Integrative Transcript and Metabolite Analysis of Nutritionally Enhanced DE-ETIOLATED1 Downregulated Tomato Fruit

Centre for Systems and Synthetic Biology, University of London, Egham, Surrey TW20 0EX, United Kingdom.
The Plant Cell (Impact Factor: 9.34). 04/2010; 22(4):1190-215. DOI: 10.1105/tpc.110.073866
Source: PubMed


Fruit-specific downregulation of the DE-ETIOLATED1 (DET1) gene product results in tomato fruits (Solanum lycopersicum) containing enhanced nutritional antioxidants, with no detrimental effects on yield. In an attempt to further our understanding of how modulation of this gene leads to improved quality traits, detailed targeted and multilevel omic characterization has been performed. Metabolite profiling revealed quantitative increases in carotenoid, tocopherol, phenylpropanoids, flavonoids, and anthocyanidins. Qualitative differences could also be identified within the phenolics, including unique formation in fruit pericarp tissues. These changes resulted in increased total antioxidant content both in the polar and nonpolar fractions. Increased transcription of key biosynthetic genes is a likely mechanism producing elevated phenolic-based metabolites. By contrast, high levels of isoprenoids do not appear to result from transcriptional regulation but are more likely related to plastid-based parameters, such as increased plastid volume per cell. Parallel metabolomic and transcriptomic analyses reveal the widespread effects of DET1 downregulation on diverse sectors of metabolism and sites of synthesis. Correlation analysis of transcripts and metabolites independently indicated strong coresponses within and between related pathways/processes. Interestingly, despite the fact that secondary metabolites were the most severely affected in ripe tomato fruit, our integrative analyses suggest that the coordinated activation of core metabolic processes in cell types amenable to plastid biogenesis is the main effect of DET1 loss of function.

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    • "SlCUL4, SlDDB1 and SlDET1 have been shown previously to function as negative regulators of plastid level and pigmentation in tomato (Mustilli et al., 1999; Lieberman et al., 2004; Liu et al., 2004; Wang et al., 2008; Enfissi et al., 2010; Powell et al., 2012; Nguyen et al., 2014). This is antagonistic to the role of the positive regulator, tomato SlGLK2 that promotes chloroplast development and metabolite accumulation (Powell et al., 2012; Nguyen et al., 2014). "
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    ABSTRACT: CULLIN4-RING ubiquitin ligases (CRL4s) as well as their targets are fundamental regulators functioning in many key developmental and stress responses in eukaryotes. In tomato (Solanum lycopersicum), molecular cloning has revealed that the underlying genes of natural spontaneous mutations high pigment 1 (hp1), high pigment 2 (hp2) and uniform ripening (u) encode UV-DAMAGED DNA BINDING PROTEIN 1 (DDB1), DE-ETIOLATED 1 (DET1) and GOLDEN 2-LIKE (GLK2), respectively. However, the molecular basis of the opposite actions of tomato GLK2 vs CUL4-DDB1-DET1 complex on regulating plastid level and fruit quality remains unknown. Here, we provide molecular evidence showing that the tomato GLK2 protein is a substrate of the CUL4-DDB1-DET1 ubiquitin ligase complex for the proteasome degradation. SlGLK2 is degraded by the ubiquitin-proteasome system, which is mainly determined by two lysine residues (K11 and K253). SlGLK2 associates with the CUL4-DDB1-DET1 E3 complex in plant cells. Genetically impairing CUL4, DDB1 or DET1 results in a retardation of SlGLK2 degradation by the 26S proteasome. These findings are relevant to the potential of nutrient accumulation in tomato fruit by mediating the plastid level and contribute to a deeper understanding of an important regulatory loop, linking protein turnover to gene regulation.
    New Phytologist 09/2015; DOI:10.1111/nph.13635 · 7.67 Impact Factor
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    • "It was documented that photomorphogenesis may be indirectly associated with the flavonoid pathway. Suppression of the DET1 gene led to increased carotenoid and flavonoid levels in tomato fruits, as well as phenylpropanoid and anthocyanidins (Davuluri et al., 2005; Enfissi et al., 2010). It is well known that HY5 plays an important role in photomorphogenic development (Chattopadhyay et al., 1998). "

    Frontiers in Plant Science 09/2015; 6:689. · 3.95 Impact Factor
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    • "Although ABA regulation of flavonoid biosynthesis has mostly regarded anthocyanin biosynthesis (Wheeler et al., 2009; Medina- Puche et al., 2014), there is also compelling evidence that a rise in foliar ABA is paralleled by an enhanced biosynthesis of UVabsorbing flavonoids, such as kaempferol and quercetin derivatives (Castellarin and Di Gaspero, 2007; Berli et al., 2011; Perrone et al., 2012). This further corroborates the hypothesis that isoprenoid and phenylpropanoid biosynthetic pathways are inter-related (Zvi et al., 2012; Enfissi et al., 2010). The matter deserves further experimentation, but opens new scenarios on the functional roles of secondary metabolites in plants severely stressed by an excess of sunlight irradiance. "
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    ABSTRACT: Plants face excess light stress on daily as well as on seasonal basis. The excess of excitation energy on cellular organelles prone to reactive oxygen species (ROS) generation is further enhanced when plants growing in full sun concurrently experience drought and heat stress. These are the very conditions that promote the biosynthesis of a wide range of secondary metabolites. Plants display a highly integrated arsenal of ROS-detoxifying agents to keep ROS concentration under control for efficient signalling, while avoiding cell death. There is evidence that primary antioxidants, i.e. antioxidant enzymes and low molecular-weight antioxidants, such as ascorbic acid and glutathione, are depleted under a severe excess of radiant energy. Here we discuss about how relevant secondary metabolites, namely isoprene, carotenoids, and flavonoids may complement the function of primary antioxidants to avoid irreversible oxidative damage, when plants experience intense, even transient stress events. We offer evidence of how plants orchestrate daily the antioxidant machinery, when challenged against multiple environmental stresses. It is indeed conceivable that daily variations in sunlight irradiance and air temperature may greatly alter the effectiveness of primary and secondary ROS-detoxifying agents. Finally, we discuss about the possible inter-relation between isoprenoid and flavonoid metabolism in plants facing high light coupled with drought and heat stress, as a consequence of severe stress-induced redox imbalance.
    Environmental and Experimental Botany 04/2015; 119. DOI:10.1016/j.envexpbot.2015.04.007 · 3.36 Impact Factor
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