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Carotenoid metabolism during bilberry (Vaccinium myrtillus L.) fruit development under different light conditions is regulated by biosynthesis and degradation

Identifieur interne : 000302 ( Main/Exploration ); précédent : 000301; suivant : 000303

Carotenoid metabolism during bilberry (Vaccinium myrtillus L.) fruit development under different light conditions is regulated by biosynthesis and degradation

Auteurs : Katja Karppinen [Finlande, Norvège] ; Laura Zoratti [Finlande] ; Marian Sarala [Finlande] ; Elisabete Carvalho ; Jenni Hirsim Ki [Finlande] ; Helmi Mentula [Finlande] ; Stefan Martens ; Hely H Ggman [Finlande] ; Laura Jaakola [Norvège]

Source :

RBID : PMC:4839083

Abstract

Background

Carotenoids are important pigments and precursors for central signaling molecules associated in fruit development and ripening. Carotenoid metabolism has been studied especially in the climacteric tomato fruit but the content of carotenoids and the regulation of their metabolism have been shown to be highly variable between fruit species. Non-climacteric berries of the genus Vaccinium are among the best natural sources of health-beneficial flavonoids but not studied previously for carotenoid biosynthesis.

Results

In this study, carotenoid biosynthetic genes, PSY, PDS, ZDS, CRTISO, LCYB, LCYE, BCH and CYP450-BCH, as well as a carotenoid cleavage dioxygenase CCD1 were identified from bilberry (V. myrtillus L.) fruit and their expression was studied along with carotenoid composition during fruit development under different photoperiod and light quality conditions. Bilberry was found to be a good source of carotenoids among fruits and berries. The most abundant carotenoids throughout the berry development were lutein and β-carotene, which were accompanied by lower amounts of 9Z-β-carotene, violaxanthin, neoxanthin, zeaxanthin, antheraxanthin and β-cryptoxanthin. The expression patterns of the biosynthetic genes in ripening fruits indicated a metabolic flux towards β-branch of the carotenoid pathway. However, the carotenoid levels decreased in both the β-branch and ε,β-branch towards bilberry fruit ripening along with increased VmCCD1 expression, similarly to VmNCED1, indicating enzymatic carotenoid cleavage and degradation. Intense white light conditions increased the expression of the carotenoid biosynthetic genes but also the expression of the cleavage genes VmCCD1 and VmNCED1, especially in unripe fruits. Instead, mature bilberry fruits responded specifically to red/far-red light wavelengths by inducing the expression of both the carotenoid biosynthetic and the cleavage genes indicating tissue and developmental stage specific regulation of apocarotenoid formation by light quality.

Conclusions

This is the first report of carotenoid biosynthesis in Vaccinium berries. Our results indicate that both transcriptional regulation of the key biosynthetic genes and the enzymatic degradation of the produced carotenoids to apocarotenoids have significant roles in the determination of the carotenoid content and have overall effect on the metabolism during the bilberry fruit ripening.

Electronic supplementary material

The online version of this article (doi:10.1186/s12870-016-0785-5) contains supplementary material, which is available to authorized users.


Url:
DOI: 10.1186/s12870-016-0785-5
PubMed: 27098458
PubMed Central: 4839083


Affiliations:


Links toward previous steps (curation, corpus...)


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L.) fruit development under different light conditions is regulated by biosynthesis and degradation</title>
<author>
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<nlm:aff id="Aff1">Genetics and Physiology Unit, University of Oulu, P.O. Box 3000, FI-90014 Oulu, Finland</nlm:aff>
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<name sortKey="Sarala, Marian" sort="Sarala, Marian" uniqKey="Sarala M" first="Marian" last="Sarala">Marian Sarala</name>
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<nlm:aff id="Aff1">Genetics and Physiology Unit, University of Oulu, P.O. Box 3000, FI-90014 Oulu, Finland</nlm:aff>
<country xml:lang="fr">Finlande</country>
<wicri:regionArea>Genetics and Physiology Unit, University of Oulu, P.O. Box 3000, FI-90014 Oulu</wicri:regionArea>
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<name sortKey="Carvalho, Elisabete" sort="Carvalho, Elisabete" uniqKey="Carvalho E" first="Elisabete" last="Carvalho">Elisabete Carvalho</name>
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<name sortKey="Hirsim Ki, Jenni" sort="Hirsim Ki, Jenni" uniqKey="Hirsim Ki J" first="Jenni" last="Hirsim Ki">Jenni Hirsim Ki</name>
<affiliation wicri:level="1">
<nlm:aff id="Aff1">Genetics and Physiology Unit, University of Oulu, P.O. Box 3000, FI-90014 Oulu, Finland</nlm:aff>
<country xml:lang="fr">Finlande</country>
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<name sortKey="Mentula, Helmi" sort="Mentula, Helmi" uniqKey="Mentula H" first="Helmi" last="Mentula">Helmi Mentula</name>
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<nlm:aff id="Aff1">Genetics and Physiology Unit, University of Oulu, P.O. Box 3000, FI-90014 Oulu, Finland</nlm:aff>
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<name sortKey="Martens, Stefan" sort="Martens, Stefan" uniqKey="Martens S" first="Stefan" last="Martens">Stefan Martens</name>
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<wicri:noCountry code="subfield">TN Italy</wicri:noCountry>
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<name sortKey="H Ggman, Hely" sort="H Ggman, Hely" uniqKey="H Ggman H" first="Hely" last="H Ggman">Hely H Ggman</name>
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<name sortKey="Jaakola, Laura" sort="Jaakola, Laura" uniqKey="Jaakola L" first="Laura" last="Jaakola">Laura Jaakola</name>
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<nlm:aff id="Aff2">Climate laboratory Holt, Department of Arctic and Marine Biology, UiT the Arctic University of Norway, NO-9037 Tromsø, Norway</nlm:aff>
<country xml:lang="fr">Norvège</country>
<wicri:regionArea>Climate laboratory Holt, Department of Arctic and Marine Biology, UiT the Arctic University of Norway, NO-9037 Tromsø</wicri:regionArea>
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<nlm:aff id="Aff4">NIBIO, Norwegian Institute of Bioeconomy Research, P.O. Box 115, NO-1431 Ås, Norway</nlm:aff>
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<title level="j">BMC Plant Biology</title>
<idno type="eISSN">1471-2229</idno>
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<div type="abstract" xml:lang="en">
<sec>
<title>Background</title>
<p>Carotenoids are important pigments and precursors for central signaling molecules associated in fruit development and ripening. Carotenoid metabolism has been studied especially in the climacteric tomato fruit but the content of carotenoids and the regulation of their metabolism have been shown to be highly variable between fruit species. Non-climacteric berries of the genus
<italic>Vaccinium</italic>
are among the best natural sources of health-beneficial flavonoids but not studied previously for carotenoid biosynthesis.</p>
</sec>
<sec>
<title>Results</title>
<p>In this study, carotenoid biosynthetic genes,
<italic>PSY, PDS, ZDS, CRTISO, LCYB, LCYE, BCH</italic>
and
<italic>CYP450-BCH</italic>
, as well as a carotenoid cleavage dioxygenase
<italic>CCD1</italic>
were identified from bilberry (
<italic>V. myrtillus</italic>
L.) fruit and their expression was studied along with carotenoid composition during fruit development under different photoperiod and light quality conditions. Bilberry was found to be a good source of carotenoids among fruits and berries. The most abundant carotenoids throughout the berry development were lutein and
<italic>β</italic>
-carotene, which were accompanied by lower amounts of 9Z-
<italic>β</italic>
-carotene, violaxanthin, neoxanthin, zeaxanthin, antheraxanthin and
<italic>β</italic>
-cryptoxanthin. The expression patterns of the biosynthetic genes in ripening fruits indicated a metabolic flux towards
<italic>β</italic>
-branch of the carotenoid pathway. However, the carotenoid levels decreased in both the
<italic>β</italic>
-branch and
<italic>ε</italic>
,
<italic>β</italic>
-branch towards bilberry fruit ripening along with increased
<italic>VmCCD1</italic>
expression, similarly to
<italic>VmNCED1</italic>
, indicating enzymatic carotenoid cleavage and degradation. Intense white light conditions increased the expression of the carotenoid biosynthetic genes but also the expression of the cleavage genes
<italic>VmCCD1</italic>
and
<italic>VmNCED1,</italic>
especially in unripe fruits. Instead, mature bilberry fruits responded specifically to red/far-red light wavelengths by inducing the expression of both the carotenoid biosynthetic and the cleavage genes indicating tissue and developmental stage specific regulation of apocarotenoid formation by light quality.</p>
</sec>
<sec>
<title>Conclusions</title>
<p>This is the first report of carotenoid biosynthesis in
<italic>Vaccinium</italic>
berries. Our results indicate that both transcriptional regulation of the key biosynthetic genes and the enzymatic degradation of the produced carotenoids to apocarotenoids have significant roles in the determination of the carotenoid content and have overall effect on the metabolism during the bilberry fruit ripening.</p>
</sec>
<sec>
<title>Electronic supplementary material</title>
<p>The online version of this article (doi:10.1186/s12870-016-0785-5) contains supplementary material, which is available to authorized users.</p>
</sec>
</div>
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<author>
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<author>
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<author>
<name sortKey="Halonen, M" uniqKey="Halonen M">M Halonen</name>
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<list>
<country>
<li>Finlande</li>
<li>Norvège</li>
</country>
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<name sortKey="Martens, Stefan" sort="Martens, Stefan" uniqKey="Martens S" first="Stefan" last="Martens">Stefan Martens</name>
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<name sortKey="Karppinen, Katja" sort="Karppinen, Katja" uniqKey="Karppinen K" first="Katja" last="Karppinen">Katja Karppinen</name>
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<name sortKey="Zoratti, Laura" sort="Zoratti, Laura" uniqKey="Zoratti L" first="Laura" last="Zoratti">Laura Zoratti</name>
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