Abstract
Carotenoid oxygenase is a key enzyme involved in the metabolism of carotenoids, which are important quality factors affecting the pigmentation and aroma of flowers and fruits, as well as main regulators of plant phytohormones, such as abscisic acid (ABA) and strigolactone (SL). To investigate the regulation of carotenoid metabolism, including ABA and SL biosynthesis by carotenoid oxygenase genes, in B. rapa and B. oleracea, we studied the expression of these genes in response to salt, drought, cold, ABA, and SL treatments. In the Brassica database, we identified genes related to carotenoid cleavage dioxygenase (CCD) 1, CCD4, CCC7, CCD8, NCED (9-cis-epoxycarotenoid dioxygenase) 2, NCED3, NCED5, NCED 6, and NCED9. We classified 15 and 14 carotenoid oxygenase candidate genes in B. rapa and B. oleracea, respectively. CCD1 and CCD4 showed similar transcription trends under abiotic stress treatment conditions in both B. rapa and B. oleracea, with expression peaking at 3–6 h post treatment before decreasing at 12 h. NCED2, NCED6, and NCED9 were responsive to ABA and SL treatments. Our results show that the phytohormone biosynthetic enzymes involved in carotenoid oxygenase pathways may be activated as multifunctional stress signaling factors with a variety of transcriptional responses via their interactions under abiotic stress treatment conditions in B. rapa and B. oleracea.
Similar content being viewed by others
References
Agustí J, Zapater M, Iglesias DJ, Cercós M, Tadeo FR, Talón M (2007) Differential expression of putative 9-cis-epoxycarotenoid oxygenases and abscisic acid accumulation in water stressed vegetative and reproductive tissues of citrus. Plant Sci 172(1):85–94
Alder A, Jamil M, Marzorati M, Bruno M, Vermathen M, Bigler P, Ghisla S, Bouwmeester H, Beyer P, Al-Babili S (2012) The path from β-carotene to carlactone, a strigolactone-like plant hormone. Science 335(6074):1348–1351
Auldridge ME, McCarty DR, Klee HJ (2006a) Plant carotenoid cleavage oxygenases and their apocarotenoid products. Curr Opin Plant Biol 9(3):315–321
Auldridge ME, Block A, Vogel JT, Dabney-Smith C, Mila I, Bouzayen M, Magallanes-Lundback M, DellaPenna D, McCarty DR, Klee HJ (2006b) Characterization of three members of the Arabidopsis carotenoid cleavage dioxygenase family demonstrates the divergent roles of this multifunctional enzyme family. Plant J 45:982–993
Brandi F, Bar E, Mourgues F, Horváth G, Turcsi E, Giuliano G, Liverani A, Tartarini S, Lewinsohn E, Rosati C (2011) Study of ‘Redhaven’ peach and its white-fleshed mutant suggests a key role of CCD4 carotenoid dioxygenase in carotenoid and norisoprenoid volatile metabolism. BMC Plant Biol 11(1):24
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(1):136
Czarnecki O, Yang J, Weston DJ, Tuskan GA, Chen JG (2013) A dual role of strigolactones in phosphate acquisition and utilization in plants. Int J Mol Sci 14(4):7681–7701
Dun EA, Germain ADS, Rameau C, Beveridge CA (2012) Antagonistic action of strigolactone and cytokinin in bud outgrowth control. Plant Physiol 158(1):487–498
Ehrenreich IM, Stafford PA, Purugganan MD (2007) The genetic architecture of shoot branching in Arabidopsis thaliana: a comparative assessment of candidate gene associations vs. quantitative trait locus mapping. Genetics 176(2):1223–1236
Endo A, Sawada Y, Takahashi H, Okamoto M, Ikegami K, Koiwai H, Seo M, Toyomasu T, Mitsuhashi W, Shinozaki K, Nakazono M, Kamiya Y, Koshiba T, Nambara E (2008) Drought induction of Arabidopsis 9-cis-epoxycarotenoid dioxygenase occurs in vascular parenchyma cells. Plant Physiol 147(4):1984–1993
Giuliano G (2014) Plant carotenoids: genomics meets multi-gene engineering. Curr Opin Plant Biol 19:111–117
Giuliano G, Al-Babili S, Lintig JV (2003) Carotenoid oxygenases: cleave it or leave it. Trends Plant Sci 8(4):145–149
Ha CV, Leyva-González MA, Osakabe Y, Tran UT, Nishiyama R, Watanabe Y, Tanaka M, Seki M, Yamaguchi S, Van Dong N, Yamaguchi-Shinozaki K, Shinozaki K, Herrera-Estrella L, Tran LSP (2014) Positive regulatory role of strigolactone in plant responses to drought and salt stress. Proc Nati Acad Sci 111(2):851–856
Hai NTL, Masuda J, Miyajima I, Thien NQ, Mojtahedi N, Hiramatsu M, Kim J, Okubo H (2012) Involvement of carotenoid cleavage dioxygenase 4 gene in tepal color change in Lilium brownii var. colchesteri. J Jpn Soc Hort Sci 81:366–373
Hannoufa A, Hossain Z (2012) Regulation of carotenoid accumulation in plants. Biocatal Agric Biotechnol 1(3):198–202
Hwang I, Jung HJ, Park JI, Yang TJ, Nou IS (2014) Transcriptome analysis of newly classified bZIP transcription factor of Brassica rapa in cold stress response. Genomics 104(3):194–202
Iuchi S, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K (2000) A stress-inducible gene for 9-cis-epoxycarotenoid dioxygenase involved in abscisic acid biosynthesis under water stress in drought-tolerant cowpea. Plant Physiol 123:553–562
Jaquinod M, Villiers F, Kieffer-Jaquinod S, Hugouvieux V, Bruley C, Garin J, Bourguignon J (2007) A proteomics dissection of Arabidopsis thaliana vacuoles isolated from cell culture. Mol Cell Proteomics 6(3):394–412
Kayum MA, Jung HJ, Park JI, Ahmed NU, Saha G, Yang TJ, Nou IS (2015) Identification and expression analysis of WRKY family genes under biotic and abiotic stresses in Brassica rapa. Mol Genet Genomics 290:79–95
Kim DH, Yamaguchi S, Lim S, Oh E, Park J, Hanada A, Kamiya Y, Choi G (2008) SOMNUS, a CCCH-type zinc finger protein in Arabidopsis, negatively regulates light-dependent seed germination downstream of PIL5. Plant Cell 20(5):1260–1277
Kim YW, Jung HJ, Park JI, Hur Y, Nou IS (2015) Response of NBS encoding resistance genes linked to both heat and fungal stress in Brassica oleracea. Plant Physiol Biochem 86:130–136
Liu S et al (2014) The Brassica oleracea genome reveals the asymmetrical evolution of polyploidy genomes. Nat Commun 5:3930
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402–408
Mitsunori S, Koshiba T (2002) Complex regulation of ABA biosynthesis in plants. Trends Plant Sci 7(1):41–48
Park JI, Ahmed NU, Jung HJ, Thamil Arasan SK, Chung MY, Cho YG, Watanabe M, Nou IS (2014) Identification and characterization of LIM gene family in Brassica rapa. BMC Genet 15(1):641
Qin X, Zeevaart JAD (1999) The 9-cis-epoxycarotenoid cleavage reaction is the key regulatory step of abscisic acid biosynthesis in water-stressed bean. Proc Natl Acad Sci 96:15354–15361
Schwartz SH, Qin X, Loewen MC (2004) The biochemical characterization of two carotenoid cleavage enzymes from Arabidopsis indicates that a carotenoid-derived compound inhibits lateral branching. J Biol Chem 279(45):46940–46945
Simkin AJ, Schwartz SH, Auldridge M, Taylor MG, Klee HJ (2004a) The tomato carotenoid cleavage dioxygenase 1 genes contribute to the formation of the flavor volatiles b-ionone, pseudoionone, and geranylacetone. Plant J 40:882–892
Simkin AJ, Underwood BA, Auldridge M, Loucas HM, Shibuya K, Schmelz E, Clark DG, Klee HJ (2004b) Circadian regulation of the PhCCD1 carotenoid cleavage dioxygenase controls emission of β-ionone, a fragrance volatile of petunia flowers. Plant Physiol 136:3504–3514
Tan BC, Joseph LM, Deng WT, Liu L, Li QB, Cline K, McCarty DR (2003) Molecular characterization of the Arabidopsis 9-cis-epoxycarotenoid dioxygenase gene family. Plant J 35(1):44–56
Thompson AJ, Jackson AC, Parker RA, Morpeth DR, Burbidge A, Tayler IB (2000) Abscisic acid biosynthesis in tomato: regulation of zeaxanthin epoxidase and 9-cis-epoxycarotenoid dioxygenase mRNAs by light/dark cycles, water stress and abscisic acid. Plant Mol Biol 42:833–845
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(7210):195–200
Walter MH, Strack D (2011) Carotenoids and their cleavage products: biosynthesis and functions. Nat Prod Rep 28:663
Wang RK, Wang CE, Fei YY, Gai JY, Zhao TJ (2013) Genome-wide identification and transcription analysis of soybean carotenoid oxygenase genes during abiotic stress treatments. Mol Biol Rep 40(8):4737–4745
Yang TJ, Kim JS, Kwon SJ, Lim KB, Choi BS, Kim JA, Jin M, Park JY, Lim MH, Kim HI, Lim YP, Kang J, Hong JH, Kim CB, Bhak J, Bancroft I, Park S (2006) Sequence-level analysis of the diploidization process in the triplicated FLOWERING LOCUS C region of Brassica rapa. Plant Cell 18(6):1339–1347
Ytterberg AJ, Peltier JB, Wijk KJV (2006) Protein profiling of plastoglobules in chloroplasts and chromoplasts. A surprising site for differential accumulation of metabolic enzymes. Plant Physiol 140(3):984–997
Yu J, Zhao M, Wang X, Tong C, Huang S, Tehrim S, Liu Y, Hua W, Liu S (2013) Bolbase: a comprehensive genomics database for Brassica oleracea. BMC Genomics 14(1):664
Acknowledgments
This study was supported by the Golden Seed Project (Center for Horticultural Seed Development, No. 213003-04-3-SB110) of the Ministry of Agriculture, Food and Rural affairs in the Republic of Korea (MAFRA).
Author information
Authors and Affiliations
Corresponding author
Electronic Supplementary Material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Kim, Y., Hwang, I., Jung, HJ. et al. Genome-Wide Classification and Abiotic Stress-Responsive Expression Profiling of Carotenoid Oxygenase Genes in Brassica rapa and Brassica oleracea . J Plant Growth Regul 35, 202–214 (2016). https://doi.org/10.1007/s00344-015-9520-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00344-015-9520-y