Get 20M+ Full-Text Papers For Less Than $1.50/day. Start a 14-Day Trial for You or Your Team.

Learn More →

Energide–cell body as smallest unit of eukaryotic life

Energide–cell body as smallest unit of eukaryotic life Abstract Background The evolutionary origin of the eukaryotic nucleus is obscure and controversial. Currently preferred are autogenic concepts; ideas of a symbiotic origin are mostly discarded and forgotten. Here we briefly discuss these issues and propose a new version of the symbiotic and archaeal origin of the eukaryotic nucleus. Scope and Conclusions The nucleus of eukaryotic cells forms via its perinuclear microtubules, the primary eukaryotic unit known also as the Energide–cell body. As for all other endosymbiotic organelles, new Energides are generated only from other Energides. While the Energide cannot be generated de novo, it can use its secretory apparatus to generate de novo the cell periphery apparatus. We suggest that Virchow’s tenet Omnis cellula e cellula should be updated as Omnis Energide e Energide to reflect the status of the Energide as the primary unit of the eukaryotic cell, and life. In addition, the plasma membrane provides feedback to the Energide and renders it protection via the plasma membrane-derived endosomal network. New discoveries suggest archaeal origins of both the Energide and its host cell. Cell body, cell theory, coenocytes, cytoskeleton, endosymbiosis, Energide, eukaryotic cell, evolution, microtubules, nucleus, syncytia PETER BARLOW AND PROBLEMS WITH THE CELL THEORY As documented by papers in this Annals of Botany special issue, the interests of Peter Barlow were wide-ranging and profound. These interests touched significantly also on the fundamental problems associated with the current version of the cell theory (Baluška et al., 1997, 1998, 2004a, b). Multinuclear cells, the supracellular nature of plants and fungi, and the many examples of cells within cells are all exceptions to cell theory. The supracellular nature of higher plants is complemented with the inherent property of animal cells of generating cytoplasmic channels known as tunnelling nanotubes (Wang et al., 2010; Zani and Edelman, 2010; Abounit and Zurzolo, 2012; Wang and Gerdes, 2012; Austefjord et al., 2014). In higher plants, migration of nuclei from cell to cell is known as cytomixis (Heslop-Harrison, 1966; Liu et al., 2007; Lone and Lone, 2013; Mursalimov et al., 2013; Kravets et al., 2017). The individuality of eukaryotic nuclei is apparent from red algal parasites, which transfer whole nuclei in their host cells, and these then redirect the host cell biology and physiology for the parasite’s benefit (Goff and Coleman, 1984, 1985, 1987, 1995; Goff and Zuccarello, 1994; Salomaki and Lane 2014). There are numerous examples of unicellular but multi-Energide coenocytic organisms, including marine algae such as Caulerpa, Cladophora and Acetabularia (Strasburger, 1913; Menzel and Elsner-Menzel, 1990; Menzel, 1994; Mine et al., 2008; Baluška et al., 2012). Probably the most flagrant violation of the current problematic version of the cell theory is provided by Ascomycota (Gladfelter, 2006; Lang et al., 2010; Roper et al., 2011) and Glomeromycota (Kuhn et al., 2001; Bewer and Wang, 2005; Jany and Pawlowska, 2010; Marleau et al., 2011; Boon et al., 2015; Young, 2015). Their fungal mycelia harbour genetically different nuclei in the same cytoplasm. In other words, these coenocytic ‘cells’ provide shelter for genomically diverse organismal units. For example, one single multinucleate spore of Glomus irregulare contains up to 1000 nuclei. In addition, large heterogeneity exists in the number of nuclei (Energides) among sister spores (Marleau et al., 2011). Moreover, non-self vegetative fusions are typical of hyphae of the arbuscular mycorrhizal fungus Glomus intraradices (Croll et al., 2009). EVOLUTION OF THE ENERGIDE–CELL BODY CONCEPT: SACHS, MAZIA AND OTHERS Discoveries of centrosomes and centrioles organizing both flagella and mitotic spindles of eukaryotic cells (Boveri, 1895; Flemming, 1891; Baltzer, 1967; Paweletz, 2001) strongly suggest that nuclei of eukaryotic cells are closely associated, via perinuclear microtubules (Baluška et al., 1997, 1998, 2004a, b), with both centrosomes and centrioles. Daniel Mazia was the first to realize that there is not only structural but also functional unity between all these organelles and he proposed the ‘cell body’ concept at the end of his scientific career (Mazia, 1987, 1993). Daniel Mazia’s cell body concept was preceded by Julius Sachs, who proposed his Energide concept in 1893 (Sachs, 1892a, b; Baluška et al., 2006). But Sachs was not aware of microtubules, centrioles and centrosomes. Under the influence of Theodor Boveri, it was Max Hartmann (1911) followed by Karl Bělař (1926) who further evolved the Energide concept in this respect (discussed in Chen, 2003). It is not known whether Daniel Mazia was aware of the Energide concept (Energidenlehre in German; see Chen, 2003) when he proposed the cell body concept in 1993 (Mazia, 1993). However, he had come to think the centrosome was potentially far more than just the organizer and initiator of microtubule synthesis. They were ‘bearers of information about cell morphology’ and that ‘something exists at a level of complexity higher than that of molecules akin to the level of the complexity of chromosomes’, and that something was what he called the ‘cell body’ (Mazia, 1987; Lyons, 2018). In 1997, 1998 and 2004, together with Peter Barlow, we updated Mazia’s hypothesis and proposed that the nucleus with perinuclear microtubules represents the smallest and basic unit of eukaryotic life (Baluška et al., 1997, 1998, 2004a, b). This hypothesis solves the problem of syncytia and coenocytes, which are incompatible with the classical cell theory stating that the whole cell is the basic unit of eukaryotic life (Baluška et al., 1997, 1998, 2004a, b, 2006). In 2009, we extended the Energide–cell body concept to central nervous systems (Agnati et al., 2009). Later, we discussed the Energide–cell body hypothesis from the perspective of the Neo-Energide concept (Baluška et al., 2006; see also Nicholson, 2010), originally proposed by Julius Sachs (Sachs, 1892a, b). Recently, the evolutionary origins of the Energide–cell body complex, as well as its eukaryotic cell, were discussed from evolutionary perspectives (Baluška and Lyons, 2018). Here, we briefly summarize the Energide–cell body concept and highlight the latest evidence of its validity. The Energide–cell body theory provides a robust explanation as to why there is eukaryotic sex and why male gametes are typically small, flagellated and motile, whereas female gametes are large, not motile and based on the actin cytoskeleton. The flagella of sperm cells are made of microtubules and typically lack any actin cytoskeleton while the larger egg cells are based primarily on the actin cytoskeleton (Baluška et al., 2004a, 2006). Importantly, nuclear pores are prototypes of cell–cell channels, resembling plasmodesmata in plants and tunnelling nanotubes in animals. The Energide–cell body concept is useful in explaining such perplexing discoveries as entosis and cannibalism in animal cells (Fais, 2007; Overholtzer et al., 2007; Janssen and Medema, 2011; Sharma and Dey, 2011). Moreover, developing erythroblasts extrude their nuclei, which are then engulfed by macrophages (Yoshida et al., 2005; Klei et al., 2017). Further examples of the independent nature of nuclei from cells include cell–cell transport of nuclei in plants (Lone and Lone, 2013; Mursalimov et al., 2013; Kravets et al., 2017) and infectious transfer of nuclei in parasitic red algae (Goff and Coleman, 1984, 1987). In contradiction to the current version of the cell theory is the unique multigenomic nature of coenocytic (multi-Energidic) Glomeromycota fungi, whose spores contain up to 1000 nuclei (Energides–cell bodies) within one huge single coenocytic cell (Marleau et al., 2011; Boon et al., 2015; Young, 2015). ARCHAEAL ORIGINS OF SYMBIOTIC ENERGIDES–CELL BODIES AND THEIR HOST CELLS (CHRONOCYTES) In the contemporary literature, diverse versions of autogenous theories for the origin of the eukaryotic cell predominate. However, it is very important to consider that, although initially treated with scepticism, the symbiotic origin of mitochondria and plastids turned out to be true. Viewing the nucleus as the primary eukaryotic endosymbiotic organelle would solve problems with the sudden appearance on the evolutionary scene of the complex eukaryotic cell, with its nucleus inherently associated with an endoplasmic reticulum and microtubular cytoskeleton. The various autogenous theories also are not able to explain why the last eukaryotic ancestors (LECAs; Woese, 1998, 2002) were complex organisms having almost all the eukaryotic features, including centrosomes, nuclei with lamina and nuclear pores, as well as the flagellar apparatus based on microtubules (Gräf et al., 2015; Grau-Bové et al., 2015; Vicente and Wordeman, 2015). All this provides evidence for the parasitic–symbiotic concept of a small motile cell, using its microtubular flagella, invading a large non-motile host cell based on the actin cytoskeleton (Baluška et al., 2004a). Recent advances in our understanding of these elusive issues reveal archaeal origins of this eukaryotic complexity (Guy and Ettema, 2011; Guy et al., 2014; Koonin and Yutin, 2014; Koonin, 2015; Eme et al., 2017; Zaremba-Niedzwiedzka et al., 2017). All these data point to the archaeal nature of both the host and guest cells that generated the LECA (Eme et al., 2017; Baluška and Lyons, 2018). Archaeal host cells [termed ‘chronocytes’ by Hartman and Fedorov (2002)] were proposed to acquire microtubule-based guest cells endosymbiotically (Baluška and Lyons, 2018), and these cells transformed into eukaryotic nuclei associated with the microtubule-based cytoskeleton. Thus, both the discovery of critical eukaryotic signature proteins (ESPs; Hartman and Fedorov, 2002) in Archaea of the ‘TACK’ superphylum (Guy and Ettema, 2011; Eme et al., 2017; Spang et al., 2017; Zaremba-Niedzwiedzka et al., 2017) and new discoveries in cell biology (summarized by Baluška and Lyons, 2018) suggest archaeal origins of both the Energides–cell bodies and their host cells. THE ENERGIDE–CELL BODY COMPLEX AS THE SMALLEST UNIT OF EUKARYOTIC LIFE Autogenous evolution is a kind of self-generated evolution (O’Malley and Müller-Wille, 2010); whereas the parasitic–symbiotic scenarios for the evolutionary origin of complex eukaryotic cells are examples of evolution by associations imposed on cells from outside (Baluška et al., 2004a, b, 2006; Klepzig et al., 2009; Sapp, 2010; Gilbert et al., 2012; Baluška and Lyons, 2018). The symbiotic origin of the nucleus as an Energide–cell body complex, as proposed in the latest version of the Neo-Energide theory (Baluška and Lyons, 2018), is supported by several unique features of eukaryotic cells that are not compatible with the diverse autogenous theories. First of all, the eukaryotic cilia and flagellar apparatus share their basal bodies with the perinuclear centrioles and centrosomes (Baluška and Lyons, 2018). Importantly, SYNE proteins, which anchor nuclei to neuromuscular synaptic junctions (Grady et al., 2005) and centre nuclear positions within eukaryotic cells (Zhu et al., 2017), are also integral proteins of ciliary rootlets (Potter et al., 2017). Relevant in this respect are algae such as Chlamydomonas and the protozoan Giardia, which have flagellar basal bodies connected to the nuclear surfaces via centrin-based contractile fibres (Salisbury, 1988; Wright et al., 1989; Koblenz et al., 2003; Dawson and House, 2010). The flagellar apparatus is an ancient eukaryotic organelle that is based on basal bodies acting as the primary microtubule-organizing centres (MTOCs) of the eukaryotic cell (Azimzadeh, 2014; Gräf et al., 2015). Nuclear pores resemble and act like classical cell–cell channels (Lee et al., 2000; Baluška et al., 2006; Bloemendal and Kück, 2013). There are also similarities between nuclear pores and flagellar entry domains (McClure-Begley and Klymkowsky, 2017; Rout and Field, 2017). Intriguingly in this respect, flagellar centrins (Salisbury, 1988; Salisbury et al., 1988) are components of plant-specific cell–cell channels (plasmodesmata; Blackman et al., 1999) and nuclear pores (Resendes et al., 2008); and also connect centrioles/centrosomes to the nuclei (Gräf et al., 2015). The symbiotic origin not only of nuclei (Baluška and Lyons, 2018) but also of cilia and flagella is strongly supported by numerous similarities between cilia/flagella and immunological synapses (Stinchcombe and Griffiths, 2014; Stinchcombe et al., 2015). There are strong parallels between ciliogenesis and the formation of immunological and cytotoxic synapses (Stinchcombe et al., 2015; Dieckmann et al., 2016). In the recently proposed updated version of the Energide–cell body theory, the endoplasmic reticulum membranes represent an outgrowth of the outer part of the nuclear envelope (Baluška and Lyons, 2018) and membranes of the Golgi apparatus represent specialized extensions of the endoplasmic reticulum (Chapman and Alliegro, 2012; Baluška and Lyons, 2018). Finally, the Energide–cell body complex is proposed to represent the primary and smallest unit of eukaryotes that can generate a complete cell, whereas de-nucleated eukaryotic cells can never generate a new Energide–cell body de novo (Baluška et al., 2006; Baluška and Lyons, 2018). This primacy of the Energide–cell body unit over the rest of the eukaryotic cell can also be seen during cell division, which invariably starts with the division of the centriole/centrosome, is followed by nuclear division and completed by cytoplasmic/cell periphery division, known as cytokinesis. The latter is instructed by the newly emerged daughter Energides–cell bodies of early cytokinetic cells. In conclusion, Rudolf Virchow’s famous tenet Omnis cellula e cellula should be updated to Omnis Energide e Energide (Baluška and Lyons, 2018). DANIEL MAZIA VERSUS LYNN MARGULIS: ENERGIDE–CELL BODY VERSUS KARYOMASTIGONT In their karyomastigont hypothesis, Lynn Margulis and her co-authors proposed the origin of the nucleus via the karyomastigont, which consisted of a nucleus and flagellar apparatus (Margulis, 1996; Margulis et al., 2000, 2005, 2006, 2007). The problematic part of the karyomastigont concept is the spirochaete origin of the tubulin-based flagellum, which should be descended from putatively Mixotricha-like ectosymbionts (Margulis, 1996; Margulis et al., 2000, 2006; König et al., 2006; Radek and Nitsch, 2007). In our recent Energide–cell body concept (Baluška and Lyons, 2018), the microtubule-based putative flagellated Archaea are proposed to invade the actin-based host cell Archaea and be transformed into the Energide–cell body. This Archaea–Archaea concept of eukaryotic origin explains why the eukaryotic nucleus is inherently associated with microtubule-based flagella via centrin-based and contractile rootlet/rhizoplast structures in evolutionarily ancient protists, including Naegleria, Giardia and Breviata (Walker et al., 2006; Minge et al., 2009; Dawson and House 2010; Fritz-Laylin and Fulton, 2016) and in flagellated algae, including Chlamydomonas reinhardtii (Salisbury, 1988; Salisbury et al., 1988; Dutcher, 2003). Later in eukaryotic evolution, the nucleus was liberated from the flagellar apparatus (sensu the akaryomastigont of Margulis and colleagues) but remained functionally coupled to cilia via basal bodies, centrioles and centrosomes (Dolan et al., 2000a, b ). Moreover, higher plant cells accomplished further liberation when their Energides–cell bodies lost corpuscular centrioles/centrosomes during land plant evolution (Mazia, 1987, 1993; Baluška et al., 1997, 1998, 2004a, b). The Energide–cell body concept provides answers as to why centrioles and basal bodies share not only the same centrin-based architecture (Dutcher, 2003; Koblenz et al., 2003; Ruiz et al., 2005), but also why their duplication is typically linked to the nucleus, accomplished only once per cell cycle (Salisbury, 1995, 2007), and why there are similarities between cilia/flagella and immunological synapses (Stinchcombe and Griffiths, 2014; Stinchcombe et al., 2015). OUTLOOK The main reason the Energide–cell body concept has essentially been ignored is because researchers have been reluctant to accept the endosymbiotic origin of the nucleus (Baluška and Lyons, 2018). A better understanding of the true nature of the eukaryotic cell is not only important for understanding the development of multicellular organisms but is also essential for our ability to cure cancer (Boveri, 1929; Mazia, 1987; Lingle et al., 2005; Cosenza and Krämer, 2016). Our understanding of the true nature of the eukaryotic cell as a symbiotic consortium organized via Energide–cell body activities is essential for our ability to comprehend life based on eukaryotic cells and their nucleus-based Energides–cell bodies. The archaeal nature of both the Energide–cell body and its host cell supports the two-domain Tree of Life (Eme et al., 2017; Spang et al., 2017). This is a real archaeal revolution in our understanding of the evolutionary origins of eukaryotic cells and their nuclei. LITERATURE CITED Abounit S, Zurzolo C. 2012. Wiring through tunneling nanotubes – from electrical signals to organelle transfer. Journal of Cell Science  125: 1089– 1098. Google Scholar CrossRef Search ADS PubMed  Agnati LF, Fuxe K, Baluška F, Guidolin D. 2009. Implications of the ‘Energide’ concept for communication and information handling in the central nervous system. Journal of Neural Transmission  11: 1037– 1052. Google Scholar CrossRef Search ADS   Austefjord MW, Gerdes HH, Wang X. 2014. Tunneling nanotubes: diversity in morphology and structure. Communicative & Integrative Biology  7: e27934. Google Scholar CrossRef Search ADS PubMed  Azimzadeh J. 2014. Exploring the evolutionary history of centrosomes. Philosophical Transactions of the Royal Society of London B Biological Sciences  369: 1650. Google Scholar CrossRef Search ADS   Baltzer F. 1967. Theodor Boveri – life and work of a great biologist 1862–1915 . Berkeley: University of California Press. Baluška F, Lyons S. 2018. Symbiotic origin of eukaryotic nucleus – from cell body to Neo-Energide. In: Sahi V, Baluška F, eds. Concepts in cell biology – history and evolution . Springer International Publishing. Baluška F, Volkmann D, Barlow PW. 1997. Nuclear components with microtubule organizing properties in multicellular eukaryotes: functional and evolutionary considerations. International Review of Cytology  175: 91– 135. Google Scholar CrossRef Search ADS PubMed  Baluška F, Lichtscheidl IK, Volkmann D, Barlow PW. 1998. The plant cell body: a cytoskeletal tool for cellular development and morphogenesis. Protoplasma  202: 1– 10. Google Scholar CrossRef Search ADS   Baluška F, Volkmann D, Barlow PW. 2004a. Eukaryotic cells and their cell bodies: cell theory revisited. Annals of Botany  94: 9– 32. Google Scholar CrossRef Search ADS   Baluška F, Volkmann D, Barlow PW. 2004b. Cell bodies in a cage. Nature  428: 371. Google Scholar CrossRef Search ADS   Baluška F, Volkmann D, Barlow PW. 2006. Cell-cell channels and their implications for cell theory. In: Baluška F, Volkmann D, Barlow PW, eds. Cell-cell channels . Landes Bioscience, 1– 18. Google Scholar CrossRef Search ADS   Baluška F, Volkmann D, Menzel D, Barlow PW. 2012. Strasburger’s legacy to mitosis and cytokinesis and its relevance for the cell theory. Protoplasma  249: 1151– 1162. Google Scholar CrossRef Search ADS PubMed  Bělař K. 1926. Der Formwechsel der Protistenkerne. Ergebnisse und Fortschritte der Zoologie . Jena: Fischer. Bewer JD, Wang M. 2005. Arbuscular mycorrhizal fungi – hyphal fusion and multigenomic structure. Nature  433: E3– E4. Google Scholar CrossRef Search ADS PubMed  Blackman LM, Harper JD, Overall RL. 1999. Localization of a centrin-like protein to higher plant plasmodesmata. European Journal of Cell Biology  78: 297– 304. Google Scholar CrossRef Search ADS PubMed  Bloemendal S, Kück U. 2013. Cell-to-cell communication in plants, animals, and fungi: a comparative review. Naturwissenschaften  100: 3– 19. Google Scholar CrossRef Search ADS PubMed  Boon E, Halary S, Bapteste E, Hijri M. 2015. Studying genome heterogeneity within the arbuscular mycorrhizal fungal cytoplasm. Genome Biology and Evolution  7: 505– 521. Google Scholar CrossRef Search ADS PubMed  Boveri T. 1895. Über das Verhalten der Centrosomen bei der Befruchtung des Seeigeleies nebst allgemeinen Bemerkungen über Centrosomen und Verwandtes. Verhandlungen der Physikalische-Medizinische Gesellschaft Würzburg  29: 1– 75. Boveri T. 1929. The origin of malignant tumors . Baltimore, MD: Williams and Wilkins. Chapman M, Alliegro MC. 2012. The karyomastigont as an evolutionary seme. Quarterly Review of Biology  87: 315– 324. Google Scholar CrossRef Search ADS PubMed  Chen H-A. 2003. Die Sexualitätstheorie und “Theoretische Biologie” von Max Hartmann in der ersten Hälfte des zwanzigsten Jahrhunderts. Sudhoffs Archiv  46: 1– 308. Cosenza MR, Krämer A. 2016. Centrosome amplification, chromosomal instability and cancer: mechanistic, clinical and therapeutic issues. Chromosome Research  24: 105– 126. Google Scholar CrossRef Search ADS PubMed  Croll D, Giovannetti M, Koch AMet al.   2009. Nonself vegetative fusion and genetic exchange in the arbuscular mycorrhizal fungus Glomus intraradices. New Phytologist  181: 924– 937. Google Scholar CrossRef Search ADS PubMed  Dawson SC, House SA. 2010. Life with eight flagella: flagellar assembly and division in Giardia. Current Opinion in Microbiology  13: 480– 490. Google Scholar CrossRef Search ADS PubMed  Dieckmann NM, Frazer GL, Asano Y, Stinchcombe JC, Griffiths GM. 2016. The cytotoxic T lymphocyte immune synapse at a glance. Journal of Cell Science  129: 2881– 2886. Google Scholar CrossRef Search ADS PubMed  Dolan MF, D’Ambrosio U, Wier AM, Margulis L. 2000a. Surface kinetosomes and disconnected nuclei of a calonymphid: ultrastructure and evolutionary significance of Snyderella tabogae. Acta Protozoologica  39: 135– 141. Dolan MF, Wier AM, Margulis L. 2000b. Budding and asymmetric reproduction of a trichomonad with as many as 1000 nuclei in karyomastigonts: Metacoronympha from Incisitermes. Acta Protozoologica  39: 275– 280. Dutcher SK. 2003. Elucidation of basal body and centriole functions in Chlamydomonas reinhardtii. Traffic  4: 443– 451. Google Scholar CrossRef Search ADS PubMed  Eme L, Spang A, Lombard J, Stairs CW, Ettema TJG. 2017. Archaea and the origin of eukaryotes. Nature Reviews Microbiology  15: 711– 723. Google Scholar CrossRef Search ADS PubMed  Fais S. 2007. Cannibalism: a way to feed on metastatic tumors. Cancer Letters  258: 155– 164. Google Scholar CrossRef Search ADS PubMed  Flemming W. 1891. Attraktionsphären und Zentralkörperchen in Gewebs- und Wanderzellen. Anatomischer Anzeiger  6: 78– 86. Fritz-Laylin LK, Fulton C. 2016. Naegleria: a classic model for de novo basal body assembly. Cilia  5: 10. Google Scholar CrossRef Search ADS PubMed  Gilbert SF, Sapp J, Tauber AI. 2012. A symbiotic view of life: we have never been individuals. Quarterly Review of Biology  87: 325– 341. Google Scholar CrossRef Search ADS PubMed  Gladfelter AS. 2006. Nuclear anarchy: asynchronous mitosis in multinucleated fungal hyphae. Current Opinion in Microbiology  9: 547– 552. Google Scholar CrossRef Search ADS PubMed  Goff LJ, Coleman AW. 1984. Transfer of nuclei from a parasite to its host. Proceedings of the National Academy of Sciences of the USA  81: 5420– 5424. Google Scholar CrossRef Search ADS PubMed  Goff LJ, Coleman AW. 1985. The role of secondary pit connections in red algal parasitism. Journal of Phycology  21: 483– 508. Google Scholar CrossRef Search ADS   Goff LJ, Coleman AW. 1987. Nuclear transfer from parasite to host: a new regulatory mechanism of parasitism. Annals of the New York Academy of Sciences  503: 402– 423. Google Scholar CrossRef Search ADS   Goff LJ, Coleman AW. 1995. Fate of parasite and host organelle DNA during cellular transformation of red algae by their parasites. Plant Cell  7: 1899– 1911. Google Scholar CrossRef Search ADS PubMed  Goff LJ, Zuccarello GC. 1994. The evolution of parasitism in red algae: cellular interactions of adelphoparasites and their hosts. Journal of Phycology  30: 695– 704. Google Scholar CrossRef Search ADS   Grady RM, Starr DA, Ackerman GL, Sanes JR, Han M. 2005. Syne proteins anchor muscle nuclei at the neuromuscular junction. Proceedings of the National Academy of Sciences of the USA  102: 4359– 4364. Google Scholar CrossRef Search ADS PubMed  Gräf R, Batsios P, Meyer I. 2015. Evolution of centrosomes and the nuclear lamina: amoebozoan assets. European Journal of Cell Biology  94: 249– 256. Google Scholar CrossRef Search ADS PubMed  Grau-Bové X, Sebé-Pedrós A1, Ruiz-Trillo I. 2015. The eukaryotic ancestor had a complex ubiquitin signaling system of archaeal origin. Molecular Biology and Evolution  32: 726– 739. Google Scholar CrossRef Search ADS PubMed  Guy L, Ettema TJ. 2011. The archaeal ‘TACK’ superphylum and the origin of eukaryotes. Trends in Microbiology  19: 580– 587. Google Scholar CrossRef Search ADS PubMed  Guy L, Saw JH, Ettema TJ. 2014. The archaeal legacy of eukaryotes: a phylogenomic perspective. Cold Spring Harbor Perspectives in Biology  6: a016022. Google Scholar CrossRef Search ADS PubMed  Hartman H, Fedorov A. 2002. The origin of the eukaryotic cell: a genomic investigation. Proceedings of the National Academy of Sciences of the USA  90: 1420– 1425. Google Scholar CrossRef Search ADS   Hartmann M. 1911. Die Konstitution der Protistenlehre und ihre Bedeutung für die Zellenlehre . Jena: Gustav Fischer. Heslop-Harrison J. 1966. Cytoplasm connections between angiosperm meiocytes. Annals of Botany  30: 221– 230. Google Scholar CrossRef Search ADS   Janssen A, Medema RH. 2011. Entosis: aneuploidy by invasion. Nature Cell Biology  13: 199– 201. Google Scholar CrossRef Search ADS PubMed  Jany JL, Pawlowska TE. 2010. Multinucleate spores contribute to evolutionary longevity of asexual Glomeromycota. American Naturalist  175: 424– 435. Google Scholar CrossRef Search ADS PubMed  Klei TR, Meinderts SM, van den Berg TK, van Bruggen R. 2017. From the cradle to the grave: the role of macrophages in erythropoiesis and erythrophagocytosis. Frontiers in Immunology  8: 73. Google Scholar CrossRef Search ADS PubMed  Klepzig KD, Adams AS, Handelsman J, Raffa KF. 2009. Symbioses: a key driver of insect physiological processes, ecological interactions, evolutionary diversification, and impacts on humans. Environmental Entomology  38: 67– 77. Google Scholar CrossRef Search ADS PubMed  Koblenz B, Schoppmeier J, Grunow A, Lechtreck KF. 2003. Centrin deficiency in Chlamydomonas causes defects in basal body replication, segregation and maturation. Journal of Cell Science  116: 2635– 2646. Google Scholar CrossRef Search ADS PubMed  Koonin EV. 2015. Origin of eukaryotes from within archaea, archaeal eukaryome and bursts of gene gain: eukaryogenesis just made easier? Philosophical Transactions of the Royal Society of London B Biological Sciences  370: 20140333. Google Scholar CrossRef Search ADS PubMed  Koonin EV, Yutin N. 2014. The dispersed archaeal eukaryome and the complex archaeal ancestor of eukaryotes. Cold Spring Harbor Perspectives in Biology  6: a016188. Google Scholar CrossRef Search ADS PubMed  König H, Li L, Wenzel M, Fröhlich J. 2006. Bacterial ectosymbionts which confer motility: Mixotricha paradoxa from the intestine of the Australian termite Mastotermes darwiniensis. Progress in Molecular and Subcellular Biology  41: 77– 96. Google Scholar CrossRef Search ADS PubMed  Kravets EA, Yemets AI, Blume YB. 2017. Cytoskeleton and nucleoskeleton involvement in processes of cytomixis in plants. Cell Biology International , in press. Google Scholar CrossRef Search ADS   Kuhn G, Hijri M, Sanders IR. 2001. Evidence for the evolution of multiple genomes in arbuscular mycorrhizal fungi. Nature  414: 745– 748. Google Scholar CrossRef Search ADS PubMed  Lang C, Grava S, van den Hoorn T, Trimble R, Philippsen P, Jaspersen SL. 2010. Mobility, microtubule nucleation and structure of microtubule-organizing centers in multinucleated hyphae of Ashbya gossypii. Molecular Biology of the Cell  21: 18– 28. Google Scholar CrossRef Search ADS PubMed  Lee JY, Yoo BC, Lucas WJ. 2000. Parallels between nuclear-pore and plasmodesmal trafficking of information molecules. Planta  210: 177– 187. Google Scholar CrossRef Search ADS PubMed  Lingle WL, Lukasiewicz K, Salisbury JL. 2005. Deregulation of the centrosome cycle and the origin of chromosomal instability in cancer. Advances in Experimental Medicine and Biology  570: 393– 421. Google Scholar CrossRef Search ADS PubMed  Liu H, Guo G-Q, He Y-K, Lu Y-P, Zheng G-C. 2007. Visualization on intercellular movement of chromatin in intact living anthers of transgenic tobacco expressing histone 2B-CFP fusion protein. Caryologia  60: 1– 20. Google Scholar CrossRef Search ADS   Lone A, Lone S. 2013. Cytomixis – a well known but less understood phenomenon in plants. International Journal of Recent Scientific Research  4: 347– 352. Lyons S, 2018. From cell to organism, the history of the cell theory . Toronto: University of Toronto Press. Margulis L. 1996. Archaeal-eubacterial mergers in the origin of Eukarya: phylogenetic classification of life. Proceedings of the National Academy of Sciences of the USA  93: 1071– 1076. Google Scholar CrossRef Search ADS PubMed  Margulis L, Dolan MF, Guerrero R. 2000. The chimeric eukaryote: origin of the nucleus from the karyomastigont in amitochondriate protists. Proceedings of the National Academy of Sciences of the USA  97: 6954– 6959. Google Scholar CrossRef Search ADS PubMed  Margulis L, Dolan MF, Whiteside JH. 2005. Imperfections and oddities in the origin of the nucleus. Paleobiology  31: 175– 191. Google Scholar CrossRef Search ADS   Margulis L, Chapman M, Guerrero R, Hall J. 2006. The last eukaryotic common ancestor (LECA): acquisition of cytoskeletal motility from aerotolerant spirochetes in the Proterozoic Eon. Proceedings of the National Academy of Sciences of the USA  103: 13080– 13085. Google Scholar CrossRef Search ADS PubMed  Margulis L, Chapman M, Dolan MF. 2007. Semes for analysis of evolution: de Duve’s peroxisomes and Meyer’s hydrogenases in the sulphurous Proterozoic eon. Nature Reviews Genetics  8. Marleau J, Dalpe Y, St-Arnaud M, Hijri M. 2011. Spore development and nuclear inheritance in arbuscular mycorrhizal fungi. BMC Evolutionary Biology  11: 51. Google Scholar CrossRef Search ADS PubMed  Mazia D. 1987. The chromosome cycle and the centrosome cycle in the mitotic cycle. International Review of Cytology  100: 49– 92. Google Scholar CrossRef Search ADS PubMed  Mazia D. 1993. The cell cycle at the cellular level. European Journal of Cell Biology  61 ( Suppl. 38): 14. McClure-Begley TD, Klymkowsky MW. 2017. Nuclear roles for cilia-associated proteins. Cilia  6: 8. Google Scholar CrossRef Search ADS PubMed  Menzel D. 1994. Cell differentiation and the cytoskeleton in Acetabularia. New Phytologist  128: 369– 393. Google Scholar CrossRef Search ADS   Menzel D, Elsner-Menzel C. 1990. The microtubule cytoskeleton in developing cysts of the green alga Acetabularia: involvement in cell wall differentiation. Protoplasma  157: 52– 63. Google Scholar CrossRef Search ADS   Mine I, Menzel D, Okuda K. 2008. Morphogenesis in giant-celled algae. International Review of Cell and Molecular Biology  266: 37– 83. Google Scholar CrossRef Search ADS PubMed  Minge MA, Silberman JD, Orr RJet al.   2009. Evolutionary position of breviate amoebae and the primary eukaryote divergence. Proceedings of the Royal Society of London B Biological Sciences  276: 597– 604. Google Scholar CrossRef Search ADS   Mursalimov SR, Sidorchuk YV, Deineko EV. 2013. New insights into cytomixis: specific cellular features and prevalence in higher plants. Planta  238: 415– 423. Google Scholar CrossRef Search ADS PubMed  Nicholson DJ. 2010. Biological atomism and cell theory. Studies in History and Philosophy of Biological and Biomedical Sciences  41: 202– 211. Google Scholar CrossRef Search ADS PubMed  O’Malley MA, Müller-Wille S. 2010. The cell as nexus: connections between the history, philosophy and science of cell biology. Studies in History and Philosophy of Biological and Biomedical Sciences  41: 169– 171. Google Scholar CrossRef Search ADS PubMed  Overholtzer M, Mailleux AA, Mouneimne Get al.   2007. A nonapoptotic cell death process, entosis, that occurs by cell-in-cell invasion. Cell  131: 966– 979. Google Scholar CrossRef Search ADS PubMed  Paweletz N. 2001. Walther Flemming: pioneer of mitosis research. Nature Reviews Molecular Cell Biology  2: 72– 75. Google Scholar CrossRef Search ADS PubMed  Potter C, Zhu W, Razafsky Det al.   2017. Multiple isoforms of nesprin1 are integral components of ciliary rootlets. Current Biology  27: 2014– 2022. Google Scholar CrossRef Search ADS PubMed  Radek R, Nitsch G. 2007. Ectobiotic spirochetes of flagellates from the termite Mastotermes darwiniensis: attachment and cyst formation. European Journal of Protistology  43: 281– 294. Google Scholar CrossRef Search ADS PubMed  Resendes KK, Rasala BA, Forbes DJ. 2008. Centrin 2 localizes to the vertebrate nuclear pore and plays a role in mRNA and protein export. Molecular and Cellular Biology  28: 1755– 1769. Roper M, Ellison C, Taylor JW, Glass NL. 2011. Nuclear and genome dynamics in multinucleate ascomycete fungi. Current Biology  21: R786– R793. Google Scholar CrossRef Search ADS PubMed  Rout MP, Field MC. 2017. The evolution of organellar coat complexes and organization of the eukaryotic cell. Annual Reviews of Biochemistry  86: 637– 657. Google Scholar CrossRef Search ADS   Ruiz F, Garreau de Loubresse N, Klotz C, Beisson J, Koll F. 2005. Centrin deficiency in Paramecium affects the geometry of basal-body duplication. Current Biology  15: 2097– 2106. Google Scholar CrossRef Search ADS PubMed  Sachs J. 1892a. Beiträge zur Zellentheorie. Energiden und Zellen. Flora  75: 57– 67. Sachs J. 1892b. Weitere Betrachtungen über Energiden und Zellen. Flora  81: 405– 434. Salisbury JL. 1988. The lost neuromotor apparatus of Chlamydomonas rediscovered. Journal of Protozoology  35: 574– 577. Google Scholar CrossRef Search ADS PubMed  Salisbury JL. 1995. Centrin, centrosomes, and mitotic spindle poles. Current Opinion in Cell Biology  7: 39– 45. Google Scholar CrossRef Search ADS PubMed  Salisbury JL. 2007. A mechanistic view on the evolutionary origin for centrin-based control of centriole duplication. Journal of Cell Physiology  213: 420– 428. Google Scholar CrossRef Search ADS   Salisbury JL, Baron AT, Sanders MA. 1988. The centrin-based cytoskeleton of Chlamydomonas reinhardtii: distribution in interphase and mitotic cells. Journal of Cell Biology  107: 635– 641. Google Scholar CrossRef Search ADS PubMed  Salomaki ED, Lane CE. 2014. Are all red algal parasites cut from the same cloth? Acta Societatis Botanicorum Poloniae  83: 369– 375. Google Scholar CrossRef Search ADS   Sapp J. 2010. Saltational symbiosis. Theory in Biosciences  129: 125– 133. Google Scholar CrossRef Search ADS PubMed  Sharma N, Dey P. 2011. Cell cannibalism and cancer. Diagnostic Cytopathology  39: 229– 233. Google Scholar PubMed  Spang A, Caceres EF, Ettema TJG. 2017. Genomic exploration of the diversity, ecology, and evolution of the archaeal domain of life. Science  357: eaaf3883. Google Scholar CrossRef Search ADS PubMed  Stinchcombe JC, Griffiths GM. 2014. Communication, the centrosome and the immunological synapse. Philosophical Transactions of the Royal Society of London B Biological Sciences  369: 20130463. Google Scholar CrossRef Search ADS PubMed  Stinchcombe JC, Randzavola LO, Angus KL, Mantell JM, Verkade P, Griffiths GM. 2015. Mother centriole distal appendages mediate centrosome docking at the immunological synapse and reveal mechanistic parallels with ciliogenesis. Current Biology  25: 3239– 3244. Google Scholar CrossRef Search ADS PubMed  Strasburger E. 1913. Pflanzliche Zellen- und Gewebelehre. In: Von Wettstein R, ed. Zellen- und Gewebelehre, Morphologie und Entwicklunggeschichte . Leipzig: Teubner, 1– 174. Vicente JJ, Wordeman L. 2015. Mitosis, microtubule dynamics and the evolution of kinesins. Experimental Cell Research  334: 61– 69. Google Scholar CrossRef Search ADS PubMed  Walker G, Dacks JB, Embley TM. 2006. Ultra-structural description of Breviata anathema, the organism previously studied as Mastigamoeba invertens. Journal of Eukaryotic Microbiology  53: 65– 78. Google Scholar CrossRef Search ADS PubMed  Wang X, Gerdes HH. 2012. Long-distance electrical coupling via tunneling nanotubes. Biochimica et Biophysica Acta  1818: 2082– 2086. Google Scholar CrossRef Search ADS PubMed  Wang X, Veruki ML, Bukoreshtliev NV, Hartveit E, Gerdes HH. 2010. Animal cells connected by nanotubes can be electrically coupled through interposed gap-junction channels. Proceedings of the National Academy of Sciences of the USA  107: 17194– 17199. Google Scholar CrossRef Search ADS PubMed  Woese CR. 1998. The universal ancestor. Proceedings of the National Academy of Sciences of the USA  95: 6854– 6859. Google Scholar CrossRef Search ADS PubMed  Woese CR. 2002. On the evolution of cells. Proceedings of the National Academy of Sciences of the USA  99: 8742– 8747. Google Scholar CrossRef Search ADS PubMed  Wright RL, Adler SA, Spanier JG, Jarvik JW. 1989. Nucleus-basal body connector in Chlamydomonas: evidence for a role in basal body segregation and against essential roles in mitosis or in determining cell polarity. Cell Motility and Cytoskeleton  14: 516– 526. Google Scholar CrossRef Search ADS   Yoshida H, Kawane K, Koike M, Mori Y, Uchiyama Y, Nagata S. 2005. Phosphatidylserine-dependent engulfment by macrophages of nuclei from erythroid precursor cells. Nature  437: 754– 758. Google Scholar CrossRef Search ADS PubMed  Young JP. 2015. Genome diversity in arbuscular mycorrhizal fungi. Current Opinion in Plant Biology  26: 113– 119. Google Scholar CrossRef Search ADS PubMed  Zani BG, Edelman ER. 2010. Cellular bridges: routes for intercellular communication and cell migration. Communicative & Integrative Biology  3: 215– 220. Google Scholar CrossRef Search ADS PubMed  Zaremba-Niedzwiedzka K, Caceres EF, Saw JHet al.   2017. Asgard archaea illuminate the origin of eukaryotic cellular complexity. Nature  541: 353– 358. Google Scholar CrossRef Search ADS PubMed  Zhu R, Antoku S, Gundersen GG. 2017. Centrifugal displacement of nuclei reveals multiple LINC complex mechanisms for homeostatic nuclear positioning. Current Biology , in press. © The Author(s) 2018. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For permissions, please e-mail: [email protected]. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Annals of Botany Oxford University Press

Energide–cell body as smallest unit of eukaryotic life

Baluška, František; Lyons, Sherrie
Annals of Botany , Volume Advance Article – Feb 21, 2018
Download PDF
5 pages

Loading next page...
 
/lp/ou_press/energide-cell-body-as-smallest-unit-of-eukaryotic-life-vTjKT9ycMb

References (110)

Publisher
Oxford University Press
Copyright
© The Author(s) 2018. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For permissions, please e-mail: [email protected].
ISSN
0305-7364
eISSN
1095-8290
DOI
10.1093/aob/mcy022
Publisher site
See Article on Publisher Site

Abstract

Abstract Background The evolutionary origin of the eukaryotic nucleus is obscure and controversial. Currently preferred are autogenic concepts; ideas of a symbiotic origin are mostly discarded and forgotten. Here we briefly discuss these issues and propose a new version of the symbiotic and archaeal origin of the eukaryotic nucleus. Scope and Conclusions The nucleus of eukaryotic cells forms via its perinuclear microtubules, the primary eukaryotic unit known also as the Energide–cell body. As for all other endosymbiotic organelles, new Energides are generated only from other Energides. While the Energide cannot be generated de novo, it can use its secretory apparatus to generate de novo the cell periphery apparatus. We suggest that Virchow’s tenet Omnis cellula e cellula should be updated as Omnis Energide e Energide to reflect the status of the Energide as the primary unit of the eukaryotic cell, and life. In addition, the plasma membrane provides feedback to the Energide and renders it protection via the plasma membrane-derived endosomal network. New discoveries suggest archaeal origins of both the Energide and its host cell. Cell body, cell theory, coenocytes, cytoskeleton, endosymbiosis, Energide, eukaryotic cell, evolution, microtubules, nucleus, syncytia PETER BARLOW AND PROBLEMS WITH THE CELL THEORY As documented by papers in this Annals of Botany special issue, the interests of Peter Barlow were wide-ranging and profound. These interests touched significantly also on the fundamental problems associated with the current version of the cell theory (Baluška et al., 1997, 1998, 2004a, b). Multinuclear cells, the supracellular nature of plants and fungi, and the many examples of cells within cells are all exceptions to cell theory. The supracellular nature of higher plants is complemented with the inherent property of animal cells of generating cytoplasmic channels known as tunnelling nanotubes (Wang et al., 2010; Zani and Edelman, 2010; Abounit and Zurzolo, 2012; Wang and Gerdes, 2012; Austefjord et al., 2014). In higher plants, migration of nuclei from cell to cell is known as cytomixis (Heslop-Harrison, 1966; Liu et al., 2007; Lone and Lone, 2013; Mursalimov et al., 2013; Kravets et al., 2017). The individuality of eukaryotic nuclei is apparent from red algal parasites, which transfer whole nuclei in their host cells, and these then redirect the host cell biology and physiology for the parasite’s benefit (Goff and Coleman, 1984, 1985, 1987, 1995; Goff and Zuccarello, 1994; Salomaki and Lane 2014). There are numerous examples of unicellular but multi-Energide coenocytic organisms, including marine algae such as Caulerpa, Cladophora and Acetabularia (Strasburger, 1913; Menzel and Elsner-Menzel, 1990; Menzel, 1994; Mine et al., 2008; Baluška et al., 2012). Probably the most flagrant violation of the current problematic version of the cell theory is provided by Ascomycota (Gladfelter, 2006; Lang et al., 2010; Roper et al., 2011) and Glomeromycota (Kuhn et al., 2001; Bewer and Wang, 2005; Jany and Pawlowska, 2010; Marleau et al., 2011; Boon et al., 2015; Young, 2015). Their fungal mycelia harbour genetically different nuclei in the same cytoplasm. In other words, these coenocytic ‘cells’ provide shelter for genomically diverse organismal units. For example, one single multinucleate spore of Glomus irregulare contains up to 1000 nuclei. In addition, large heterogeneity exists in the number of nuclei (Energides) among sister spores (Marleau et al., 2011). Moreover, non-self vegetative fusions are typical of hyphae of the arbuscular mycorrhizal fungus Glomus intraradices (Croll et al., 2009). EVOLUTION OF THE ENERGIDE–CELL BODY CONCEPT: SACHS, MAZIA AND OTHERS Discoveries of centrosomes and centrioles organizing both flagella and mitotic spindles of eukaryotic cells (Boveri, 1895; Flemming, 1891; Baltzer, 1967; Paweletz, 2001) strongly suggest that nuclei of eukaryotic cells are closely associated, via perinuclear microtubules (Baluška et al., 1997, 1998, 2004a, b), with both centrosomes and centrioles. Daniel Mazia was the first to realize that there is not only structural but also functional unity between all these organelles and he proposed the ‘cell body’ concept at the end of his scientific career (Mazia, 1987, 1993). Daniel Mazia’s cell body concept was preceded by Julius Sachs, who proposed his Energide concept in 1893 (Sachs, 1892a, b; Baluška et al., 2006). But Sachs was not aware of microtubules, centrioles and centrosomes. Under the influence of Theodor Boveri, it was Max Hartmann (1911) followed by Karl Bělař (1926) who further evolved the Energide concept in this respect (discussed in Chen, 2003). It is not known whether Daniel Mazia was aware of the Energide concept (Energidenlehre in German; see Chen, 2003) when he proposed the cell body concept in 1993 (Mazia, 1993). However, he had come to think the centrosome was potentially far more than just the organizer and initiator of microtubule synthesis. They were ‘bearers of information about cell morphology’ and that ‘something exists at a level of complexity higher than that of molecules akin to the level of the complexity of chromosomes’, and that something was what he called the ‘cell body’ (Mazia, 1987; Lyons, 2018). In 1997, 1998 and 2004, together with Peter Barlow, we updated Mazia’s hypothesis and proposed that the nucleus with perinuclear microtubules represents the smallest and basic unit of eukaryotic life (Baluška et al., 1997, 1998, 2004a, b). This hypothesis solves the problem of syncytia and coenocytes, which are incompatible with the classical cell theory stating that the whole cell is the basic unit of eukaryotic life (Baluška et al., 1997, 1998, 2004a, b, 2006). In 2009, we extended the Energide–cell body concept to central nervous systems (Agnati et al., 2009). Later, we discussed the Energide–cell body hypothesis from the perspective of the Neo-Energide concept (Baluška et al., 2006; see also Nicholson, 2010), originally proposed by Julius Sachs (Sachs, 1892a, b). Recently, the evolutionary origins of the Energide–cell body complex, as well as its eukaryotic cell, were discussed from evolutionary perspectives (Baluška and Lyons, 2018). Here, we briefly summarize the Energide–cell body concept and highlight the latest evidence of its validity. The Energide–cell body theory provides a robust explanation as to why there is eukaryotic sex and why male gametes are typically small, flagellated and motile, whereas female gametes are large, not motile and based on the actin cytoskeleton. The flagella of sperm cells are made of microtubules and typically lack any actin cytoskeleton while the larger egg cells are based primarily on the actin cytoskeleton (Baluška et al., 2004a, 2006). Importantly, nuclear pores are prototypes of cell–cell channels, resembling plasmodesmata in plants and tunnelling nanotubes in animals. The Energide–cell body concept is useful in explaining such perplexing discoveries as entosis and cannibalism in animal cells (Fais, 2007; Overholtzer et al., 2007; Janssen and Medema, 2011; Sharma and Dey, 2011). Moreover, developing erythroblasts extrude their nuclei, which are then engulfed by macrophages (Yoshida et al., 2005; Klei et al., 2017). Further examples of the independent nature of nuclei from cells include cell–cell transport of nuclei in plants (Lone and Lone, 2013; Mursalimov et al., 2013; Kravets et al., 2017) and infectious transfer of nuclei in parasitic red algae (Goff and Coleman, 1984, 1987). In contradiction to the current version of the cell theory is the unique multigenomic nature of coenocytic (multi-Energidic) Glomeromycota fungi, whose spores contain up to 1000 nuclei (Energides–cell bodies) within one huge single coenocytic cell (Marleau et al., 2011; Boon et al., 2015; Young, 2015). ARCHAEAL ORIGINS OF SYMBIOTIC ENERGIDES–CELL BODIES AND THEIR HOST CELLS (CHRONOCYTES) In the contemporary literature, diverse versions of autogenous theories for the origin of the eukaryotic cell predominate. However, it is very important to consider that, although initially treated with scepticism, the symbiotic origin of mitochondria and plastids turned out to be true. Viewing the nucleus as the primary eukaryotic endosymbiotic organelle would solve problems with the sudden appearance on the evolutionary scene of the complex eukaryotic cell, with its nucleus inherently associated with an endoplasmic reticulum and microtubular cytoskeleton. The various autogenous theories also are not able to explain why the last eukaryotic ancestors (LECAs; Woese, 1998, 2002) were complex organisms having almost all the eukaryotic features, including centrosomes, nuclei with lamina and nuclear pores, as well as the flagellar apparatus based on microtubules (Gräf et al., 2015; Grau-Bové et al., 2015; Vicente and Wordeman, 2015). All this provides evidence for the parasitic–symbiotic concept of a small motile cell, using its microtubular flagella, invading a large non-motile host cell based on the actin cytoskeleton (Baluška et al., 2004a). Recent advances in our understanding of these elusive issues reveal archaeal origins of this eukaryotic complexity (Guy and Ettema, 2011; Guy et al., 2014; Koonin and Yutin, 2014; Koonin, 2015; Eme et al., 2017; Zaremba-Niedzwiedzka et al., 2017). All these data point to the archaeal nature of both the host and guest cells that generated the LECA (Eme et al., 2017; Baluška and Lyons, 2018). Archaeal host cells [termed ‘chronocytes’ by Hartman and Fedorov (2002)] were proposed to acquire microtubule-based guest cells endosymbiotically (Baluška and Lyons, 2018), and these cells transformed into eukaryotic nuclei associated with the microtubule-based cytoskeleton. Thus, both the discovery of critical eukaryotic signature proteins (ESPs; Hartman and Fedorov, 2002) in Archaea of the ‘TACK’ superphylum (Guy and Ettema, 2011; Eme et al., 2017; Spang et al., 2017; Zaremba-Niedzwiedzka et al., 2017) and new discoveries in cell biology (summarized by Baluška and Lyons, 2018) suggest archaeal origins of both the Energides–cell bodies and their host cells. THE ENERGIDE–CELL BODY COMPLEX AS THE SMALLEST UNIT OF EUKARYOTIC LIFE Autogenous evolution is a kind of self-generated evolution (O’Malley and Müller-Wille, 2010); whereas the parasitic–symbiotic scenarios for the evolutionary origin of complex eukaryotic cells are examples of evolution by associations imposed on cells from outside (Baluška et al., 2004a, b, 2006; Klepzig et al., 2009; Sapp, 2010; Gilbert et al., 2012; Baluška and Lyons, 2018). The symbiotic origin of the nucleus as an Energide–cell body complex, as proposed in the latest version of the Neo-Energide theory (Baluška and Lyons, 2018), is supported by several unique features of eukaryotic cells that are not compatible with the diverse autogenous theories. First of all, the eukaryotic cilia and flagellar apparatus share their basal bodies with the perinuclear centrioles and centrosomes (Baluška and Lyons, 2018). Importantly, SYNE proteins, which anchor nuclei to neuromuscular synaptic junctions (Grady et al., 2005) and centre nuclear positions within eukaryotic cells (Zhu et al., 2017), are also integral proteins of ciliary rootlets (Potter et al., 2017). Relevant in this respect are algae such as Chlamydomonas and the protozoan Giardia, which have flagellar basal bodies connected to the nuclear surfaces via centrin-based contractile fibres (Salisbury, 1988; Wright et al., 1989; Koblenz et al., 2003; Dawson and House, 2010). The flagellar apparatus is an ancient eukaryotic organelle that is based on basal bodies acting as the primary microtubule-organizing centres (MTOCs) of the eukaryotic cell (Azimzadeh, 2014; Gräf et al., 2015). Nuclear pores resemble and act like classical cell–cell channels (Lee et al., 2000; Baluška et al., 2006; Bloemendal and Kück, 2013). There are also similarities between nuclear pores and flagellar entry domains (McClure-Begley and Klymkowsky, 2017; Rout and Field, 2017). Intriguingly in this respect, flagellar centrins (Salisbury, 1988; Salisbury et al., 1988) are components of plant-specific cell–cell channels (plasmodesmata; Blackman et al., 1999) and nuclear pores (Resendes et al., 2008); and also connect centrioles/centrosomes to the nuclei (Gräf et al., 2015). The symbiotic origin not only of nuclei (Baluška and Lyons, 2018) but also of cilia and flagella is strongly supported by numerous similarities between cilia/flagella and immunological synapses (Stinchcombe and Griffiths, 2014; Stinchcombe et al., 2015). There are strong parallels between ciliogenesis and the formation of immunological and cytotoxic synapses (Stinchcombe et al., 2015; Dieckmann et al., 2016). In the recently proposed updated version of the Energide–cell body theory, the endoplasmic reticulum membranes represent an outgrowth of the outer part of the nuclear envelope (Baluška and Lyons, 2018) and membranes of the Golgi apparatus represent specialized extensions of the endoplasmic reticulum (Chapman and Alliegro, 2012; Baluška and Lyons, 2018). Finally, the Energide–cell body complex is proposed to represent the primary and smallest unit of eukaryotes that can generate a complete cell, whereas de-nucleated eukaryotic cells can never generate a new Energide–cell body de novo (Baluška et al., 2006; Baluška and Lyons, 2018). This primacy of the Energide–cell body unit over the rest of the eukaryotic cell can also be seen during cell division, which invariably starts with the division of the centriole/centrosome, is followed by nuclear division and completed by cytoplasmic/cell periphery division, known as cytokinesis. The latter is instructed by the newly emerged daughter Energides–cell bodies of early cytokinetic cells. In conclusion, Rudolf Virchow’s famous tenet Omnis cellula e cellula should be updated to Omnis Energide e Energide (Baluška and Lyons, 2018). DANIEL MAZIA VERSUS LYNN MARGULIS: ENERGIDE–CELL BODY VERSUS KARYOMASTIGONT In their karyomastigont hypothesis, Lynn Margulis and her co-authors proposed the origin of the nucleus via the karyomastigont, which consisted of a nucleus and flagellar apparatus (Margulis, 1996; Margulis et al., 2000, 2005, 2006, 2007). The problematic part of the karyomastigont concept is the spirochaete origin of the tubulin-based flagellum, which should be descended from putatively Mixotricha-like ectosymbionts (Margulis, 1996; Margulis et al., 2000, 2006; König et al., 2006; Radek and Nitsch, 2007). In our recent Energide–cell body concept (Baluška and Lyons, 2018), the microtubule-based putative flagellated Archaea are proposed to invade the actin-based host cell Archaea and be transformed into the Energide–cell body. This Archaea–Archaea concept of eukaryotic origin explains why the eukaryotic nucleus is inherently associated with microtubule-based flagella via centrin-based and contractile rootlet/rhizoplast structures in evolutionarily ancient protists, including Naegleria, Giardia and Breviata (Walker et al., 2006; Minge et al., 2009; Dawson and House 2010; Fritz-Laylin and Fulton, 2016) and in flagellated algae, including Chlamydomonas reinhardtii (Salisbury, 1988; Salisbury et al., 1988; Dutcher, 2003). Later in eukaryotic evolution, the nucleus was liberated from the flagellar apparatus (sensu the akaryomastigont of Margulis and colleagues) but remained functionally coupled to cilia via basal bodies, centrioles and centrosomes (Dolan et al., 2000a, b ). Moreover, higher plant cells accomplished further liberation when their Energides–cell bodies lost corpuscular centrioles/centrosomes during land plant evolution (Mazia, 1987, 1993; Baluška et al., 1997, 1998, 2004a, b). The Energide–cell body concept provides answers as to why centrioles and basal bodies share not only the same centrin-based architecture (Dutcher, 2003; Koblenz et al., 2003; Ruiz et al., 2005), but also why their duplication is typically linked to the nucleus, accomplished only once per cell cycle (Salisbury, 1995, 2007), and why there are similarities between cilia/flagella and immunological synapses (Stinchcombe and Griffiths, 2014; Stinchcombe et al., 2015). OUTLOOK The main reason the Energide–cell body concept has essentially been ignored is because researchers have been reluctant to accept the endosymbiotic origin of the nucleus (Baluška and Lyons, 2018). A better understanding of the true nature of the eukaryotic cell is not only important for understanding the development of multicellular organisms but is also essential for our ability to cure cancer (Boveri, 1929; Mazia, 1987; Lingle et al., 2005; Cosenza and Krämer, 2016). Our understanding of the true nature of the eukaryotic cell as a symbiotic consortium organized via Energide–cell body activities is essential for our ability to comprehend life based on eukaryotic cells and their nucleus-based Energides–cell bodies. The archaeal nature of both the Energide–cell body and its host cell supports the two-domain Tree of Life (Eme et al., 2017; Spang et al., 2017). This is a real archaeal revolution in our understanding of the evolutionary origins of eukaryotic cells and their nuclei. LITERATURE CITED Abounit S, Zurzolo C. 2012. Wiring through tunneling nanotubes – from electrical signals to organelle transfer. Journal of Cell Science  125: 1089– 1098. Google Scholar CrossRef Search ADS PubMed  Agnati LF, Fuxe K, Baluška F, Guidolin D. 2009. Implications of the ‘Energide’ concept for communication and information handling in the central nervous system. Journal of Neural Transmission  11: 1037– 1052. Google Scholar CrossRef Search ADS   Austefjord MW, Gerdes HH, Wang X. 2014. Tunneling nanotubes: diversity in morphology and structure. Communicative & Integrative Biology  7: e27934. Google Scholar CrossRef Search ADS PubMed  Azimzadeh J. 2014. Exploring the evolutionary history of centrosomes. Philosophical Transactions of the Royal Society of London B Biological Sciences  369: 1650. Google Scholar CrossRef Search ADS   Baltzer F. 1967. Theodor Boveri – life and work of a great biologist 1862–1915 . Berkeley: University of California Press. Baluška F, Lyons S. 2018. Symbiotic origin of eukaryotic nucleus – from cell body to Neo-Energide. In: Sahi V, Baluška F, eds. Concepts in cell biology – history and evolution . Springer International Publishing. Baluška F, Volkmann D, Barlow PW. 1997. Nuclear components with microtubule organizing properties in multicellular eukaryotes: functional and evolutionary considerations. International Review of Cytology  175: 91– 135. Google Scholar CrossRef Search ADS PubMed  Baluška F, Lichtscheidl IK, Volkmann D, Barlow PW. 1998. The plant cell body: a cytoskeletal tool for cellular development and morphogenesis. Protoplasma  202: 1– 10. Google Scholar CrossRef Search ADS   Baluška F, Volkmann D, Barlow PW. 2004a. Eukaryotic cells and their cell bodies: cell theory revisited. Annals of Botany  94: 9– 32. Google Scholar CrossRef Search ADS   Baluška F, Volkmann D, Barlow PW. 2004b. Cell bodies in a cage. Nature  428: 371. Google Scholar CrossRef Search ADS   Baluška F, Volkmann D, Barlow PW. 2006. Cell-cell channels and their implications for cell theory. In: Baluška F, Volkmann D, Barlow PW, eds. Cell-cell channels . Landes Bioscience, 1– 18. Google Scholar CrossRef Search ADS   Baluška F, Volkmann D, Menzel D, Barlow PW. 2012. Strasburger’s legacy to mitosis and cytokinesis and its relevance for the cell theory. Protoplasma  249: 1151– 1162. Google Scholar CrossRef Search ADS PubMed  Bělař K. 1926. Der Formwechsel der Protistenkerne. Ergebnisse und Fortschritte der Zoologie . Jena: Fischer. Bewer JD, Wang M. 2005. Arbuscular mycorrhizal fungi – hyphal fusion and multigenomic structure. Nature  433: E3– E4. Google Scholar CrossRef Search ADS PubMed  Blackman LM, Harper JD, Overall RL. 1999. Localization of a centrin-like protein to higher plant plasmodesmata. European Journal of Cell Biology  78: 297– 304. Google Scholar CrossRef Search ADS PubMed  Bloemendal S, Kück U. 2013. Cell-to-cell communication in plants, animals, and fungi: a comparative review. Naturwissenschaften  100: 3– 19. Google Scholar CrossRef Search ADS PubMed  Boon E, Halary S, Bapteste E, Hijri M. 2015. Studying genome heterogeneity within the arbuscular mycorrhizal fungal cytoplasm. Genome Biology and Evolution  7: 505– 521. Google Scholar CrossRef Search ADS PubMed  Boveri T. 1895. Über das Verhalten der Centrosomen bei der Befruchtung des Seeigeleies nebst allgemeinen Bemerkungen über Centrosomen und Verwandtes. Verhandlungen der Physikalische-Medizinische Gesellschaft Würzburg  29: 1– 75. Boveri T. 1929. The origin of malignant tumors . Baltimore, MD: Williams and Wilkins. Chapman M, Alliegro MC. 2012. The karyomastigont as an evolutionary seme. Quarterly Review of Biology  87: 315– 324. Google Scholar CrossRef Search ADS PubMed  Chen H-A. 2003. Die Sexualitätstheorie und “Theoretische Biologie” von Max Hartmann in der ersten Hälfte des zwanzigsten Jahrhunderts. Sudhoffs Archiv  46: 1– 308. Cosenza MR, Krämer A. 2016. Centrosome amplification, chromosomal instability and cancer: mechanistic, clinical and therapeutic issues. Chromosome Research  24: 105– 126. Google Scholar CrossRef Search ADS PubMed  Croll D, Giovannetti M, Koch AMet al.   2009. Nonself vegetative fusion and genetic exchange in the arbuscular mycorrhizal fungus Glomus intraradices. New Phytologist  181: 924– 937. Google Scholar CrossRef Search ADS PubMed  Dawson SC, House SA. 2010. Life with eight flagella: flagellar assembly and division in Giardia. Current Opinion in Microbiology  13: 480– 490. Google Scholar CrossRef Search ADS PubMed  Dieckmann NM, Frazer GL, Asano Y, Stinchcombe JC, Griffiths GM. 2016. The cytotoxic T lymphocyte immune synapse at a glance. Journal of Cell Science  129: 2881– 2886. Google Scholar CrossRef Search ADS PubMed  Dolan MF, D’Ambrosio U, Wier AM, Margulis L. 2000a. Surface kinetosomes and disconnected nuclei of a calonymphid: ultrastructure and evolutionary significance of Snyderella tabogae. Acta Protozoologica  39: 135– 141. Dolan MF, Wier AM, Margulis L. 2000b. Budding and asymmetric reproduction of a trichomonad with as many as 1000 nuclei in karyomastigonts: Metacoronympha from Incisitermes. Acta Protozoologica  39: 275– 280. Dutcher SK. 2003. Elucidation of basal body and centriole functions in Chlamydomonas reinhardtii. Traffic  4: 443– 451. Google Scholar CrossRef Search ADS PubMed  Eme L, Spang A, Lombard J, Stairs CW, Ettema TJG. 2017. Archaea and the origin of eukaryotes. Nature Reviews Microbiology  15: 711– 723. Google Scholar CrossRef Search ADS PubMed  Fais S. 2007. Cannibalism: a way to feed on metastatic tumors. Cancer Letters  258: 155– 164. Google Scholar CrossRef Search ADS PubMed  Flemming W. 1891. Attraktionsphären und Zentralkörperchen in Gewebs- und Wanderzellen. Anatomischer Anzeiger  6: 78– 86. Fritz-Laylin LK, Fulton C. 2016. Naegleria: a classic model for de novo basal body assembly. Cilia  5: 10. Google Scholar CrossRef Search ADS PubMed  Gilbert SF, Sapp J, Tauber AI. 2012. A symbiotic view of life: we have never been individuals. Quarterly Review of Biology  87: 325– 341. Google Scholar CrossRef Search ADS PubMed  Gladfelter AS. 2006. Nuclear anarchy: asynchronous mitosis in multinucleated fungal hyphae. Current Opinion in Microbiology  9: 547– 552. Google Scholar CrossRef Search ADS PubMed  Goff LJ, Coleman AW. 1984. Transfer of nuclei from a parasite to its host. Proceedings of the National Academy of Sciences of the USA  81: 5420– 5424. Google Scholar CrossRef Search ADS PubMed  Goff LJ, Coleman AW. 1985. The role of secondary pit connections in red algal parasitism. Journal of Phycology  21: 483– 508. Google Scholar CrossRef Search ADS   Goff LJ, Coleman AW. 1987. Nuclear transfer from parasite to host: a new regulatory mechanism of parasitism. Annals of the New York Academy of Sciences  503: 402– 423. Google Scholar CrossRef Search ADS   Goff LJ, Coleman AW. 1995. Fate of parasite and host organelle DNA during cellular transformation of red algae by their parasites. Plant Cell  7: 1899– 1911. Google Scholar CrossRef Search ADS PubMed  Goff LJ, Zuccarello GC. 1994. The evolution of parasitism in red algae: cellular interactions of adelphoparasites and their hosts. Journal of Phycology  30: 695– 704. Google Scholar CrossRef Search ADS   Grady RM, Starr DA, Ackerman GL, Sanes JR, Han M. 2005. Syne proteins anchor muscle nuclei at the neuromuscular junction. Proceedings of the National Academy of Sciences of the USA  102: 4359– 4364. Google Scholar CrossRef Search ADS PubMed  Gräf R, Batsios P, Meyer I. 2015. Evolution of centrosomes and the nuclear lamina: amoebozoan assets. European Journal of Cell Biology  94: 249– 256. Google Scholar CrossRef Search ADS PubMed  Grau-Bové X, Sebé-Pedrós A1, Ruiz-Trillo I. 2015. The eukaryotic ancestor had a complex ubiquitin signaling system of archaeal origin. Molecular Biology and Evolution  32: 726– 739. Google Scholar CrossRef Search ADS PubMed  Guy L, Ettema TJ. 2011. The archaeal ‘TACK’ superphylum and the origin of eukaryotes. Trends in Microbiology  19: 580– 587. Google Scholar CrossRef Search ADS PubMed  Guy L, Saw JH, Ettema TJ. 2014. The archaeal legacy of eukaryotes: a phylogenomic perspective. Cold Spring Harbor Perspectives in Biology  6: a016022. Google Scholar CrossRef Search ADS PubMed  Hartman H, Fedorov A. 2002. The origin of the eukaryotic cell: a genomic investigation. Proceedings of the National Academy of Sciences of the USA  90: 1420– 1425. Google Scholar CrossRef Search ADS   Hartmann M. 1911. Die Konstitution der Protistenlehre und ihre Bedeutung für die Zellenlehre . Jena: Gustav Fischer. Heslop-Harrison J. 1966. Cytoplasm connections between angiosperm meiocytes. Annals of Botany  30: 221– 230. Google Scholar CrossRef Search ADS   Janssen A, Medema RH. 2011. Entosis: aneuploidy by invasion. Nature Cell Biology  13: 199– 201. Google Scholar CrossRef Search ADS PubMed  Jany JL, Pawlowska TE. 2010. Multinucleate spores contribute to evolutionary longevity of asexual Glomeromycota. American Naturalist  175: 424– 435. Google Scholar CrossRef Search ADS PubMed  Klei TR, Meinderts SM, van den Berg TK, van Bruggen R. 2017. From the cradle to the grave: the role of macrophages in erythropoiesis and erythrophagocytosis. Frontiers in Immunology  8: 73. Google Scholar CrossRef Search ADS PubMed  Klepzig KD, Adams AS, Handelsman J, Raffa KF. 2009. Symbioses: a key driver of insect physiological processes, ecological interactions, evolutionary diversification, and impacts on humans. Environmental Entomology  38: 67– 77. Google Scholar CrossRef Search ADS PubMed  Koblenz B, Schoppmeier J, Grunow A, Lechtreck KF. 2003. Centrin deficiency in Chlamydomonas causes defects in basal body replication, segregation and maturation. Journal of Cell Science  116: 2635– 2646. Google Scholar CrossRef Search ADS PubMed  Koonin EV. 2015. Origin of eukaryotes from within archaea, archaeal eukaryome and bursts of gene gain: eukaryogenesis just made easier? Philosophical Transactions of the Royal Society of London B Biological Sciences  370: 20140333. Google Scholar CrossRef Search ADS PubMed  Koonin EV, Yutin N. 2014. The dispersed archaeal eukaryome and the complex archaeal ancestor of eukaryotes. Cold Spring Harbor Perspectives in Biology  6: a016188. Google Scholar CrossRef Search ADS PubMed  König H, Li L, Wenzel M, Fröhlich J. 2006. Bacterial ectosymbionts which confer motility: Mixotricha paradoxa from the intestine of the Australian termite Mastotermes darwiniensis. Progress in Molecular and Subcellular Biology  41: 77– 96. Google Scholar CrossRef Search ADS PubMed  Kravets EA, Yemets AI, Blume YB. 2017. Cytoskeleton and nucleoskeleton involvement in processes of cytomixis in plants. Cell Biology International , in press. Google Scholar CrossRef Search ADS   Kuhn G, Hijri M, Sanders IR. 2001. Evidence for the evolution of multiple genomes in arbuscular mycorrhizal fungi. Nature  414: 745– 748. Google Scholar CrossRef Search ADS PubMed  Lang C, Grava S, van den Hoorn T, Trimble R, Philippsen P, Jaspersen SL. 2010. Mobility, microtubule nucleation and structure of microtubule-organizing centers in multinucleated hyphae of Ashbya gossypii. Molecular Biology of the Cell  21: 18– 28. Google Scholar CrossRef Search ADS PubMed  Lee JY, Yoo BC, Lucas WJ. 2000. Parallels between nuclear-pore and plasmodesmal trafficking of information molecules. Planta  210: 177– 187. Google Scholar CrossRef Search ADS PubMed  Lingle WL, Lukasiewicz K, Salisbury JL. 2005. Deregulation of the centrosome cycle and the origin of chromosomal instability in cancer. Advances in Experimental Medicine and Biology  570: 393– 421. Google Scholar CrossRef Search ADS PubMed  Liu H, Guo G-Q, He Y-K, Lu Y-P, Zheng G-C. 2007. Visualization on intercellular movement of chromatin in intact living anthers of transgenic tobacco expressing histone 2B-CFP fusion protein. Caryologia  60: 1– 20. Google Scholar CrossRef Search ADS   Lone A, Lone S. 2013. Cytomixis – a well known but less understood phenomenon in plants. International Journal of Recent Scientific Research  4: 347– 352. Lyons S, 2018. From cell to organism, the history of the cell theory . Toronto: University of Toronto Press. Margulis L. 1996. Archaeal-eubacterial mergers in the origin of Eukarya: phylogenetic classification of life. Proceedings of the National Academy of Sciences of the USA  93: 1071– 1076. Google Scholar CrossRef Search ADS PubMed  Margulis L, Dolan MF, Guerrero R. 2000. The chimeric eukaryote: origin of the nucleus from the karyomastigont in amitochondriate protists. Proceedings of the National Academy of Sciences of the USA  97: 6954– 6959. Google Scholar CrossRef Search ADS PubMed  Margulis L, Dolan MF, Whiteside JH. 2005. Imperfections and oddities in the origin of the nucleus. Paleobiology  31: 175– 191. Google Scholar CrossRef Search ADS   Margulis L, Chapman M, Guerrero R, Hall J. 2006. The last eukaryotic common ancestor (LECA): acquisition of cytoskeletal motility from aerotolerant spirochetes in the Proterozoic Eon. Proceedings of the National Academy of Sciences of the USA  103: 13080– 13085. Google Scholar CrossRef Search ADS PubMed  Margulis L, Chapman M, Dolan MF. 2007. Semes for analysis of evolution: de Duve’s peroxisomes and Meyer’s hydrogenases in the sulphurous Proterozoic eon. Nature Reviews Genetics  8. Marleau J, Dalpe Y, St-Arnaud M, Hijri M. 2011. Spore development and nuclear inheritance in arbuscular mycorrhizal fungi. BMC Evolutionary Biology  11: 51. Google Scholar CrossRef Search ADS PubMed  Mazia D. 1987. The chromosome cycle and the centrosome cycle in the mitotic cycle. International Review of Cytology  100: 49– 92. Google Scholar CrossRef Search ADS PubMed  Mazia D. 1993. The cell cycle at the cellular level. European Journal of Cell Biology  61 ( Suppl. 38): 14. McClure-Begley TD, Klymkowsky MW. 2017. Nuclear roles for cilia-associated proteins. Cilia  6: 8. Google Scholar CrossRef Search ADS PubMed  Menzel D. 1994. Cell differentiation and the cytoskeleton in Acetabularia. New Phytologist  128: 369– 393. Google Scholar CrossRef Search ADS   Menzel D, Elsner-Menzel C. 1990. The microtubule cytoskeleton in developing cysts of the green alga Acetabularia: involvement in cell wall differentiation. Protoplasma  157: 52– 63. Google Scholar CrossRef Search ADS   Mine I, Menzel D, Okuda K. 2008. Morphogenesis in giant-celled algae. International Review of Cell and Molecular Biology  266: 37– 83. Google Scholar CrossRef Search ADS PubMed  Minge MA, Silberman JD, Orr RJet al.   2009. Evolutionary position of breviate amoebae and the primary eukaryote divergence. Proceedings of the Royal Society of London B Biological Sciences  276: 597– 604. Google Scholar CrossRef Search ADS   Mursalimov SR, Sidorchuk YV, Deineko EV. 2013. New insights into cytomixis: specific cellular features and prevalence in higher plants. Planta  238: 415– 423. Google Scholar CrossRef Search ADS PubMed  Nicholson DJ. 2010. Biological atomism and cell theory. Studies in History and Philosophy of Biological and Biomedical Sciences  41: 202– 211. Google Scholar CrossRef Search ADS PubMed  O’Malley MA, Müller-Wille S. 2010. The cell as nexus: connections between the history, philosophy and science of cell biology. Studies in History and Philosophy of Biological and Biomedical Sciences  41: 169– 171. Google Scholar CrossRef Search ADS PubMed  Overholtzer M, Mailleux AA, Mouneimne Get al.   2007. A nonapoptotic cell death process, entosis, that occurs by cell-in-cell invasion. Cell  131: 966– 979. Google Scholar CrossRef Search ADS PubMed  Paweletz N. 2001. Walther Flemming: pioneer of mitosis research. Nature Reviews Molecular Cell Biology  2: 72– 75. Google Scholar CrossRef Search ADS PubMed  Potter C, Zhu W, Razafsky Det al.   2017. Multiple isoforms of nesprin1 are integral components of ciliary rootlets. Current Biology  27: 2014– 2022. Google Scholar CrossRef Search ADS PubMed  Radek R, Nitsch G. 2007. Ectobiotic spirochetes of flagellates from the termite Mastotermes darwiniensis: attachment and cyst formation. European Journal of Protistology  43: 281– 294. Google Scholar CrossRef Search ADS PubMed  Resendes KK, Rasala BA, Forbes DJ. 2008. Centrin 2 localizes to the vertebrate nuclear pore and plays a role in mRNA and protein export. Molecular and Cellular Biology  28: 1755– 1769. Roper M, Ellison C, Taylor JW, Glass NL. 2011. Nuclear and genome dynamics in multinucleate ascomycete fungi. Current Biology  21: R786– R793. Google Scholar CrossRef Search ADS PubMed  Rout MP, Field MC. 2017. The evolution of organellar coat complexes and organization of the eukaryotic cell. Annual Reviews of Biochemistry  86: 637– 657. Google Scholar CrossRef Search ADS   Ruiz F, Garreau de Loubresse N, Klotz C, Beisson J, Koll F. 2005. Centrin deficiency in Paramecium affects the geometry of basal-body duplication. Current Biology  15: 2097– 2106. Google Scholar CrossRef Search ADS PubMed  Sachs J. 1892a. Beiträge zur Zellentheorie. Energiden und Zellen. Flora  75: 57– 67. Sachs J. 1892b. Weitere Betrachtungen über Energiden und Zellen. Flora  81: 405– 434. Salisbury JL. 1988. The lost neuromotor apparatus of Chlamydomonas rediscovered. Journal of Protozoology  35: 574– 577. Google Scholar CrossRef Search ADS PubMed  Salisbury JL. 1995. Centrin, centrosomes, and mitotic spindle poles. Current Opinion in Cell Biology  7: 39– 45. Google Scholar CrossRef Search ADS PubMed  Salisbury JL. 2007. A mechanistic view on the evolutionary origin for centrin-based control of centriole duplication. Journal of Cell Physiology  213: 420– 428. Google Scholar CrossRef Search ADS   Salisbury JL, Baron AT, Sanders MA. 1988. The centrin-based cytoskeleton of Chlamydomonas reinhardtii: distribution in interphase and mitotic cells. Journal of Cell Biology  107: 635– 641. Google Scholar CrossRef Search ADS PubMed  Salomaki ED, Lane CE. 2014. Are all red algal parasites cut from the same cloth? Acta Societatis Botanicorum Poloniae  83: 369– 375. Google Scholar CrossRef Search ADS   Sapp J. 2010. Saltational symbiosis. Theory in Biosciences  129: 125– 133. Google Scholar CrossRef Search ADS PubMed  Sharma N, Dey P. 2011. Cell cannibalism and cancer. Diagnostic Cytopathology  39: 229– 233. Google Scholar PubMed  Spang A, Caceres EF, Ettema TJG. 2017. Genomic exploration of the diversity, ecology, and evolution of the archaeal domain of life. Science  357: eaaf3883. Google Scholar CrossRef Search ADS PubMed  Stinchcombe JC, Griffiths GM. 2014. Communication, the centrosome and the immunological synapse. Philosophical Transactions of the Royal Society of London B Biological Sciences  369: 20130463. Google Scholar CrossRef Search ADS PubMed  Stinchcombe JC, Randzavola LO, Angus KL, Mantell JM, Verkade P, Griffiths GM. 2015. Mother centriole distal appendages mediate centrosome docking at the immunological synapse and reveal mechanistic parallels with ciliogenesis. Current Biology  25: 3239– 3244. Google Scholar CrossRef Search ADS PubMed  Strasburger E. 1913. Pflanzliche Zellen- und Gewebelehre. In: Von Wettstein R, ed. Zellen- und Gewebelehre, Morphologie und Entwicklunggeschichte . Leipzig: Teubner, 1– 174. Vicente JJ, Wordeman L. 2015. Mitosis, microtubule dynamics and the evolution of kinesins. Experimental Cell Research  334: 61– 69. Google Scholar CrossRef Search ADS PubMed  Walker G, Dacks JB, Embley TM. 2006. Ultra-structural description of Breviata anathema, the organism previously studied as Mastigamoeba invertens. Journal of Eukaryotic Microbiology  53: 65– 78. Google Scholar CrossRef Search ADS PubMed  Wang X, Gerdes HH. 2012. Long-distance electrical coupling via tunneling nanotubes. Biochimica et Biophysica Acta  1818: 2082– 2086. Google Scholar CrossRef Search ADS PubMed  Wang X, Veruki ML, Bukoreshtliev NV, Hartveit E, Gerdes HH. 2010. Animal cells connected by nanotubes can be electrically coupled through interposed gap-junction channels. Proceedings of the National Academy of Sciences of the USA  107: 17194– 17199. Google Scholar CrossRef Search ADS PubMed  Woese CR. 1998. The universal ancestor. Proceedings of the National Academy of Sciences of the USA  95: 6854– 6859. Google Scholar CrossRef Search ADS PubMed  Woese CR. 2002. On the evolution of cells. Proceedings of the National Academy of Sciences of the USA  99: 8742– 8747. Google Scholar CrossRef Search ADS PubMed  Wright RL, Adler SA, Spanier JG, Jarvik JW. 1989. Nucleus-basal body connector in Chlamydomonas: evidence for a role in basal body segregation and against essential roles in mitosis or in determining cell polarity. Cell Motility and Cytoskeleton  14: 516– 526. Google Scholar CrossRef Search ADS   Yoshida H, Kawane K, Koike M, Mori Y, Uchiyama Y, Nagata S. 2005. Phosphatidylserine-dependent engulfment by macrophages of nuclei from erythroid precursor cells. Nature  437: 754– 758. Google Scholar CrossRef Search ADS PubMed  Young JP. 2015. Genome diversity in arbuscular mycorrhizal fungi. Current Opinion in Plant Biology  26: 113– 119. Google Scholar CrossRef Search ADS PubMed  Zani BG, Edelman ER. 2010. Cellular bridges: routes for intercellular communication and cell migration. Communicative & Integrative Biology  3: 215– 220. Google Scholar CrossRef Search ADS PubMed  Zaremba-Niedzwiedzka K, Caceres EF, Saw JHet al.   2017. Asgard archaea illuminate the origin of eukaryotic cellular complexity. Nature  541: 353– 358. Google Scholar CrossRef Search ADS PubMed  Zhu R, Antoku S, Gundersen GG. 2017. Centrifugal displacement of nuclei reveals multiple LINC complex mechanisms for homeostatic nuclear positioning. Current Biology , in press. © The Author(s) 2018. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For permissions, please e-mail: [email protected].

Journal

Annals of Botany – Oxford University Press

Published: Feb 21, 2018

There are no references for this article.