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J. Biol. Chem., Vol. 283, Issue 36, 24816-24825, September 5, 2008

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Cytosolic and Plastoglobule-targeted Carotenoid Dioxygenases from Crocus sativus Are Both Involved in β-Ionone Release^*

Angela Rubio, José Luís Rambla, Marcella Santaella, M. Dolores Gómez, Diego Orzaez, Antonio Granell, and Lourdes Gómez-Gómez¹

From the Sección de Biotecnología, Instituto de Desarrollo Regional, ETSIA, Universidad de Castilla-La Mancha, Campus Universitario s/n, Albacete, 02071 and the Instituto de Biología Molecular y Celular de Plantas, Consejo Superior de Investigacíones Científicas-Universidad Politécnica de Valencia, Ingeniero Fausto Elio s/n, 46022 Valencia, Spain

Saffron, the processed stigma of Crocus sativus, is characterized by the presence of several apocarotenoids that contribute to the color, flavor, and aroma of the spice. However, little is known about the synthesis of aroma compounds during the development of the C. sativus stigma. The developing stigma is nearly odorless, but before and at anthesis, the aromatic compound β-ionone becomes the principal norisoprenoid volatile in the stigma. In this study, four carotenoid cleavage dioxygenase (CCD) genes, CsCCD1a, CsCCD1b, CsCCD4a, and CsCCD4b, were isolated from C. sativus. Expression analysis showed that CsCCD1a was constitutively expressed, CsCCD1b was unique to the stigma tissue, but only CsCCD4a and -b had expression patterns consistent with the highest levels of β-carotene and emission of β-ionone derived during the stigma development. The CsCCD4 enzymes were localized in plastids and more specifically were present in the plastoglobules. The enzymatic activities of CsCCD1a, CsCCD1b, and CsCCD4 enzymes were determined by Escherichia coli expression, and subsequent analysis of the volatile products was generated by GC/MS. The four CCDs fell in two phylogenetically divergent dioxygenase classes, but all could cleave β-carotene at the 9,10(9',10') positions to yield β-ionone. The data obtained suggest that all four C. sativus CCD enzymes may contribute in different ways to the production of β-ionone. In addition, the location and precise timing of β-ionone synthesis, together with its known activity as a fragrance and insect attractant, suggest that this volatile may have a role in Crocus pollination.

Received for publication, May 26, 2008 , and in revised form, June 27, 2008.

^* This work was supported by Ministerio de Educación y Ciencia Grants BIO2003-05259 and BIO2006-00841. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ To whom correspondence should be addressed. Tel.: 34-967599200 (ext. 2612); Fax: 34-967599233; E-mail: marialourdes.gomez{at}uclm.es.

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