Interference with Clp protease impairs carotenoid accumulation during tomato fruit ripening

D’Andrea, Lucio; Simón-Moya, Miguel; Llorente, Briardo; Llamas, Ernesto; Marro, Mónica; Loza-Álvarez, Pablo; Li, Li; Rodríguez‐Concepción, Manuel

doi:10.1093/jxb/erx491

Cited by 64 publications

(61 citation statements)

References 52 publications

(103 reference statements)

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“…Recent work indicates that both AP2/EREBPs and WRKYs play important roles in plastid retrograde signalling (Phukan et al ., , ). Heat shock proteins are associated with chromoplast differentiation and carotenoid accumulation in tomato (D'Andrea et al ., ; Neta‐Sharir et al ., ). Among the 13 common genes at AtOR His early fruit developmental stages, 8 of them are heat shock proteins (Table S9).…”

Section: Discussionmentioning

confidence: 99%

Ectopic expression of ORANGE promotes carotenoid accumulation and fruit development in tomato

Yazdani

Sun

Yuan

et al. 2018

Plant Biotechnology Journal

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Carotenoids are critically important to plants and humans. The ORANGE (OR) gene is a key regulator for carotenoid accumulation, but its physiological roles in crops remain elusive. In this study, we generated transgenic tomato ectopically overexpressing the Arabidopsis wild-type OR (AtOR ) and a 'golden SNP'-containing OR (AtOR ). We found that AtOR initiated chromoplast formation in very young fruit and stimulated carotenoid accumulation at all fruit developmental stages, uncoupled from other ripening activities. The elevated levels of carotenoids in the AtOR lines were distributed in the same subplastidial fractions as in wild-type tomato, indicating an adaptive response of plastids to sequester the increased carotenoids. Microscopic analysis revealed that the plastid sizes were increased in both AtOR and AtOR lines at early fruit developmental stages. Moreover, AtOR overexpression promoted early flowering, fruit set and seed production. Ethylene production and the expression of ripening-associated genes were also significantly increased in the AtOR transgenic fruit at ripening stages. RNA-Seq transcriptomic profiling highlighted the primary effects of OR overexpression on the genes in the processes related to RNA, protein and signalling in tomato fruit. Taken together, these results expand our understanding of OR in mediating carotenoid accumulation in plants and suggest additional roles of OR in affecting plastid size as well as flower and fruit development, thus making OR a target gene not only for nutritional biofortification of agricultural products but also for alteration of horticultural traits.

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Section: Discussionmentioning

confidence: 99%

Ectopic expression of ORANGE promotes carotenoid accumulation and fruit development in tomato

Yazdani

Sun

Yuan

et al. 2018

Plant Biotechnology Journal

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“…PSY is also regulated at the enzyme level in response to a variety of factors, including plastidial sublocalization [63,64] (see Section 2.1.3 below). Similar to DXS and other MEP pathway enzymes, the levels and activity of PSY and other carotenoid pathway enzymes can also be regulated by the Clp protease [65,66], a mechanism that likely contributes to coordinate carotenoid biosynthesis with the supply of their metabolic precursors. Other mechanisms regulating PSY activity in different plant systems are (1) direct interaction with the ORANGE (Or) chaperone [67,68], (2) direct interaction with the STAY-GREEN protein [69], and (3) negative feedback by downstream carotenoids [70,71].…”

Section: Biosynthetic Pathwaymentioning

confidence: 99%

“…In one of them, expression of a N. tabacum gene encoding LCYB driven by the Arabidopsis UBQ3 promoter resulted in enhanced levels of β-carotene in tomato fruit (up to 3-fold, 783 μg/g DW) with negligible changes of other carotenoids, including lycopene [259]. The second work investigated the activity of the fruit Clp protease during ripening [66]. Down-regulation of this protease disrupted normal chromoplasts differentiation and caused an increased accumulation of DXS and PSY enzymes but also of the Or chaperone, eventually resulting in ripe fruits with 2-fold higher levels of β-carotene but normal levels of lycopene [66].…”

Section: Tomato (Solanum Lycopersicon)mentioning

confidence: 99%

“…The second work investigated the activity of the fruit Clp protease during ripening [66]. Down-regulation of this protease disrupted normal chromoplasts differentiation and caused an increased accumulation of DXS and PSY enzymes but also of the Or chaperone, eventually resulting in ripe fruits with 2-fold higher levels of β-carotene but normal levels of lycopene [66].…”

Section: Tomato (Solanum Lycopersicon)mentioning

confidence: 99%

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A global perspective on carotenoids: Metabolism, biotechnology, and benefits for nutrition and health

Rodríguez‐Concepción

Ávalos

Bonet

et al. 2018

Progress in Lipid Research

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750

584

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Carotenoids are lipophilic isoprenoid compounds synthesized by all photosynthetic organisms and some non-photosynthetic prokaryotes and fungi. With some notable exceptions, animals (including humans) do not produce carotenoids de novo but take them in their diets. In photosynthetic systems carotenoids are essential for photoprotection against excess light and contribute to light harvesting, but perhaps they are best known for their properties as natural pigments in the yellow to red range. Carotenoids can be associated to fatty acids, sugars, proteins, or other compounds that can change their physical and chemical properties and influence their biological roles. Furthermore, oxidative cleavage of carotenoids produces smaller molecules such as apocarotenoids, some of which are important pigments and volatile (aroma) compounds. Enzymatic breakage of carotenoids can also produce biologically active molecules in both plants (hormones, retrograde signals) and animals (retinoids). Both carotenoids and their enzymatic cleavage products are associated with other processes positively impacting human health. Carotenoids are widely used in the industry as food ingredients, feed additives, and supplements. This review, contributed by scientists of complementary disciplines related to carotenoid research, covers recent advances and provides a perspective on future directions on the subjects of carotenoid metabolism, biotechnology, and nutritional and health benefits.

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“…Transmission electron microscopy. Transmission electron microscopy of plant leaves was performed as previously described (D'Andrea et al, 2018).…”

Section: Methodsmentioning

confidence: 99%

Synthetic biogenesis of chromoplasts from leaf chloroplasts

Llorente

Torres‐Montilla

Morelli

et al. 2019

Preprint

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Plastids, the defining organelles of plant cells, undergo physiological and morphological changes to fulfill distinct biological functions. In particular, the differentiation of chloroplasts into chromoplasts results in an enhanced storage capacity for carotenoids with industrial and nutritional value such as betacarotene (pro-vitamin A). Here, we show that synthetically inducing a burst in the production of phytoene, the first committed intermediate of the carotenoid pathway, elicits an artificial chloroplast-to-chromoplast differentiation in leaves. Phytoene overproduction initially interferes with photosynthesis, acting as a metabolic threshold switch mechanism that weakens chloroplast identity. In a second stage, phytoene conversion into downstream carotenoids is required for the differentiation of chromoplasts. Our findings reveal that lowering the photosynthetic capacity of chloroplasts and increasing the production of carotenoids are not just the consequence but an absolute requirement for chromoplast differentiation, which additionally involves a concurrent reprogramming of nuclear gene expression and plastid morphology for improved carotenoid storage.

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Interference with Clp protease impairs carotenoid accumulation during tomato fruit ripening

Abstract: The stromal Clp protease complex influences chromoplast differentiation and ensures proper carotenoid metabolism during tomato fruit ripening, probably in co-ordination with plastidial chaperones.

Cited by 64 publications

References 52 publications

Ectopic expression of ORANGE promotes carotenoid accumulation and fruit development in tomato

Ectopic expression of ORANGE promotes carotenoid accumulation and fruit development in tomato

A global perspective on carotenoids: Metabolism, biotechnology, and benefits for nutrition and health

Synthetic biogenesis of chromoplasts from leaf chloroplasts

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