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Genome-wide identification and transcription analysis of soybean carotenoid oxygenase genes during abiotic stress treatments

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Abstract

Carotenoid oxygenase is a key enzyme in carotenoid metabolism leading to the synthesis of two phytohormones, abscisic acid (ABA) and strigolactone, as well as norisoprenoids. Few studies have analyzed inter-relationship of the metabolic networks of these three substances. In this present paper, soybean carotenoid oxygenase genes were identified to reveal their phylogenetic relationships, and the transcriptional response of these genes to four abiotic stresses (NaCl, PEG, high and low temperature) and ABA treatment were investigated to characterize their potential roles in plant resistance. Positive selection was found in the branches of carotenoid cleavage dioxygenase (CCD1), CCD8 and NCED (9-cis-epoxycarotenoid oxygenase), indicating an adaptive evolution in these clades. In soybean eight carotenoid oxygenase genes were identified. The transcriptional responses of almost all of them under stress and ABA conditions were significantly altered when assessed by quantitative polymerase chain reaction. Notably, CCD1 and CCD4, previously known as the key genes in norisoprenoids metabolism, showed especially strong responses to the abiotic stresses and ABA treatment. Furthermore, transcription levels of CCD7 and CCD8, key genes for the strigolactone pathway, highly increased during ABA treatment providing further evidence that ABA is involved in regulating strigolactone metabolism. All of the carotenoid oxygenase genes in soybean are involved in plant abiotic stress physiology, and ABA is presumed to be a core regulatory substance. These findings provide some insights into the mechanisms that underlie the regulation of tolerance response to abiotic stresses in soybean.

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References

  1. Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Method Enzymol 148:350–382

    Article  CAS  Google Scholar 

  2. Schwartz SH, Tan BC, Gage DA, Zeevaart JAD, McCarty DR (1997) Specific oxidative cleavage of carotenoids by VP14 of maize. Science 276(5320):1872–1874

    Article  PubMed  CAS  Google Scholar 

  3. Kloer DP, Ruch S, Al-Babili S, Beyer P, Schulz GE (2005) The structure of a retinal-forming carotenoid oxygenase. Science 308(5719):267–269

    Article  PubMed  CAS  Google Scholar 

  4. Auldridge ME, McCarty DR, Klee HJ (2006) Plant carotenoid cleavage oxygenases and their apocarotenoid products. Curr Opin Plant Biol 9(3):315–321

    Article  PubMed  CAS  Google Scholar 

  5. Winterhalter P, Schreier P (1994) C13-norisoprenoid glycosides in plant tissues: an overview on their occurrence, composition and role as flavor precursors. Flavour Fragr J 9(6):281–287

    Article  CAS  Google Scholar 

  6. Ibdah M, Azulay Y, Portnoy V, Wasserman B, Bar E, Meir A, Burger Y, Hirschberg J, Schaffer AA, Katzir N, Tadmor Y, Lewinsohn E (2006) Functional characterization of CmCCD1, a carotenoid cleavage dioxygenase from melon. Phytochemistry 67(15):1579–1589

    Article  PubMed  CAS  Google Scholar 

  7. 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 oxygenase in carotenoid and norisoprenoid volatile metabolism. BMC Plant Biol 11(-):24

    Article  PubMed  CAS  Google Scholar 

  8. 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

    Article  PubMed  CAS  Google Scholar 

  9. Dun EA, Brewer PB, Beveridge CA (2009) Strigolactones: discovery of the elusive shoot branching hormone. Trends Plant Sci 14(7):364–372

    Article  PubMed  CAS  Google Scholar 

  10. Ongaro V, Leyser O (2008) Hormonal control of shoot branching. J Exp Bot 59(1):67–74

    Article  PubMed  CAS  Google Scholar 

  11. Zhu JH, Verslues PE, Zheng X, Lee BH, Zhan XQ, Manabe Y, Sokolchik I, Zhu YM, Dong CH, Zhu JK, Hasegawa PM, Bressan RA (2005) HOS10 encodes an R2R3-type MYB transcription factor essential for cold acclimation in plants. PNAS 102(28):9966–9971

    Article  PubMed  CAS  Google Scholar 

  12. Xie ZM, Zou HF, Lei G, Wei W, Zhou QY, Niu CF, Liao Y, Tian AG, Ma B, Zhang WK, Zhang JS, Chen SY (2009) Soybean trihelix transcription factors GmGT-2A and GmGT-2B improve plant tolerance to abiotic stresses in transgenic Arabidopsis thaliana. PLoS One 4(9):e6898

    Article  PubMed  Google Scholar 

  13. Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56:165–185

    Article  PubMed  CAS  Google Scholar 

  14. Benschop JJ, Millenaar FF, Smeets ME, van Zanten M, Voesenek LA, Peeters AJ (2007) Abscisic acid antagonizes ethylene-induced hyponastic growth in Arabidopsis thaliana. Plant Physiol 143(2):1013–1023

    Article  PubMed  CAS  Google Scholar 

  15. Guo AY, Zhu QH, Chen X, Luo JC (2007) GSDS: a gene structure display server. Yi Chuan 29(8):1023–1026

    Article  PubMed  CAS  Google Scholar 

  16. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24(8):1596–1599

    Article  PubMed  CAS  Google Scholar 

  17. Yang ZH (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24(8):1586–1591

    Article  CAS  Google Scholar 

  18. 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

    Article  Google Scholar 

  19. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3(6):1101–1108

    Article  PubMed  CAS  Google Scholar 

  20. Vallabhaneni R, Bradbury LM, Wurtzel ET (2010) The Carotenoid oxygenase gene family in maize, sorghum, and rice. Arch Biochem Biophys 504(1):104–111

    Article  PubMed  CAS  Google Scholar 

  21. Booker J, Auldridge M, McCarty D, Klee H, Leyser O (2004) MAX3/CCD7 is a carotenoid cleavage dioxygenase required for the synthesis of a novel plant signaling molecule. Curr Biol 14(14):1232–1238

    Article  PubMed  CAS  Google Scholar 

  22. Leyser O (2003) Regulation of shoot branching by auxin. Trends Plant Sci 8(11):541–545

    Article  CAS  Google Scholar 

  23. Demuth JP, Hahn MW (2009) The life and death of gene families. BioEssays 31(1):29–39

    Article  PubMed  Google Scholar 

  24. Zhang JZ (2003) Evolution by gene duplication: an update. Trends Ecol Evol 18(6):292–298

    Article  Google Scholar 

  25. Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, Oxford

    Google Scholar 

  26. Iuchi S, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki KA (2000) Stress-inducible gene for 9-cis-epoxycarotenoid dioxygenase involved in abscisic acid biosynthesis under water stress in drought-tolerant cowpea. Plant Physiol 123(2):553–562

    Article  CAS  Google Scholar 

  27. Rubio A, Rambla JL, Santaella M, Gómez MD, Orzaez D, Granell A, Gómez LG (2008) Cytosolic and plastoglobule-targeted carotenoid dioxygenases from Crocus sativus are both involved in β-ionone release. J Biol Chem 283(36):24816–24825

    Article  CAS  Google Scholar 

  28. Iuchi S, Kobayashi M, Taji T, Naramoto M, Seki M, Kato T, Tabata S, Kakubari Y, Yamaguchi-Shinozaki K, Shinozaki K (2001) Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid oxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis thaliana. Plant J 27(4):325–333

    Article  PubMed  CAS  Google Scholar 

  29. López-Ráez JA, Kohlen W, Charnikhova T, Mulder P, Undas AK, Sergeant MJ, Verstappen F, Bugg TDH, Thompson AJ, Ruyter-Spira C, Bouwmeester H (2010) Does abscisic acid affect strigolactone biosynthesis? New Phytol 18(2):343–354

    Article  Google Scholar 

  30. Jose AMR, Rafael LM, Horst V, Juan AO, Jutta LM, Jose MGG (2011) Ethylene-dependent/ethylene-independent ABA regulation of tomato plants colonized by arbuscular mycorrhiza fungi. New Phytol 190(1):193–205

    Article  Google Scholar 

  31. Hartmann T (2007) From waste products to ecochemicals: fifty years research of plant secondary metabolism. Phytochemistry 68(22):2831–2846

    Article  PubMed  CAS  Google Scholar 

  32. Zhang R, Yang C, Wang C, Wei ZG, Xia DA, Wang YF, Liu GF, Wang YC (2012) Time-course analyses of abscisic acid level and the expression of genes involved in abscisic acid biosynthesis in the leaves of Betula platyphylla. Mol Biol Rep 39(3):2505–2513

    Article  PubMed  CAS  Google Scholar 

  33. Zhang L, Ma G, Kato M, Yamawaki K, Takagi T, Kiriiwa Y, Ikoma Y, Matsumoto H, Yoshioka T, Nesumi H (2012) Regulation of carotenoid accumulation and the expression of carotenoid metabolic genes in citrus juice sacs in vitro. J Exp Bot 63(2):871–886

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Key Basic Research Program of China (2010CB1259, 2011CB1093), the National Hightech R&D Program of China (2012AA101106), the Natural Science Foundation of China (31271750).

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Authors and Affiliations

  1. Soybean Research Institute, National Center for Soybean Improvement, MOA Key Laboratory for Biology and Genetic Improvement of Soybean (General), National Key Laboratory for Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University, Nanjing, 210095, Jiangsu, People’s Republic of China

    Rui-Kai Wang, Chun-E Wang, Yun-Yan Fei, Jun-Yi Gai & Tuan-Jie Zhao

  2. College of Life Science, Jiujiang University, Jiujiang, 332005, Jiangxi, People’s Republic of China

    Rui-Kai Wang & Chun-E Wang

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  1. Rui-Kai Wang
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  2. Chun-E Wang
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  5. Tuan-Jie Zhao
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Correspondence to Tuan-Jie Zhao.

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11033_2013_2570_MOESM1_ESM.jpg

Supplementary Fig 1. Heat map of carotenoid oxygenase gene expression under four stress conditions and ABA treatment. The genes were clustered by Heatmap Builder 1.0 using −ΔΔCT (X-axis) data. (JPEG 332 kb)

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Wang, RK., Wang, CE., Fei, YY. et al. Genome-wide identification and transcription analysis of soybean carotenoid oxygenase genes during abiotic stress treatments. Mol Biol Rep 40, 4737–4745 (2013). https://doi.org/10.1007/s11033-013-2570-y

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  • DOI: https://doi.org/10.1007/s11033-013-2570-y

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