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Theoretical and Applied Genetics

, Volume 127, Issue 1, pp 179–191 | Cite as

Association of molecular markers derived from the BrCRISTO1 gene with prolycopene-enriched orange-colored leaves in Brassica rapa

  • Seohee Lee
  • Sang-Choon Lee
  • Dong Hae Byun
  • Dong Young Lee
  • Jee Young Park
  • Jong Hoon Lee
  • Hyun Oh Lee
  • Sang Hyun Sung
  • Tae-Jin YangEmail author
Original Paper

Abstract

Key message

Sequence polymorphism in BrCRTISO1, encoding carotenoid isomerase, is identified in orange-colored B. rapa , and three resulting gene-based markers will be useful for marker-assisted breeding of OC cultivars.

Abstract

Carotenoids are color pigments that are important for protection against excess light in plants and essential sources of retinols and vitamin A for animals. We identified a single recessive gene that might cause orange-colored (OC) inner leaves in Brassica rapa. The inner leaves of the OC cultivar were enriched in lycopene-like compounds, specifically prolycopene and its isomers, which can be a useful functional trait for Kimchi cabbage. We used a candidate gene approach based on the 21 genes in the carotenoid pathway to identify a candidate gene responsible for the orange color. Among them, we focused on two carotenoid isomerase (CRTISO) genes, BrCRTISO1 and BrCRTISO2. The expression of BrCRTISO1 was higher than that of BrCRTISO2 in a normal yellow-colored (YE) cultivar, but full-length BrCRTISO1 transcripts were not detected in the OC cultivar. Genomic sequence analysis revealed that BrCRTISO1 of the OC cultivar had many sequence variations, including single nucleotide polymorphisms (SNPs) and insertions and deletions (InDels), compared to that of the YE cultivar. We developed molecular makers for the identification of OC phenotype based on the polymorphic regions within BrCRTISO1 in B. rapa breeding. The BrCRTISO1 gene and its markers identified in this study are novel genetic resources and will be useful for studying the carotenoid biosynthesis pathway as well as developing new cultivars with unique carotenoid contents in Brassica species.

Keywords

Carotenoid Inbred Line Lycopene Chinese Cabbage Carotenoid Biosynthesis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We thank Rira Ha, Jae Kwang Kim, Hyeon Ju Lee, and Ho Jun Joh for their technical assistance. This study was supported by the Technology Development Program for Agriculture and Forestry (609001-05), Ministry for Food, Agriculture, Forestry and Fisheries, Republic of Korea.

Ethical standards

The experiments comply with the current laws of the country in which they were performed.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

122_2013_2209_MOESM1_ESM.pptx (391 kb)
Supplementary material 1 (PPTX 391 kb)
122_2013_2209_MOESM2_ESM.docx (29 kb)
Supplementary material 2 (DOCX 29 kb)
122_2013_2209_MOESM3_ESM.docx (2.1 mb)
Supplementary material 3 (DOCX 2192 kb)

References

  1. Albert GI, Hoeller U, Schierle J, Neuringer M, Johnson EJ, Schalch W (2008) Metabolism of lutein and zeaxanthin in rhesus monkeys: identification of (3R,6′R)- and (3R,6′S)-3′-dehydro-lutein as common metabolites and comparison to humans. Comp Biochem Physiol B: Biochem Mol Biol 151:70–78CrossRefGoogle Scholar
  2. Albrecht M, Takaichi S, Misawa N, Schnurr G, Böger P, Sandmann G (1997) Synthesis of atypical cyclic and acyclic hydroxy carotenoids in Escherichia coli transformants. J Biotechnol 58:177–185PubMedCrossRefGoogle Scholar
  3. Allen GD, Flores-Vergara MA, Krasynanski S, Kumar S, Hompson WF (2006) A modified protocol for rapid DNA isolation from plant tissues using cetyltrimethylammonium bromide. Nat Protoc 1:2320–2325PubMedCrossRefGoogle Scholar
  4. Bartley GE, Scolnik PA (1995) Plant carotenoids: pigments for photoprotection, visual attraction, and human health. Plant Cell 7:1027–1038PubMedCentralPubMedGoogle Scholar
  5. Bartley GE, Viitanen PV, Bacot KO, Scolnik PA (1992) A tomato gene expressed during fruit ripening encodes an enzyme of the carotenoid biosynthesis pathway. J Biol Chem 267:5036–5039PubMedGoogle Scholar
  6. Beyer P, Al-Babili S, Ye X, Lucca P, Schaub P, Welsch R, Potrykus I (2002) Golden rice: introducing the beta-carotene biosynthesis pathway into rice endosperm by genetic engineering to defeat vitamin A deficiency. J Nutr 132:506S–510SPubMedGoogle Scholar
  7. Beyer P, Mayer M, Kleinig H (1989) Molecular oxygen and the state of geometric isomerism of intermediates are essential in the carotene desaturation and cyclization reactions in daffodil chromoplasts. Eur J Biochem 184:141–150PubMedCrossRefGoogle Scholar
  8. Bird CR, Ray JA, Fletcher JD, Boniwell JM, Bird AS, Teulieres C, Blain I, Bramley PM, Schuch W (1991) Using Antisense RNA to study gene function: inhibition of carotenoid biosynthesis in transgenic tomatoes. Nat Biotechnol 9:635–639CrossRefGoogle Scholar
  9. Bohoyo-Gil D, Dominguez-Valhondo D, Garcia-Parra JJ, González-Gómez D (2012) UHPLC as a suitable methodology for the analysis of carotenoids in food matrix. Eur Food Res Technol 235:1055–1061CrossRefGoogle Scholar
  10. Cazzonelli CI, Cuttriss AJ, Cossetto SB, Pye W, Crisp P, Whelan J, Finnegan EJ, Turnbull C, Pogson BJ (2009) Regulation of carotenoid composition and shoot branching in Arabidopsis by a chromatin modifying histone methyltransferase, SDG8. Plant Cell 21:39–53PubMedCentralPubMedCrossRefGoogle Scholar
  11. Cheng F, Liu S, Wu J, Fang L, Sun S, Liu B, Li P, Hua W, Wang X (2011) BRAD, the genetics and genomics database for Brassica plants. BMC Plant Biol 11:136PubMedCentralPubMedCrossRefGoogle Scholar
  12. Crisp P, Walkey DGA, Bellman E, Roberts E (1975) A mutation affecting curd colour in cauliflower (Brassica oleracea L. var. Botrytis DC). Euphytica 24:173–176CrossRefGoogle Scholar
  13. Dickson MH, Lee CH, Blamble AE (1988) Orange-curd high carotene cauliflower inbreds, NY 156, NY 163, and NY 165. Hort Science 23:778–779Google Scholar
  14. Ducreux LJM, Morris WL, Hedley PE, Shepherd T, Davies HV, Millam S, Taylor MA (2005) Metabolic engineering of high carotenoid potato tubers containing enhanced levels of β-carotene and lutein. J Exp Bot 56:81–89PubMedGoogle Scholar
  15. Feng H, Li Y, Liu Z, Liu J (2012) Mapping of or, a gene conferring orange color on the inner leaf of the Chinese cabbage (Brassica rapa L. ssp. pekinensis). Mol Breed 29:235–244CrossRefGoogle Scholar
  16. Fester T, Schmidt D, Lohse S, Walter MH, Giuliano G, Bramley PM, Fraser PD, Hause B, Strack D (2002) Stimulation of carotenoid metabolism in arbuscular mycorrhizal roots. Planta 216:148–154PubMedCrossRefGoogle Scholar
  17. Fujisawa M, Takita E, Harada H, Sakurai N, Suzuki H, Ohyama K, Shibata D, Misawa N (2009) Pathway engineering of Brassica napus seeds using multiple key enzyme genes involved in ketocarotenoid formation. J Exp Bot 60:1319–1332PubMedCrossRefGoogle Scholar
  18. Glenn EB, Pablo AS, Peter B (1999) Two Arabidopsis thaliana carotene desaturases, phytoene desaturase and ζ-carotene desaturase, expressed in Escherichia coli, catalyze a poly-cis pathway to yield pro-lycopene. Eur J Biochem 259:396–403CrossRefGoogle Scholar
  19. Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pagès V, Dun EA, Pillot J, Letisse F, Matusova R, Danoun R, Portais J, Bouwmeester H, Bècard G, Beveridge CA, Rameau C, Rochange SF (2008) Strigolactone inhibition of shoot branching. Nature 455:189–194PubMedCrossRefGoogle Scholar
  20. Hengartner U, Bernhard K, Meyer K (1992) Synthesis, isolation and NMR-spectroscopic characterization of fourteen (Z)-isomers of lycopene and of some acetylenic didehydro- and tetradehydrolycopenes. Helv Chim Acta 75:1848–1865CrossRefGoogle Scholar
  21. Isaacson T, Ronen G, Zamir D, Hirschberg J (2002) Cloning of tangerine from tomato reveals a carotenoid isomerase essential for the production of β-carotene and xanthophylls in plants. Plant Cell 14:333–342PubMedCentralPubMedCrossRefGoogle Scholar
  22. Khachik F, Beecher GR, Vanderslice JT, Furrow G (1988) Liquid chromatographic artifacts and peak distortion: sample-solvent interactions in the separation of carotenoids. Anal Chem 60:807–811PubMedCrossRefGoogle Scholar
  23. Lee SC, Lim MH, Kim JA, Lee SI, Kim JS, Jin M, Kwon SJ, Mun JH, Kim YK, Kim HU, Hur Y, Park BS (2008) Transcriptome analysis in Brassica rapa under the abiotic stresses using Brassica 24 K oligo microarray. Mol Cells 26:595–605PubMedGoogle Scholar
  24. Li L, Lu S, Cosman KM, Earle ED, Garvin DF, O’Neill J (2006) β-Carotene accumulation induced by the cauliflower Or gene is not due to an increased capacity of biosynthesis. Phytochemistry 67:1177–1184PubMedCrossRefGoogle Scholar
  25. Li L, Paolillo DJ, Parthasarathy MV, DiMuzio EM, Garvin DF (2001) A novel gene mutation that confers abnormal patterns of β-carotene accumulation in cauliflower (Brassica oleracea var. botrytis). Plant J 26:59–67PubMedCrossRefGoogle Scholar
  26. Lopez AB, Eck JV, Conlin BJ, Paolillo DJ, O’Neilland J, Li L (2008) Effect of the cauliflower Or transgene on carotenoid accumulation and chromoplast formation in transgenic potato tubers. J Bot 59:213–223Google Scholar
  27. Lu S, Eck JV, Zhou X, Lopez AB, O’Halloran DM, Cosman KM, Conlin BJ, Paolillo DJ, Garvin DF, Vrebalov J, Kochia LV, Küpper H, Earle ED, Cao J, Li L (2006) The cauliflower Or gene encodes a DnaJ cysteine-rich domain-containing protein that mediates high levels of β-carotene accumulation. Plant cell 18:3594–3605PubMedCentralPubMedCrossRefGoogle Scholar
  28. Matsumoto E, Yasui C, Ohi M, Tsukada M (1998) Linkage analysis of RFLP markers for clubroot resistance and pigmentation in Chinese cabbage (Brassica rapa ssp. pekinensis). Euphytica 104:79–86CrossRefGoogle Scholar
  29. Melendez-Martinez AJ, Stinco CM, Liu C, Wang XD (2013) A simple HPLC method for the comprehensive analysis of cis/trans (Z/E) geometrical isomers of carotenoids for nutritional studies. Food Chem 138:1341–1350PubMedCrossRefGoogle Scholar
  30. Paine JA, Shipton CA, Chaggar S, Howells RM, Kennedy MJ, Vernon J, Wright SY, Hinchliffe E, Adams JL, Silverstone AL, Drake R (2005) Improving the nutritional value of golden rice through increased pro-vitamin A content. Nat Biotechnol 23:482–487PubMedCrossRefGoogle Scholar
  31. Park H, Kreunen SS, Cuttriss AJ, DellaPenna D, Pogson BJ (2002) Identification of the carotenoid isomerase provides insight into carotenoid biosynthesis, prolamellar body formation, and photomorphogenesis. Plant Cell 14:321–332PubMedCentralPubMedCrossRefGoogle Scholar
  32. Ray J, Bird C, Maunders M, Grierson D, Schuch W (1987) Sequence of pTOM5, a ripening related cDNA from tomato. Nucleic Acids Res 15:10587PubMedCentralPubMedCrossRefGoogle Scholar
  33. Richelle M, Lambelet P, Rytz A, Tavazzi I, Mermoud AF, Juhel C, Borel P, Bortlik K (2012) The proportion of lycopene isomers in human plasma is modulated by lycopene isomer profile in the meal but not by lycopene preparation. Br J Nutr 107:1482–1488PubMedCrossRefGoogle Scholar
  34. Römer S, Fraser PD, Kiano JW, Shipton CA, Misawa N, Schuch W, Bramley PM (2000) Elevation of the provitamin A content of transgenic tomato plants. Nat Biotechnol 18:666–669PubMedCrossRefGoogle Scholar
  35. Ruiz-Sola MÁ, Rodríguez-Concepción M (2012) Carotenoid biosynthesis in Arabidopsis: a colorful pathway. Arabidopsis Book 10:e0158PubMedCentralPubMedCrossRefGoogle Scholar
  36. Schmidt R, Bancroft I (2011) Genetics and genomics of the Brassicaceae. Plant genetics and genomics: crops and models, vol 9 Springer, New YorkGoogle Scholar
  37. Schwartz SH, Tan BC, Gage DA, Zeevaart JAD, McCarty DR (1997) Specific oxidative cleavage of carotenoids by VP14 of maize. Science 276:1872–1874PubMedCrossRefGoogle Scholar
  38. Shewmaker CK, Sheehy JA, Daley M, Colburn S, Ke DY (1999) Seed-specific overexpression of phytoene synthase: increase in carotenoids and other metabolic effects. Plant J 20:401–412PubMedCrossRefGoogle Scholar
  39. Sun Z, Shen S, Wang C, Wang H, Hu Y, Jiao J, Ma T, Tian B, Hua Y (2009) A novel carotenoid 1,2-hydratase (CruF) from two species of the non-photosynthetic bacterium Deinococcus. Microbiology 155:2775–2783PubMedCrossRefGoogle Scholar
  40. Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T, Takeda-Kamiya N, Magome H, Kamiya Y, Shirasu K, Yoneyama K, Kyozuka J, Yamaguchi S (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455:195–200PubMedCrossRefGoogle Scholar
  41. Wang X, Wang H, Wang J, Sun R, Wu J, Liu S, Bai Y, Mun JH, Bancroft I, Cheng F, Huang S, Li X, Hua W, Wang J, Wang X, Freeling M, Pires JC, Paterson AH, Chalhoub B, Wang B, Hayward A, Sharpe AG, Park BS, Weisshaar B, Liu B, Li B, Liu B, Tong C, Song C, Duran C, Peng C, Geng C, Koh C, Lin C, Edwards D, Mu D, Shen D, Soumpourou E, Li F, Fraser F, Conant G, Lassalle G, King GJ, Bonnema G, Tang H, Wang H, Belcram H, Zhou H, Hirakawa H, Abe H, Guo H, Wang H, Jin H, Parkin IA, Batley J, Kim JS, Just J, Li J, Xu J, Deng J, Kim JA, Li J, Yu J, Meng J, Wang J, Min J, Poulain J, Wang J, Hatakeyama K, Wu K, Wang L, Fang L, Trick M, Links MG, Zhao M, Jin M, Ramchiary N, Drou N, Berkman PJ, Cai Q, Huang Q, Li R, Tabata S, Cheng S, Zhang S, Zhang S, Huang S, Sato S, Sun S, Kwon SJ, Choi SR, Lee TH, Fan W, Zhao X, Tan X, Xu X, Wang Y, Qiu Y, Yin Y, Li Y, Du Y, Liao Y, Lim Y, Narusaka Y, Wang Y, Wang Z, Li Z, Wang Z, Xiong Z, Zhang Z, Brassica rapa Genome Sequencing Project Consortium (2011) The genome of the mesopolyploid crop species Brassica rapa. Nat Genet 43:1035–1039PubMedCrossRefGoogle Scholar
  42. Watanabe M, Musumi K, Ayugase J (2011) Carotenoid pigment composition, polyphenol content, and antioxidant activities of extracts from orange-colored Chinese cabbage. LWT-Food Sci Technol 44:1971–1975CrossRefGoogle Scholar
  43. Wills RBH, Rangga A (1996) Determination of carotenoids in Chinese vegetables. Food Chem 56:451–455CrossRefGoogle Scholar
  44. Ye X, Al-Babili S, Klöti A, Zhang J, Lucca P, Beyer P, Potrykus I (2000) Engineering the provitamin A (β-carotene) biosynthetic pathway into (carotenoid-free) rice endosperm. Science 287:303–305PubMedCrossRefGoogle Scholar
  45. Zhang F, Wang G, Wang M, Liu X, Zhao X, Yu Y, Zhang D, Yu S (2008) Identification of SCAR markers linked to or, a gene inducing β-carotene accumulation in Chinese cabbage. Euphytica 164:463–471CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Seohee Lee
    • 1
  • Sang-Choon Lee
    • 1
  • Dong Hae Byun
    • 2
  • Dong Young Lee
    • 3
  • Jee Young Park
    • 1
  • Jong Hoon Lee
    • 1
  • Hyun Oh Lee
    • 1
  • Sang Hyun Sung
    • 3
  • Tae-Jin Yang
    • 1
    Email author
  1. 1.Department of Plant Science, Plant Genomics and Breeding Institute, and Research Institute for Agriculture and Life Sciences, College of Agriculture and Life SciencesSeoul National UniversitySeoulRepublic of Korea
  2. 2.Chinese Cabbage and Breeding CompanyIcheonRepublic of Korea
  3. 3.College of Pharmacy and Research Institute of Pharmaceutical ScienceSeoul National UniversitySeoulRepublic of Korea

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