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Abstract
Possible crosstalk between the carotenoid and porphyrin biosynthetic pathways under photooxidative conditions was investigated by using their biosynthetic inhibitors, norflurazon (NF) and oxyfluorfen (OF). High levels of protoporphyrin IX (Proto IX) accumulated in rice plants treated with OF, whereas Proto IX decreased in plants treated with NF. Both NF and OF treatments resulted in greater decreases in MgProto IX, MgProto IX methyl ester, and protochlorophyllide. Activities and transcript levels of most porphyrin biosynthetic enzymes, particularly in the Mg-porphyrin branch, were greatly down-regulated in NF and OF plants. In contrast, the transcript levels of GSA, PPO1, and CHLD as well as FC2 and HO2 were up-regulated in NF-treated plants, while only moderate increases in FC2 and HO2 were observed in the early stage of OF treatment. Phytoene, antheraxanthin, and zeaxanthin showed high accumulation in NF-treated plants, whereas other carotenoid intermediates greatly decreased. Transcript levels of carotenoid biosynthetic genes, PSY1 and PDS, decreased in response to NF and OF, whereas plants in the later stage of NF treatment exhibited up-regulation of BCH and VDE as well as recovery of PDS. However, perturbed porphyrin biosynthesis by OF did not noticeably influence levels of carotenoid metabolites, regardless of the strong down-regulation of carotenoid biosynthetic genes. Both NF and OF plants appeared to provide enhanced protection against photooxidative damage, not only by scavenging of Mg-porphyrins, but also by up-regulating FC2, HO2, and Fe-chelatase, particularly with increased levels of zeaxanthin via up-regulation of BCH and VDE in NF plants. On the other hand, the up-regulation of GSA, PPO1, and CHLD under inhibition of carotenogenic flux may be derived from the necessity to recover impaired chloroplast biogenesis during photooxidative stress. Our study demonstrates that perturbations in carotenoid and porphyrin biosynthesis coordinate the expression of their biosynthetic genes to sustain plastid function at optimal levels by regulating their metabolic flux in plants under adverse stress conditions.
Highlights
Chlorophylls and carotenoids are the most widely distributed pigments and essential for ubiquitous structural components of the photosynthetic apparatus
Our study demonstrates the importance of tight coordination between the carotenoid and porphyrin biosynthetic pathways, which plays an important role in photoprotection of plants against photodamage and in chloroplast biogenesis
To investigate the effect of differential photooxidative stress on porphyrin biosynthesis, we examined photooxidation-induced changes in levels of porphyrin biosynthetic intermediates
Summary
Chlorophylls and carotenoids are the most widely distributed pigments and essential for ubiquitous structural components of the photosynthetic apparatus. Carotenoid pigments assist in harvesting light energy, function as photo-protectants and antioxidants, and protect the photosynthetic apparatus by quenching harmful reactive oxygen species (ROS) produced by overexcitation of chlorophylls (Krinsky, 1989; Havaux, 1998; Joyard et al, 2009; Murchie and Niyogi, 2011) Their metabolic pathways of synthesis and degradation are tightly controlled to provide adequate amounts of each metabolite (carotenoids/tetrapyrroles) (Cornah et al, 2003; Tanaka and Tanaka, 2007; Lätari et al, 2015; Chayut et al, 2017) and avoid the phototoxic accumulation of intermediates (tetrapyrroles) (Phung et al, 2011). Accumulated Protogen IX leaks from the plastid and is converted to Proto IX, a photosensitizing compound that promotes photodynamic stress and non-enzymatic lipid peroxidation, by non-specific peroxidases in the cytoplasm (Duke et al, 1991; Jacobs and Jacobs, 1993)
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