Dinoflagellate nucleus contains an extensive endomembrane network, the nuclear net

Gregory S. Gavelis, Maria Herranz, Kevin C. Wakeman, Christina Ripken, Satoshi Mitarai, Gillian Gile, Patrick J. Keeling, Brian S. Leander

Research output: Contribution to journalArticle

Abstract

Dinoflagellates are some of the most common eukaryotic cells in the ocean, but have very unusual nuclei. Many exhibit a form of closed mitosis (dinomitosis) wherein the nuclear envelope (NE) invaginates to form one or more trans-nuclear tunnels. Rather than contact spindles directly, the chromatids then bind to membrane-based kinetochores on the NE. To better understand these unique mitotic features, we reconstructed the nuclear architecture of Polykrikos kofoidii in 3D using focused ion beam scanning electron microscopy (FIB-SEM) in conjunction with high-pressure freezing, freeze-substitution, TEM, and confocal microscopy. We found that P. kofoidii possessed six nuclear tunnels, which were continuous with a reticulating network of membranes that has thus far gone unnoticed. These membranous extensions interconnect the six tunnels while ramifying throughout the nucleus to form a “nuclear net.” To our knowledge, the nuclear net is the most elaborate endomembrane structure described within a nucleus. Our findings demonstrate the utility of tomographic approaches for detecting 3D membrane networks and show that nuclear complexity has been underestimated in Polykrikos kofoidii and, potentially, in other dinoflagellates.

Original languageEnglish (US)
Article number839
JournalScientific Reports
Volume9
Issue number1
DOIs
StatePublished - Dec 1 2019

Fingerprint

Dinoflagellida
Nuclear Envelope
Membranes
Freeze Substitution
Kinetochores
Chromatids
Eukaryotic Cells
Mitosis
Confocal Microscopy
Oceans and Seas
Electron Scanning Microscopy
Freezing
Ions
Pressure

ASJC Scopus subject areas

  • General

Cite this

Gavelis, G. S., Herranz, M., Wakeman, K. C., Ripken, C., Mitarai, S., Gile, G., ... Leander, B. S. (2019). Dinoflagellate nucleus contains an extensive endomembrane network, the nuclear net. Scientific Reports, 9(1), [839]. https://doi.org/10.1038/s41598-018-37065-w

Dinoflagellate nucleus contains an extensive endomembrane network, the nuclear net. / Gavelis, Gregory S.; Herranz, Maria; Wakeman, Kevin C.; Ripken, Christina; Mitarai, Satoshi; Gile, Gillian; Keeling, Patrick J.; Leander, Brian S.

In: Scientific Reports, Vol. 9, No. 1, 839, 01.12.2019.

Research output: Contribution to journalArticle

Gavelis, GS, Herranz, M, Wakeman, KC, Ripken, C, Mitarai, S, Gile, G, Keeling, PJ & Leander, BS 2019, 'Dinoflagellate nucleus contains an extensive endomembrane network, the nuclear net', Scientific Reports, vol. 9, no. 1, 839. https://doi.org/10.1038/s41598-018-37065-w
Gavelis, Gregory S. ; Herranz, Maria ; Wakeman, Kevin C. ; Ripken, Christina ; Mitarai, Satoshi ; Gile, Gillian ; Keeling, Patrick J. ; Leander, Brian S. / Dinoflagellate nucleus contains an extensive endomembrane network, the nuclear net. In: Scientific Reports. 2019 ; Vol. 9, No. 1.
@article{364f6df4831848ef8279548661ee1088,
title = "Dinoflagellate nucleus contains an extensive endomembrane network, the nuclear net",
abstract = "Dinoflagellates are some of the most common eukaryotic cells in the ocean, but have very unusual nuclei. Many exhibit a form of closed mitosis (dinomitosis) wherein the nuclear envelope (NE) invaginates to form one or more trans-nuclear tunnels. Rather than contact spindles directly, the chromatids then bind to membrane-based kinetochores on the NE. To better understand these unique mitotic features, we reconstructed the nuclear architecture of Polykrikos kofoidii in 3D using focused ion beam scanning electron microscopy (FIB-SEM) in conjunction with high-pressure freezing, freeze-substitution, TEM, and confocal microscopy. We found that P. kofoidii possessed six nuclear tunnels, which were continuous with a reticulating network of membranes that has thus far gone unnoticed. These membranous extensions interconnect the six tunnels while ramifying throughout the nucleus to form a “nuclear net.” To our knowledge, the nuclear net is the most elaborate endomembrane structure described within a nucleus. Our findings demonstrate the utility of tomographic approaches for detecting 3D membrane networks and show that nuclear complexity has been underestimated in Polykrikos kofoidii and, potentially, in other dinoflagellates.",
author = "Gavelis, {Gregory S.} and Maria Herranz and Wakeman, {Kevin C.} and Christina Ripken and Satoshi Mitarai and Gillian Gile and Keeling, {Patrick J.} and Leander, {Brian S.}",
year = "2019",
month = "12",
day = "1",
doi = "10.1038/s41598-018-37065-w",
language = "English (US)",
volume = "9",
journal = "Scientific Reports",
issn = "2045-2322",
publisher = "Nature Publishing Group",
number = "1",

}

TY - JOUR

T1 - Dinoflagellate nucleus contains an extensive endomembrane network, the nuclear net

AU - Gavelis, Gregory S.

AU - Herranz, Maria

AU - Wakeman, Kevin C.

AU - Ripken, Christina

AU - Mitarai, Satoshi

AU - Gile, Gillian

AU - Keeling, Patrick J.

AU - Leander, Brian S.

PY - 2019/12/1

Y1 - 2019/12/1

N2 - Dinoflagellates are some of the most common eukaryotic cells in the ocean, but have very unusual nuclei. Many exhibit a form of closed mitosis (dinomitosis) wherein the nuclear envelope (NE) invaginates to form one or more trans-nuclear tunnels. Rather than contact spindles directly, the chromatids then bind to membrane-based kinetochores on the NE. To better understand these unique mitotic features, we reconstructed the nuclear architecture of Polykrikos kofoidii in 3D using focused ion beam scanning electron microscopy (FIB-SEM) in conjunction with high-pressure freezing, freeze-substitution, TEM, and confocal microscopy. We found that P. kofoidii possessed six nuclear tunnels, which were continuous with a reticulating network of membranes that has thus far gone unnoticed. These membranous extensions interconnect the six tunnels while ramifying throughout the nucleus to form a “nuclear net.” To our knowledge, the nuclear net is the most elaborate endomembrane structure described within a nucleus. Our findings demonstrate the utility of tomographic approaches for detecting 3D membrane networks and show that nuclear complexity has been underestimated in Polykrikos kofoidii and, potentially, in other dinoflagellates.

AB - Dinoflagellates are some of the most common eukaryotic cells in the ocean, but have very unusual nuclei. Many exhibit a form of closed mitosis (dinomitosis) wherein the nuclear envelope (NE) invaginates to form one or more trans-nuclear tunnels. Rather than contact spindles directly, the chromatids then bind to membrane-based kinetochores on the NE. To better understand these unique mitotic features, we reconstructed the nuclear architecture of Polykrikos kofoidii in 3D using focused ion beam scanning electron microscopy (FIB-SEM) in conjunction with high-pressure freezing, freeze-substitution, TEM, and confocal microscopy. We found that P. kofoidii possessed six nuclear tunnels, which were continuous with a reticulating network of membranes that has thus far gone unnoticed. These membranous extensions interconnect the six tunnels while ramifying throughout the nucleus to form a “nuclear net.” To our knowledge, the nuclear net is the most elaborate endomembrane structure described within a nucleus. Our findings demonstrate the utility of tomographic approaches for detecting 3D membrane networks and show that nuclear complexity has been underestimated in Polykrikos kofoidii and, potentially, in other dinoflagellates.

UR - http://www.scopus.com/inward/record.url?scp=85060812346&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85060812346&partnerID=8YFLogxK

U2 - 10.1038/s41598-018-37065-w

DO - 10.1038/s41598-018-37065-w

M3 - Article

C2 - 30696854

AN - SCOPUS:85060812346

VL - 9

JO - Scientific Reports

JF - Scientific Reports

SN - 2045-2322

IS - 1

M1 - 839

ER -