Abstract
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This research reveals that the up-regulated expression of multiple capsaicinoid biosynthetic genes in pericarp tissue leads to the elevation of total capsaicinoid content in chili pepper fruit.
Abstract
Capsaicinoids are health-functional compounds that are produced uniquely in chili pepper fruits. A high capsaicinoid level is one of the major parameters determining the commercial quality and health-promoting properties of chili peppers. To investigate the mechanisms responsible for its high contents, we compared an extremely pungent cultivar ‘Trinidad Moruga Scorpion Yellow’ (MY) with other cultivars of different pungency levels (Fushimi-amanaga, Takanotsume, Red Habanero). Capsaicinoid concentrations were markedly higher in MY fruit (23.9 mg/g DW) than in other pungent cultivars including ‘Red Habanero’ (HB) fruit (14.3 mg/g DW). Comparative analysis of MY and HB reveals that both cultivars accumulated similar capsaicinoid concentrations in the placental septum, with that in the HB pericarp (1.8 mg/g DW) being markedly lower than that in the placental septum (69.1 mg/g DW). The capsaicinoid concentration in HB fruit is dependent on the placental septum, as reported in other accessions. Therefore, even though placental septum tissue contains high capsaicinoid concentrations, those in the pericarp and seeds attenuated its total content. In contrast, the MY pericarp exhibited a markedly higher concentration (23.2 mg/g DW). A qRT-PCR analysis revealed that multiple capsaicinoid biosynthetic pathway genes (Pun1, pAMT, KAS, and BCAT) were strongly up-regulated in placental septum of pungent cultivars. The genes were expressed exclusively in the MY pericarp, but were barely detected in the pericarps of other pungent cultivars. Collectively, the present study indicates that the up-regulated expression of these genes not only in placental septum but also in pericarp plays an important role in driving capsaicinoid accumulation in the whole fruit.






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- 4CL:
-
4-Coumaroyl-CoA ligase
- ACL:
-
Acyl carrier protein
- ACS:
-
Acyl-CoA synthetase
- BCAT:
-
Branched-chain amino acid transferase
- BCKDH:
-
Branched-chain α-ketoacid dehydrogenase
- C3H:
-
Coumaric acid 3-hydroxylase
- C4H:
-
Cinnamic acid 4-hydroxylase
- COMT:
-
Caffeic acid O-methyl transferase
- DAF:
-
Days after flowering
- FAT:
-
Acyl-ACP thioesterase
- HCT:
-
Hydroxycinnamoyl transferase
- KAS:
-
β-Ketoacyl-ACP synthase
- PAL:
-
Phenylalanine ammonia-lyase
- pAMT:
-
Putative aminotransferase
- qRT-PCR:
-
Quantitative reverse transcription-polymerase chain reaction
References
Aluru MR, Mazourek M, Landry LG, Curry J, Jahn M, O’Connell M (2003) Differential expression of fatty acid synthase genes, Acl, Fat and Kas, in Capsicum fruit. J Exp Bot 54:1655–1664
Arce-Rodríguez ML, Ochoa-Alejo N (2015) Silencing AT3 gene reduces the expression of pAmt, BCAT, Kas, and Acl genes involved in capsaicinoid biosynthesis in chili pepper fruits. Biol Plant 59:477–484
Aza-Gonzalez C, Nunez-Palenius HG, Ochoa-Alejo N (2011) Molecular biology of capsaicinoid biosynthesis in chili pepper (Capsicum spp.). Plant Cell Rep 30:695–706
Ben-Chaim A, Borovsky Y, Falise M, Mazourek M, Kang BC, Paran I, Jahn M (2006) QTL analysis for capsaicinoid content in Capsicum. Theor Appl Genet 113:1481–1490
Blum E, Mazourek M, O’Connell M, Curry J, Thorup T, Liu KD, Jahn M, Paran I (2003) Molecular mapping of capsaicinoid biosynthesis genes and quantitative trait loci analysis for capsaicinoid content in Capsicum. Theor Appl Genet 108:79–86
Bosland PW, Baral JB (2007) ‘Bhut Jolokia’—the world’s hottest known chile pepper is a putative naturally occurring interspecific hybrid. HortScience 42:222–224
Bosland PW, Votava EJ (2000) Peppers: vegetable and spice capsicums. CABI Publishing, New York
Bosland PW, Coon D, Reeves G (2012) ‘Trinidad Moruga Scorpion’ pepper is the world’s hottest measured chile pepper at more than two million Scoville heat units. Hort Technol 22:534–538
Bosland PW, Coon D, Cooke PH (2015) Novel formation of ectopic (nonplacental) capsaicinoid secreting vesicles on fruit walls explains the morphological mechanism for super-hot chile peppers. J Am Soc Hort Sci 140:253–256
Canto-Flick A, Balam-Uc E, Bello-Bello JJ, Lecona-Guzman C, Solís-Marroquin D, Aviles-Vinas S, Gomez-Uc E, Lopez-Puc G, Santana-Buzzy N, Iglesias-Andreu LG (2008) Capsaicinoids content in Habanero pepper (Capsicum chinense Jacq.): hottest known cultivars. HortScience 43:1344–1349
Curry J, Aluru M, Mendoza M, Nevarez J, Melendrez M, O’Connell MA (1999) Transcripts for possible capsaicinoid biosynthetic genes are differentially accumulated in pungent and non-pungent Capsicum spp. Plant Sci 148:47–57
Han K, Jeong HJ, Sung J, Keum YS, Cho MC, Kim JH, Kwon JK, Kim BD, Kang BC (2013) Biosynthesis of capsinoid is controlled by the Pun1 locus in pepper. Mol Breed 31:537–548
Iwai K, Suzuki T, Fujiwake H (1979) Formation and accumulation of pungent principles of hot pepper fruits, capsaicin and its analogues in Capsicum annuum var. annuum cv. Karayatsubusa at different growth stages after flowering. Agric Biol Chem 43:2493–2498
Keyhaninejad N, Curry J, Romero J, O’Connell MA (2014) Fruit specific variability in capsaicinoid accumulation and transcription of structural and regulatory genes in Capsicum fruit. Plant Sci 215–216:59–68
Kirii E, Goto T, Yoshida Y, Yasuba K, Tanaka Y (2016) Non-pungency in a Japanese Chili Pepper Landrace (Capsicum annuum) is Caused by a Novel Loss-of-function Pun1 Allele. The Hortic J. doi:10.2503/hortj.MI-148
Lang YQ, Kisaka H, Sugiyama R, Nomura K, Morita A, Watanabe T, Tanaka Y, Yazawa S, Miwa T (2009) Functional loss of pamt results in biosynthesis of capsinoids, capsaicinoid analogs, in Capsicum annuum cv. CH-19 sweet. Plant J 59:953–961
Luo XJ, Peng J, Li YJ (2011) Recent advances in the study on capsaicinoids and capsinoids. Eur J Pharmacol 650:1–7
Mazourek M, Pujar A, Borovsky Y, Paran I, Mueller L, Jahn MM (2009) A dynamic interface for capsaicinoid systems biology. Plant Physiol 150:1806–1821
Nelson EK, Dawson LE (1923) The constitution of capsaicin, the pungent principle of Capsicum. III. J Am Chem Soc 45:2179–2181
Pino J, Sauri-Duch E, Marbot R (2006) Changes in volatile compounds of Habanero chile pepper (Capsicum chinense Jack. cv. Habanero) at two ripening stages. Food Chem 94:394–398
Stewart C, Kang BC, Liu K, Mazourek M, Moore SL, Yoo EY, Kim BD, Paran I, Jahn MM (2005) The Pun1 gene for pungency in pepper encodes a putative acyltransferase. Plant J 42:675–688
Stewart C, Mazourek M, Stellari GM, O’Connell M, Jahn M (2007) Genetic control of pungency in C. chinense via the Pun1 locus. J Exp Bot 58:979–991
Suzuki T, Fujiwake H, Iwai K (1980) Intracellular localization of capsaicin and its analogues, capsaicinoid, in Capsicum fruit 1. Microscopic investigation of the structure of the placenta of Capsicum annuum var. annuum cv. Karayatsubusa. Plant Cell Physiol 21:839–853
Tanaka Y, Sonoyama T, Muraga Y, Koeda S, Goto T, Yoshida Y, Yasuba K (2015) Multiple loss-of-function putative aminotransferase alleles contribute to low pungency and capsinoid biosynthesis in Capsicum chinense. Mol Breed 35:142
Vogt T (2010) Phenylpropanoid biosynthesis. Mol Plant 3:2–20
Wahyuni Y, Ballester AR, Sudarmonowati E, Bino RJ, Bovy AG (2011) Metabolite biodiversity in pepper (Capsicum) fruits of thirty-two diverse accessions: variation in health-related compounds and implications for breeding. Phytochemistry 72:1358–1370
Wahyuni Y, Ballester AR, Tikunov Y, de Vos RCH, Pelgrom KTB, Maharijaya A, Sudarmonowati E, Bino RJ, Bovy AG (2013) Metabolomics and molecular marker analysis to explore pepper (Capsicum sp.) biodiversity. Metabolomics 9:130–144
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This study was supported by a Grant-in-Aid for Young Scientists (B) (No. 15K18640), Japan.
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Communicated by Q. Zhao.
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Tanaka, Y., Nakashima, F., Kirii, E. et al. Difference in capsaicinoid biosynthesis gene expression in the pericarp reveals elevation of capsaicinoid contents in chili peppers (Capsicum chinense). Plant Cell Rep 36, 267–279 (2017). https://doi.org/10.1007/s00299-016-2078-8
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DOI: https://doi.org/10.1007/s00299-016-2078-8

