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Plant Molecular Biology Reporter

, Volume 36, Issue 4, pp 663–674 | Cite as

Carotenoid Accumulation and Distinct Transcript Profiling of Structural Genes Involved in Carotenoid Biosynthesis in Celery

  • Jing-Wen Li
  • Jing Ma
  • Kai Feng
  • Jie-Xia Liu
  • Feng Que
  • Ai-Sheng Xiong
Original Paper
  • 73 Downloads

Abstract

Carotenoids, a diverse group of pigments, participate in various biological processes in plants and contribute to an important quality trait for many plants. Celery is an important leafy vegetable crop, and the leaf is the main edible organ. However, the molecular mechanism of carotenoid biosynthetic pathway in celery has yet to be characterized. Here, two celery varieties with obviously different appearances, ‘Liuhe yellow heart celery’ and ‘Ventura’, were selected to study the carotenoid accumulation and distinct transcript profiling of structural genes involved in carotenoid biosynthesis. The contents of lutein, β-carotene, and α-carotene of leaf blades and petioles of celery were determined by UPLC at 30, 45, and 60 days after germination (DAG). In the two celery varieties, the highest lutein content was 14.56 mg/g DW (dry weight) in leaf blades of ‘Ventura’ at 45 DAG. The lowest lutein content was 1.56 mg/g DW in petioles of ‘Liuhe yellow heart celery’ at 60 DAG. The highest β-carotene content was 0.42 mg/g DW in leaf blades of ‘Ventura’ at 45 DAG. The lowest β-carotene content was 0.07 mg/g DW in petioles of ‘Liuhe yellow heart celery’ at 45 DAG. Lutein and β-carotene contents in leaf blades were higher than that in petioles. The contents of lutein and β-carotene in ‘Ventura’ were higher than that in ‘Liuhe yellow heart celery’. The relative expression levels of structural genes involved in carotenoid biosynthesis were also detected. The contents of lutein and β-carotene were correlated with the transcription level of genes involved in carotenoid biosynthesis. The relative expression of AgPSY1 and AgLCYE in ‘Ventura’ was significantly higher than that in ‘Liuhe yellow heart celery’ at three growth stages. The content of α-carotene could not detected in leaves of the two celery cultivars. These results provide potential insights into carotenoid biosynthetic pathway in celery during growth and development.

Keywords

Celery Carotenoids Lutein β-Carotene α-Carotene Gene expression 

Abbreviations

ABA

abscisic acids

ANOVA

one-way analysis of variance

CRTISO

carotenoid isomerase

DAG

day after germination

DMAPP

dimethylallyl diphosphate

DW

dry weight

GGPP

geranylgeranyl diphosphates

IPP

isopentenyl diphosphate

LCYB

lycopene β-cyclase

LCYE

lycopene ε-cyclase

MEP

2-C-methyl-d-erythritol 4-phosphate

PDS

phytoene desaturase

PSY

phytoene synthase

RT-qPCR

quantitative real-time polymerase chain reaction

UPLC

ultra performance liquid chromatography

ZDS

ξ-carotene isomerase

Z-ISO

ξ-carotene desaturase

Notes

Authors’ Contribution

AS Xiong and JW Li conceived and designed the experiments. JW Li, J Ma, K Feng, and JX Liu performed the experiments. JW Li and F Que. analyzed the data. AS Xiong contributed reagents/materials/analysis tools. JW Li wrote the paper. AS Xiong and K Feng revised the paper. All authors read and approved the final manuscript.

Funding Information

The research was supported by the New Century Excellent Talents in University (NCET-11-0670); National Natural Science Foundation of China (31272175); Jiangsu Natural Science Foundation (BK20130027); and Priority Academic Program Development of Jiangsu Higher Education Institutions.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

References

  1. Baron M, Davies S, Alexander L, Snellgrove D, Sloman KA (2008) The effect of dietary pigments on the coloration and behaviour of flame-red dwarf gourami, Colisa lalia. Anim Behav 75(3):1041–1051.  https://doi.org/10.1016/j.anbehav.2007.08.014 CrossRefGoogle Scholar
  2. Blumberg JB (1995) Considerations of the scientific substantiation for antioxidant vitamins and beta-carotene in disease prevention. Am J Clin Nutr 62(6 Suppl):1521S–1526S.  https://doi.org/10.1093/ajcn/62.6.1521S CrossRefPubMedGoogle Scholar
  3. Cao S, Liang M, Shi L, Shao J, Song C, Bian K, Chen W, Yang Z (2017) Accumulation of carotenoids and expression of carotenogenic genes in peach fruit. Food Chem 214:137–146.  https://doi.org/10.1016/j.foodchem.2016.07.085 CrossRefPubMedGoogle Scholar
  4. Cazzonelli CI, Pogson BJ (2010) Source to sink: regulation of carotenoid biosynthesis in plants. Trends Plant Sci 15(5):266–274.  https://doi.org/10.1016/j.tplants.2010.02.003 CrossRefPubMedGoogle Scholar
  5. Chen MD, Zhu HS, Wen QF, Hong-Qi MA, Lin YZ (2013) Determination of carotenoids in strawberry by UPLC. J Fruit Sci 30(4):706–711Google Scholar
  6. Cunningham FX, Gantt E (1998) Genes and enzymes of carotenoid biosynthesis in plants. Annu Rev Plant Physiol Plant Mol Biol 49:557–583.  https://doi.org/10.1146/annurev.arplant.49.1.557 CrossRefPubMedGoogle Scholar
  7. Cunningham FX Jr, Chamovitz D, Misawa N, Gantt E, Hirschberg J (1993) Cloning and functional expression in Escherichia coli of a cyanobacterial gene for lycopene cyclase, the enzyme that catalyzes the biosynthesis of beta-carotene. FEBS Lett 328(1–2):130–138.  https://doi.org/10.1016/0014-5793(93)80980-9 CrossRefPubMedGoogle Scholar
  8. Diretto G, Tavazza R, Welsch R, Pizzichini D, Mourgues F, Papacchioli V, Beyer P, Giuliano G (2006) Metabolic engineering of potato tuber carotenoids through tuber-specific silencing of lycopene epsilon cyclase. BMC Plant Biol 6(13):13.  https://doi.org/10.1186/1471-2229-6-13 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Ducreux LJ, Morris WL, Hedley PE, Shepherd T, Davies HV, Millam S, Taylor MA (2005) Metabolic engineering of high carotenoid potato tubers containing enhanced levels of beta-carotene and lutein. J Exp Bot 56(409):81–89.  https://doi.org/10.1093/jxb/eri016 CrossRefPubMedGoogle Scholar
  10. Feng K, Xu ZS, Liu JX, Li JW, Wang F, Xiong AS (2018) Isolation, purification, and characterization of AgUCGalT1, a galactosyltransferase involved in anthocyanin galactosylation in purple celery (Apium graveolens L.). Planta 247(6):1363–1375.  https://doi.org/10.1007/s00425-018-2870-5 CrossRefPubMedGoogle Scholar
  11. Frei B (1995) Cardiovascular disease and nutrient antioxidants: role of low-density lipoprotein oxidation. Crit Rev Food Sci Nutr 35(1–2):83–98.  https://doi.org/10.1080/10408399509527689 CrossRefPubMedGoogle Scholar
  12. Gemma F, Georgina S, Shaista N, Chao B, Teresa C, Zhu C, Paul C (2010) Travel advice on the road to carotenoids in plants. Plant Sci 179(1):28–48.  https://doi.org/10.1080/10408399509527689 CrossRefGoogle Scholar
  13. Giorio G, Stigliani AL, D'Ambrosio C (2008) Phytoene synthase genes in tomato (Solanumlycopersicum L.) - new data on the structures, the deduced amino acid sequences and the expression patterns. FEBS J 275(3):527–535.  https://doi.org/10.1111/j.1742-4658.2007.06219.x CrossRefPubMedGoogle Scholar
  14. Goto T, Kondo T (2010) Structure and molecular stacking of anthocyanins—flower color variation. Angew Chem Int Edit 30(1):17–33.  https://doi.org/10.1002/chem.200701914 CrossRefGoogle Scholar
  15. Havaux M (2014) Carotenoid oxidation products as stress signals in plants. Plant J 79(4):597–606.  https://doi.org/10.1111/tpj.12386 CrossRefPubMedGoogle Scholar
  16. Helaly AA, Baek JP, Mady E, Eldekashy MHZ, Craker L (2015) Phytochemical analysis of some celery accessions. J Med Act Plant 4(1):1–7.  https://doi.org/10.7275/R5542KJF CrossRefGoogle Scholar
  17. Hirschberg J (2001) Carotenoid biosynthesis in flowering plants. Curr Opin Plant Biol 4(3):210–218CrossRefPubMedGoogle Scholar
  18. Hornero-Méndez D, Gómez-Ladrón DGR, Mínguez-Mosquera MI (2000) Carotenoid biosynthesis changes in five red pepper (Capsicum annuum L.) cultivars during ripening. Cultivar selection for breeding. J Agric Food Chem 48(9):3857–3864CrossRefPubMedGoogle Scholar
  19. Hörtensteiner S (2004) The loss of green color during chlorophyll degradation--a prerequisite to prevent cell death? Planta 219(2):191–194.  https://doi.org/10.1007/s00425-004-1231-8 CrossRefPubMedGoogle Scholar
  20. Isaacson T, Ronen G, Zamir D, Hirschberg J (2002) Cloning of tangerine from tomato reveals a carotenoid isomerase essential for the production of beta-carotene and xanthophylls in plants. Plant Cell 14(2):333–342.  https://doi.org/10.1105/tpc.010303 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Jia XL, Wang GL, Xiong F, Yu XR, Xu ZS, Wang F, Xiong AS (2015) De novo assembly, transcriptome characterization, lignin accumulation, and anatomic characteristics: novel insights into lignin biosynthesis during celery leaf development. Sci Rep 5:8259.  https://doi.org/10.1038/srep08259 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Joanna F, Květoslava B (2014) Potential role of carotenoids as antioxidants in human health and disease. Nutrients 6(2):466–488.  https://doi.org/10.3390/nu6020466 CrossRefGoogle Scholar
  23. Krinsky NI, Johnson EJ (2005) Carotenoid actions and their relation to health and disease. Mol Asp Med 26(6):459–516.  https://doi.org/10.1016/j.mam.2005.10.001 CrossRefGoogle Scholar
  24. Li MY, Wang F, Jiang Q, Ma J, Xiong AS (2014) Identification of SSRs and differentially expressed genes in two cultivars of celery (Apium graveolens L.) by deep transcriptome sequencing. Hortic Res 1:10.  https://doi.org/10.1038/hortres.2014.10 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Li MY, Feng W, Qian J, Wang GL, Chang T, Xiong AS (2016) Validation and comparison of reference genes for qPCR normalization of celery (Apium graveolens) at different development stages. Front Plant Sci 7:313.  https://doi.org/10.3389/fpls.2016.00313 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Li MY, Hou XL, Wang F, Tan GF, Xu ZS, Xiong AS (2018) Advances in the research of celery, an important Apiaceae vegetable crop. Crit Rev Biotechnol 38(2):172–183.  https://doi.org/10.1080/07388551.2017.1312275 CrossRefPubMedGoogle Scholar
  27. Liu L, Shao Z, Zhang M, Wang Q (2015) Regulation of carotenoid metabolism in tomato. Mol Plant 8(1):28–39.  https://doi.org/10.1093/mp/ssu121 CrossRefPubMedGoogle Scholar
  28. Liu G, Yang X, Xu J, Zhang M, Hou Q, Zhu L, Huang Y, Xiong AS (2017) Morphological observation, RNA-Seq quantification, and expression profiling: novel insight into grafting-responsive carotenoid biosynthesis in watermelon grafted onto pumpkin rootstock. Acta Biochim Biophys Sin 49(3):216–227.  https://doi.org/10.1093/abbs/gmw132 CrossRefPubMedGoogle Scholar
  29. Lopez AB, Van Eck J, Conlin BJ, Paolillo DJ, O'Neill J, Li L (2008) Effect of the cauliflower Or transgene on carotenoid accumulation and chromoplast formation in transgenic potato tubers. J Exp Bot 59(2):213–223.  https://doi.org/10.1093/jxb/erm299 CrossRefPubMedGoogle Scholar
  30. Lv P, Li N, Liu H, Gu H, Zhao WE (2015) Changes in carotenoid profiles and in the expression pattern of the genes in carotenoid metabolisms during fruit development and ripening in four watermelon cultivars. Food Chem 174:52–59.  https://doi.org/10.1016/j.foodchem.2014.11.022 CrossRefPubMedGoogle Scholar
  31. Ma J, Xu Z, Tan G, Wang F, Xiong AS (2017) Distinct transcription profile of genes involved in carotenoid biosynthesis among six different color carrot (Daucus carota L.) cultivars. Acta Biochim Biophys Sin 49(9):817–826.  https://doi.org/10.1093/abbs/gmx081 CrossRefPubMedGoogle Scholar
  32. Ma J, Li JW, Xu ZS, Wang F, Xiong AS (2018) Transcriptome profiling of genes involving in carotenoid biosynthesis and accumulation between leaf and root of carrot (Daucus carota L.). Acta Biochim Biophys Sin 50(5):481–490.  https://doi.org/10.1093/abbs/gmy027 CrossRefPubMedGoogle Scholar
  33. Meier S, Tzfadia O, Vallabhaneni R, Gehring C, Wurtzel ET (2011) A transcriptional analysis of carotenoid, chlorophyll and plastidial isoprenoid biosynthesis genes during development and osmotic stress responses in Arabidopsis thaliana. BMC Syst Biol 5:77.  https://doi.org/10.1186/1752-0509-5-77 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Nijveldt RJ, van Nood E, van Hoorn DE, Boelens PG, van Norren K, van Leeuwen PA (2001) Flavonoids: a review of probable mechanisms of action and potential applications. Am J Clin Nutr 74(4):418–425.  https://doi.org/10.1093/ajcn/74.4.418 CrossRefPubMedGoogle Scholar
  35. Nisar N, Li L, Lu S, Khin NC, Pogson BJ (2015) Carotenoid metabolism in plants. Mol Plant 8(1):68–82.  https://doi.org/10.1016/j.molp.2014.12.007 CrossRefPubMedGoogle Scholar
  36. Ohmiya A (2013) Qualitative and quantitative control of carotenoid accumulation in flower petals. Sci Hortic-Amsterdam 163(6):10–19.  https://doi.org/10.1016/j.scienta.2013.06.018 CrossRefGoogle Scholar
  37. Polívka T, Frank HA (2010) Molecular factors controlling photosynthetic light-harvesting by carotenoids. Acc Chem Res 43(8):1125–1134.  https://doi.org/10.1021/ar100030m CrossRefPubMedPubMedCentralGoogle Scholar
  38. Poppel G (1993) Carotenoids and cancer: an update with emphasis on human intervention studies. Eur J Cancer 29A(9):1335–1344CrossRefPubMedGoogle Scholar
  39. Prabhala RH, Braune LM, Garewal HS, Watson RR (2010) Influence of beta-carotene on immune functions. Ann N Y Acad Sci 691(1):262–263.  https://doi.org/10.1111/j.1749-6632.1993.tb26189.x CrossRefGoogle Scholar
  40. Rodríguez-Concepción M (2010) Supply of precursors for carotenoid biosynthesis in plants. Arch Biochem Biophys 504(1):118–122.  https://doi.org/10.1016/j.abb.2010.06.016 CrossRefPubMedGoogle Scholar
  41. Rodriguez-Concepcion M, Stange C (2013) Biosynthesis of carotenoids in carrot: an underground story comes to light. Arch Biochem Biophys 539(2):110–116.  https://doi.org/10.1016/j.abb.2013.07.009 CrossRefPubMedGoogle Scholar
  42. Rodriguez-Uribe L, Guzman I, Rajapakse W, Richins RD, O'Connell MA (2012) Carotenoid accumulation in orange-pigmented Capsicum annuum fruit, regulated at multiple levels. J Exp Bot 63(1):517–526.  https://doi.org/10.1093/jxb/err302 CrossRefPubMedGoogle Scholar
  43. Romanová D, Vachálková A, Cipák L, Ovesná Z, Rauko P (2001) Study of antioxidant effect of apigenin, luteolin and quercetin by DNA protective method. Neoplasma 48(2):104–107PubMedGoogle Scholar
  44. Ronen G, Cohen M, Zamir D, Hirschberg J (1999) Regulation of carotenoid biosynthesis during tomato fruit development: expression of the gene for lycopene epsilon-cyclase is down-regulated during ripening and is elevated in the mutant Delta. Plant J 17(4):341–351CrossRefPubMedGoogle Scholar
  45. Ruiz-Sola MÁ, Rodríguez-Concepción M (2012) Carotenoid biosynthesis in Arabidopsis: a colorful pathway. Arabidopsis Book 10:e0158.  https://doi.org/10.1199/tab.0158 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3(6):1101–1108CrossRefPubMedGoogle Scholar
  47. Sowbhagya HB (2014) Chemistry, technology, and nutraceutical functions of celery (Apium graveolens L.): an overview. Crit Rev Food Sci Nutr 54(3):389–398.  https://doi.org/10.1080/10408398.2011.586740 CrossRefPubMedGoogle Scholar
  48. Tadmor Y, King S, Levi A, Davis A, Meir A, Wasserman B, Hirschberg J, Lewinsohn E (2005) Comparative fruit colouration in watermelon and tomato. Food Res Int 38(8):837–841.  https://doi.org/10.1016/j.foodres.2004.07.011 CrossRefGoogle Scholar
  49. Tan GF, Wang F, Ma J, Zhang XY, Xiong AS (2017a) Analysis of anthocyanin and apigenin contents and the expression profiles of biosynthesis-related genes in the purple and non-purple varieties of celery. Acta Hortic Sin 44(7):1327–1334Google Scholar
  50. Tan GF, Ma J, Zhang XY, Xu ZS, Xiong AS (2017b) AgFNS overexpression increase apigenin and decrease anthocyanins in petioles of transgenic celery. Plant Sci 263:31–38.  https://doi.org/10.1016/j.plantsci.2017.07.001 CrossRefPubMedGoogle Scholar
  51. Tanaka Y, Sasaki N, Ohmiya A (2008) Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids. Plant J 54(4):733–749.  https://doi.org/10.1111/j.1365-313X.2008.03447.x CrossRefPubMedGoogle Scholar
  52. Walter MH, Strack D (2011) Carotenoids and their cleavage products: biosynthesis and functions. Nat Prod Rep 42(28):663–692.  https://doi.org/10.1039/c0np00036a CrossRefGoogle Scholar
  53. Welsch R, Arango J, Bär C, Salazar B, Albabili S, Beltrán J, Chavarriaga P, Ceballos H, Tohme J, Beyer P (2010) Provitamin A accumulation in cassava (Manihot esculenta) roots driven by a single nucleotide polymorphism in a phytoene synthase gene. Plant Cell 22(10):3348–3356.  https://doi.org/10.1105/tpc.110.077560 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Wurtzel ET (2004) Chapter five genomics, genetics, and biochemistry of maize carotenoid biosynthesis. Recent Adv Phytochem 38(38):85–110CrossRefGoogle Scholar
  55. Xu ZS, Feng K, Que F, Wang F, Xiong AS (2017) A MYB transcription factor, DcMYB6, is involved in regulating anthocyanin biosynthesis in purple carrot taproots. Sci Rep 7:45324.  https://doi.org/10.1038/srep45324 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Yamagishi M, Kishimoto S, Nakayama M (2010) Carotenoid composition and changes in expression of carotenoid biosynthetic genes in tepals of Asiatic hybrid lily. Plant Breed 129(1):100–107.  https://doi.org/10.1111/j.1439-0523.2009.01656.x CrossRefGoogle Scholar
  57. Yoshida K, Mori M, Kondo T (2009) Blue flower color development by anthocyanins: from chemical structure to cell physiology. Nat Prod Rep 26(7):884–915.  https://doi.org/10.1039/b800165k CrossRefPubMedGoogle Scholar
  58. Yu B, Lydiate DJ, Young LW, Schäfer UA, Hannoufa A (2008) Enhancing the carotenoid content of Brassica napus seeds by downregulating lycopene epsilon cyclase. Transgenic Res 17(4):573–585.  https://doi.org/10.1007/s11248-007-9131-xTransgenic CrossRefPubMedGoogle Scholar
  59. Yuan H, Zhang J, Nageswaran D, Li L (2015) Carotenoid metabolism and regulation in horticultural crops. Hortic Res 2:15036.  https://doi.org/10.1038/hortres.2015.36 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Jing-Wen Li
    • 1
  • Jing Ma
    • 1
  • Kai Feng
    • 1
  • Jie-Xia Liu
    • 1
  • Feng Que
    • 1
  • Ai-Sheng Xiong
    • 1
  1. 1.State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of HorticultureNanjing Agricultural UniversityNanjingChina

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