Abstract
AbstractNitric oxide (NO) is a ubiquitous gaseous messenger, but we know little about its early evolution. Here, we analyzed NO synthases (NOS) in four different species of placozoans—one of the early-branching animal lineages. In contrast to other invertebrates studied, Trichoplax and Hoilungia have three distinct NOS genes, including PDZ domain-containing NOS. Using ultra-sensitive capillary electrophoresis assays, we quantified nitrites (products of NO oxidation) and l-citrulline (co-product of NO synthesis from l-arginine), which were affected by NOS inhibitors confirming the presence of functional enzymes in Trichoplax. Using fluorescent single-molecule in situ hybridization, we showed that distinct NOSs are expressed in different subpopulations of cells, with a noticeable distribution close to the edge regions of Trichoplax. These data suggest both the compartmentalized release of NO and a greater diversity of cell types in placozoans than anticipated. NO receptor machinery includes both canonical and novel NIT-domain containing soluble guanylate cyclases as putative NO/nitrite/nitrate sensors. Thus, although Trichoplax and Hoilungia exemplify the morphologically simplest free-living animals, the complexity of NO-cGMP-mediated signaling in Placozoa is greater to those in vertebrates. This situation illuminates multiple lineage-specific diversifications of NOSs and NO/nitrite/nitrate sensors from the common ancestor of Metazoa and the preservation of conservative NOS architecture from prokaryotic ancestors.
Funder
Human Frontiers Scientific Program
National Science Foundation
Swiss National Science Foundation
Publisher
Springer Science and Business Media LLC
Reference106 articles.
1. Moroz, L. L. & Kohn, A. B. Parallel evolution of nitric oxide signaling: Diversity of synthesis and memory pathways. Front. Biosci. 16, 2008–2051. https://doi.org/10.2741/3837 (2011).
2. Astier, J., Mounier, A., Santolini, J., Jeandroz, S. & Wendehenne, D. The evolution of nitric oxide signalling diverges between animal and green lineages. J. Exp. Bot. 70, 4355–4364. https://doi.org/10.1093/jxb/erz088 (2019).
3. Santolini, J. What does “NO-Synthase” stand for ?. Front. Biosci. 24, 133–171 (2019).
4. Moncada, S., Palmer, R. M. & Higgs, E. A. Nitric oxide: Physiology, pathophysiology, and pharmacology. Pharmacol. Rev. 43, 109–142 (1991).
5. Ignarro, L. J. 1003 (Academic Press, San Diego, 2000).
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