Abstract
Plant dicarboxylate carriers (DICs) transport a wide range of dicarboxylates across the mitochondrial inner membrane. The Arabidopsis thaliana DIC family is composed of three genes (AtDIC1, 2 and 3), whereas two genes (EgDIC1 and EgDIC2) have been retrieved in Eucalyptus grandis. Here, by combining in silico and in planta analyses, we provide evidence that DICs are partially redundant, important in plant adaptation to environmental stresses and part of a low-oxygen response in both species. AtDIC1 and AtDIC2 are present in most plant species and have very similar gene structure, developmental expression patterns and absolute expression across natural Arabidopsis accessions. In contrast, AtDIC3 seems to be an early genome acquisition found in Brassicaceae and shows relatively low (or no) expression across these accessions. In silico analysis revealed that both AtDICs and EgDICs are highly responsive to stresses, especially to cold and submergence, while their promoters are enriched for stress-responsive transcription factors binding sites. The expression of AtDIC1 and AtDIC2 is highly correlated across natural accessions and in response to stresses, while no correlation was found for AtDIC3. Gene ontology enrichment analysis suggests a role for AtDIC1 and AtDIC2 in response to hypoxia, and for AtDIC3 in phosphate starvation. Accordingly, the investigated genes are induced by submergence stress in A. thaliana and E. grandis while AtDIC2 overexpression improved seedling survival to submergence. Interestingly, the induction of AtDIC1 and AtDIC2 is abrogated in the erfVII mutant that is devoid of plant oxygen sensing, suggesting that these genes are part of a conserved hypoxia response in Arabidopsis.
Highlights
Dicarboxylates are required in essential plant metabolic pathways including the metabolism of fatty acids, the synthesis of amino acids and gluconeogenesis [1]
Dicarboxylate Carriers Are Widely Distributed in the Plant Kingdom
While EgDIC1 is located on chromosome 9 and has a single transcript variant, EgDIC2 is located on chromosome 6 and encodes two distinct transcript variants (EgDIC2 X1 and X2) (Figure 1b)
Summary
Dicarboxylates are required in essential plant metabolic pathways including the metabolism of fatty acids, the synthesis of amino acids and gluconeogenesis [1]. The transcriptional up-regulation elicited by touch was proposed to address a physiological change since a significant reduction in DIC substrates such as succinate and citrate was observed in treated plants [9] In this context, AtDIC2 was recently shown to promote the export of cytosolic malate in exchange for mitochondrial citrate [10], an activity that contributes for the maintenance of metabolic homeostasis, especially under stressful conditions. Influenced by different factors, the main metabolic responses to oxygen deficiency involve alterations in the levels of tricarboxylic acid cycle (TCA) intermediates, including the accumulation of succinate and malate In this regard, given their transport characteristics, DICs have been suggested to contribute to the metabolic adjustments required for plant adaptation to low-oxygen conditions, a feature that is supported by the reported induction of AtDIC2 under hypoxia and anoxia [13]. America have been facing problems associated with short-term hypoxia mainly due to soil compaction [14] and a better understanding of the underlying molecular mechanisms implicated in adaptation to hypoxia in woody plants is of special interest
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