic biology.Crossref | GoogleScholarGoogle Scholar | 30361256PubMed | 30361256PubMed |

Yoo HJ, Park WJ, Lee G-M, Oh C-S, Yeam I, Won D-C, Kim CK, Lee JM (2017) Inferring the genetic determinants of fruit colors in tomato by carotenoid profiling. Molecules 22, 764
Inferring the genetic determinants of fruit colors in tomato by carotenoid profiling.Crossref | GoogleScholarGoogle Scholar |

Yuan H, Zhang J, Nageswaran D, Li L (2015) Carotenoid metabolism and regulation in horticultural crops. Horticulture Research 2, 15036
Carotenoid metabolism and regulation in horticultural crops.Crossref | GoogleScholarGoogle Scholar | 26504578PubMed | 26504578PubMed |

Zhai S, Li G, Sun Y, Song J, Li J, Song G, Li Y, Ling H, He Z, Xia X (2016) Genetic analysis of Phytoene Synthase 1 (Psy1) gene function and regulation in common wheat. BMC Plant Biology 16, 228
Genetic analysis of Phytoene Synthase 1 (Psy1) gene function and regulation in common wheat.Crossref | GoogleScholarGoogle Scholar | 27769185PubMed | 27769185PubMed |

Zhang W, Ruan J, Ho THD, You Y, Yu T, Quatrano RS (2005) Cis-regulatory element based targeted gene finding: genome-wide identification of abscisic acid-and abiotic stress-responsive genes in Arabidopsis thaliana. Bioinformatics 21, 3074–3081.
Cis-regulatory element based targeted gene finding: genome-wide identification of abscisic acid-and abiotic stress-responsive genes in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 15890746PubMed | 15890746PubMed |