Genetic control of non-pungency in pepper (Capsicum sp.) (mini-review)

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Todorka SREBCHEVA Bojin BOJINOV

Abstract

Abstract. The species of genus Capsicum are synthesizing capsaicinoids – alkaloids that give pungency in peppers. The most pungent capsaicinoids are capsaicin and dihydrocapsaicin. Capsaicin is the component of chili peppers which is irritant for mammals, including humans, and produces a sensation of burning in any tissue with which it comes into contact. Pungency as a feature has two aspects – quantitative and qualitative – affected by the way the general biosynthetic pathway of capsaicin and other capsaicinoids’ synthesis is affected. Capsaicin is synthesized in the interlocular septum of plants of the Capsicum genus and its production is qualitatively controlled by the Pun1 locus. It was found that the locus contains a putative acyltransferase. Several mutant alleles of Pun1 gene were identified through classical breeding methods as responsible for the loss of pungency. Furthermore, the mutation in another locus (Pun2) was also found to affect the levels of capsaicin production thus providing evidence for the presence of a second gene with a major epistatic effect on capsaicin production. Here we review the current state of the knowledge accumulated so far as regards the alleles and their interactions that affect the production of this compound. The less pronounced effects of other genes in the biosynthetic pathway and some transcription factors are also discussed.


Key words: Pepper; Capsicum; Pungency; Genetic control.

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How to Cite
SREBCHEVA, Todorka; BOJINOV, Bojin. Genetic control of non-pungency in pepper (Capsicum sp.) (mini-review). Stiinta agricola, [S.l.], n. 2, p. 57-63, jan. 2019. ISSN 2587-3202. Available at: <https://sa.uasm.md/index.php/sa/article/view/615>. Date accessed: 25 aug. 2019.
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References

1. ALURU, M.R., MAZOUREK, M., LANDRY, L.G. et al. (2003). Differential expression of fatty acid synthase genes, Acl, Fat and Kas, in Capsicum fruit. In: Journal of Experimental Botany, vol. 54, pp. 1655-1664.
2. ANANTHAN, R., SUBHASH, K., LONGVAH, T. (2018). Capsaicinoids, amino acid and fatty acid profiles in different fruit components of the world hottest Naga king chilli (Capsicum chinense Jacq). In: Food Chemistry, vol. 238, pp. 51-57.
3. AZA-GONZÁLEZ, C., Núñez-Palenius, H. G., Ochoa-Alejo, N. (2011). Molecular biology of capsaicinoid biosynthesis in chili pepper (Capsicum spp.). In: Plant Cell Reports, vol. 30, pp. 695–706.
4. BEN-CHAIM, A., BOROVSKY, Y., FALISE, M., MAZOUREK, M. et al. (2006). QTL analysis for capsaicinoid content in Capsicum. In: Theoretical and Applied Genetics, vol. 113, pp. 1481-1490.
5. BEN-CHAIM, A., GRUBE, R.C., LAPIDOT, M., JAHN, M., PARAN, I. (2001). Identification of quantitative trait loci associated with resistance to cucumber mosaic virus in Capsicum annuum. In: Theoretical and Applied Genetics, vol. 102, pp. 1213-1220.
6. BENETT, D.J., KIRBY, G.W. (1968). Constitution and biosynthesis of capsaicin. In: Journal of the Chemical Society C: Organic, pp. 442-446.
7. BLUM, E., LIU, K., MAZOUREK, M., YOO, E.Y., JAHN, M., PARAN, I. (2002). Molecular mapping of the C locus for presence of pungency in Capsicum. In: Genome, vol. 45, pp. 702-705.
8. BLUM, E., MAZOUREK, M., O’CONNELL, M. et al. (2003). Molecular mapping of capsaicinoid biosynthesis genes and quantitative trait loci analysis for capsaicinoid content in Capsicum. In: Theoretical and Applied Genetics, vol. 108, pp. 79–86.
9. BOGUSZ Junior, S., MARÇO, P. H., VALDERRAMA, P. et al. (2015). Analysis of volatile compounds in Capsicumspp. by headspace solid-phase microextraction and GC × GC-TOFMS. In: Analytical Methods, vol. 7, pp. 521-529.
10. BOSWELL, V. R. (1937). Improvement and genetics of tomatoes, peppers, and eggplant. In: Yearbook of Agriculture. Ed. H. A. Wallace. Washington: United States Government Printing Office. pp. 176–206.
11. CARVALHO, S. I. C., RAGASSI, C. F., BIANCHETTI, L. B. et al. (2014). Morphological and genetic relationships between wild and domesticated forms of peppers (Capsicum frutescens L. and C. chinense Jacquin). In: Genetics and Molecular Research, vol. 13, pp. 7447-7464.
12. CATERINA, M. J., SCHUMACHER, M. A., TOMINAGA, M. et al. (1997). The capsaicin receptor: a heatactivated ion channel in the pain pathway. In: Nature, vol. 389, p. 816.
13. DAS, S., TEJA, K. C., DUARY, B. et al. (2016). Impact of nutrient management, soil type and location on the accumulation of capsaicin in Capsicum chinense (Jacq.): One of the hottest chili in the world. In: Scientia Horticulturae, vol. 213, pp. 354-366.
14. De AGUIAR, A. C., SALES, L. P., COUTINHO, J. P. et al. (2013). Supercritical carbon dioxide extraction of Capsicum peppers: Global yield and capsaicinoid content. In: Journal of Supercritical Fluids, vol. 81, pp. 210-216.
15. Deshpande, R. B. (1935). Studies in Indian chillies: IV. Inheritance of pungency in Capsicum annuum L. In: Indian Journal of Agricultural Sciences, vol. 5, pp. 513-516.
16. GARCÉS-CLAVER, A., GIL-ORTEGA, R., Álvarez-Fernández, A., Arnedo-Andrés, M. S. (2007). Inheritance of Capsaicin and Dihydrocapsaicin, determined by HPLC-ESI/MS, in an intraspecific cross of Capsicumannuum L. In: Journal of Agricultural and Food Chemistry, vol. 55, pp. 6951-6957.
17. GIUFFRIDA, D., DUGO, P., TORRE, G. et al. (2013). Characterization of 12 Capsicum varieties by evaluation of their carotenoid profile and pungency determination. In: Food Chemistry, vol. 140, pp. 794-802.
18. GOVINDARAJAN, V. S., SATHYANARAYANA, M. N. (1991). Capsicum — production, technology, chemistry, and quality. Part V: Impact on physiology, pharmacology, nutrition, and metabolism; structure, pungency, pain, and desensitization sequences. In: Critical Reviews in Food Science and Nutrition, vol. 29, pp. 435-474.
19. HALIKOWSKI-SMITH, S. (2015). In the shadow of a pepper-centric historiography: Understanding the global diffusion of capsicums in the sixteenth and seventeenth centuries. In: Journal of Ethnopharmacology, vol. 167, pp. 64-77.
20. HAN, K., JEONG, H., SUNG, J., KEUM, Y. et al. (2013). Biosynthesis of capsinoid is controlled by the Pun1 locus in pepper. In: Molecular Breeding, vol. 31, pp. 537–548.
21. IBARRA-TORRES, P., VALADEZ-MOCTEZUMA, E. et al. (2015). Inter- and intraspecific differentiation of Capsicum annuum and Capsicum pubescens using ISSR and SSR markers. In: Scientia Horticulturae, vol. 181, pp. 137-146.
22. IWAI, K., SUZUKI, T., FUJIWAKE, H. (1979). Formation and Accumulation of Pungent Principle of Hot Pepper Fruits, Capsaicin and Its Analogues, in Capsicum annuun var. annuun cv. Karayatsubusa at Different Growth Stages after Flowering. In: Agricultural and Biological Chemistry, vol. 43, pp. 2493-2498.
23. KEYHANINEJAD, N., CURRY, J., ROMERO, J., O’CONNELL, M. A. (2014). Fruit specific variability in capsaicinoid accumulation and transcription of structural and regulatory genes in Capsicum fruit. In: Plant Science, vol. 215-216, pp. 59-68.
24. KIM, M.W., KIM, S.J., KIM, S.H., KIM, B.D. (2001). Isolation of cDNA clones differentially accumulated in the placenta of pungent pepper by suppression subtractive hybridization. In: Molecullar Cells, vol. 11, pp. 213-219.
25. KIM, S., PARK, M., YEOM, S.-I., KIM, Y.-M., LEE, J.M. et al. (2014). Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum species. In: Nature Genetics, vol. 46, p. 270.
26. KIRII, E., GOTO, T., YOSHIDA, Y., YASUBA, K.-i., TANAKA, Y. (2017). Non-pungency in a Japanese Chili Pepper Landrace (Capsicum annuum) is Caused by a Novel Loss-of-function Pun1 Allele. In: The Horticulture Journal, vol. 86, pp. 61-69.
27. KOBATA, K., SUGAWARA, M., MIMURA, M., YAZAWA, S., WATANABE, T. (2013). Potent production of capsaicinoids and capsinoids by Capsicum peppers. In: Journal of Agricultural and Food Chemistry, vol. 61, pp. 11127-11132.
28. LAHBIB, K., DABBOU, S., BOK, S. E. L., PANDINO, G., LOMBARDO, S., GAZZAH, M. E. L. (2017). Variation of biochemical and antioxidant activity with respect to the part of Capsicum annuum fruit from Tunisian autochthonous cultivars. In: Industrial Crops and Products, vol. 104, pp. 164-170.
29. LEE, C.-J., YOO, E., SHIN, J., HYUN SHIN, J. et al. (2005). Non-pungent Capsicum contains a deletion in the capsaicinoid synthetase gene, which allows early detection of pungency with SCAR markers. In: Molecules and Cells, vol. 19, pp. 262-267.
30. LEETE, E., LOUDEN, M. C. L. (1968). Biosynthesis of capsaicin and dihydrocapsaicin in Capsicum frutescens. In: Journal of the American Chemical Society, vol. 90, pp. 6837-6841.
31. LEFEBVRE, V., PALLOIX, A., CARANTA, C., POCHARD, E. (1995). Construction of an intraspecific integrated linkage map of pepper using molecular markers and doubled-haploid progenies. In: Genome, vol. 38, pp. 112-121.
32. MAZOUREK, M., PUJAR, A., BOROVSKY, Y., PARAN, I., MUELLER, L., JAHN, M. M. (2009). A Dynamic Interface for Capsaicinoid Systems Biology. In: Plant Physiology, vol. 150, pp. 1806-1821.
33. MOREIRA, A. F. P., RUAS, P. M., RUAS, C. D. F., BABA, V. Y. et al. (2018). Genetic diversity, population structure and genetic parameters of fruit traits in Capsicum chinense. In: Scientia Horticulturae, vol. 236, pp. 1-9.
34. NELSON, E.K., DAWSON, L.E. (1923). The constitution of capsaicin, the pungent principle of Capsicum. III. In: Journal of the American Chemical Society, vol. 45, pp. 2179-2181.
35. QIN, C., YU, C., SHEN, Y., FANG, X., CHEN, L., MIN, J., CHENG, J., ZHAO, S., XU, M. et al. (2014). Whole-genome sequencing of cultivated and wild peppers provides insights into Capsicum domestication and specialization. In: Proceedings of the National Academy of Sciences of the USA, vol. 111, pp. 5135-5140.
36. REDDY, U.K., ALMEIDA, A., ABBURI, V. L., ALAPARTHI, S. B., UNSELT, D., HANKINS, G., PARK, M., CHOI, D., NIMMAKAYALA, P. (2014). Identification of Gene-Specific Polymorphisms and Association with Capsaicin Pathway Metabolites in Capsicum annuum L. collections. In: PLoS One, vol. 9, e86393. https://doi.org/10.1371/journal.pone.0086393
37. SÁNCHEZ-SEGURA, L., TÉLLEZ-MEDINA, D. I., EVANGELISTA-LOZANO, S., GARCÍA-ARMENTA, E. et al. (2015). Morpho-structural description of epidermal tissues related to pungency of Capsicum species. In: Journal of Food Engineering, vol. 152, pp. 95-104.
38. SCOVILLE, W. L. (1912). Note on capsicums. In: The Journal of the American Pharmaceutical Association, vol. 1, pp. 453-454.
39. SOUSA, E. T., De M. RODRIGUES, F., MARTINS, C. C. et al. (2006). Multivariate optimization and HS-SPME/GC-MS analysis of VOCs in red, yellow and purple varieties of Capsicum chinense sp. peppers. In: Microchemical Journal, vol. 82, pp. 142-149.
40. STELLARI, G.M., MAZOUREK, M., JAHN, M. M. (2010). Contrasting modes for loss of pungency between cultivated and wild species of Capsicum. In: Heredity, vol. 104, pp. 460-471.
41. STEWART, C., JR. , MAZOUREK, M., STELLARI, G. M., O’CONNELL, M., JAHN, M. (2007). Genetic control of pungency in C. chinense via the Pun1 locus. In: Journal of Experimental Botany, vol. 58, pp. 979-991.
42. STEWART, C., KANG, B.-C., LIU, K., MAZOUREK, M. et al. (2005). The Pun1 gene for pungency in pepper encodes a putative acyltransferase. In: The Plant Journal, vol. 42, pp. 675-688.
43. SUGITA, T., KINOSHITA, T., KAWANO, T., YUJI, K., YAMAGUCHI, K. et al. (2005). Rapid Construction of a Linkage Map using High-efficiency Genome Scanning/AFLP and RAPD, Based on an Intraspecific, Doubled-haploid Population of Capsicum annuum. In: Breeding Science, vol. 55, pp. 287-295.
44. 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. Karayatsubusa1. In: Plant and Cell Physiology vol. 21, pp. 839-853.
45.. TANAKA, Y., YONEDA, H., HOSOKAWA, M., MIWA, T., YAZAWA, S. (2014). Application of markerassisted selection in breeding of a new fresh pepper cultivar (Capsicum annuum) containing capsinoids, lowpungent capsaicinoid analogs. In: Scientia Horticulturae, vol. 165, pp. 242-245.
46. TANKSLEY, S. D., BERNATZKY, R., LAPITAN, N. L., PRINCE, J. P. (1988). Conservation of gene repertoire but not gene order in pepper and tomato. In: Proceedings of the National Academy of Sciences of the USA, vol. 85, pp. 6419-6423. ISSN 0027-8424
47. THRESH, J. C. (1876). Isolation of capsaicin. In: The Pharmaceutical Journal and Transactions, vol. 6, pp. 941–947.
48. TSABALLA, A., GANOPOULOS, I., TIMPLALEXI, A., ALIKI, X., BOSMALI, I., IRINI, N.-O., ATHANASIOS, T., MADESIS, P. (2015). Molecular characterization of Greek pepper (Capsicum annuum L) landraces with neutral (ISSR) and gene-based (SCoT and EST-SSR) molecular markers. In: Biochemical Systematics and Ecology, vol. 59, pp. 256-263.
49. ZHANG, X.-m., ZHANG, Z.-h., GU, X.-z., MAO, S.-l., Li, X.-x., CHADŒUF, J., PALLOIX, A., WANG, L.-h., ZHANG, B.-x. (2016). Genetic diversity of pepper (Capsicum spp.) germplasm resources in China reflects selection for cultivar types and spatial distribution. In: Journal of Integrative Agriculture, vol. 15, pp. 1991-2001.