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Dev Genes Evol. 2017 Nov;227(6):375-387. doi: 10.1007/s00427-017-0576-5. Epub 2017 Jan 20.

Characterization of the cell polarity gene crumbs during the early development and maintenance of the squid-vibrio light organ symbiosis.

Author information

1
School of Medicine and Public Health, Department of Medical Microbiology and Immunology, University of Wisconsin, Madison, WI, 53706, USA. smpeyer@wisc.edu.
2
McPherson Eye Research Institute, University of Wisconsin, Madison, WI, 53706, USA. smpeyer@wisc.edu.
3
School of Medicine and Public Health, Department of Medical Microbiology and Immunology, University of Wisconsin, Madison, WI, 53706, USA.
4
Department of Molecular and Cell Biology, University of California-Berkeley, Berkeley, CA, 94720, USA.
5
School of Medicine and Public Health, Department of Medical Microbiology and Immunology, University of Wisconsin, Madison, WI, 53706, USA. mcfallng@hawaii.edu.
6
McPherson Eye Research Institute, University of Wisconsin, Madison, WI, 53706, USA. mcfallng@hawaii.edu.
7
Pacific Biosciences Research Center, University of Hawaii at Manoa, Honolulu, HI, 96822, USA. mcfallng@hawaii.edu.

Abstract

The protein Crumbs is a determinant of apical-basal cell polarity and plays a role in apoptosis of epithelial cells and their protection against photodamage. Using the squid-vibrio system, a model for development of symbiotic partnerships, we examined the modulation of the crumbs gene in host epithelial tissues during initiation and maintenance of the association. The extracellular luminous symbiont Vibrio fischeri colonizes the apical surfaces of polarized epithelia in deep crypts of the Euprymna scolopes light organ. During initial colonization each generation, symbiont harvesting is potentiated by the biochemical and biophysical activity of superficial ciliated epithelia, which are several cell layers from the crypt epithelia where the symbionts reside. Within hours of crypt colonization, the symbionts induce the cell death mediated regression of the remote superficial ciliated fields. However, the crypt cells directly interacting with the symbiont are protected from death. In the squid host, we characterized the gene and encoded protein during light organ morphogenesis and in response to symbiosis. Features of the protein sequence and structure, phylogenetic relationships, and localization patterns in the eye supported assignment of the squid protein to the Crumbs family. In situ hybridization revealed that the crumbs transcript shows opposite expression at the onset of symbiosis in the two different regions of the light organ: elevated levels in the superficial epithelia were attenuated whereas low levels in the crypt epithelia were turned up. Although a rhythmic association in which the host controls the symbiont population over the day-night cycle begins in the juvenile upon colonization, cycling of crumbs was evident only in the adult organ with peak expression coincident with maximum symbiont population and luminescence. Our results provide evidence that crumbs responds to symbiont cues that induce developmental apoptosis and to symbiont population dynamics correlating with luminescence-based stress throughout the duration of the host-microbe association.

KEYWORDS:

Apoptosis; Cephalopod; Eye; Photophore; Photoreceptor; Squid vibrio; Symbiosis

PMID:
28105525
PMCID:
PMC5519459
DOI:
10.1007/s00427-017-0576-5
[Indexed for MEDLINE]
Free PMC Article

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