Biologia plantarum 64: 504-511, 2020 | DOI: 10.32615/bp.2020.068

Comprehensive transcriptome analyses of different Crocus flower tissues uncover genes involved in crocin biosynthesis

H.M. SHU*, S.Q. GUO, W.C. NI*
Institute of Industrial Crops, Jiangsu Academy of Agricultural Sciences, Nanjing 210014, P.R. China

The stigma of Crocus sativus is used in traditional Chinese medicine and has drawn attention as a rich source of crocin, a compound with a reported activity that counters various cancers, depression, and cardiovascular diseases. However, our knowledge of crocin biosynthesis in Crocus is still limited. To identify the genes that encode key enzymes responsible for crocin production, transcriptome analyses of Crocus stigma, petal, and stamen were performed. There were 109 136 unigenes in the three Crocus flower tissues: 10 862 unigenes were expressed explicitly in stigmas. A total of 469 and 335 down-regulated differentially expressed genes in comparison to stigmas were detected in stamens and petals, respectively. There were 290 down-regulated genes in both tissues. The gene ontology enrichment and Kyoto Encyclopedia of Genes and Genomes analysis revealed that most genes in the two tissues served a similar function. The results of the differences of gene expression among the three tissues showed that most of the carotenoid pathway genes in stigmas had a high expression which was a benefit for producing zeaxanthin, a substrate of crocin. Fourteen candidate genes were identified in Crocus from the co-down-regulated genes, and the genes were expressed explicitly in stigmas and were predicted to be involved in crocin biosynthesis. Overall, the expressions of genes in the crocin biosynthesis pathway in the three Crocus flower tissues had a positive relationship with their crocin content, and some new candidate genes related to crocin biosynthesis were identified. The results can help elucidate the crocin biosynthesis pathway in Crocus.

Keywords: carotenoids, differentially expressed genes, petal, stamen, stigma, unigenes, zeaxanthin.

Received: March 3, 2020; Revised: May 4, 2020; Accepted: May 7, 2020; Published online: July 16, 2020Show citation

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SHU, H.M., GUO, S.Q., & NI, W.C. (2020). Comprehensive transcriptome analyses of different Crocus flower tissues uncover genes involved in crocin biosynthesis. Biologia plantarum, 64, 504-511. doi: 10.32615/bp.2020.068.
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    References

    1. Agayev, Y.M., Fernandez, J.A., Zarifi, E.: Clonal selection of saffron (Crocus sativus L.): the first optimistic experimental results. - Euphytica 169: 81-99, 2009. Go to original source...
    2. Agayev, Y.M., Shakib, A.M., Soheilivand, S., Fathim M.: Breeding of saffron (Crocus sativus): possibilities and problems. - Acta Hort. 739: 203-207, 2007. Go to original source...
    3. Ahrazem, O., Rubio-Moraga, A., Trapero-Mozos, A., Climent, M.F.L., Gomez-Cadenas, A., Gomez-Gomez, L.: Ectopic expression of a stress-inducible glycosyltransferase from saffron enhances salt and oxidative stress tolerance in Arabidopsis while alters anchor root formation. - Plant Sci. 234: 60-73, 2015. Go to original source...
    4. Baba, S.A., Malik, A.H., Wani, Z.A., Mohiuddin, T., Shah, Z., Abbas, N., Ashraf, N.: Phytochemical analysis and antioxidant activity of different tissue types of Crocus sativus and oxidative stress alleviating potential of saffron extract in plants, bacteria, and yeast. - S. Afr. J. Bot. 99: 80-87, 2015a. Go to original source...
    5. Baba, S.A., Mohiuddin, T., Basu, S., Swarnkar, M.K., Malik, A.H., Wani, Z.A., Abbas, N., Singh, A.K., and Ashraf, N.: Comprehensive transcriptome analysis of Crocus sativus for discovery and expression of genes involved in apocarotenoid biosynthesis. - BMC Genomics 16: 698, 2015b. Go to original source...
    6. Bouvier, F., Suire, C., Mutterer, J., Camara, B.: Oxidative remodeling of chromoplast carotenoids: identification of the carotenoid dioxygenase CsCCD and CsZCD genes involved in Crocus secondary metabolite biogenesis. - Plant Cell 15: 47-62, 2003. Go to original source...
    7. D'Agostino, N., Pizzichini, D., Chiusano, M.L., Giuliano, G.: An EST database from saffron stigmas. - BMC Plant Biol. 7: 53, 2007. Go to original source...
    8. Demurtas, O.C., Frusciante, S., Ferrante, P., Diretto, G., Azad, N.H., Pietrella, M., Aprea, G., Taddei, A.R., Romano, E., Mi, J., Al-Babili, A., Frigerio, L., Giuliano, G.: Candidate enzymes for saffron crocin biosynthesis are localized in multiple cellular compartments. - Plant Physiol. 177: 990-1006, 2018. Go to original source...
    9. Douglas, M.H., Smallfield, B.M., Wallace, A.R., McGimpsey, J.A.: Saffron (Crocus sativus L.): The effect of mother corm size on progeny multiplication, flower and stigma production. - Sci Hort. 166: 50-58, 2014. Go to original source...
    10. Fernandez, J.: Biology, biotechnology and biomedicine of saffron. - Recent Res. Dev. Plant Sci. 2: 127-159, 2004.
    11. Frusciante, S., Diretto, G., Bruno, M., Ferrante, P., Pietrella, M., Prado-Cabrero, A., Beyer, P., Gomez-Gom, L., Al-Babili, S., Giuliano, G.: Novel carotenoid cleavage dioxygenase catalyzes the first dedicated step in saffron crocin biosynthesis. - Proc. nat. Acad. Sci. USA 111: 12246-12251, 2014. Go to original source...
    12. Gainer, J.L., Brumgard, F.B. Using excess volume of mixing to correlate diffusivities in liquids. - Chem. Eng. Commun. 15: 323-329, 1982. Go to original source...
    13. Grabherr, M.G., Haas, B.J., Yassour, M., Levin, J.Z., Thompson, D.A., Amit, I., Adiconis, X., Fan, L., Raychowdhury, R., Zeng, Q., Chen, Z., Mauceli. E., Hacohen, N., Gnirke, A., Rhind, N., Palma, F., Birren, B.W., Nusbaum, C., Lindblad-Toh, K., Friedman, N., Regev, A.: Full-length transcriptome assembly from RNA-Seq data without a reference genome. - Nat. Biotechnol. 29: 644-652, 2011. Go to original source...
    14. Gresta, F., Avola, G., Lombardo, G.M., Siracusa, L., Ruberto, G.: Analysis of flowering, stigmas yield and qualitative traits of saffron (Crocus sativus L.) as affected by environmental conditions. - Sci Hort. 119: 320-324, 2009. Go to original source...
    15. Gresta, F., Lombardo, G.M., Siracusa, L., Ruberto, G.: 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 Agr. 88: 1144-1150, 2010.
    16. Hosseinzadeh, H., Sadeghnia, H.R., Ghaeni, F.A., Motamedshariaty, V.S., Mohajeri, S.A.: Effects of saffron (Crocus sativus L.) and its active constituent, crocin, on recognition and spatial memory after chronic cerebral hypoperfusion in rats. - Phytotheraphy Res. 26: 381-386, 2012. Go to original source...
    17. Jain, M., Srivastava, P.L., Verma, M., Ghangal, R., Garg, R.: De novo transcriptome assembly and comprehensive expression profiling in Crocus sativus to gain insights into apocarotenoid biosynthesis. - Sci. Rep. 6: 22456, 2016. Go to original source...
    18. Ji, A., Jia, J., Xu, Z., Li, Y., Bi, W., Ren, F., He, C., Liu, J., Hu, K., Song, J.: Transcriptome-guided mining of genes involved in crocin biosynthesis. - Front. Plant Sci. 8: 518, 2017. Go to original source...
    19. Juan, J.A., Corcoles, H.L., Munoz, R.M., Picornell, M.R.: Yield and yield components of saffron under different cropping systems. - Ind. Crop Prod. 30: 212-219, 2009. Go to original source...
    20. Kanehisa, M., Araki, M., Goto, S., Hattori, M., Hirakawa, M., Itoh, M., Katayama, T., Kawashima, S., Okuda, S., Tokimatsu, T., Yamanishi, Y.: KEGG for linking genomes to life and the environment. - Nucl. Acids Res. 36(S1): 480-484, 2008.
    21. Li, B., Dewey, C.: RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. - BMC Bioinformatics 12: 323, 2011. Go to original source...
    22. Livak, K.J., Schmittgen, T.D.: Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT Method. - Methods. 25: 402-408, 2001. Go to original source...
    23. Mao, X., Cai, T., Olyarchuk, J.G., Wei, L.: Automated genome annotation and pathway identification using the KEGG orthology (KO) as a controlled vocabulary. - Bioinformatics 21: 3787-3793, 2005. Go to original source...
    24. Molina, R.V., Valero, M., Navarro, Y., Guardiola, J.L., Garcia-Luis, A.: Temperature effects on flower formation in saffron (Crocus sativus L.). - Sci. Hort. 103: 361-379, 2005. Go to original source...
    25. Mortazavi, A., Williams, B.A., McCue, K., Schaeffer, L., Wold, A.: Mapping and quantifying mammalian transcriptomes by RNA-Seq. - Nat. Methods 5: 621-628, 2008. Go to original source...
    26. Razavi, B.M., Hosseinzadeh, H., Movassaghi, A.R., Imenshahidi, M., Abnous, K.: Protective effect of crocin on diazinon induced cardiotoxicity in rats in subchronic exposure. - Chemicobiol. Interact. 203: 547-555, 2013. Go to original source...
    27. Rezaee, R., Hosseinzadeh, H.: Safranal: from an aromatic natural product to a rewarding pharmacological agent. - Iran J. basic med. Sci. 16: 12-26, 2013.
    28. Storey, J.D., Tibshirani, R.: Statistical significance for genome wide studies. - Proc. nat. Acad. Sci. USA 100: 9440-9445, 2003. Go to original source...
    29. Wang. Y., Han. T., Zhu, Y., Zheng, C.J., Ming, Q.L., Rahman, K., Qin, L.P.: Antidepressant properties of bioactive fractions from the extract of Crocus sativus L. - J. Natur. Med. 64: 24-30, 2010. Go to original source...
    30. Young, M.D., Wakefield, M.J., Smyth, G.K., Oshlack, A.: Gene ontology analysis for RNA-seq: accounting for selection bias. - Genome Biol. 11: R14, 2010. Go to original source...

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