4.7 Article

The diversification and lineage-specific expansion of nitric oxide signaling in Placozoa: insights in the evolution of gaseous transmission

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SCIENTIFIC REPORTS
卷 10, 期 1, 页码 -

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NATURE PUBLISHING GROUP
DOI: 10.1038/s41598-020-69851-w

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资金

  1. Human Frontiers Science Program [RGP0060/2017]
  2. National Science Foundation [1146575, 1557923, 1548121, 1645219]
  3. Swiss National Science Foundation [31003A_182732]
  4. Swiss National Science Foundation (SNF) [31003A_182732] Funding Source: Swiss National Science Foundation (SNF)
  5. Division Of Integrative Organismal Systems
  6. Direct For Biological Sciences [1548121] Funding Source: National Science Foundation

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Nitric 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.

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