The short life of the Hoyle organ of Sepia officinalis: formation, differentiation and degradation by programmed cell death
The short life of the Hoyle organ of Sepia officinalis: formation, differentiation and degradation by programmed cell death
0 A. Palumbo Department of Biology and Evolution of Marine Organisms, Stazione Zoologica Anton Dohrn , Naples , Italy
1 N. Cyran (&) W. Klepal Core Facility Cell Imaging and Ultrastructural Research, Faculty of Life Sciences, University of Vienna , Vienna , Austria
2 Guest editors: Erica A. G. Vidal, Ian G. Gleadall & Natalie Moltschaniswskyi / Advances in Cephalopod Ecology and Life Cycles
3 J. von Byern Ludwig Boltzmann Institute for Experimental and Clinical Traumatology, Austrian Cluster for Tissue Regeneration , Vienna , Austria
4 J. von Byern Max F Perutz Laboratories, Centre for Integrative Bioinformatics Vienna, University of Veterinary Medicine, Medical University of Vienna, University of Vienna , Vienna , Austria
5 Y. Staedler J. Scho ̈nenberger Division of Structural and Functional Botany, Department of Botany and Biodiversity Research, University of Vienna , Vienna , Austria
6 E. A. G. Vidal Center for Marine Studies, University of Parana - UFPR , Pontal do Parana , Brazil
Cephalopods encapsulate their eggs in protective egg envelopes. To hatch from this enclosure, most cephalopod embryos release egg shell-digesting choriolytic enzymes produced by the Hoyle organ (HO). After hatching, this gland becomes inactive and rapidly degrades by programmed cell death. We aim to characterize morphologically the development, maturation and degradation of the gland throughout embryonic and first juvenile stages in Sepia officinalis. Special focus is laid on cell death mechanisms and the presence of nitric oxide synthase during gland degradation. Hatching enzyme has been examined in view of metallic contents, commonly amplifying enzyme effectiveness. HO gland cells are first visualized at embryonic stage 23; secretion is observed from stage 27 onwards. Degradation of the HO occurs after hatching within two days by the rarely observed autophagic process, recognized for the first time in cephalopods. Nitric oxide synthase immunopositivity was not found in the HO cells after hatching, suggesting a possible NO role in cell death signalling. Although the HO 'life course' chronology in S. officinalis is similar to other cephalopods, gland degradation occurs by autophagy instead of necrosis. Eggs that combine a large perivitelline space
-
and multi-layered integument seem to require a more
complex and large gland system.
Introduction
Cephalopods have a great variety of egg encapsulation
mechanisms that can consist of from a single chorionic
coat without protective jelly envelopes in
octopodiformes to a multi-layer spirally coiled jelly coat in
most decapodiformes
(von Boletzky, 1986)
. Eggs can
be released individually or in egg masses, which size,
shape, structure and consistency also vary
substantially among species
(von Boletzky, 1986, 1998)
.
The hatching gland in cephalopods, referred to as
the HO (Hoyle organ)
(Wintrebert, 1928; Yung Ko
Ching, 1930)
, represents a co-adaptation of the
embryo to overcome the barrier imposed by the egg
envelopes, across which it has to move freely during
hatching. A close association is expected between egg
encapsulation design and the morphology of the HO
(von Boletzky, 2012). Therefore, detailed information
on the morphology and the process of formation and
degradation of the HO should have special value in
clarifying how the gland system has evolved among
species with assorted encapsulation mechanisms. This
in turn would provide a foundation for the
understanding of the ecological and evolutionary
significance of the HO.
In cephalopods, the HO is an epithelial organ
restricted to the posterior part of the dorsal mantle
surface. Shortly before hatching, the HO is fully
developed and releases proteolytic enzymes
(Denuce
& Formisano, 1982)
that weaken the egg integument so
that it becomes permeable to water, resulting in an
increase in osmotic pressure within the perivitelline
space
(von Boletzky, 2003)
. Instantly after hatching, a
bulk degradation of the gland takes place and is
accomplished within a few hours to a few days
(von
Orelli, 1959)
.
The HO generally consists of only one type of
glandular cells, which synthesize electron-dense
granules, spherical to polygonal in shape (depending on the
charging level)
(Cyran et al., 2013)
. In several
decapodiform species (e.g. Sepiella japonica Sasaki, 1929,
Sepia officinalis Linnaeus, 1758, Loligo sp. Lamarck,
1798, Sepioteuthis lessoniana Fe´russac [in Lesson],
1831, Architeuthis sp. Steenstrup, 1857), these granules
differ in the later stage of development by containing
electron-lucent inclusions
(Matsuno & Ouji, 1988;
Arnold & Singley, 1989; Cyran et al., 2013)
named
‘‘bipartite dense granules’’
(Arnold & Singley, 1989)
.
No information is available on the metal ion content
of the hatching enzyme of cephalopods and the
environmental and biological factors that regulate its
avail (...truncated)