The ParaHox gene Gsx patterns the apical organ and central nervous system but not the foregut in scaphopod and cephalopod mollusks

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Wollesen, Tim
Monje, Sonia Victoria Rodriguez
McDougall, Carmel
Degnan, Bernard M
Wanninger, Andreas
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2015
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Background: It has been hypothesized that the ParaHox gene Gsx patterned the foregut of the last common bilaterian ancestor. This notion was corroborated by Gsx expression in three out of four lophotrochozoan species, several ecdysozoans, and some deuterostomes. Remarkably, Gsx is also expressed in the bilaterian anterior-most central nervous system (CNS) and the gastropod and annelid apical organ. To infer whether these findings are consistent with other mollusks or even lophotrochozoans, we investigated Gsx expression in developmental stages of representatives of two other molluscan classes, the scaphopod Antalis entalis and the cephalopod Idiosepius notoides. Results: Gsx is not expressed in the developing digestive tract of Antalis entalis and Idiosepius notoides. Instead, it is expressed in cells of the apical organ in the scaphopod trochophore and in two cells adjacent to this organ. Latestage trochophores express Aen-Gsx in cells of the developing cerebral and pedal ganglia and in cells close to the pavilion, mantle, and foot. In postmetamorphic specimens, Aen-Gsx is expressed in the cerebral and pedal ganglia, the foot, and the nascent captacula. In early squid embryos, Ino-Gsx is expressed in the cerebral, palliovisceral, and optic ganglia. In late-stage embryos, Ino-Gsx is additionally expressed close to the eyes and in the supraesophageal and posterior subesophageal masses and optic lobes. Developmental stages close to hatching express Ino-Gsx only close to the eyes. Conclusions: Our results suggest that Gsx expression in the foregut might not be a plesiomorphic trait of the Lophotrochozoa as insinuated previously. Since neither ecdysozoans nor deuterostomes express Gsx in their gut, a role in gut formation in the last common bilaterian ancestor appears unlikely. Gsx is consistently expressed in the bilaterian anterior-most CNS and the apical organ of lophotrochozoan larvae, suggesting a recruitment of Gsx into the formation of this organ in the Lophotrochozoa. The cephalopod posterior subesophageal mass and optic ganglia and the scaphopod pedal ganglia also express Gsx. In summary, Gsx expression only appears to be conserved in the anteriormost brain region during evolution. Accordingly, Gsx appears to have been recruited into the formation of other expression domains, e.g., the apical organ or the foregut, in some lophotrochozoans

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EvoDevo

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6

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© 2015 Wollesen et al. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

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Biochemistry and cell biology

Evolutionary biology

Evolutionary biology not elsewhere classified

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