A microtubule organizing centre (MTOC) is responsible for the production of the sperm flagellum in Matsucoccus feytaudi (Hemiptera: Coccoidea)

Paoli, Francesco; Roversi, Pio Federico; Gottardo, Marco; Callaini, Giuliano; Mercati, David; Dallai, Romano

doi:10.1016/j.asd.2015.03.002

Cited by 10 publications

(4 citation statements)

References 37 publications

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“…Interestingly, the sperm of the highly specialized sternorrhynch subgroup Coccoidea have lost a conventional flagellar axoneme, and regained their motility through a flagellum produced by an acentriolar microtubule‐organizing centre (Paoli et al. ,b).…”

Section: Discussionmentioning

confidence: 99%

The evolution of insect sperm − an unusual character system in a megadiverse group

Gottardo

Dallai

Mercati

et al. 2016

J Zool Syst Evol Res

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Spermatozoa provide an unusual character system, with a limited number of components organized in a single cell. Similar spermatozoa occur in groups widely separated in the phylogenetic tree of Metazoa. Nevertheless, the character system contains phylogenetic information. Hexapoda have acquired spermatophores along with the switch from aquatic to terrestrial habitats, and related to this, a multitude of different sperm types. The aim of this study is a formal evaluation of the phylogenetic information content of spermatozoa. For the first time, sperm characters are coded for formal phylogenetic analyses. Different approaches are used and compared. Mainly due to a high level of homoplasy, the evaluation of sperm characters alone is insufficient for a reconstruction of the phylogeny of the group. Yet, a reliable reconstruction of the evolution of insect sperm is possible when character transformations are assessed using a phylogeny based on extensive molecular data. Important changes took place in the early evolution of Hexapoda. Sperm characters support some major clades (e.g. Hexapoda, Dicondylia, Polyneoptera, Psocodea), but important steps in the evolution are not reflected by transformations of spermatozoa, notably the rise of Pterygota or Holometabola. Important innovations are the formation of mitochondrial derivatives and the acquisition of accessory microtubules. Some features are conservative, whereas others evolved rapidly (e.g. presence or absence of the acrosome vesicle). Some groups are conservative in their sperm features (e.g. Odonata, Heteroptera), whereas the evolution of spermatozoa was distinctly accelerated in others (e.g. Ephemeroptera). The rate of evolution can change drastically in closely related groups. Profound changes in the morphologically uniform Zoraptera underline that sperm evolution can follow a pattern very different from the general somatic morphology. The mode of character reconstruction preferred here will be useful for the evaluation of specialized morphological character systems and strengthen the concept of evolutionary morphology.

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Section: Discussionmentioning

confidence: 99%

The evolution of insect sperm − an unusual character system in a megadiverse group

Gottardo

Dallai

Mercati

et al. 2016

J Zool Syst Evol Res

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“…The constant presence of F‐actin in the gametes from the various examined districts of T. liliifolia , however, never found in spermatozoa of other invertebrates, leads us to hypothesize, instead, the involvement of this cytoskeletal component in flagellar movements in both male and female genital tracts. It is worthy of note, moreover, the marked F‐actin positivity found immediately posterior to the nucleus, at an area corresponding to the basal body region; it cannot be excluded that the F‐actin could be a component of the pericentriolar material (also called centriolar adjunct material ), closely wrapped around the microtubules of the basal body during the spermiogenesis of several insects, including T. liliifolia (Dallai, ; Gatenby and Tahmisian ; Guerra et al, ; Jamieson, ; Paoli et al, ; Phillips, ; Viscuso et al, ; Vitale et al, ). Furthermore, this hypothesis is supported by the lacking of positivity for α‐tubulin at that area: the pericentriolar material, in fact, could prevent the specific anti‐α‐tubulin antibody from penetrating in that sperm region.…”

Section: Discussionmentioning

confidence: 99%

Fluorescence microscopy study on the cytoskeletal displacements during sperm differentiation in the bush‐cricket Tylopsis liliifolia (Fabricius) (Orthoptera: Tettigoniidae)

Viscuso

Federico

Saccone

et al. 2015

Microscopy Res & Technique

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A study by fluorescence microscopy has been carried out on male gametes from testicular follicles, seminal vesicles, spermatophores, and seminal receptacles of the bush-cricket Tylopsis liliifolia, focusing the attention on localization and movements of F-actin and α-tubulin during sperm differentiation, since data in this respect are lacking in the Orthoptera. F-actin and α-tubulin positivity was detected in the testicular follicles, in particular at the bridges connecting spermatids of a same clone and around their nucleus, during the first differentiation stages. During the following differentiation stages in the testes, F-actin was found at one of the spermatid poles and then, during nucleus elongation, at the whole acrosomal region. A peculiar F-actin-positivity was found at the flagellum, more markedly immediately posterior to the nucleus, at the basal body region of the gametes from the testicular follicles and from the other examined districts. Other interesting data from our investigations concerns the α-tubulin displacements during the differentiation stages of the spermatid and a constant absence of α-tubulin-positivity where the centrioles are located. No positivity was also found for both α-tubulin and nuclear markers at the anterior region of the gamete, where the acrosomal wings are localized. Our results, compared with what is so far known in literature for the insects, lead us to assert that microfilaments and microtubules undergo gradual displacements, markedly in the testicular follicles, during the morphogenesis of the male gamete of T. liliifolia aimed to its organization and motility and probably also to its interaction with the female gamete.

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“…However, these centrioles do not organize a functional axoneme at the onset of spermiogenesis. An axial structure consisting of single microtubules arranged in circular arrays assemble from a peripheral cluster of electron-dense material ( Figure 9B) containing g-tubulin [171]. These findings raise the question of how several insect species have elaborated controls over centriole/basal body conversion during spermatogenesis and how they have inactivated the usual switch between centrosome organization and axoneme nucleation.…”

Section: Exceptions To the Conventional Presence Of Sperm With Singlementioning

confidence: 98%

“…However, the sperm motility is supported by a bundle of singlet microtubules interconnected by short bridges of a dynein-like protein [207]. In the archaeococcid Matsucoccus, the early spermatids have a conventional non-functional centriole that does not give origin to the axoneme, but a microtubule-dependent structure is organized far from the centrioles by a peripheral non-centrosome organizing center [171]. This finding supports the hypothesis about the "autonomous" centriole origin through a sequence of events starting from a bundle of polarized microtubules that later should have contacted the plasma membrane and then protruded outward the cell to give origin to an atypical motile structure [208][209][210][211].…”

Section: The Peculiar Tale Of the Progressive Loss Of Sperm Flagella mentioning

confidence: 99%

Centrioles and Ciliary Structures during Male Gametogenesis in Hexapoda: Discovery of New Models

Riparbelli

Persico

Dallai

et al. 2020

Cells

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Centrioles are-widely conserved barrel-shaped organelles present in most organisms. They are indirectly involved in the organization of the cytoplasmic microtubules both in interphase and during the cell division by recruiting the molecules needed for microtubule nucleation. Moreover, the centrioles are required to assemble cilia and flagella by the direct elongation of their microtubule wall. Due to the importance of the cytoplasmic microtubules in several aspects of the cell life, any defect in centriole structure can lead to cell abnormalities that in humans may result in significant diseases. Many aspects of the centriole dynamics and function have been clarified in the last years, but little attention has been paid to the exceptions in centriole structure that occasionally appeared within the animal kingdom. Here, we focused our attention on non-canonical aspects of centriole architecture within the Hexapoda. The Hexapoda is one of the major animal groups and represents a good laboratory in which to examine the evolution and the organization of the centrioles. Although these findings represent obvious exceptions to the established rules of centriole organization, they may contribute to advance our understanding of the formation and the function of these organelles.Thus, the increase of g-tubulin leads to an increase in the nucleation of both astral and spindle microtubules, which drive the assembly of a functional spindle.At the heart of the centrosome there is a pair of centrioles, two microtubule-based barrel-shaped organelles of defined length and diameter [29], that warrants the integrity and the supramolecular organization of the centrosome itself. The coiled-coil proteins, pericentrin-like protein (PLP) and Cep152/Asterless form the scaffold for the matrix proteins Cep192/Spd-2, Cep215/Cnn and g-tubulin.It was observed PLP's C termini are located close to the centriole wall [26].In addition, to be the reference point for the organization of the centrosomal material, the centrioles may also act as templates for the axoneme assembly in cilia and flagella, that are involved in signalling and motility [30]. Therefore, the proper organization and dynamics of the centrioles are mandatory to ensure healthy cell life. Structural anomalies of the centrioles are found in several human cancers [31][32][33][34][35][36] and can be the cause of a spectrum of pathologies spanning from infertility to ciliopathies [37,38].Since, the centrioles impact upon several aspects of cell development and physiology, their structure and function have been studied over the years. However, this analysis was mainly addressed to examine centrioles in a few model organisms, such as Chlamydomonas reinhardtii, Caenorhabditis elegans, Drosophila melanogaster, and some vertebrate cell lines. From these studies emerge a highly conserved organization of the centrioles. However, investigations in different animal groups revealed distinct and sometimes important differences in the architecture of the centrioles [39,40]. Therefore, the analysi...

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A microtubule organizing centre (MTOC) is responsible for the production of the sperm flagellum in Matsucoccus feytaudi (Hemiptera: Coccoidea)

Cited by 10 publications

References 37 publications

The evolution of insect sperm − an unusual character system in a megadiverse group

The evolution of insect sperm − an unusual character system in a megadiverse group

Fluorescence microscopy study on the cytoskeletal displacements during sperm differentiation in the bush‐cricket Tylopsis liliifolia (Fabricius) (Orthoptera: Tettigoniidae)

Centrioles and Ciliary Structures during Male Gametogenesis in Hexapoda: Discovery of New Models

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