A Cytosolic Pathway for the Conversion of Hydroxypyruvate to Glycerate during Photorespiration in Arabidopsis

Abstract

Deletion of any of the core enzymes of the photorespiratory cycle, one of the major pathways of plant primary metabolism, results in severe air-sensitivity of the respective mutants. The peroxisomal enzyme hydroxypyruvate reductase (HPR1) represents the only exception to this rule. This indicates the presence of extraperoxisomal reactions of photorespiratory hydroxypyruvate metabolism. We have identified a second hydroxypyruvate reductase, HPR2, and present genetic and biochemical evidence that the enzyme provides a cytosolic bypass to the photorespiratory core cycle in Arabidopsis thaliana. Deletion of HPR2 results in elevated levels of hydroxypyruvate and other metabolites in leaves. Photosynthetic gas exchange is slightly altered, especially under long-day conditions. Otherwise, the mutant closely resembles wild-type plants. The combined deletion of both HPR1 and HPR2, however, results in distinct air-sensitivity and a dramatic reduction in photosynthetic performance. These results suggest that photorespiratory metabolism is not confined to chloroplasts, peroxisomes, and mitochondria but also extends to the cytosol. The extent to which cytosolic reactions contribute to the operation of the photorespiratory cycle in varying natural environments is not yet known, but it might be dynamically regulated by the availability of NADH in the context of peroxisomal redox homeostasis.

Serine Acts as a Metabolic Signal for the Transcriptional Control of Photorespiration-Related Genes in Arabidopsis

“…Arabidopsis wild-type and hpr1 mutant plants were grown side by side to growth stage 5.1 (Boyes et al, 2001) in normal air under a 10/14-h day/night regime. This particular photorespiratory mutant is deficient in the peroxisomal enzyme HPR1, causing a partially redirected photorespiratory carbon flux (Timm et al, 2008(Timm et al, , 2011. As a consequence of that, hpr1 is characterized by a slightly retarded metabolism through the photorespiration core cycle, which in turn only causes a very "mild" photorespiratory phenotype (Timm and Bauwe, 2013).…”

“…These data were compared with corresponding data collected for an HPR1-deficient mutant. The hpr1 mutant differs from other photorespiratory mutants, because two bypasses to the HPR1 reaction allow the extraperoxisomal conversion of HP into glycerate and, consequently, wild-type-like growth in ambient air (Timm et al, 2008(Timm et al, , 2011. Due to the only moderate impact on metabolism and growth, it was possible to examine whether this genetic defect in photorespiratory flux alters the diurnal regulation of the capacity of the photorespiratory pathway.…”

“…Most null mutants of photorespiratory enzymes are heavily impaired in photorespiratory conditions (Timm and Bauwe, 2013;Timm et al, 2012b) and cannot be easily used for such experiments. In contrast, the presence of a cytosolic bypass allows mutants deficient in HPR1 to grow in a wild-type-like manner in normal air (Timm et al, 2008(Timm et al, , 2011. Since photorespiratory carbon flow is not blocked but rather partially redirected in this mutant, hpr1 represents a suitable intermediate between the wild type and the more impaired photorespiratory mutants and, therefore, can be used to study diel changes in the capacity of the photorespiratory pathway.…”

Alteration of the Interconversion of Pyruvate and Malate in the Plastid or Cytosol of Ripening Tomato Fruit Invokes Diverse Consequences on Sugar But Similar Effects on Cellular Organic Acid, Metabolism, and Transitory Starch Accumulation

“…They were subsequently extracted in 100% methanol and processed exactly as described (Timm et al, 2008). The metabolic fate of these substrates was subsequently assessed exactly as described previously (Tieman et al, 2006).…”

On the Discordance of Metabolomics with Proteomics and Transcriptomics: Coping with Increasing Complexity in Logic, Chemistry, and Network Interactions Scientific Correspondence

“…While this occurs at the level of transcription, transcript processing, and translation, it can be argued that the extent of redundancy of isoforms and duplication of pathways is at least as great in central metabolism (e.g. the TCA cycle, the photorespiratory pathway, or Suc degradation; Timm et al, 2008;Barratt et al, 2009;Araú jo et al, 2012).…”