A mutant allele of ζ-carotene isomerase (Z-ISO) is associated with the yellow pigmentation of the “Pinalate” sweet orange mutant and reveals new insights into its role in fruit carotenogenesis

[Background] Fruit coloration is one of the main quality parameters of Citrus fruit primarily determined by genetic factors. The fruit of ordinary sweet orange (Citrus sinensis) displays a pleasant orange tint due to accumulation of carotenoids, representing β,β-xanthophylls more than 80% of the total content. ‘Pinalate’ is a spontaneous bud mutant, or somatic mutation, derived from sweet orange ‘Navelate’, characterized by yellow fruits due to elevated proportions of upstream carotenes and reduced β,β-xanthophylls, which suggests a biosynthetic blockage at early steps of the carotenoid pathway.

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Main Authors: Rodrigo, María Jesús, Lado, Joanna, Alós, Enriqueta, Alquézar García, Berta, Dery, Orly, Hirschberg, Joseph, Zacarías, Lorenzo
Other Authors: Agencia Estatal de Investigación (España)
Format: artículo biblioteca
Published: BioMed Central 2019-11-04
Subjects:Carotenoids, ζ-Carotene isomerase, Citrus fruit, Mutant, Pigmentation, Ripening, Gene expression,
Online Access:http://hdl.handle.net/10261/194244
http://dx.doi.org/10.13039/501100011033
http://dx.doi.org/10.13039/501100000921
http://dx.doi.org/10.13039/501100003977
http://dx.doi.org/10.13039/501100003329
http://dx.doi.org/10.13039/501100003339
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id dig-iata-es-10261-194244
record_format koha
institution IATA ES
collection DSpace
country España
countrycode ES
component Bibliográfico
access En linea
databasecode dig-iata-es
tag biblioteca
region Europa del Sur
libraryname Biblioteca del IATA España
topic Carotenoids
ζ-Carotene isomerase
Citrus fruit
Mutant
Pigmentation
Ripening
Gene expression
Carotenoids
ζ-Carotene isomerase
Citrus fruit
Mutant
Pigmentation
Ripening
Gene expression
spellingShingle Carotenoids
ζ-Carotene isomerase
Citrus fruit
Mutant
Pigmentation
Ripening
Gene expression
Carotenoids
ζ-Carotene isomerase
Citrus fruit
Mutant
Pigmentation
Ripening
Gene expression
Rodrigo, María Jesús
Lado, Joanna
Alós, Enriqueta
Alquézar García, Berta
Dery, Orly
Hirschberg, Joseph
Zacarías, Lorenzo
A mutant allele of ζ-carotene isomerase (Z-ISO) is associated with the yellow pigmentation of the “Pinalate” sweet orange mutant and reveals new insights into its role in fruit carotenogenesis
description [Background] Fruit coloration is one of the main quality parameters of Citrus fruit primarily determined by genetic factors. The fruit of ordinary sweet orange (Citrus sinensis) displays a pleasant orange tint due to accumulation of carotenoids, representing β,β-xanthophylls more than 80% of the total content. ‘Pinalate’ is a spontaneous bud mutant, or somatic mutation, derived from sweet orange ‘Navelate’, characterized by yellow fruits due to elevated proportions of upstream carotenes and reduced β,β-xanthophylls, which suggests a biosynthetic blockage at early steps of the carotenoid pathway.
author2 Agencia Estatal de Investigación (España)
author_facet Agencia Estatal de Investigación (España)
Rodrigo, María Jesús
Lado, Joanna
Alós, Enriqueta
Alquézar García, Berta
Dery, Orly
Hirschberg, Joseph
Zacarías, Lorenzo
format artículo
topic_facet Carotenoids
ζ-Carotene isomerase
Citrus fruit
Mutant
Pigmentation
Ripening
Gene expression
author Rodrigo, María Jesús
Lado, Joanna
Alós, Enriqueta
Alquézar García, Berta
Dery, Orly
Hirschberg, Joseph
Zacarías, Lorenzo
author_sort Rodrigo, María Jesús
title A mutant allele of ζ-carotene isomerase (Z-ISO) is associated with the yellow pigmentation of the “Pinalate” sweet orange mutant and reveals new insights into its role in fruit carotenogenesis
title_short A mutant allele of ζ-carotene isomerase (Z-ISO) is associated with the yellow pigmentation of the “Pinalate” sweet orange mutant and reveals new insights into its role in fruit carotenogenesis
title_full A mutant allele of ζ-carotene isomerase (Z-ISO) is associated with the yellow pigmentation of the “Pinalate” sweet orange mutant and reveals new insights into its role in fruit carotenogenesis
title_fullStr A mutant allele of ζ-carotene isomerase (Z-ISO) is associated with the yellow pigmentation of the “Pinalate” sweet orange mutant and reveals new insights into its role in fruit carotenogenesis
title_full_unstemmed A mutant allele of ζ-carotene isomerase (Z-ISO) is associated with the yellow pigmentation of the “Pinalate” sweet orange mutant and reveals new insights into its role in fruit carotenogenesis
title_sort mutant allele of ζ-carotene isomerase (z-iso) is associated with the yellow pigmentation of the “pinalate” sweet orange mutant and reveals new insights into its role in fruit carotenogenesis
publisher BioMed Central
publishDate 2019-11-04
url http://hdl.handle.net/10261/194244
http://dx.doi.org/10.13039/501100011033
http://dx.doi.org/10.13039/501100000921
http://dx.doi.org/10.13039/501100003977
http://dx.doi.org/10.13039/501100003329
http://dx.doi.org/10.13039/501100003339
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spelling dig-iata-es-10261-1942442021-12-28T16:07:36Z A mutant allele of ζ-carotene isomerase (Z-ISO) is associated with the yellow pigmentation of the “Pinalate” sweet orange mutant and reveals new insights into its role in fruit carotenogenesis Rodrigo, María Jesús Lado, Joanna Alós, Enriqueta Alquézar García, Berta Dery, Orly Hirschberg, Joseph Zacarías, Lorenzo Agencia Estatal de Investigación (España) Consejo Superior de Investigaciones Científicas (España) Israel Science Foundation European Cooperation in Science and Technology Ministerio de Economía y Competitividad (España) Ministerio de Ciencia, Innovación y Universidades (España) Rodrigo, María Jesús [0000-0003-2668-0684] Carotenoids ζ-Carotene isomerase Citrus fruit Mutant Pigmentation Ripening Gene expression [Background] Fruit coloration is one of the main quality parameters of Citrus fruit primarily determined by genetic factors. The fruit of ordinary sweet orange (Citrus sinensis) displays a pleasant orange tint due to accumulation of carotenoids, representing β,β-xanthophylls more than 80% of the total content. ‘Pinalate’ is a spontaneous bud mutant, or somatic mutation, derived from sweet orange ‘Navelate’, characterized by yellow fruits due to elevated proportions of upstream carotenes and reduced β,β-xanthophylls, which suggests a biosynthetic blockage at early steps of the carotenoid pathway. [Results] To identify the molecular basis of ‘Pinalate’ yellow fruit, a complete characterization of carotenoids profile together with transcriptional changes in carotenoid biosynthetic genes were performed in mutant and parental fruits during development and ripening. ‘Pinalate’ fruit showed a distinctive carotenoid profile at all ripening stages, accumulating phytoene, phytofluene and unusual proportions of 9,15,9′-tri-cis- and 9,9′-di-cis-ζ-carotene, while content of downstream carotenoids was significantly decreased. Transcript levels for most of the carotenoid biosynthetic genes showed no alterations in ‘Pinalate’; however, the steady-state level mRNA of ζ-carotene isomerase (Z-ISO), which catalyses the conversion of 9,15,9′-tri-cis- to 9,9′-di-cis-ζ-carotene, was significantly reduced both in ‘Pinalate’ fruit and leaf tissues. Isolation of the ‘Pinalate’ Z-ISO genomic sequence identified a new allele with a single nucleotide insertion at the second exon, which generates an alternative splicing site that alters Z-ISO transcripts encoding non-functional enzyme. Moreover, functional assays of citrus Z-ISO in E.coli showed that light is able to enhance a non-enzymatic isomerization of tri-cis to di-cis-ζ-carotene, which is in agreement with the partial rescue of mutant phenotype when ‘Pinalate’ fruits are highly exposed to light during ripening. [Conclusion] A single nucleotide insertion has been identified in ‘Pinalate’ Z-ISO gene that results in truncated proteins. This causes a bottleneck in the carotenoid pathway with an unbalanced content of carotenes upstream to β,β-xanthophylls in fruit tissues. In chloroplastic tissues, the effects of Z-ISO alteration are mainly manifested as a reduction in total carotenoid content. Taken together, our results indicate that the spontaneous single nucleotide insertion in Z-ISO is the molecular basis of the yellow pigmentation in ‘Pinalate’ sweet orange and points this isomerase as an essential activity for carotenogenesis in citrus fruits. Financial support of the research grants AGL2012–34576 and AGL2015–70218 (Ministerio Economía y Competitividad, Spain), and RTI2018-095131-B-I00 (Ministerio Ciencia, Innovacion y Universidades, Spain). Work in the group of JH was supported by Israel Science Foundation Grant 850/13. MJR, LZ, JH and OD are members of Eurocaroten (COST_Action CA15136). MJR and LZ belong to CaRed (Spanish Carotenoid Network BIO2017–90877-REDT, Ministerio de Ciencia, Innovación y Universidades, Spain). Authors acknowledge support of the publication fee by the CSIC Open Access Publication Support Initiative through its Unit of Information Resources for Research (URICI). Peer reviewed 2019-11-10T04:50:20Z 2019-11-10T04:50:20Z 2019-11-04 2019-11-10T04:50:21Z artículo http://purl.org/coar/resource_type/c_6501 BMC Plant Biology 19(1): 465 (2019) http://hdl.handle.net/10261/194244 10.1186/s12870-019-2078-2 1471-2229 http://dx.doi.org/10.13039/501100011033 http://dx.doi.org/10.13039/501100000921 http://dx.doi.org/10.13039/501100003977 http://dx.doi.org/10.13039/501100003329 http://dx.doi.org/10.13039/501100003339 31684878 #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# RTI2018-095131-B-I00/AEI/10.13039/501100011033 BIO2017-90877-REDT/AEI/10.13039/501100011033 info:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/AGL2015-70218-R info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/RTI2018-095131-B-I00 info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/BIO2017-90877-REDT Publisher's version https://doi.org/10.1186/s12870-019-2078-2 Sí open BioMed Central