Ultrastructural analysis of the aberrant axoneme morphogenesis in thrips (Thysanoptera, Insecta)

Paccagnini, Eugenio; Mencarelli, Caterina; Mercati, David; Afzelius, Björn A.; Dallai, Romano

doi:10.1002/cm.20212

Cited by 17 publications

(6 citation statements)

References 31 publications

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“…All lice show a highly aberrant male meiosis, but PGE has only been confirmed in one species, the human body louse (McMeniman & Barker, ). The only other occurrence of a sperm flagellum containing two or more axonemes is found in the haplodiploid thrips (Thysanoptera) (Baccetti et al ., , Paccagnini et al ., ). For the remaining two origins of PGE, one in the coffee borer beetle and one in mites, there is no direct information on centrosome or axoneme structure, but centrosomes and axonemes are absent from the male germ line of all mites studied to date (Florek & Witalinski, ).…”

Section: Ultraconserved or Ultravariablementioning

confidence: 99%

Evolutionary problems in centrosome and centriole biology

Ross

Normark

2015

J of Evolutionary Biology

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Centrosomes have been an enigma to evolutionary biologists. Either they have been the subject of ill‐founded speculation or they have been ignored. Here, we highlight evolutionary paradoxes and problems of centrosome and centriole evolution and seek to understand them in the light of recent advances in centrosome biology. Most evolutionary accounts of centrosome evolution have been based on the hypothesis that centrosomes are replicators, independent of the nucleus and cytoplasm. It is now clear, however, that this hypothesis is not tenable. Instead, centrosomes are formed de novo each cell division, with the presence of an old centrosome regulating, but not essential for, the assembly of a new one. Centrosomes are the microtubule‐organizing centres of cells. They can potentially affect sensory and motor characters (as the basal body of cilia), as well as the movements of chromosomes during cell division. This latter role does not seem essential, however, except in male meiosis, and the reasons for this remain unclear. Although the centrosome is absent in some taxa, when it is present, its structure is extraordinarily conserved: in most taxa across eukaryotes, it does not appear to evolve at all. And yet a few insect groups display spectacular hypertrophy of the centrioles. We discuss how this might relate to the unusual reproductive system found in these insects. Finally, we discuss why the fate of centrosomes in sperm and early embryos might differ between different groups of animals.

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Section: Ultraconserved or Ultravariablementioning

confidence: 99%

Evolutionary problems in centrosome and centriole biology

Ross

Normark

2015

J of Evolutionary Biology

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“…Three are found in Halopthrips (Paccagnini et al. ). Among animal sperm, the multiflagellate condition with about 100 flagella is unique to Mastotermes (Riparbellim et al.…”

Section: Resultsmentioning

confidence: 99%

“…Two axonemes produced by a couple of centrioles are present in Goniodes and Liposcelis . Three are found in Halopthrips (Paccagnini et al 2007). Among animal sperm, the multiflagellate condition with about 100 flagella is unique to Mastotermes (Riparbellim et al 2009).…”

Section: Acrosomal Complexmentioning

confidence: 98%

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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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“…Each centriole nucleates an axoneme that projects outside the cell as a flagellum ( Figure 8C). Later, during spermiogenesis, the three flagella fuse their plasma membrane to form a large microtubular bundle of 27 units consisting of doublet and singlet microtubules ( Figure 8C) [168,169]. Remarkably, the spermatid of the termite Mastotermes has one hundred centrioles that nucleate as many independent flagella [126,127].…”

Section: Exceptions To the Conventional Presence Of Sperm With Singlementioning

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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Ultrastructural analysis of the aberrant axoneme morphogenesis in thrips (Thysanoptera, Insecta)

Cited by 17 publications

References 31 publications

Evolutionary problems in centrosome and centriole biology

Evolutionary problems in centrosome and centriole biology

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

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

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