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Flower cultivation regimes affect apocarotenoid accumulation and gene expression during the development of saffron stigma

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Abstract

The quality of commercial saffron largely depends on apocarotenoid levels. Whether they are affected by different flower cultivation regimes remains unknown. In present study, apocarotenoid levels and the expression profiles of 12 genes related to apocarotenoid biosynthesis between field- and indoor-cultivated Crocus sativus L. were analyzed during stigma development. Under both cultivation regimes, apocarotenoid accumulation and gene expression showed similar profiles, first sharply increasing and then gradually decreasing with stigma development, which suggested the coordinated function of gene expression and apocarotenoid accumulation. However, the rate of increase/decrease varied widely between two blossom regimes at different developmental stages. Based on correlation analysis, βCH1 and ZDS seemed to play a more crucial role in apocarotenoid accumulation under both cultivation regimes. At anthesis, the total apocarotenoid level in saffron cultivated in the field was higher than that cultivated indoors. This may be due to lower gene expression levels in the apocarotenoid pathway, especially βCH1, ZDS, and CCD2, and higher CCD4a and NCED expression in the competitive pathway in saffron cultivated indoors than that in the field, which indicated higher conversion in apocarotenoid biosynthesis flux from crocins and picrocrocin synthesis to β-ionone and the ABA biosynthetic branch in saffron cultivated indoors. These results provide valuable information for modifying planting mode to enhance saffron quality.

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References

  • Ahrazem O, Rubio-Moraga A, López RC, Gómez-Gómez L (2010) The expression of a chromoplast-specific lycopene beta cyclase gene is involved in the high production of saffron's apocarotenoid precursors. J Exp Bot 61:105–119

    CAS  PubMed  Google Scholar 

  • Ahrazem O, Rubio-moraga A, Trapero A, Gómez-Gómez L (2012) Developmental and stress regulation of gene expression for a 9-cis-epoxycarotenoid dioxygenase, CstNCED, isolated from Crocus sativus stigmas. J Exp Bot 63:681–694

    CAS  PubMed  Google Scholar 

  • Ahrazem O, Rubio-Moraga A, Nebauer SG, Molina RV, Gómez-Gómez L (2015a) Saffron: its phytochemistry, developmental processes and biotechnological prospects. J Agric Food Chem 63:8751–8764

    CAS  PubMed  Google Scholar 

  • Ahrazem O, Rubio-moraga A, Jimeno ML, Gómez-Gómez L (2015b) Structural characterization of highly glucosylated crocins and regulation of their biosynthesis during flower development in Crocus. Front Plant Sci 6:53–85

    Google Scholar 

  • Ahrazem O, Rubio-Moraga A, Berman J, Capell T, Christou P, Zhu CF, Gómez-Gómez L (2016) The carotenoid cleavage dioxygenase CCD2 catalysing the synthesis of crocetin in spring crocuses and saffron is a plastidial enzyme. New Phytol 209:650–663

    CAS  PubMed  Google Scholar 

  • Ahrazem O, Diretto G, Argandoña J, Rubio-Moraga A, Julve JM, Orzáez D, Granell A, Gómez-Gómez L (2017) Evolutionarily distinct carotenoid cleavage dioxygenases are responsible for crocetin production in Buddleja davidii. J Exp Bot 68:4663–4677

    CAS  PubMed  Google Scholar 

  • Ahrazem O, Diretto G, Argandoña Picazo J, Fiore A, Rubio-Moraga A, Rial C, Varela RM, Macias FA, Castillo R, Romano E, Gómez-Gómez L (2019) The specialized roles in carotenogenesis and apocarotenogenesis of the phytoene synthase gene family in saffron. Front Plant Sci 10:1–16

    Google Scholar 

  • Cardone L, Castronuovo D, Perniola M, Cicco N, Candido V (2019) Evaluation of corm origin and climatic conditions on saffron (Crocus sativus L.) yield and quality. J Sci Food Agric 99:5858–5869

    CAS  PubMed  Google Scholar 

  • Castillo R, Fernández JA, Gómez-Góme L (2005) Implications of carotenoid biosynthetic genes in apocarotenoid formation during the stigma development of Crocus sativus and its closer relatives. Plant Physiol 139:674–689

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chaouqi S, Moratalla-Lopez N, Lage M, Lorenzo C, Alonso GL, Guedira T (2018) Effect of drying and storage process on Moroccan saffron quality. Food Biosci 22:146–153

    CAS  Google Scholar 

  • Cheng L, Han M, Yang LM, Yang L, Sun Z, Zhang T (2018) Changes in the physiological characteristics and baicalin biosynthesis metabolism of Scutellaria baicalensis Georgi under drought stress. Ind Crops Prod 122:473–482

    CAS  Google Scholar 

  • Demurtas OC, Frusciante S, Ferrante P, Diretto G, Azad NH, Pietrella M, Aprea G, Taddei AR, Romano E, Mi JN, Al-Babili S, Frigerio L, Giuliano G (2018) Candidate enzymes for saffron crocin biosynthesis are localized in multiple cellular compartments. Plant Physiol 177:990–1006

    CAS  PubMed  PubMed Central  Google Scholar 

  • Feng XB, Qian XD, Han SW, Yao C, Yuan YM, Zhou GF (2018) Extracted apocarotenoids from saffron stigmas and evaluated the quality of saffron. Nat Prod Res 32:225–228

    CAS  Google Scholar 

  • Frusciante S, Diretto G, Bruno M, Ferrante P, Pietrella M, Prado-Cabrero A, Rubio-Moraga A, Beyer P, Gomez-Gomez L, Al-Babili S, Giuliano G (2014) Novel carotenoid cleavage dioxygenase catalyzes the first dedicated step in saffron crocin biosynthesis. Proc Natl Acad Sci USA 111:12246–12251

    CAS  PubMed  Google Scholar 

  • González-Villagra J, Cohen JD, Reyes-Díaz MM (2019) Abscisic acid (ABA) is involved in phenolic compounds biosynthesis, mainly anthocyanins, in leaves of Aristotelia chilensis plants (Mol.) subjected to drought stress. Physiol Plant 165:855–866

    PubMed  Google Scholar 

  • Gracia L, Perez-Vidal C, Gracia-Lopez C (2009) Automated cutting system to obtain the stigmas of the saffron flower. Biosyst Eng 104:8–17

    Google Scholar 

  • Gregory MJ, Menary RC, Davies NW (2005) Effect of drying temperature and air flow on the production and retention of secondary metabolites in saffron. J Agric Food Chem 53:5969–5975

    CAS  PubMed  Google Scholar 

  • Gresta F, Lombardo GM, Siracusa L, Ruberto G (2008a) Saffron, an alternative crop for sustainable agricultural systems. A review. Agron Sustain Dev 28:95–112

    CAS  Google Scholar 

  • Gresta F, Lombardo GM, Siracusa L, Ruberto G (2008b) Effect of mother corm dimension and sowing time on stigma yield, daughter corms and qualitative aspects of saffron (Crocus sativus L.) in a Mediterranean environment. J Sci Food Agric 88:1144–1150

    CAS  Google Scholar 

  • Gresta F, Avola G, Lombardo GM, Siracusa L, Ruberto G (2009) Analysis of flowering, stigmas yield and qualitative traits of saffron (Crocus sativus L.) as affected by environmental conditions. Sci Hortic 119:320–324

    Google Scholar 

  • Huang Y, Guo YM, Liu YT, Zhang F, Wang ZK, Wang HY, Wang F, Li DP, Mao DD, Luan S, Liang MZ, Chen LB (2018) 9-cis-epoxycarotenoid dioxygenase 3 regulates plant growth and enhances multi-abiotic stress tolerance in rice. Front Plant Sci 9:1–18

    Google Scholar 

  • Jain M, Srivastava PL, Verma M, Ghangal R, Garg R (2016) De novo transcriptome assembly and comprehensive expression profiling in Crocus sativus to gain insights into apocarotenoid biosynthesis. Sci Rep 6:1–13

    CAS  Google Scholar 

  • Kashani L, Eslatmanesh S, Saedi N, Niroomand N, Ebrahimi M, Hosseinian M, Foroughifar T, Salimi S, Akhondzadeh S (2017) Comparison of saffron versus fluoxetine in treatment of mild to moderate postpartum depression: a double-blind, randomized clinical trial. Pharmacopsychiatry 50:64–68

    CAS  PubMed  Google Scholar 

  • Khanali M, Shahvarooghi Farahani S, Shojaei H, Elhami B (2017) Life cycle environmental impacts of saffron production in Iran. Environ Sci Pollut Res 24:4812–4821

    CAS  Google Scholar 

  • Khorasanchi Z, Shafiee M, Kermanshahi F, Khazaei M, Ryzhikov M, Parizadeh MR, Kermanshahi B, Ferns GA, Avan A, Hassanian SM (2018) Crocus sativus a natural food coloring and flavoring has potent anti-tumor properties. Phytomedicine 43:21–27

    CAS  PubMed  Google Scholar 

  • Lage M, Cantrell CL (2009) Quantification of saffron (Crocus sativus L.) metabolites crocins, picrocrocin and safranal for quality determination of the spice grown under different environmental Moroccan conditions. Sci Hortic 121:366–373

    CAS  Google Scholar 

  • Lee YI, Chen MC, Lin L, Chung MC, Leu WM (2018) Increased expression of 9-cis-epoxycarotenoid dioxygenase, PtNCED1, associated with inhibited seed germination in a terrestrial orchid, Phaius tankervilliae. Front Plant Sci 9:1–13

    Google Scholar 

  • Liu JD, Chen N, Yang J, Yang B, Ouyang Z, Wu CX, Yuan Y, Wang WH, Chen M (2018) An integrated approach combining HPLC, GC/MS, NIRS, and chemometrics for the geographical discrimination and commercial categorization of saffron. Food Chem 253:284–292

    CAS  PubMed  Google Scholar 

  • Liu J, Hasanuzzaman M, Wen HL, Zhang J, Peng T, Sun HW, Zhao QZ (2019) High temperature and drought stress cause abscisic acid and reactive oxygen species accumulation and suppress seed germination growth in rice. Protoplasma 256:1217–1227

    CAS  PubMed  Google Scholar 

  • Maggi L, Carmona M, Zalacain A, Kanakis CD, Anastasaki E, Tarantilis PA, Polissiou MG, Alonso GL (2010) Changes in saffron volatile profile according to its storage time. Food Res Int 43:1329–1334

    CAS  Google Scholar 

  • Milajerdi A, Djafarian K, Hosseini B (2016) The toxicity of saffron (Crocus sativus L.) and its constituents against normal and cancer cells. J Nutr Intermed Metab 3:23–32

    Google Scholar 

  • Molina RV, Valero M, Navarro Y, Guardiola JL, García-Luis A (2005) Temperature effects on flower formation in saffron (Crocus sativus L.). Sci Hortic 103:361–379

    Google Scholar 

  • Moraga AR, Nohales PF, Pérez JAF, Gómez-Gómez L (2004) Glucosylation of the saffron apocarotenoid crocetin by a glucosyltransferase isolated from Crocus sativus stigmas. Planta 219:955–966

    CAS  PubMed  Google Scholar 

  • Patel S, Sarwat M, Khan TH (2017) Mechanism behind the anti-tumour potential of saffron (Crocus sativus L.): the molecular perspective. Critic Rev Oncol Hematol 115:27–35

    Google Scholar 

  • Pfister S, Meyer P, Steck A, Pfander H (1996) Isolation and structure elucidation of carotenoid-glycosyl esters in gardenia fruits (Gardenia jasminoides Ellis) and saffron (Crocus sativus Linne). J Agric Food Chem 44:2612–2615

    CAS  Google Scholar 

  • Rahaiee S, Moini S, Hashemi M, Shojaosadati SA (2015) Evaluation of antioxidant activities of bioactive compounds and various extracts obtained from saffron (Crocus sativus L.): a review. J Food Sci Technol 52:1881–1888

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shafiee M, Arekhi S, Omranzadeh A, Sahebkar A (2018) Saffron in the treatment of depression, anxiety and other mental disorders: current evidence and potential mechanisms of action. J Affect Disord 227:330–337

    CAS  PubMed  Google Scholar 

  • Shahi T, Assadpour E, Jafari SM (2016) Main chemical compounds and pharmacological activities of stigmas and tepals of 'red gold'; saffron. Trends Food Sci Technol 58:69–78

    CAS  Google Scholar 

  • Sharma M, Kaul S, Dhar MK (2018) Transcript profiling of carotenoid/apocarotenoid biosynthesis genes during corm development of saffron (Crocus sativus L.). Protoplasma 256:249–260

    PubMed  Google Scholar 

  • Siracusa L, Gresta F, Avola G, Lombardo GM, Ruberto G (2010) Influence of corm provenance and environmental condition on yield and apocarotenoid profiles in saffron (Crocus sativus L.). J Food Compos Anal 23:394–400

    CAS  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China [Grant Numbers 81673528, 81403032] and Zhejiang Province public welfare technology application research project [Grant Numbers 2017C32069, LGN18H280001].

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ZGF conceived the study, designed the experiments, and wrote the manuscript. LLQ, LJM, LJ, YC, SP, LKH, and DY carried out the experiments and analyzed the data. QLP and QXD helped to guide the experiments and revise the manuscript. All authors read and approved the final manuscript.

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Correspondence to Luping Qin.

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Communicated by Cecile Segonzac.

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Zhou, G., Li, L., Lu, J. et al. Flower cultivation regimes affect apocarotenoid accumulation and gene expression during the development of saffron stigma. Hortic. Environ. Biotechnol. 61, 473–484 (2020). https://doi.org/10.1007/s13580-020-00248-4

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