Abstract
Key messageAnalysis of carotenoid-accumulating roots revealed that oxidative carotenoid degradation yields glyoxal and methylglyoxal. Our data suggest that these compounds are detoxified via the glyoxalase system and re-enter primary metabolic pathways.Carotenoid levels in plant tissues depend on the relative rates of synthesis and degradation. We recently identified redox enzymes previously known to be involved in the detoxification of fatty acid-derived reactive carbonyl species which were able to convert apocarotenoids into corresponding alcohols and carboxylic acids. However, their subsequent metabolization pathways remain unresolved. Interestingly, we found that carotenoid-accumulating roots have increased levels of glutathione, suggesting apocarotenoid glutathionylation to occur. In vitro and in planta investigations did not, however, support the occurrence of non-enzymatic or enzymatic glutathionylation of β-apocarotenoids. An alternative breakdown pathway is the continued oxidative degradation of primary apocarotenoids or their derivatives into the shortest possible oxidation products, namely glyoxal and methylglyoxal, which also accumulated in carotenoid-accumulating roots. In fact, combined transcriptome and metabolome analysis suggest that the high levels of glutathione are most probably required for detoxifying apocarotenoid-derived glyoxal and methylglyoxal via the glyoxalase pathway, yielding glycolate and d-lactate, respectively. Further transcriptome analysis suggested subsequent reactions involving activities associated with photorespiration and the peroxisome-specific glycolate/glyoxylate transporter. Finally, detoxified primary apocarotenoid degradation products might be converted into pyruvate which is possibly re-used for the synthesis of carotenoid biosynthesis precursors. Our findings allow to envision carbon recycling during carotenoid biosynthesis, degradation and re-synthesis which consumes energy, but partially maintains initially fixed carbon via re-introducing reactive carotenoid degradation products into primary metabolic pathways.
Highlights
Carotenoids are tetraterpenes serving a multitude of functions in plants as essential photosynthetic pigments, substrates for phytohormone biosynthesis and colorants of fruits and flowers contributing to sexual reproduction of plants (Yuan et al 2015; Baranski and Cazzonelli 2016)
Using carotenoid-accumulating Arabidopsis roots, we found that β-apocarotenoids which represent reactive electrophile species (RES) with α,β-unsaturated carbonyl moieties are metabolized by a set of enzymes so far known as detoxifiers of reactive carbonyl species (RCS; Fig. 1)
We reported that transgenic Arabidopsis calli and roots accumulating β-carotene and β-apocarotenoids accumulate the reactive carbonyl species methylglyoxal (C3) and glyoxal (C2) (Schaub et al 2018; Koschmieder et al 2020), potentially representing terminal oxidation products of β-carotene and/or carotenoids in general (Fig. 1)
Summary
Carotenoids are tetraterpenes serving a multitude of functions in plants as essential photosynthetic pigments, substrates for phytohormone biosynthesis and colorants of fruits and flowers contributing to sexual reproduction of plants (Yuan et al 2015; Baranski and Cazzonelli 2016). Knowledge on carotenoid catabolism, initiated by oxidative cleavage of their polyunsaturated hydrocarbon backbone, has only improved more recently and is a key determinant of steady-state carotenoid levels. Flux through carotenoid biosynthesis is by far higher than the steady-state levels observed, a fact that supports the significance and extent of carotenoid turnover (Simkin et al 2003; Lätari et al 2015; Koschmieder et al 2020). In vitro and in planta investigations suggest that non-enzymatic carotenoid oxidation yields polymeric aggregates, called co-polymers, most likely representing the largest portion of degraded carotenoid in high carotenoid tissues such as carrot roots or Golden Rice endosperm (Britton 1995; Burton et al 2014; Schaub et al 2017, 2018; Mogg and Burton 2020). Co-polymers slowly decompose by scission to yield apocarotenoids and many short-chain metabolites upon secondary cleavage of remaining double bonds and further metabolism
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