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Long-distance communication by specialized cellular projections during pigment pattern development and evolution.

Eom DS, Bain EJ, Patterson LB, Grout ME, Parichy DM - Elife (2015)

Bottom Line: Changes in gene activity are essential for evolutionary diversification.Projections depended on microfilaments and microtubules, exhibited meandering trajectories, and stabilized on target cells to which they delivered membraneous vesicles.By contrast, the uniformly patterned pearl danio lacked such projections, concomitant with Colony stimulating factor 1-dependent changes in xanthophore differentiation that likely curtail signaling available to melanophores.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Washington, Seattle, United States.

ABSTRACT
Changes in gene activity are essential for evolutionary diversification. Yet, elucidating the cellular behaviors that underlie modifications to adult form remains a profound challenge. We use neural crest-derived adult pigmentation of zebrafish and pearl danio to uncover cellular bases for alternative pattern states. We show that stripes in zebrafish require a novel class of thin, fast cellular projection to promote Delta-Notch signaling over long distances from cells of the xanthophore lineage to melanophores. Projections depended on microfilaments and microtubules, exhibited meandering trajectories, and stabilized on target cells to which they delivered membraneous vesicles. By contrast, the uniformly patterned pearl danio lacked such projections, concomitant with Colony stimulating factor 1-dependent changes in xanthophore differentiation that likely curtail signaling available to melanophores. Our study reveals a novel mechanism of cellular communication, roles for differentiation state heterogeneity in pigment cell interactions, and an unanticipated morphogenetic behavior contributing to a striking difference in adult form.

No MeSH data available.


Related in: MedlinePlus

Interspecific chimeras reveal non-autonomous effects on pattern and aox5+ cell behaviors.(A) In zebrafish→pearl chimeras, well-organized stripes of zebrafish cells formed but only when all three classes of zebrafish pigment cells (inset: x, xanthophore; m, melanophore; i, iridophores) were present and in the vicinity of other zebrafish tissues (blue outline, donor myotomes). Ten adult chimeras analyzed. (B) In pearl→albino zebrafish chimeras (in which host melanophores were present but unpigmented), pearl melanophores were confined to stripes, adopting a zebrafish-like arrangement; stripe-interstripe boundaries are indicated by dashed white lines and interstripes by yellow-orange bars at left. (C) Pearl aox5+ cells frequently developed in zebrafish hosts at embryonic/early larval stages (N=90 aox5+ chimeras), yet these same cells typically died by prior to time-lapse imaging during adult pigment pattern formation, here apparent by fragmentation and extrusion of GFP+ debris, typical of pigment cell death in zebrafish (Lang et al., 2009; Parichy et al., 1999). (D) Prior to extrusion, rare, surviving pearl danio aox5+ cells could extend numerous airinemes in zebrafish hosts (3 airinemes are shown; *, aox5+ cell fragmenting during imaging). Scale bars: 100 µm (A, for A and B); 20 µm (C); 50 µm (D).DOI:http://dx.doi.org/10.7554/eLife.12401.038
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fig6s1: Interspecific chimeras reveal non-autonomous effects on pattern and aox5+ cell behaviors.(A) In zebrafish→pearl chimeras, well-organized stripes of zebrafish cells formed but only when all three classes of zebrafish pigment cells (inset: x, xanthophore; m, melanophore; i, iridophores) were present and in the vicinity of other zebrafish tissues (blue outline, donor myotomes). Ten adult chimeras analyzed. (B) In pearl→albino zebrafish chimeras (in which host melanophores were present but unpigmented), pearl melanophores were confined to stripes, adopting a zebrafish-like arrangement; stripe-interstripe boundaries are indicated by dashed white lines and interstripes by yellow-orange bars at left. (C) Pearl aox5+ cells frequently developed in zebrafish hosts at embryonic/early larval stages (N=90 aox5+ chimeras), yet these same cells typically died by prior to time-lapse imaging during adult pigment pattern formation, here apparent by fragmentation and extrusion of GFP+ debris, typical of pigment cell death in zebrafish (Lang et al., 2009; Parichy et al., 1999). (D) Prior to extrusion, rare, surviving pearl danio aox5+ cells could extend numerous airinemes in zebrafish hosts (3 airinemes are shown; *, aox5+ cell fragmenting during imaging). Scale bars: 100 µm (A, for A and B); 20 µm (C); 50 µm (D).DOI:http://dx.doi.org/10.7554/eLife.12401.038

Mentions: To test if species differences in airineme production reflect evolutionary changes that are autonomous or non-autonomous to the xanthophore lineage, we transplanted cells between zebrafish and pearl danio (Parichy and Turner, 2003a; Quigley et al., 2004). Zebrafish aox5+ cells in pearl danio hosts extended airinemes at reduced frequencies, similar to that of pearl danio aox5+ cells (Figure 6A-right; Video 18). We interpret this observation, as well as aox5+ cell behaviors in reciprocal transplants, and adult pigment patterns of chimeras (Figure 6—figure supplement 1), as indicating species differences that are non-autonomous to the xanthophore lineage. These results are consistent with prior analyses that implicated cis-regulatory changes affecting environmentally produced xanthogenic Csf1 in the earlier and broader differentiation of xanthophores and altered melanophore pattern of pearl danio (Patterson et al., 2014). We therefore asked whether Csf1 alone could be responsible for species differences in airineme production. Consistent with this idea, overexpression of Csf1 in zebrafish resulted in a 22% reduction in airineme frequency within 24 hr and an 86% reduction after complete xanthophore differentiation, as in pearl (Figure 6A-right; Video 19).Video 18.Zebrafish aox5+ cells transplanted to pearl hosts behaved like pearl aox5+ cells.


Long-distance communication by specialized cellular projections during pigment pattern development and evolution.

Eom DS, Bain EJ, Patterson LB, Grout ME, Parichy DM - Elife (2015)

Interspecific chimeras reveal non-autonomous effects on pattern and aox5+ cell behaviors.(A) In zebrafish→pearl chimeras, well-organized stripes of zebrafish cells formed but only when all three classes of zebrafish pigment cells (inset: x, xanthophore; m, melanophore; i, iridophores) were present and in the vicinity of other zebrafish tissues (blue outline, donor myotomes). Ten adult chimeras analyzed. (B) In pearl→albino zebrafish chimeras (in which host melanophores were present but unpigmented), pearl melanophores were confined to stripes, adopting a zebrafish-like arrangement; stripe-interstripe boundaries are indicated by dashed white lines and interstripes by yellow-orange bars at left. (C) Pearl aox5+ cells frequently developed in zebrafish hosts at embryonic/early larval stages (N=90 aox5+ chimeras), yet these same cells typically died by prior to time-lapse imaging during adult pigment pattern formation, here apparent by fragmentation and extrusion of GFP+ debris, typical of pigment cell death in zebrafish (Lang et al., 2009; Parichy et al., 1999). (D) Prior to extrusion, rare, surviving pearl danio aox5+ cells could extend numerous airinemes in zebrafish hosts (3 airinemes are shown; *, aox5+ cell fragmenting during imaging). Scale bars: 100 µm (A, for A and B); 20 µm (C); 50 µm (D).DOI:http://dx.doi.org/10.7554/eLife.12401.038
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4764569&req=5

fig6s1: Interspecific chimeras reveal non-autonomous effects on pattern and aox5+ cell behaviors.(A) In zebrafish→pearl chimeras, well-organized stripes of zebrafish cells formed but only when all three classes of zebrafish pigment cells (inset: x, xanthophore; m, melanophore; i, iridophores) were present and in the vicinity of other zebrafish tissues (blue outline, donor myotomes). Ten adult chimeras analyzed. (B) In pearl→albino zebrafish chimeras (in which host melanophores were present but unpigmented), pearl melanophores were confined to stripes, adopting a zebrafish-like arrangement; stripe-interstripe boundaries are indicated by dashed white lines and interstripes by yellow-orange bars at left. (C) Pearl aox5+ cells frequently developed in zebrafish hosts at embryonic/early larval stages (N=90 aox5+ chimeras), yet these same cells typically died by prior to time-lapse imaging during adult pigment pattern formation, here apparent by fragmentation and extrusion of GFP+ debris, typical of pigment cell death in zebrafish (Lang et al., 2009; Parichy et al., 1999). (D) Prior to extrusion, rare, surviving pearl danio aox5+ cells could extend numerous airinemes in zebrafish hosts (3 airinemes are shown; *, aox5+ cell fragmenting during imaging). Scale bars: 100 µm (A, for A and B); 20 µm (C); 50 µm (D).DOI:http://dx.doi.org/10.7554/eLife.12401.038
Mentions: To test if species differences in airineme production reflect evolutionary changes that are autonomous or non-autonomous to the xanthophore lineage, we transplanted cells between zebrafish and pearl danio (Parichy and Turner, 2003a; Quigley et al., 2004). Zebrafish aox5+ cells in pearl danio hosts extended airinemes at reduced frequencies, similar to that of pearl danio aox5+ cells (Figure 6A-right; Video 18). We interpret this observation, as well as aox5+ cell behaviors in reciprocal transplants, and adult pigment patterns of chimeras (Figure 6—figure supplement 1), as indicating species differences that are non-autonomous to the xanthophore lineage. These results are consistent with prior analyses that implicated cis-regulatory changes affecting environmentally produced xanthogenic Csf1 in the earlier and broader differentiation of xanthophores and altered melanophore pattern of pearl danio (Patterson et al., 2014). We therefore asked whether Csf1 alone could be responsible for species differences in airineme production. Consistent with this idea, overexpression of Csf1 in zebrafish resulted in a 22% reduction in airineme frequency within 24 hr and an 86% reduction after complete xanthophore differentiation, as in pearl (Figure 6A-right; Video 19).Video 18.Zebrafish aox5+ cells transplanted to pearl hosts behaved like pearl aox5+ cells.

Bottom Line: Changes in gene activity are essential for evolutionary diversification.Projections depended on microfilaments and microtubules, exhibited meandering trajectories, and stabilized on target cells to which they delivered membraneous vesicles.By contrast, the uniformly patterned pearl danio lacked such projections, concomitant with Colony stimulating factor 1-dependent changes in xanthophore differentiation that likely curtail signaling available to melanophores.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Washington, Seattle, United States.

ABSTRACT
Changes in gene activity are essential for evolutionary diversification. Yet, elucidating the cellular behaviors that underlie modifications to adult form remains a profound challenge. We use neural crest-derived adult pigmentation of zebrafish and pearl danio to uncover cellular bases for alternative pattern states. We show that stripes in zebrafish require a novel class of thin, fast cellular projection to promote Delta-Notch signaling over long distances from cells of the xanthophore lineage to melanophores. Projections depended on microfilaments and microtubules, exhibited meandering trajectories, and stabilized on target cells to which they delivered membraneous vesicles. By contrast, the uniformly patterned pearl danio lacked such projections, concomitant with Colony stimulating factor 1-dependent changes in xanthophore differentiation that likely curtail signaling available to melanophores. Our study reveals a novel mechanism of cellular communication, roles for differentiation state heterogeneity in pigment cell interactions, and an unanticipated morphogenetic behavior contributing to a striking difference in adult form.

No MeSH data available.


Related in: MedlinePlus