Photoprotective Role of Photosynthetic and Non-Photosynthetic Pigments in Phillyrea latifolia: Is Their “Antioxidant” Function Prominent in Leaves Exposed to Severe Summer Drought?

Carotenoids and phenylpropanoids play a dual role of limiting and countering photooxidative stress. We hypothesize that their “antioxidant” function is prominent in plants exposed to summer drought, when climatic conditions exacerbate the light stress. To test this, we conducted a field study on Phillyrea latifolia, a Mediterranean evergreen shrub, carrying out daily physiological and biochemical analyses in spring and summer. We also investigated the functional role of the major phenylpropanoids in different leaf tissues. Summer leaves underwent the most severe drought stress concomitantly with a reduction in radiation use efficiency upon being exposed to intense photooxidative stress, particularly during the central hours of the day. In parallel, a significant daily variation in both carotenoids and phenylpropanoids was observed. Our data suggest that the morning-to-midday increase in zeaxanthin derived from the hydroxylation of ß-carotene to sustain non-photochemical quenching and limit lipid peroxidation in thylakoid membranes. We observed substantial spring-to-summer and morning-to-midday increases in quercetin and luteolin derivatives, mostly in the leaf mesophyll. These findings highlight their importance as antioxidants, countering the drought-induced photooxidative stress. We concluded that seasonal and daily changes in photosynthetic and non-photosynthetic pigments may allow P. latifolia leaves to avoid irreversible photodamage and to cope successfully with the Mediterranean harsh climate.

FERONIA Confers Resistance to Photooxidative Stress in Arabidopsis

Plants absorb light energy required for photosynthesis, but excess light can damage plant cells. To protect themselves, plants have developed diverse signaling pathways which are activated under high-intensity light. Plant photoprotection mechanisms have been mainly investigated under conditions of extremely high amount of light; thus, it is largely unknown how plants manage photooxidative damage under moderate light intensities. In the present study, we found that FERONIA (FER) is a key protein that confers resistance to photooxidative stress in plants under moderate light intensity. FER-deficient mutants were highly susceptible to increasing light intensity and exhibited photobleaching even under moderately elevated light intensity (ML). Light-induced expression of stress genes was largely diminished by the fer-4 mutation. In addition, excitation pressure on Photosystem II was significantly increased in fer-4 mutants under ML. Consistently, reactive oxygen species, particularly singlet oxygen, accumulated in fer-4 mutants grown under ML. FER protein abundance was found to be elevated after exposure to ML, which is indirectly affected by the ubiquitin-proteasome pathway. Altogether, our findings showed that plants require FER-mediated photoprotection to maintain their photosystems even under moderate light intensity.

A Complex Network of Sigma Factors and sRNA StsR Regulates Stress Responses in R. sphaeroides

Adaptation of bacteria to a changing environment is often accompanied by remodeling of the transcriptome. In the facultative phototroph Rhodobacter sphaeroides the alternative sigma factors RpoE, RpoHI and RpoHII play an important role in a variety of stress responses, including heat, oxidative stress and nutrient limitation. Photooxidative stress caused by the simultaneous presence of chlorophylls, light and oxygen is a special challenge for phototrophic organisms. Like alternative sigma factors, several non-coding sRNAs have important roles in the defense against photooxidative stress. RNAseq-based transcriptome data pointed to an influence of the stationary phase-induced StsR sRNA on levels of mRNAs and sRNAs with a role in the photooxidative stress response. Furthermore, StsR also affects expression of photosynthesis genes and of genes for regulators of photosynthesis genes. In vivo and in vitro interaction studies revealed that StsR, that is under control of the RpoHI and RpoHII sigma factors, targets rpoE mRNA and affects its abundance by altering its stability. RpoE regulates expression of the rpoHII gene and, consequently, expression of stsR. These data provide new insights into a complex regulatory network of protein regulators and sRNAs involved in defense against photooxidative stress and the regulation of photosynthesis genes.

Distribution of the Water-Soluble Astaxanthin Binding Carotenoprotein (AstaP) in Scenedesmaceae

Photooxidative stress-inducible water-soluble astaxanthin-binding proteins, designated as AstaP, were identified in two Scenedesmaceae strains, Coelastrella astaxanthina Ki-4 and Scenedesmus obtusus Oki-4N; both strains were isolated under high light conditions. These AstaPs are classified as a novel family of carotenoprotein and are useful for providing valuable astaxanthin in water-soluble form; however, the distribution of AstaP orthologs in other microalgae remains unknown. Here, we examined the distribution of AstaP orthologs in the family Scenedesmaceae with two model microalgae, Chlamydomonas reinhardtii and Chlorella variabilis. The expression of AstaP orthologs under photooxidative stress conditions was detected in cell extracts of Scenedesmaceae strains, but not in model algal strains. Aqueous orange proteins produced by Scenedesmaceae strains were shown to bind astaxanthin. The protein from Scenedesmus costatus SAG 46.88 was purified. It was named ScosAstaP and found to bind astaxanthin. The deduced amino acid sequence from a gene encoding ScosAstaP showed 62% identity to Ki-4 AstaP. The expression of the genes encoding AstaP orthologs was shown to be inducible under photooxidative stress conditions; however, the production amounts of AstaP orthologs were estimated to be approximately 5 to 10 times lower than that of Ki-4 and Oki-4N.

Diverse Biosynthetic Pathways and Protective Functions against Environmental Stress of Antioxidants in Microalgae

Eukaryotic microalgae have been classified into several biological divisions and have evolutionarily acquired diverse morphologies, metabolisms, and life cycles. They are naturally exposed to environmental stresses that cause oxidative damage due to reactive oxygen species accumulation. To cope with environmental stresses, microalgae contain various antioxidants, including carotenoids, ascorbate (AsA), and glutathione (GSH). Carotenoids are hydrophobic pigments required for light harvesting, photoprotection, and phototaxis. AsA constitutes the AsA-GSH cycle together with GSH and is responsible for photooxidative stress defense. GSH contributes not only to ROS scavenging, but also to heavy metal detoxification and thiol-based redox regulation. The evolutionary diversity of microalgae influences the composition and biosynthetic pathways of these antioxidants. For example, α-carotene and its derivatives are specific to Chlorophyta, whereas diadinoxanthin and fucoxanthin are found in Heterokontophyta, Haptophyta, and Dinophyta. It has been suggested that AsA is biosynthesized via the plant pathway in Chlorophyta and Rhodophyta and via the Euglena pathway in Euglenophyta, Heterokontophyta, and Haptophyta. The GSH biosynthetic pathway is conserved in all biological kingdoms; however, Euglenophyta are able to synthesize an additional thiol antioxidant, trypanothione, using GSH as the substrate. In the present study, we reviewed and discussed the diversity of microalgal antioxidants, including recent findings.

Light-Triggered Carotenogenesis in Myxococcus xanthus: New Paradigms in Photosensory Signaling, Transduction and Gene Regulation

Myxobacteria are Gram-negative δ-proteobacteria found predominantly in terrestrial habitats and often brightly colored due to the biosynthesis of carotenoids. Carotenoids are lipophilic isoprenoid pigments that protect cells from damage and death by quenching highly reactive and toxic oxidative species, like singlet oxygen, generated upon growth under light. The model myxobacterium Myxococcus xanthus turns from yellow in the dark to red upon exposure to light because of the photoinduction of carotenoid biosynthesis. How light is sensed and transduced to bring about regulated carotenogenesis in order to combat photooxidative stress has been extensively investigated in M. xanthus using genetic, biochemical and high-resolution structural methods. These studies have unearthed new paradigms in bacterial light sensing, signal transduction and gene regulation, and have led to the discovery of prototypical members of widely distributed protein families with novel functions. Major advances have been made over the last decade in elucidating the molecular mechanisms underlying the light-dependent signaling and regulation of the transcriptional response leading to carotenogenesis in M. xanthus. This review aims to provide an up-to-date overview of these findings and their significance.