Genetic and molecular regulation of colour and pungency in Hot pepper (Capsicum spp): A review

MANISHA MANGAL; ARPITA SRIVASTAVA; B S TOMAR

doi:10.56093/ijas.v88i3.78389

Authors

MANISHA MANGAL Senior Scientist, ICAR-Indian Agricultural Research Institute, New Delhi 110 012
ARPITA SRIVASTAVA Scientist, ICAR-Indian Agricultural Research Institute, New Delhi 110 012
B S TOMAR Head, Division of Vegetable Science, ICAR-Indian Agricultural Research Institute, New Delhi 110 012

https://doi.org/10.56093/ijas.v88i3.78389

Keywords:

Capsaicin, Capsaicinoids, Capsicum, Carotenoids, Oleoresin

Abstract

Chilli (Capsicum spp) is an important horticultural crop both from its economic importance point of view and its nutritional value. It is an excellent source of natural colours and nutraceutical compounds. Chilli is a popular food ingredient in many parts of the world because of its two special attributes pungency and colour. It is pungent because of capsaicinoid alkaloids which get accumulated in the placenta of maturing fruits. The most abundant components of these compounds are capsaicin and dihydrocapsaicin. Capsaicinoids give a peppery flavour to meals and have various other interesting properties and applications such as antioxidant, antimutagenic and antitumoral activities. In addition, it possesses a number of pigments which impart it different colours. Various molecular explanations have been proposed for specific colour and pungency in peppers. An understanding of the regulation of the carotenoid as well as capsaicinoid pathways is necessary to manipulate these two traits in chilli. This article deals with the current state of knowledge of the molecular biology of these two traits in the genus Capsicum.

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References

Abraham-Juárez M R, Rocha-Granados M C, López M G, Rivera- Bustamante R F and Ochoa-Alejo N. 2008. Virus-induced silencing of Comt, pAmt and Kas genes results in a reduction of capsaicinoid accumulation in chili pepper fruits. Planta 227: 681–95. DOI: https://doi.org/10.1007/s00425-007-0651-7

Aluru M R, Mazourek M, Landry L G, Curry J, Jahn M and O’Connell M A. 2003. Differential expression of fatty acid synthase genes, Acl, Fat and Kas, in Capsicum fruit. Journal of Experimental Botany 54: 1655–64. DOI: https://doi.org/10.1093/jxb/erg176

Anon. 2009. Post harvest profile of chilli. Directorate of Marketing and Inspection, Ministry of agriculture, Department of agriculture and cooperation, GoI, Nagpur.

Arora R, Gill N S, Chauhan G and Rana A C. 2011. An overview about versatile molecule capsaicin. International Journal of Pharmaceutical Sciences and Drug Research 3(4): 280–6.

Bai C, Twyman R M, Farre G, Sanahuja G, Christou P, Capell T and Zhu C. 2011. A golden era: pro-vitamin A enhancement in diverse crops. In vitro Cellular and Developmental Biology Plant 47: 205–22. DOI: https://doi.org/10.1007/s11627-011-9363-6

Ben-Chaim A, Brodsky Y, Falise M, Mazourek M, Kang B C, Paran I and Jahn M. 2006. QTL analysis for capsaicinoid content in Capsicum. Theoretical and Applied Genetics 113: 1481–90. DOI: https://doi.org/10.1007/s00122-006-0395-y

Bennett D J and Kirby G W. 1968. Constitution and biosynthesis of capsaicin. J Chem Soc: 442–6. DOI: https://doi.org/10.1039/j39680000442

Billing J and Sherman P W. 1998. Antimicrobial functions of spices: why some like it hot. Quarterly Review of Biology 73: 3–49. DOI: https://doi.org/10.1086/420058

Blum E, Liu K, Mazourek M, Yoo E Y, Jahn M and Paran I. 2002. Molecular mapping of the C locus for presence of pungency in Capsicum. Genome 45: 702–5. DOI: https://doi.org/10.1139/g02-031

Blum E, Mazourek M, O’Connell M, Curry J, Thorup T, Liu K D, Jahn M and Paran I. 2003. Molecular mapping of capsaicinoid biosynthesis genes and quantitative trait loci analysis for capsaicinoid content in Capsicum. Theoretical and Applied Genetics 108: 79–86. DOI: https://doi.org/10.1007/s00122-003-1405-y

Borovsky Y, Tadmor Y, Bar E, Meir A, Lewinsohn E and Paran I. 2013. Induced mutation in β-carotene hydroxylase results in accumulation of β-carotene and conversion of red to orange color in pepper fruits. Theoretical and Applied Genetics 126: 557–65. DOI: https://doi.org/10.1007/s00122-012-2001-9

Bosland P W and Walker S J. 2010. Measuring chile pepper heat. Guide-237, New Mexico State University, http://aces.nmsu.edu/pubs/_h/h-237.pdf.

Bouvier F, Backhaus R A and Camara B. 1998. Induction and control of chromoplast-specific carotenoid genes by oxidative stress. Journal of Biological Chemistry 273: 30651–9. DOI: https://doi.org/10.1074/jbc.273.46.30651

Bouvier F, d’Harlingue A, Hugueney P, Marin E, Marion-Poll A and Camara B. 1996. Xanthophyll biosynthesis: cloning, expression, functional reconstitution, and regulation of b-cyclohexenyl carotenoid epoxidase from pepper (Capsicum annuum). Journal of Biological Chemistry 271: 28861–267. DOI: https://doi.org/10.1074/jbc.271.46.28861

Caterina M J, Schumacher M A, Tominaga M, Rosen T A, Levine J D and Julius D. 1997. The capsaicin receptor: A heat-activated ion channel in the pain pathway. Nature 389: 816–24. DOI: https://doi.org/10.1038/39807

Curry J, Aluru M, Mendoza M, Nevarez J, Melendrez M and O’Connell M A. 1999. Transcripts for possible capsaicinoid biosynthetic genes are differentially accumulated in pungent and non-pungent Capsicum spp. Plant Science 148: 47–57. DOI: https://doi.org/10.1016/S0168-9452(99)00118-1

Deli J, Molnar P, Matus Z and Toth G. 2001. Carotenoid composition in the fruits of red paprika (Capsicum annuum var. lycopersiciforme rubrum) during ripening: biosynthesis of carotenoids in red paprika. Journal of Agricultural and Food Chemistry 49: 1517–23. DOI: https://doi.org/10.1021/jf000958d

Della Penna D and Pogson B J. 2006. Vitamin synthesis in plants: tocopherols and carotenoids. Annual Review of Plant Biology 57: 711–38. DOI: https://doi.org/10.1146/annurev.arplant.56.032604.144301

Deshpande R B. 1935. Studies in Indian chillies: 4. Inheritance of pungency in Capsicum annuum L. Indian Journal of Agricultural Sciences 5: 513–6.

Diretto G, Al-Babili S, Tavazza R, Scossa F, Papacchioli V, Migliore M, Beyer P and Giuliano G. 2010. Transcriptional-metabolic networks in b-carotene-enriched potato tubers: the long and winding road to the golden phenotype. Plant Physiology 154: 899–912. DOI: https://doi.org/10.1104/pp.110.159368

Estabrook E M and Senguptagopalan C. 1991. Differential expression of phenylalanine ammonia-lyase and chalcone synthase during soybean nodule development. Plant Cell 3: 299–308. DOI: https://doi.org/10.1105/tpc.3.3.299

Fahrendorf T and Dixon R A. 1993. Stress responses in alfalfa (Medicago sativa L).18. Molecular-cloning and expression of the elicitorinducible cinnamate 4-hydroxylase cytochrome-P450. Archives of Biochemistry and Biophysics 305: 509–15. DOI: https://doi.org/10.1006/abbi.1993.1454

Fujiwake H, Suzuki T and Iwai K. 1982a. Intracellular distribution of enzymes and intermediates involved in biosynthesis of capsaicin and its analogues in Capsicum fruits. Agricultural and Biological Chemistry 46: 2685–9. DOI: https://doi.org/10.1271/bbb1961.46.2685

Fujiwake H, Suzuki T and Iwai K. 1982b. Capsaicinoid formation in the protoplast from placenta of Capsicum fruits. Agricultural and Biological Chemistry 46: 2591–2. DOI: https://doi.org/10.1271/bbb1961.46.2591

Gómez-García M R and Ochoa-Alejo N. 2013. Biochemistry and molecular biology of carotenoid biosynthesis in chili peppers (Capsicum spp.). International Journal of Molecular Sciences 14:19025–53. DOI: https://doi.org/10.3390/ijms140919025

Gowri G, Bugos R C, Campbell W H, Maxwell C A and Dixon R A. 1991. Stress responses in alfalfa (Medicago sativa L).10. Molecular cloning and expression of S-adenosyl-L-methionine-caffeic acid 3-O-methyltransferase, a key enzyme of lignin biosynthesis. Plant Physiology 97: 7–14. DOI: https://doi.org/10.1104/pp.97.1.7

Greenleaf W H. 1986. Pepper Breeding. (In) Breeding Vegetable Crops, pp: 67-134. Bassett, M.J. (Ed.). AVI Publishing Co., Westport, CT., USA.

Guzman I, Hambly S, Romero J, Bosland P and O’Connell M. 2010. Variability of carotenoid biosynthesis in orange coloured Capsicum spp. Plant Science 179: 49–59. DOI: https://doi.org/10.1016/j.plantsci.2010.04.014

Ha S H, Kim J B, Park J S, Lee S W and 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. J Exp Bot 58: 3135–44. DOI: https://doi.org/10.1093/jxb/erm132

Harvell K and Bosland P W. 1997. The environment produces a significant effect on pungency of chillies. Hort Science 32: 1292. DOI: https://doi.org/10.21273/HORTSCI.32.7.1292

Hosamani M M. 1993. Chilli crop (Capsicum annuum L.). University of Agricultural Sciences, Dharwad, Karnataka.

Howard L R, Talcot S T, Brenes C H and Villalon B. 2000. Changes in phytochemical and antioxidant activity of selected pepper cultivars (Capsicum species) as influenced by maturity. Journal of Agriculture and Food Chemistry 48(5): 1713–20. DOI: https://doi.org/10.1021/jf990916t

Hugueney P, Badillo A, Chen H C, Klein A, Hirschberg J, Camara B and Kuntz M. 1995. Metabolism of cyclic carotenoids: a model for the alteration of this biosynthetic pathway in Capsicum annuum chromoplasts. Plant Journal 8: 417–24. DOI: https://doi.org/10.1046/j.1365-313X.1995.08030417.x

Huh J, Kang B, Nahm S, Kim S, Ha K, Lee M and B Kim. 2001. A candidate gene approach identified phytoene synthase as the locus for mature fruit colour in red pepper (Capsicum spp.). Theoretical and Applied Genetics 102: 524–30. DOI: https://doi.org/10.1007/s001220051677

Hurtado-Hernandez H, and Smith P. 1985. Inheritance of mature fruit colour in Capsicum annuum L. Journal of Heredity 76: 211–3. DOI: https://doi.org/10.1093/oxfordjournals.jhered.a110070

Khyadagi K S. 2009. ‘Multilevel appraisal, quality parameters and suitability of promising chilli cultivars (Capsicum annuum L.) for conventional products’. Ph D thesis, University of Agricultural Sciences, Dharwad, Karnataka.

Kim M, Kim S, Kim S and Kim B D. 2001. Isolation of cDNA clones differentially accumulated in the placenta of pungent pepper by suppression subtractive hybridization. Molecules and Cells 11: 213–9.

Lang Y, Yanagawa S, Sasanuma T and Sasakuma T. 2004. Orange fruit colour in Capsicum due to deletion of capsanthin-capsorubin synthesis gene. Breeding Science 54: 33–9. DOI: https://doi.org/10.1270/jsbbs.54.33

Lang Y Q, Kisaka H, Sugiyama R, Nomura K, Morita A, Watanabe T, Tanaka Y, Yazawa S and Miwa T. 2009. Functional loss of pAMT results in biosynthesis of capsinoids, capsaicinoid analogs in Capsicum annuum cv. CH-19 Sweet. Plant Journal 59: 953–61. DOI: https://doi.org/10.1111/j.1365-313X.2009.03921.x

Lee C J, Yoo E Y, Shin J, Lee J, Hwang H S and Kim B D. 2005. Nonpungent Capsicum contains a deletion in the capsaicinoid synthetase gene, which allows early detection of pungency with SCAR markers. Molecules and Cells 19: 262–7.

Leete E and Louden M. 1968. Biosynthesis of capsaicin and

dihydrocapsaicin in Capsicum frutescens. J Amer Chem Soc 90: 6837–41.

Lefebvre V, Kuntz M, Camara B and Palloix A. 1998. The capsanthincapsorubin synthase gene: a candidate gene for the y locus controlling the red fruit colour in pepper. Plant Molecular Biology 36: 785–9. DOI: https://doi.org/10.1023/A:1005966313415

Li Z, Wang S, Gui X L, Chang X B and 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: 61996. DOI: https://doi.org/10.1371/journal.pone.0061996

Liu S, Li W, Wu Y, Chen C and Lei J. 2013. De novo transcriptome assembly in chili pepper (Capsicum frutescens) to identify genes involved in the biosynthesis of capsaicinoids. Plos one 8(1): e48156(1-8). DOI: https://doi.org/10.1371/journal.pone.0048156

Loaiza-Figueroa F and Tanksley SD. 1988. Genetics of a second locus determining pungency in chili peppers (Capsicum). Journal of Heredity 79: 314–5.

Markus F, Daood H G, Kapitany J and Biacs P A. 1999. Change in the carotenoid and antioxidant content of spice red pepper (Paprika) as a function of ripening and some technological factors. Journal of Agricultural and Food Chemistry. 47: 100–7. DOI: https://doi.org/10.1021/jf980485z

Mazourek M, Pujar A, Borovsky Y, Paran I, Mueller L and Jahn M M. 2009. A dynamic interface for capsaicinoid systems biology. Plant Physiology 150: 1806–21. DOI: https://doi.org/10.1104/pp.109.136549

Minamiyama Y, Kinoshita S, Inaba K and Inoue M. 2005. Development of a cleaved amplified polymorphic sequence (CAPS) marker linked to pungency in pepper. Plant Breeding 24: 288–91. DOI: https://doi.org/10.1111/j.1439-0523.2005.01101.x

Nelson E K and Dawson L E. 1923. Constitution of capsaicin, the pungent principle of Capsicum. III. Journal of the American Chemical Society 45: 2179–81. DOI: https://doi.org/10.1021/ja01662a023

Paran I and van der Knaap E. 2007. Genetic and molecular regulation of fruit and plant domestication traits in tomato and pepper. Journal of Experimental Botany 58: 3841–52. DOI: https://doi.org/10.1093/jxb/erm257

Popovsky S and Paran I. 2000. Molecular genetics of the y locus in pepper: its relation to capsanthin-capsorubin synthase and to fruit colour. Theoretical and Applied Genetics 101: 86–9. DOI: https://doi.org/10.1007/s001220051453

Prasath D and Ponnuswami V. 2008. Breeding for extractable colour and pungency in Capsicum – A review. Vegetable Sience 35(1): 1–9.

Reddy M V B and Sasikala P. 2013. Capsaicin and colour extraction from different varieties of green and red chilli peppers of Andhra Pradesh. International Journal of Advanced Scientific and Technical Research 2(3): 554–72.

Rodríguez-Uribe L, Guzman I, Rajapakse W, Richins R D and O’Connell M A. 2012. Carotenoid accumulation in orange-pigmented Capsicum fruit, regulated at multiple levels. Journal of Experimental Botany 63: 517–26. DOI: https://doi.org/10.1093/jxb/err302

Romer S, Hugueney P, Bouvier F, Camara B and Kuntz M. 1993. Expression of the genes encoding the early carotenoid biosynthetic enzymes in Capsicum annuum. Biochemical and Biophysical Research Communications 196: 1414–21. DOI: https://doi.org/10.1006/bbrc.1993.2410

Sanatombi K and Sharma G J. 2008. Capsaicin content and pungency of different Capsicum spp. cultivars. Notulae botanicae Horti Agrobotanici Cluj-Napoca 36(2): 89–90.

Sanchez-Sanchez H, Gonzalez-Hernandez V A, Cruz-Perez A B, Perez-Grajales M, Gutierrez-Espinosa M A, Gardea-Bejar G A and Gomez-Lim M A. 2010. Inheritance of capsaicinoids in manzano hot chilli pepper (Capsicum pubescens R. and P.). Agrociencia 44(6): 655–65.

Schaub P, Al-Babili S, Drake R and Beyer P. 2005. Why is golden rice golden (yellow) instead of red? Plant Physiology 138: 441–50. DOI: https://doi.org/10.1104/pp.104.057927

Simkin A J, Zhu C, Kuntz M and Sandmann G. 2003. Light-dark regulation of carotenoid biosynthesis in pepper (Capsicum annuum) leaves. Journal of Plant Physiology 160: 439–43. DOI: https://doi.org/10.1078/0176-1617-00871

Somos A. 1984. The Paprika. Akade´miai Kiado, Budapest.

Stewart C, Kang B C, Liu K, Mazourek M, Moore S L, Yoo E Y, Kim B D, Paran I and Jahn M M. 2005. The Pun1 gene for pungency in pepper encodes a putative acyltransferase. Plant Journal 42: 675–88. DOI: https://doi.org/10.1111/j.1365-313X.2005.02410.x

Stewart C, Mazourek M, Stellari G M, O’Connell M and Jahn M. 2007. Genetic control of pungency in C. chinense via the Pun1 locus. Journal of Experimental Botany 58: 979–91. DOI: https://doi.org/10.1093/jxb/erl243

Sukrasno N and Yeoman M M. 1993. Phenylpropanoid metabolism during growth and development of Capsicum frutescens fruits. Phytochemistry 32: 839–44. DOI: https://doi.org/10.1016/0031-9422(93)85217-F

Supalkova V, Stavelikova H, Krizkova S, Adam V, Horna A, Havel L, Ryant P, Babula P and Kizek R. 2007. Study of capsaicin content in various parts of pepper fruit by liquid chromatography with electrochemical detection. Acta Chimica Slovenica 54: 55–9.

Surh Y J. 2002. More than spice: capsaicin in hot chili peppers makes tumor cells commit suicide. Journal of the National Cancer Institute 94: 1263–5. DOI: https://doi.org/10.1093/jnci/94.17.1263

Sutoh K, Kobata K, Yazawa S and Watanabe T. 2006. Capsinoid is biosynthesized from phenylalanine and valine in a non-pungent pepper, Capsicum annuum L. cv. CH-19 Sweet. Bioscience, Biotechnology and Biochemistry 70: 1513–1516. DOI: https://doi.org/10.1271/bbb.50665

Tewksbury J J and Nabhan G P. 2001. Seed dispersal: directed deterrence by capsaicin in chillies. Nature 412: 403–4. DOI: https://doi.org/10.1038/35086653

Tewksbury J J, Reagan K M, Machnicki N J, Carlo T A, Haak D C, Penaloza A L C and Levey D J. 2008. Evolutionary ecology of pungency in wild chilies. Proceedings of the National Academy of Sciences 105: 11808–11. DOI: https://doi.org/10.1073/pnas.0802691105

Thiele R, Mueller-Seitz E and Petz M. 2008. Chili pepper fruits: presumed precursors of fatty acids characteristic for capsaicinoids. Journal of Agricultural and Food Chemistry 56: 4219–24. DOI: https://doi.org/10.1021/jf073420h

Thorup T, Tanyolac B, Livingstone K, Popovsky S, Paran I and Jahn M. 2000. Candidate gene analysis of organ pigmentation loci in the Solanaceae. Proceedings of the National Academy of Sciences 97: 11192–7. DOI: https://doi.org/10.1073/pnas.97.21.11192

USDA. 2011. Vegetables and melons yearbook: dataset. http://usda.mannlib.cornell.edu/MannUsda/viewDocumentInfo.do?documentID¼1212.

Von Lintig J. 2010. Colours with functions: elucidating the biochemical and molecular basis of carotenoid metabolism. Annual Review of Nutrition 30: 5.1–5.22. DOI: https://doi.org/10.1146/annurev-nutr-080508-141027

Votava E J and Bosland P W. 2002. Novel sources of non-pungency in Capsicum species. Capsicum and Eggplant Newsletter 21: 66–8.

Wahyuni Y, Ballester A R, Sudarmonowati E, Bino R J and Bovy A G. 2011. Metabolite diversity in pepper (Capsicum) fruits of thirty-two diverse accessions: variation in health-related compounds and implications for breeding. Phytochemistry 72: 1358–70. DOI: https://doi.org/10.1016/j.phytochem.2011.03.016

Wall M, Waddell C and Bosland P. 2001. Variation in b-carotene and total carotenoid content in fruits of Capsicum. HortScience 36: 746–9. DOI: https://doi.org/10.21273/HORTSCI.36.4.746

Webber H .1911. Preliminary notes on pepper hybrids. Am Breed Assoc Annu Rep 7: 188–99. DOI: https://doi.org/10.1093/jhered/os-7.1.188

Yarnes S C, Hamid A,Wo R C, Hill S, Theresa A, Stoffel K M, Van Deynze A and Gulick P. 2013. Identification of QTLs for capsaicinoids, fruit quality, and plant architecture-related traits in an interspecific Capsicum RIL population. Genome 56(1): 61. DOI: https://doi.org/10.1139/gen-2012-0083

Zewdie Y and Bosland P W. 2000a. Capsaicinoid inheritance in an interspecific hybridization of Capsicum annuum × C. chinense. Journal of the American Society for Horticultural Science 125: 448–53. DOI: https://doi.org/10.21273/JASHS.125.4.448

Zewdie Y and Bosland P W. 2000b. Evaluation of genotype, environment and genotype-by-environment interaction for capsaicinoids in Capsicum annuum L. Euphytica 111: 185–90. DOI: https://doi.org/10.1023/A:1003837314929

Zewdie-Tarekegn Y. 1999. Genetic study of capsaicinoids (pungency) in chillie, Capsicum spp. Ph D thesis, New Mexico State.