Abstract
Lipoxygenase (LOX) plays important roles in fatty acid oxidation and lipid mediator biosynthesis. In this study, we give first insights into brown algal LOX evolution. Whole genome searches revealed four, three, and eleven LOXs in Ectocarpus siliculosus, Cladosiphon okamuranus, and Saccharina japonica, respectively. In phylogenetic analyses, LOXs from brown algae form a robust clade with those from prokaryotes, suggesting an ancestral origin and slow evolution. Brown algal LOXs were divided into two clades, C1 and C2 in a phylogenetic tree. Compared to the two species of Ectocarpales, LOX gene expansion occurred in the kelp S. japonica through tandem duplication and segmental duplication. Selection pressure analysis showed that LOX genes in brown algae have undergone strong purifying selection, while the selective constraint in the C2 clade was more relaxed than that in the C1 clade. Furthermore, within each clade, LOXs of S. japonica evolved under more relaxed selection constraints than E. siliculosus and C. okamuranus. Structural modeling showed that unlike LOXs of plants and animals, which contain a β barrel in the N-terminal part of the protein, LOXs in brown algae fold into a single domain. Analysis of previously published transcriptomic data showed that LOXs in E. siliculosus are responsive to hyposaline, hypersaline, oxidative, and copper stresses. Moreover, clear divergence of expression patterns was observed among different life stages, as well as between duplicate gene pairs. In E. siliculosus, all four LOXs are male-biased in immature gametophytes, and mature gametophytes showed significantly higher LOX mRNA levels than immature gametophytes and sporophytes. In S. japonica, however, our RNA-Seq data showed that most LOXs are highly expressed in sporophytes. Even the most recently duplicated gene pairs showed divergent expression patterns, suggesting that functional divergence has likely occurred since LOX genes duplicated, which potentially contributes to the production of various oxylipins in brown algae.
Highlights
Lipid oxidation is an essential biological process in all living organisms and is subject to both developmental and environmental regulation (Liavonchanka and Feussner, 2006)
In S. japonica, E. siliculosus, and C. okamuranus, three, one, and two LOXs were predicted to be located in the chloroplast, respectively
In order to perform phylogenetic analysis, we searched for the LOX genes in other organisms, including oomycetes, Phaeodactylum tricornutum, Thalassiosira pseudonana, Fragilariopsis cylindrus, Nannochloropsis gaditana, and Emiliania huxleyi, all of which, together with brown algae belong to the Stramenopiles and Haptophytes
Summary
Lipid oxidation is an essential biological process in all living organisms and is subject to both developmental and environmental regulation (Liavonchanka and Feussner, 2006). Lipoxygenases (LOX; EC 1.13.11.12) constitute an important group of enzymes responsible for this kind of lipid metabolism They are non-haem iron-containing dioxygenases that catalyze the addition of oxygen to polyunsaturated fatty acids (PUFAs) to produce hydroperoxides, which are further converted into a series of biologically active compounds collectively named oxylipins (Fatima et al, 2017). The abundant linoleic acid and linolenic acid are major substrates of LOXs in plants, while the principal substrate in animals is arachidonic acid (Porta and Rocha-Sosa, 2001) Derived oxylipins, such as jasmonic acid in plants or prostaglandins and leukotrienes in animals, are important bio-regulators and participate in a wide range of physiological functions, including the regulation of growth, development, and senescence, the mediation of stress responses (Bueno et al, 2001; Hou et al, 2015), or the maintenance of cell homeostasis (Molina and Donaire, 2002; Ackermann et al, 2017)
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