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Review
. 2022 May;259(3):487-593.
doi: 10.1007/s00709-021-01665-7. Epub 2021 Dec 23.

Ciliary transition zone evolution and the root of the eukaryote tree: implications for opisthokont origin and classification of kingdoms Protozoa, Plantae, and Fungi

Thomas Cavalier-Smith  1
Affiliations
Review

Ciliary transition zone evolution and the root of the eukaryote tree: implications for opisthokont origin and classification of kingdoms Protozoa, Plantae, and Fungi

Thomas Cavalier-Smith. Protoplasma. 2022 May.

Abstract

I thoroughly discuss ciliary transition zone (TZ) evolution, highlighting many overlooked evolutionarily significant ultrastructural details. I establish fundamental principles of TZ ultrastructure and evolution throughout eukaryotes, inferring unrecognised ancestral TZ patterns for Fungi, opisthokonts, and Corticata (i.e., kingdoms Plantae and Chromista). Typical TZs have a dense transitional plate (TP), with a previously overlooked complex lattice as skeleton. I show most eukaryotes have centriole/TZ junction acorn-V filaments (whose ancestral function was arguably supporting central pair microtubule-nucleating sites; I discuss their role in centriole growth). Uniquely simple malawimonad TZs (without TP, simpler acorn) pinpoint the eukaryote tree's root between them and TP-bearers, highlighting novel superclades. I integrate TZ/ciliary evolution with the best multiprotein trees, naming newly recognised major eukaryote clades and revise megaclassification of basal kingdom Protozoa. Recent discovery of non-photosynthetic phagotrophic flagellates with genome-free plastids (Rhodelphis), the sister group to phylum Rhodophyta (red algae), illuminates plant and chromist early evolution. I show previously overlooked marked similarities in cell ultrastructure between Rhodelphis and Picomonas, formerly considered an early diverging chromist. In both a nonagonal tube lies between their TP and an annular septum surrounding their 9+2 ciliary axoneme. Mitochondrial dense condensations and mitochondrion-linked smooth endomembrane cytoplasmic partitioning cisternae further support grouping Picomonadea and Rhodelphea as new plant phylum Pararhoda. As Pararhoda/Rhodophyta form a robust clade on site-heterogeneous multiprotein trees, I group Pararhoda and Rhodophyta as new infrakingdom Rhodaria of Plantae within subkingdom Biliphyta, which also includes Glaucophyta with fundamentally similar TZ, uniquely in eukaryotes. I explain how biliphyte TZs generated viridiplant stellate-structures.

Keywords: Acorn-V filaments; Glaucophyta; Infrakingdom Rhodaria; Picozoa; Rhodelphis; Transitional plate.

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Conflict of interest statement

I have no conflicts of interest or competing interests.

Figures

Fig. 1.
Fig. 1.
Ciliary transition zones (TZ): conserved and variable features. A. Simple type I TZ, exemplified by the metamonad flagellate Trichomonas, with single dense transitional plate (TP) between the outer doublets at which the central pair (cp) microtubules end. Cross sections on right show axoneme (2-4) and centriole (5-6) structure at levels indicated on the longitudinal section on left. 3 shows Y-links;4 shows transitional fibres (TF). C = triplet C fibre. (After Casper fig. 32 by permission). B. Glaucophyte Cyanophora paradoxa; Y-link zone extends above TP to the transitional constriction (c); it has Y-links but no doublet spokes (s) or dynein arms unlike the distal motile axoneme. A small dense axosome (a) terminates cp just above TP. (After Mignot et al. Fig. 2A, B by permission.)C. Chrysophyte alga Uroglena type I TZ, like most heterokonts has a dense transitional helix (TH) above TP just inside the doublets. Its small dense axosome (a) is attached to a central axosomal thickening (AX) of TP; small arrow = short hub linking a to TP. Its dense annular connector (ac) links doublets tightly to the ciliary membrane only slightly distal to TP. A central dense hub (asterisk) is present immediately below TP just distal to the point (arrowhead) where centriolar triplet C tubules end and TFs attach. aV = probable acorn-V filaments (From Hibberd Fig. 1, by permission). D.Rhodelphis limneticus (Biliphyta class Rhodelphea) like glaucophytes has its constriction and associated ac plus a diaphragm or distal plate (dp) well distal to TP, and extended Y-link zone (Y, wide arrows); sP is probably a secondary plate attached just below cp's axosome, but it is possible that 'sP' and 'TP' are actually TP and aV instead (see text; from Gawryluk et al. Fig. 1r by permission). H = hub; cl = cylinder-like nonagonal tube, E-F. Type II TZ in gill cilia of bivalve mollusc Elliptio, with an extended Y-link zone because TP and the constriction have both moved together further from the plasma membrane than in A or C, making Y-links especially obvious in cross sections (E). F shows a secondary plate below TP and absence of spokes in TZ. ce= centriole. (E-F from Gilula and Satir ( fig. 14, 15) by permission.)
Fig. 2.
Fig. 2.
Alternative phylogenies for kingdom Plantae. A. This topology with green plants sister to Rhodaria is supported by both chloroplast- and nuclear-coded multiprotein trees and most likely correct. B. Some nuclear-coded multiprotein trees suggest instead that green plants are sisters of glaucophytes but no recent well sampled multiprotein chloroplast trees support this. There is essentially no credible multiprotein tree support for the third possibility that Biliphyta are a clade. Therefore biliphytes are almost certainly ancestral to green plants and green plant characters are evolutionarily derived from biliphyte ones
Fig. 3.
Fig. 3.
Ciliary and centriolar structure of Viridiplantae as shown by Chlamydomonas reinhardtii. A. Drawing shows LS of cilium and centriole (G) and six TSs at levels A-F. B. LS through isolated centriole/TZ complex shows physical connection of centrioles via striated connector (sc), of TZ to ciliary plasma membrane via two annular connexions (ac) and transitional fibres (TF), and of dense plate (d) to sc despite cell homogenisation. C. Tomographic slice of freeze-substituted wild-type TZ showing that the 'H cross piece' separating distal and proximal basal cylinders is composite: the base of the longer distal cylinder is denser than the distal septum of the shorter proximal cylinder. Note that the proximal septum (not included in diagram A) has a central granule (visible also in B) connected by an oblique linker to the acorn-V, which is more clearly distinct from the centriole in H after detergent extraction that removes centriolar matrix but retains acorn-V. One cp mt apparently is lodged within the lumen of the distal of basal cylinder (or attached to a distal septum or matrix within it); diagram misleadingly shows empty lumen. D, E. TSs of distal (D) and proximal (E) TZ stellate structures in cell homogenates without detergent treatment showing ciliary coats and that the distal basal cylinder has more dense material around its inner-facing obtuse star points. D. Arrows mark paired granules characteristic of Y-links. E. Arrows mark projections into lumen of B tubules. The central granule implies that this section includes the proximal transverse plate (pTP) and part of its linker to the underlying acorn-V (in LS in H). F. TS through TFs and acorn-V filament system in detergent-extracted isolated ciliary apparatus. V filaments are attached to doublets 4, 5; doublets 3-6 show distal parts of C tubules but the five linked to peripheral acorn filaments do not. G. Anticentrin gold-label extends through link between acorn-V and TP. H. Medial LS of detergent extracted cilium showing detergent resistant-membrane remnant linked by acs to doublets and proximal septum of proximal basal cylinder joined to radially asymmetric acorn-V (aV) by a slanting centrin link (arrowhead) shown separately in L to allow labelling and to demonstrate that both acs are horizontal, not slanting towards TP. tr = double stellate region of TZ. cw= centriole cartwheel zone. Radial asymmetry of acorn-V and centriolar regular A/B tubule inner projections throughout centriole above cartwheel are obvious as matrix is dissolved. I. TS of cartwheel in isolated centriole (no detergent extraction). J. Tangential LS of isolated TZ/centriole (no detergent) showing end of C tubules (c), two acs, 2-mt root (R), TF; arrows mark end-on doublet outer projections, arrowheads A-C connections; d = dense fibres at centriole proximal end. K. Negatively contrasted transverse view of isolated TZ (no detergent) resolves doublet mt protofilaments (t) and protein subunits of star filaments (s), of A-tubule feet (f), of Y-links, and of filaments of the basal cylinder (c); surface coat (fc) is outside the ciliary membrane (fm). ac material partially obscures Y-links. H = dense material thickening basal cylinder filaments to resemble a dense hub. (A, B, D, E, I-K from Cavalier-Smith ( figs 5, 13, 14, 15, 17, 18, 22); C from O'Toole et al. ( Fig. 3F); F, H from Geimer and Melkonian ( fig. 1G,K), and G from Geimer and Melkonian ( fig. 1.8), all by permission.)
Fig. 4.
Fig. 4.
Cercozoan TZ hub-lattice and nonagonal fibres. A. Transverse slice through TZ/centriole junction of Bigelowiella natans showing superimposed hub-lattice structure and acorn-V filament system; doublets numbered following Geimer and Melkonian (2004) assuming that the slender filament just outside the more prominent circumferential filament (white arrows) surrounding the central density (likely the dense TP centre labelled in B) is the acorn filament (black arrows). Asterisk marks the hub densities. The more obvious peripheral lattice is best seen between doublets 4-8. Y = Y-links. TF = transitional fibres. A'. transverse section (TS) (serial section immediately distal to A and proximal to C) includes the axosomal plate and cp base and grazes some peripheral filaments. A'', A'''.Viridiraptor invadens from Hess and Melkonian ( Figs 6C,D) by permission. A'' TS of acorn-V complex, A''' slightly more distal thus including acorn-V plus parts of the proximal lattice between doublets 4-8 like that in A. Aiv TS of proximal hub (= central ring). B. Longitudinal section (LS) through Bigelowiella natans TZ. The bracket embraces the transition plate (TP) and acorn-V system (located at the mid level of the transitional fibres, TF) that are both partially included in A; the proximal hub (H) and lattice (L, exceedingly thin) are tightly sandwiched between them. The axosomal plate (ap) terminates the central pair (cp) microtubules. The axosomal plate (ap) has a bounding filament (smallest arrow) that begins at the base of the nonagonal filament (NF) that begins just below the end of cp. ap and the major thickening of TP are eccentric and linked by less dense material. C. TS of Bigelowiella natans distal TZ through the nonagonal fibre (large arrow). A-B links (small arrows) are double, each part oppositely kinked to give a diamond profile. A', A-C, from Moestrup and Sengco ( Figs 6B-D, I) by permission.) C', C'' Viridiraptor invadens from Hess and Melkonian ( Figs 5C2, E) by permission; C' TZ at level of axosomal plate (a) and nonagonal tube (n); C'' at level of proximal hub (='central ring') and its spokes. D. TZ of Metromonas simplex long posterior cilium showing thick TP and proximal diaphragm (di) well separated from the acorn-V (aV); enlargement (E) shows filaments (L) linking di to broad end of hub (H); arrows mark the protruding lateral rods. (D/E from Mylnikova and Mylinkov (2011) by permission.) F. Sainouron acronematica TS of TZ hub-lattice of posterior ciliary TZ. tu = upper TF. Arrows indicate extra crescentic structures on certain doublets. G. Section immediately distal to the dense hub-spoke in F, showing faint central granule, surrounding starfish-like structure (like the axosome in C', so represents the axosome best seen in LS in Fig. 5 upper insert of Cavalier-Smith et al. 2008) and barely visible nonagonal fibre (arrow). H. Helkesimastix marina LS through posterior centriole and TZ; arrow indicates the short hub of the hub-lattice structure, proximal to the cp axosome (a); bracket and small arrows show likely position of acorn-V complex. H' TS of H. marina short cilium (lacking cp) shows TP lattice more clearly than in L. I. Katabia gromovi TS of most proximal TZ possibly grazing centriolar acorn lumenal filament (small arrows) numbered after Geimer and Melkonian (2004) (From Karpov et al. (, Fig. 49) by permission). J, K. Massisteria voersi TZs with axosome (a) and axosomal plate (ap) above TP.(J, K from Mylnikov et al. . Figs 11, 9 by permission.) L. Helkesimastix marina long cilium TS straddling cp (only 1 mt at this level; see text) and TP junction. M. Katabia gromovi TZ LS from Karpov et al. ( Fig. 27) by permission. cp is directly attached to tp. H=hub. aV= putative acorn-V. di=TZ diaphragm, not the same as the centriole structure that Karpov et al. (2003a) also labelled diaphragm in their Fig. 49. N. Sainouron acronematica LS of posterior ciliary TZ and chamfered centriole also showing putative acorn-V filaments immediately proximal to the thick hub-spoke structure; ac is in line with the latter's mid point. s = spiral fibre; arrows mark TP. O. Sainouron acronematica LS of posterior ciliary TZ and centriole. h=distal hub of hub-lattice. TF= lower transitional fibre ac marks the position of the annular connector in typical eukaryotes with longer TZ, which in Sainouron in F was called tu as it is a discrete fibre not obscured by dense matrix as usual. Small arrow shows central connector between fainter cp axosome (a); lr= projecting lateral rods. White arrows indicate triangular section peripheral thickening of TP. White lines mark likely thickness of acorn-V complex. (F, G, N, O from Cavalier-Smith et al. ( Figs 4e, f, b; 3f); H, H' L from Cavalier-Smith et al. ( Figs 4C, D, 5E) by permission.)
Fig. 5.
Fig. 5.
Ciliary TZ and centriolar ultrastructure comparisons in ciliates, relatives, and other model systems. A. Paramecium tetraurelia TZ in LS; A axosome; ac annular connection; AL alveolar linker; AP alveolar plate; aVacorn-V system; ca cortical alveolus; cp centre pair mts; TF transition fibre; TP transition plate. Arrows mark 'loose ring' distal to TP. B. Tetrahymena pyriformis TZ in LS. Note that TP and AP are radially symmetric but differ in substructure, whereas aY is radially asymmetric. C. Trypanosoma brucei (Euglenozoa) type II TZ in LS with long Y-link zone (Y) below TP, which is not connected to aV (level with TFs). Procentriole also capped by an aV but still lacks TFs. CW cartwheel. c'T. bruceii TS of acorn-V (arrow). c'' Chlamydomonas reinhardtii TS of isolated TZ showing two nested lumenal acorn filaments (more proximal than Fig. 3F). D. Paramecium tetraurelia centriole TS at level of AP and ALs grazing circumferential fibre (thick arrow); ca cortical alveoli; C tubules (long arrows) incomplete; asterisks mark A-tubule inner projections. short white arrows show radial linkers to A-B links. E. Tetrahymena pyriformis TS of AP lattice whose spokes point between centriolar triplets. F. Chlamydomonas reinhardtii LS of isolated TZ showing detergent resistant membrane fragment (double arrowheads) adhering to ac (long arrow) and TFs; and asymmetric linker (short arrow) from proximal basal cylinder proximal septum to aV. G. Paramecium tetraurelia TS of TZ grazing top of aV. H. Paramecium tetraurelia TS of TZ grazing bottom of TP, showing Y-links (Y) and A-B links (AB). I. Paramecium tetraurelia TS of TZ including the loose ring and/or lateral part of TP lattice and the extended cp mt. J, K. Paramecium tetraurelia median and tangential LSs of TZ showing four gyres of spiral fibre proximal to TP; a axosome. L. Paramecium tetraurelia TS of AP lattice; circumferential fibre (arrow) more complete than in D. M. Paramecium tetraurelia TS of peripheral TP surrounding central axosome (A) and extreme base of single cp mt. (A, D, G-M from Dute and Kung ( Figs 8, 12, 15, 11, 13, 20. 21, 7); B, E from Allen ; C from Lacomble et al. ( Fig. 2A); c' from Lacomble et al. ( Fig. 4A); c'' from Geimer and Melkonian ( fig. 4.38); F from Geimer and Melkonian ( Fig. 3C) by permission.) N. Miozoan alveolate Colponema aff. loxodes from Mylnikova and Mylnikov ( Fig 2b) by permission. O. Colponema vietnamica. Tikhonenkov et al. ( Fig. 4e) by permission. P, Q Thraustochytrid heterokont Schizochytrium aggregatum from Kazama ( Figs 7A,D) by permission. R. Heterokont oomycete pseudofungus Phytophthora parasitica. Barr and Allan ( Fig. 4) by permission.
Fig. 6.
Fig. 6.
Ciliary transition zones (TZ) of glaucophytes (A-D, F-O) compared with Rhodelphis (E, S, T). A-C serial longitudinal sections (LS) through Cyanophora cuspidata cilia (from Heiss et al. Fig. 3A-C by permission). A median, B lateral section of anterior cilium; its centriole is joined by the multilayered connective (MC) to the microtubular base of the multilayer structure (MLS) serving as the right root (PRR) of the posterior centriole. A. The thick transitional plate (TP) is concave upwards but in some cells was flat, implying that the slender fibre connecting it to the axosome (a) at the base of the central pair (cp) can transmit force from cp to distort the flexible TP. The TZ has a broader constriction (c) than drawn for C. paradoxa (Fig. 1B but similar to the actual C. paradoxa constriction: D); TZ extends from transitional fibres (TF) to the transverse white line. Y-links (small white arrows) below c join doublets to the ciliary membrane. A slender dense basal cylinder (cl) with periodic substructure is on the inner face of the doublets between TP and the short black arrow. In the distal TZ (region d) a cylinder of larger granules (asterisks) lies further from the doublets (similarly to TH in Fig. 1C). The basal cylinder and d region cylinder subunits both differ from the spokes (s) in the standard 9+2 region distal to TZ where cp exhibits its standard prominent projections (p). CW = centriolar cartwheel hub. B of the same cilium shows standard dynein arms (a) distal to the white line and Y-links (Y) in TZ. B* TS of C. cuspidata anterior cilium TP (From Heiss et al. Fig. 7A by permission). C. Median LS of C. cuspidata posterior cilium shows the same regional differentiation of TZ substructure (cl and d region) as the anterior cilium (A,B), cylinder (cl) substructure more apparent. D. Cyanophora paradoxa LS of posterior cilium. Axosome (a) has more distinct proximal extension than in A. Note transition helix (TH, overlooked by Mignot et al.) distal to constriction (c) and that distal septum (arrow) extends to central pair (cp). From Mignot et al. ( Fig. 8) by permission. E. Rhodelphis limneticus TP and double axosome. From Gawryluk et al. ( Fig. 1i) by permission. F. Cyanophora cuspidata TZ LS showing less deformed TP; from Heiss et al. ( Fig. 9C) by permission. G. Glaucocystis geitleri 9+0 pseudocilium in LS showing normal centriole with CW but no cp distal to TP. H-J are transverse sections (TSs) at levels 11, 14, 9; H through mid-region 11 shows reduplicated TP lattice. I through the basal cylinder (cl) showing it is a nonagonal tube (NT) attached to A tubules. J through distal region (level 9) of G. nostochinearum pseudocilia shows 9 outer singlets and probably a rudimentary cp. (G-J from Schnepf Figs 8, 9, 11, 14, by permission.) K. LS of G. nostochinearum pseudocilium shows a long TZ with disorganised material only in cp region, but a clear periodic basal nonagonal tube (NT); both centrioles (=BB) have a proximal cartwheel (c). (From Kies Fig. 14 by permission.) L-N. Cyanoptyche gloeocystis TZs of motile cilia (from Kies figs 12, 13, 15, by permission). L. Distal TZ around cp: doublets joined by single A-B links are attached by thick radial linkers to cylindrical nonagonal tube (NT) and to the membrane by Y-links (arrowheads). M. Median TZ section through transitional plate (TP), NT and Y-links; asterisks mark 9 peripheral densities. N. Basal TZ section through TFs close to acorn level showing dense peripheral granules (g). O-R. Gloeochaete wittrockiana from Kies Figs 12, 13, 15, 51 by permission. O. Interference contrast light micrograph of a separated vegetative cell showing long non-motile pseudocilia without cps plus electron microscope transverse sections at three levels: bottom left, through doublets within the thick base where central dense material replaces cp; upper, median of the long, thin acroneme where B tubules are absent and A tubules remain linked to the membrane; bottom right, basal section though transition from centriolar triplets (left) to TZ doublets (right) that includes the (?partially disorganised) radially asymmetric acorn-V structure of Geimer and Melkonian (2004). P. Chromium-shadowed electron micrograph of zoospore with motile cilia. Q. TS through motile 9+2 axoneme with cp (left) and TZ basal cylinder (cl) and Y links (right). Small arrows mark the dense granules at the membrane ends of the Y-link arms seen also in Chlamydomonas (Fig. 2). R. LS showing TP and putative acorn-V (aV); vF = striated connection between centrioles. S-U. Rhodelphis limneticus TZs from Gawryluk et al. ( Figs 1q,r and extended data Fig. 1e) by permission: S. TS showing Y-links from doublet partitions to membrane (m); the basal cylinder (cl) is a NT linked to A tubules. T. Rhodelphis ciliary LS showing standard cp projections (p) where cp penetrates the distal plate (dp, just above the constriction c). The white arrow marks where TZ structure changes from proximal dense cylinder (cl) near the doublets to a slenderer structure (asterisk) nearer cp. The axosomal plate (ap) central knob is distinct both from the axosome (a) and TP. TP and ap both deformed, unlike in E, U. Y= Y-links. The thick centriolar root is likely a MLS. U. TP region of posterior cilium; unlike in P TP and cp are undistorted; ap (white arrow) is more septum-like than in E making plates seem double. A central hub (right of the asterisk) connects the cp base to TP
Fig. 7.
Fig. 7.
Ciliary transition zone of picozoan/picobiliphyte Picomonas judraskeda (A-J) compared with the glaucophyte Cyanophora (K), Rhodelphis (L) and heterokont Synura (M). A-B. Slightly and peripheral for centriole, B peripheral for axoneme and near median for centriole; both show TP (original label tr1). A basal cylinder (cl) of periodic substructure extends from the central pair (cp) axosome (ax) region to just below the constriction (c). The distal plate (dp, originally called tr2) extends across the entire axoneme but stains very faintly close to cp as in Cyanophora Fig. 6D. Spokes (s) are evident above dp. Y-links are present between TP and c. C-G. Consecutive TSs through TZ at approximate positions c-g in B. C-E show nonagonal substructure of the basal cylinder surrounding cp, enlarged in C inset. Cylinder and cp are absent in F, replaced by a dense central hub and faint peripheral lattice or web of fine fibres connecting it to the doublets; the hub probably represents a structure labelled ax in A, H, I. G shows transversely sectioned ciliary membrane, so is probably not below TP as the g label in B implies but just above it; thus it passes through the dense dish-shaped structure marked by the uTP (upper TP) arrow in I, implying that this central disc has a 9-fold star structure. H. Picomonas anterior cilium in LS. Distal plate (dp) is just distal to constriction c. The cp axosome is more substantially distal to and distinct from the TP's central thickening. The basal cylinder extends from just below c to just above ax (ending at the short arrows). I. Picomonas posterior cilium in LS. The TP central thickening is bipartite, its upper part (uTP) is dish-shaped. The axosome (ax) resembles a short dense central hub (H). J. Picomonas anterior cilium in LS; cl (note periodic substructure) ends distinctly below dp. A-J from Seenivasan et al. (A-I from Fig. 5; J from Fig. 2D) by permission. K. Glaucophyte Cyanophora paradoxa posterior cilium; the anterior septum (as) is marginally distal to the constriction (c). From Mignot et al. ( Fig. 6), by permission. L. Rhodelphis cilium; dp is just distal to c. From Gawryluk et al. ( Fig. 1F). M. Synura uvella (chrysomonad heterokont) cilium with transition helix (TH) with about 10 gyres immediately distal to TP. The cp-terminating axosome is distinct from the upper and lower central dense TP projections. The constriction (c) is opposite the axosome not distal to it as in Biliphyta
Fig. 8
Fig. 8
Ciliary transition zones of Cryptista and Telonema. A. Cryptomonas reticulata From Lucas ( Fig. 17B). by permission. Large arrow marks centriolar connection, small arrow A-tubule feet between TP and acorn-V complex (aV). Arrowheads show three distinct acs. Note distinct axosomal (ap) and upper plates (up). B. Cryptophyte Hemiselmis amylosa from Clay and Kugrens ( fig. 12) by permission. C. Goniomonas avonlea (Cryptomonada: Goniomonadea) From Kim and Archibald ( fig. 10A) by permission: arrow marks nonagonal tube. D. Hatena arenicola (Cryptista: Leucocryptea). Diagram of LS plus TSs at levels G, H, I; from Okamoto and Inouye ( Fig. 7D, G, H) by permission (arows mark sub-TP nonagonal tube), I inludes TP. E. Aberrant goniomonad relative Hemiarma marina from Shiratori and Ishida ( Fig. 6A, C-E) by permission; LS plus 3 TSs on right at positions shown by black arrows; s = TP near its junction with doublets; white arrows show recurved part of TP between s and its thicker central disc; arrowhead marks nonagonal fibre seen on middle TS; C constriction; Y Y-links. F-H. Palpitomonas bilix (Cryptista: subphylum Palpitia) from Yabuki et al. ( Figs 4C, 7) by permission. G. arrow marks cp base; white arrowheads A-tubule feet (and possibly sub-TP nonagonal tube). H. White arrow marks likely sub-TP nonagonal tube. I. Telonema subtilis (harosan phylum Telonemia) from Yabuki et al. ( Fig. 2K) by permission. J. Kathablepharis ovalis (Cryptista: Cryptomonada, Leucocryptea) C constriction; arrow level of upper plate. K--M 'Kathablepharis' G-2 (likely really a new undescribed genus: see text; J-M from Lee et al. ( Figs 26, 27, 29, 30) by permission). K. shows exceptional orthogonality of centrioles connected by massive striated connector as in Palpitomonas. L. LS shows TH above constriction (c). M. TS shows 18-gonal tube (arrow). ac annular connexion, ap axosomal plate, aV putative acorn-V complex, ax axosome, c constriction, cp central pair mts, TF transition fibre, TH transition helix, TP transition plate, up upper plate, Y Y-links
Fig. 9.
Fig. 9.
Ciliary transition zones of Haptista. A-D. Pavlovophyceae: A-C Diacronema vlkianum from Green and Hibberd ( Fig. VIF,G,J) by permission. A. Bipartite central filament connects axosome (a) to TP; distal to TP between arrowheads A tubules have short dense inner projections (likely A-tubule feet without extra attached structures) distinct from longer spokes, s. ?aV putative aV; cp central pair mts. B. TS through central filament showing Y-shaped A-tubule feet. C. TS proximal to TP through nonagonal tube (NT) and double diamond-shaped A-B links (arrows). D. Pavlova granifera from Green ( Fig. 14) by permission. E-H. Isochrysis galbana (Prymnesiophyceae: Isochrysidales) from Hori and Green ( Figs 3B, 8A-C). E. LS showing cylindrical axosome (a) linked by central filament to central disc of hat-like TP (large arrow), Y-links (Y) and tripartite ac beside the tripartite annular septum (as) perforated by cp; small arrow marks A-tubule feet as in F. F. TS of proximal TZ with A-tubule feet and grazing a NT (arrow). G. Section serial to F at TZ/centriole junction including the asymmetric acorn-V filaments. H. shows central filament more clearly. I, J. Alveidia: I. Ancoracysta twista from Janouškovec et al. ( Fig. S1P) by permission. J. Ancoracysta marisrubri from Mylnikov ( Fig. 3A) as 'Colponema' by permission; arrows mark cryptomonad-like axosomal plate. K-Z Prymnesiophyceae: K, L. Prymnesiales: Hyalolithus neolepis from Yoshida et al. ( Fig. 8A,B) showing 'top-hat'-like TP and flat distal partition (dp). M, N. Phaeocystales: Phaeocystis poucheti Parke et al. ( Figs 26, 27, 35). M. LS showing basal cylinder between TP and distal partition (dp). inset * shows basal cylinder in TS linked to doublets by faint A-tubule feet. N. TP with irregular lattice central filament and 18 radial links (A-tubule feet and links to A-B links). O. P. Coccolithales: Pleurochrysis sp. from Inouye and Pienaar ( Figs 11, 12). O. TZ TS showing spiral fibre attached to A-tubule feet and A-B links with thin radial connectors to inner dense ring. P. TZ dense rings in LS. Q. Coccolithales: Calyptrosphaera radiata from Sym and Kawachi ( Fig. 26) by permission; top-hat like TP connected by central filament (arrow) to axosome. R. Coccolithales: Cruciplacolithus neohelis from Kawachi and Inouye ( Fig. 5) by permission. S-Z Prymnesiales: S-X. Prymnesium parvum from Manton ( figs 17 18; 9. 10. 13, 14) by permission. S. Central filament (f) connects axosome (a) to TP centre; arrow marks polygonal filaments; T. U-X mark approximate positions of TSs U-X. U. peripheral filaments join alternate A-tubule feet. V. TS near base of TZ at level of TFs and putative acorn-V. W. peripheral filaments joining alternate A-tubule feet overlap to make pseudo star points. X. TS embraces top-hat shaped TP and base of central filament (white arrow); black arrows mark interdoublet star points. Y, Y', Z.Chrysochromulina chiton Manton ( Figs 5, 10, 30) by permission. Oblique LSs (Y, Y') show dp and tripartite ac. Z. TZ TS with central filament (thin arrow) and A-B links (thick arrows)
Fig. 10
Fig. 10
Green plant (A-M) and chromist TZs compared. A. Nephroselmis (=Heteromastix) rotunda (Prasinophytina: Nephrophyceae): cp is linked to the axosomal plate (ap) by central filament (arrow); TP is associated with proximal (P) not distal (D) basal cylinder. B. LS, C. TSs of Pyramimonas orientalis (Prasinophytina: Pyramimonadophyceae) cf coiled fibre (=TH); s stellate structure. D. E.Mesostigma viride (Charophyta: Mesostigmatophyceae). F.Nephroselmis (=Heteromastix) rotunda proximal stellate structure. G.Coleochaete pulvinata(Charophyta) zoospore TZ LS. H.Chlamydomonas reinhardtii (Chlorophyceae: Chlamydomonadales) standard glutaraldehyde plus osmium fixation; cp base lodged within distal basal cylinder; L linker between proximal basal cylinder lower septum and acorn-V (aV); TP centrally of medium density granules stretched within peripheral ring (TPr) is sandwiched between more amorphous, denser base of distal cylinder and lighter, more alveolate distal septum of proximal cylinder. I.Polytoma obtusum (Chlorophyceae: Chlamydomonadales) osmium fixation; TS of proximal stellate structure, long arrows marks intermediate star-point, short ones simpler A-B links. J-M.Chlamydomonas reinhardtii tomographic slices of freeze-substituted wild-type TZ. J. LS showing that the 'H cross piece' separating distal and proximal basal cylinders is a trilaminar composite: the base of the longer distal cylinder (large arrow) is denser than the underlying thin TP, and the distal septum of the shorter proximal cylinder is alveolate thus lighter still. Note that the proximal lower septum (ls, not included in Fig. 3A diagram) has a central granule connected by an oblique linker (L) to the acorn-V, which is more clearly distinct from the centriole (c) in Q after detergent extraction that removes centriolar matrix but retains acorn-V. K. TS though the upper part of the distal stellate structure; the lattice within the basal cylinder (finer than in L, coarser than in M) probably represents its distal septum (s in J). L. upper septum of proximal stellate structure with coarse lattice within the basal cylinder; arrows mark radial interdoublet supports. M. Tomogram at level of amorphous/finely latticed TP; TPr TP ring. N.Prymnesium parvum(Haptista) TP showing central filament and peripheral star-points. O TP TS, P TP LS of Platysulcus tardus (Heterokonta, Bigyra). Q.Chlamydomonas reinhardtii LS of isolated TZ showing detergent resistant membrane fragment (M, double arrowheads) adhering to ac (long arrow) and TFs; and asymmetric linker (L) from proximal basal cylinder proximal septum to aV. R-X Heterokonta: R.Thraustochytrium aureum TZ (Bigyra: Labyrinthulea). S-V Pseudofungi: S.Rhizidiomyces apophysatus (Hyphochytrea). T-V Oomycetes: T, U.Phytophthora parasitica. V.Saprolegnia diclina. W, XPicomonas juradskaya (Plantae, Biliphyta). W. TZ distal hub, enlargement of Fig. 7F. X. TZ upper TP, enlargement of Fig. 7G. A, F, N from Manton ( Fig. 11, 20, 21); B, C from Moestrup and Thomsen ( Fig. 40, 41); D, E from Melkonian ( Figs 11, 23); G from Sluiman ( Fig. 26); H from Ringo ( Fig. 32); I from Lang Fig. 2J-M. from O'Toole et al. ( Fig. 3C-F), O, P from Shiratori et al. ( Fig. 2F, J); Q from Geimer and Melkonian ( Fig. 3C); R-U from Barr and Allan ( Fig. 3C, 10, 15, 18B, 35); V,W from Seenivasan et al. ( Figs 5Bf,g) by permission
Fig. 11.
Fig. 11.
Relationships between all major eukaryote clades based on multiprotein sequence trees. Clades classified as kingdoms, subkingdoms and infrakingdoms are in capitals of correspondingly decreasing size; the others are mostly phyla (marked by blobs) or super or subphyla; classes end in -ea, orders in -ida. Clades not treated as taxa are in lower case. The tree is rooted between Malawimonada and discaria as the text explains. Site-heterogeneous trees are contradictory about whether Apusozoa is paraphyletic, as suggested by a 159-protein, 68-taxa tree (Brown et al. 2013) or a 351-protein, 61-taxa tree (Brown et al. 2018) and shown here, or holophyletic as on a 253-protein, 151 taxon tree (Gawryluk et al. 2019); both contradictory positions of breviates and apusomonads had maximal statistical 'support'! The position of Haptista is controversial; only some multiprotein trees group them with Cryptista as shown, which a shared lateral transfer makes most likely (Cavalier-Smith 2018), others grouping them as sister to Harosa or (probably erroneously) put cryptists with Plantae. If Plantae, Chromista, and Discicristata were shown as single clades only 21 would be needed to represent the entire diversity of eukaryotes or 20 if Apusozoa are holophyletic (consistent with ultrastructure)
Fig. 12.
Fig. 12.
Miozoan TZ diversity (C-T) compared with Thraustochytrium (A, B). A, B.Thraustochytrium sp. from Kazama ( figs 4, 18) by permission. A. LS showing bell-shape is shorter than in Schizochytrium (Fig. 5P) and the distal constriction (c) wider. B. TS showing only a single cp mt within the basal cylinder. C.Colponema vietnamica (Protalveolata: Colponemea) showing single cp mt penetrating the basal cylinder, which (as in Thraustochytrium: A) has a definite dense base (white arrow) distinct from TP—thus is not muff-like (i.e., open at both ends; close-up from L*). From Tikhonenkov et al. ( fig. 5A) by permission. D-I Perkinsozoa: white arrows mark transverse disc to which both cp mts attach; asterisk marks upper septum of basal cylinder distinct from TP; c is thin-walled distal cylinder. D, E.Perkinsus sp. from Coss et al. ( Figs 23, 24) by permission. F-IParvilucifera. F.P. rostrataG and G*.P. prorocentri from Leander and Hoppenrath ( figs 40, 48) by permission. H.P. infectans type strain posterior cilium from Norén et al. ( Fig. 29) by permission. I.P. infectans RCC2816. F, I. from Lepelletier et al. ( figs 5D,G) by permission. J-N Dinoflagellata white arrows mark peri-cp cylinder. J-L. Myzodinea J.Psammosa pacifica Okamoto et al. ( fig. 4B) by permission. K, L.Colpovora (=Colpodella) unquis from Mylnikov ( fig. 1d) by permission: K anterior, L posterior cilium. L*.Colponema vietnamica centriole (ce) and TZ). M, N. Peridinea:Woloszynskia micra from Leadbeater and Dodge ( fig 13, 17). O-W Apicomplexa, O-V Apicomonadea: O.Chromera velia from Oborník et al. ( fig. 43) by permission. P. Colpodella pseudoedax from Mylnikov and Mylnikov ( fig. 3.4) by permission. Q, R.Colpodella edax clone BE (type) from Mylnikov et al. ( fig. 2B,D) by permission. S, T.Voromonas pontica (as Colpodella sp. G-3) From Mylnikov et al. ( fig. 2B,D) by permission. U.Voromonas (=Colpodella) pontica clone G-3(type) from Mylnikov ( fig. 1d) by permission. S-U fixed in 2% OsO4 + 0.6% glutaraldehyde mixture V.Voromonas pontica from Cavalier-Smith and Chao ( fig. 3B) by permission. Fixation in 1% OsO4 + 2% glutaraldehyde mixture. W. CoccideaEimeria acervulina Fernando ( fig. 5) by permission
Fig. 13.
Fig. 13.
TZ diversity in Sulcozoa (A-N Diphylleida, L-W Planomonadida) and diatoms (X-g). A-D.Collodictyon triciliatum from Brugerolle et al. ( Fig. 1d, e, g) by permission. A, B. Cilium 2 (A) and cilium 1 (B) LSs of same cell broken at constriction (arrowheads in A). S sleeve around cp; ax axosome; asterisk second discoid at TZ base linked to ax by hub (H); st peripheral star around sleeve. white arrows mark C tubule end, thin arrow putative thin acorn lattice; f centriolar A-B feet; N nonagonal tube in prominent centriolar distal plate (clearer in B; disrupted in A by TZ structures being pushed into centriole lumen). B inset:Chlamydomonas proximal acorn-V lattice from Geimer and Melkonian (2005) for comparison with C. C.Collodictyon TS at TF level includes centriolar nonagonal tube and grazes the putative acorn structure (doublets numbered as in Chlamydomonas (B inset). D.Collodictyon TS of cp within sleeve and surrounding stellate structure and Y links (Y). E-H.Sulcomonas lacustris from Brugerolle ( figs 5+ a, c, d). E. TFs at centriole/TZ junction (level a in G); likely represents faint asymmetric acorn filaments superimposed on underlying rotationally symmetric centriolar distal ring with radial linkers. F. TS of level c in G showing cp (arrows) tightly enclosed by dense sleeve. G. LS (1 tangential, 2 median) of ciliary bases showing absence of complex TZ structures between acorn (just distal to a) and TP/constriction(c) levels. H. TS through fluted (star-like in section) basal cylinder (c) at level d in G where spokes and arms are absent from doublets, replaced by inner (straight) and outer (V-shaped)A-B links. I-NDiphylleia rotans from Brugerolle and Patterson (1990 as Aulacomomonas submarina figs 10-14, 16) by permission.J. LS of TZ; in Y-link zone (Y) below white line doublets lack spokes and arms; TP separates distal basal cylinder (BC) and four distinct proximal TZ zone. c constriction level with sleeve, a axosome, H narrow and wide hubs; tp centriolar distal plate. J-M. TSs of Diphylleia TZ. J at level 3 through axosome showing Y-links (Y) and single set of A-B links (arrow). K at level 2 embracing narrow (on left) and wide hub (right) junction. L at level 1 at TFs and triplet doublet junction (note filled C tubules as in C); section includes acorn homologue and base of overlying hub), possibly also grazing underlying centriolar plate hub, superimposed; arrowheads mark putative peripheral acorn filament. M. level 4 through sleeve and cp; radial links as D but surrounding basal cylinder comprises discrete densities opposite A-B links (arrow) not star-like as in Collodictyon (C). O.Planomonas micra anterior cilium with basal cylinder (c arrow) around central pair mts (within ciliary pocket) from Cavalier-Smith et al.  fig. 6C by permission. P-WAncyromonas sigmoides from Heiss et al. ( figs 4A, 2D, 3B, C, 5C, D, F, G) by permission. P. LS showing central mts (cp) surrounded by short dense basal cylinder (long arrows) terminating at an axosome (a) connected by asymmetric short links (? sandwiched acorn-homologue?) to dense material (asterisk) in the distal centre of the centriole (ce); small arrow marks end of C tubule; less dense thin material (?TP) between a and doublets may be the peripheral zone of TP. Q. LS of anterior cilium with central pair mts (cp) projecting into acroneme; a axosome; pc posterior centriole; arrow distal transverse centriolar plate. R. posterior cilium TS grazing the axosome (long arrow) to which one cp mt clearly abuts; arrowheads mark circumferential filaments (? zig-zag or starlike) associated with A-tubule feet. S. Anterior cilium within ciliary pocket showing upper zone of basal cylinder, i.e., distal to R fig. 3C. T-W.non-consecutive serial sections of another posterior cilium (B tubule lumens filled; T-U within posterior ciliary pocket). T. at distal end of centriole; arrowheads mark filaments of its irregular lattice, partially obscured by central dense matrix (*); thin arrow marks A-tubule tubule foot from which lumenal filaments diverge; TF transition fibre. U. most proximal TZ with only one cp mt contacting axosome (arrow) surrounded by irregular lattice that may represent TP; denser granules (arrowheads) may be parts of underlying acorn or overlying basal cylinder. V. at level of basal cylinder of 9 discontinuous granules (arrowheads opposite doublets); 2 cp mts. W. in ventral groove after exiting ciliary pocket; some dynein arms appear, cylinder and spokes largely absent; cp mts surrounded by denser zone. X. Centric diatom Melosira monoiliformis var. octogona long centriole with prominent cartwheel in LS. Asterisk marks annular connection, and black arrow the dense material linking Y-link stems axially. Y. Centric diatom Thalassiosira lacustris LS showing short centriole with very short cartwheel. Black arrow marks dense central zone of TP seen in TS in g; white arrow marks interdoublet centriolar dnesities seen in TS in i,j. Z-e.Melosira Consecutive TSs through transition zone (Z-d) to upper centriole (e). Z straddles axoneme base and uppermost TZ showing dynein arms, nonagonal fibre, and A-tubule feet. a, b show Y-link (Y) dense bases . a. embraces extremely thin TP showing a central pair of densities (arrowheads) where cp would originally have been attached and peripheral links to doublets. b. acorn-like structure with axosome-like aymmetric density at base of Y-link zone and double A-B links. c. TF zone with hints of acorn filaments. d. TZ/centriole transition. e. upper centriole doublets with single A-B links. f-j.Thalassiosira TSs. f-h. Consecutive TSs though lower TZ. f. Y-link zone. g. section embracing TP lattice with central densities (arrowheads) and transition between Y-links/ac and TFs. putative acorn. i,j. Consecutive TSs through lower part of doublet centriole showing interdoublet dense rods. Figs X-g from Idei et al. ( figs 4b, 5b, c, d, h, i, 7d, 8b,c, d, e, f, g) by permission
Fig. 14.
Fig. 14.
Metamonad TZ diversity: Trimastigida (A-D, F-O), Fornicata (E). A.Paratrimastix eleionoma axosome/TZ structure bell-shaped in LS; AB anterior centriole. B.Trimastix marina posterior cilium LS; axosome (a) terminating cp is separated from centriolar distal central density (asterisk) by less dense asymmetric material (acorn-complex in C); arrows mark ends of C tubules. C.Trimastix marina anterior centriole/TZ junction with six triplets and three doublets (numbered as in Geimer and Melkonian 2004); arrows mark peripheral and part of lumenal acorn filaments, overlying centriolar density (asterisk). D.Paratrimastix pyriformis distal TZ with Y-links(Y) and fluted basal cylinder surrounding cp. E, F. Fornicata:Carpediemonas membranifera posterior cilium TZ LS and anterior cilium TS of upper TZ; c end of C tubule; a axosome; arrow, possible lumenal acorn filament. G, H.Trimastix marina anterior cilium adjacent serial sections; G upper TZ including axosomal zone around cp, H lower TZ/centriole junction. I.Paratrimastix pyriformis TZ showing outer starlike lattice with tenuous connectors to denser axosome. J.Paratrimastix pyriformis tangential LS. KParatrimastix eleionoma anterior cilium TZ. L.Paratrimastix eleionoma posterior cilium upper TZ. M.P. eleionoma right cilium TZ with nonagonal fibre and axosome. N-P.Paratrimastix eleionoma consecutive serial TSs of right cilium base (N), TZ/centriole junction (O), and distal centriole (P). A, K M-P from Simpson et al. ( Fig. 2h, j-m, 3b); B, C, G, H— from Zhang et al. ( figs 7E,F, 8C,D); D, J from O'Kelly et al. ( figs 24, 7);. E, F from Simpson and Patterson ( fig. 2i, j) by permission
Fig. 15.
Fig. 15.
Malawimonada transition zones (A-G Malawimonas I-M Gefionella) compared with divergent outgroups (fungi, parabasalian metamonads and a rhizarian); four insets show magnified TZ central lattices from diverse natate lineages). A-GMalawimonas jakobiformis from O'Kelly and Nerad ( figs 10, 11-14) by permission. A. axosome (arrow) at cp base; note absence of TP between it and centriole (ce)l scale bar 250 nm. B-E consecutive serial section though anterior centriole (B proximal cartwheel and anterior fan (F) mts, C distal with dense fibre (DF) and striated band (sb) connectors to posterior centriole), TZ (D), and 9+2 axoneme base (E), showing absence of a symmetric TP lattice and transitional fibres (TF) only on doublets abutting plasma membrane. D. (enlarged and rotated in G for comparison with H; arrow marks grazed base of second cp mt.) shows semicircular filament linking A-tubule feet of doublets 7-9, 1, 2 only (numbered assuming homology with Chlamydomonas acorn peripheral filament in H). In E. arrows mark faint filaments linking five doublets, 7-2) only. F. LS through antiparallel centrioles showing TZs (arrow) recessed below the cell surface on their inner linked sides. InsetCalkinsia (Euglenozoa: Postgaardea) axosomal filamment TS magnified from Fig. 17C. G inset.Chlamydomonas reinhardtii irregular coarse lattice of distal septum of proximal TZ basal cylinder; tomogram from O'Toole et al. ( fig. 3C) by permission. H.C. reinhardtii acorn-V complex from Geimer and Melkonian ( fig. 2E) by permission. I-MGefionella okellyi from Heiss et al. ( figs 3a, 2a, g) by permission. I. Oblique LS medially through axoneme cp and tangentially though posterior centriole (ce) showing termination of C tubules (arrows) and Y-link zone (Y) thus TZ and centriole much longer than Malawimonas. J. Median LS shows cp starts below cell surface. A ciliary constriction (large arrows) is barely visible, putative TFs diffuse, and basal attachments of cp asymmetric (thicker/denser on one side: white arrow) and level with putative TF bases; arrowhead indicates C tubule ends; cw cartwheel. K. LS confirming asymmetry of cp basal attachment (white arrow marks thicker side), arrow marks likely C tubule end. Inset *Viridiraptor (Rhizaria) axosome lattice magnified from Fig. 17T. L. M. consecutive TSs from a series of five spanning posterior centriole, TZ and spoked 9+2 axoneme. L. Proximal TS with peripheral acorn filament and lemon-shaped axosomal plate with dense irregular lattice linked by radial connections to acorn filament; large black arrows mark triangular linkers to membrane from doublets 8, 9, shorter than typical TFs or Y-links, small ones the lumenal edge of the axosomal plate that may hide a lumenal acorn filament; asterisk marks hint of a mt base and position to which V filaments from doublets 4 and 5 converge in discarian TZs; f fibrillar arc to which doublets 1-5 attach by putative Y-links). M. distal TZ with cp, A-B links (AB), and tenuous circumferential filaments linking double ends of A-tubule feet (arrows); membrane linkers shorter for doublets 8,9. Lower inset. Lattice from Chlamydomonas distal basal cylinder's distal septum tomogram for comparison (magnified from Fig. 10K). N.Olpidium brassicae (Fungi: Zygomycota: Zoomycetes) barren centriole (bc) and ciliated centriole attached to common striated rhizoplast showing TFs and end of C tubules (arrows). O.Phlyctochytrium irregulare (Chytridiomycetes) acorn-like structure from McNitt ( fig. 3) by permission. P.Chlamydomonas reinhardtii acorn-V complex slightly more proximal than H from Geimer and Melkonian ( fig. 2E) by permission. Q.Olpidium brassicae TS of TZ base; acorn-V clearer than in O; note peripheral acorn filaments (arrowheads), lumenal acorn filament (arrows) and putative V-filaments (V); doublets (3, 5, 6 with faint/partial C tubules) numbered as in P; the granule (asterisk) absent in Chlamydomonas might be underlying centriolar as in N. R.Stygiella (= Jakoba) incarcerata (Eozoa, Jakobea) from Simpson and Patterson ( fig 3A). Fuzzy section showing TP/axosomal plate (lower left) apparently superimposed on partial nonagonal fibre (arrowheads).Olpidium brassicae more distal TS than Q at Y-link (Y) level including ?partial/grazing coarse irregular lattice (asterisks) slung from doublets, A-B links, and A-tubule feet. S.Olpidium brassicae. TS of TZ including or grazing the TP, showing its irregular lattice (asterisks) that occupies the whole area within the A-B links (arrowheads);ac annular connexion. T, U, X-Z. Metamonada: Parabasalia. T.Holomastigotoides TZ LS; the putative amorphous TP is immediately beneath the axosome (a) terminating cp and underlain by an asymmetric acorn complex (aV). U.Trichonympha showing asymmetry of cp attachments; the longer mt (white arrow) is attached laterally to the crescentic body (cb) and basally to the putative TP which immediately overlies the putative acorn-complex (aV) V, W.Viridiraptor invadens (Rhizaria, Cercozoa) TSs of separate TZs showing acorn-V at slightly different levels: V similar to Chlamydomonas in Fig 3F. W. more like slightly more proximal Chlamydomonas in P. X-Z.Pseudotrichonympha serial sections through TZ showing crescentic body (cb) and acorn filaments (in Z); L faint lattice. Z. Acorn-V superimposed on extreme base of longer cp mt (arrowhead) and likely also peripheral star-like boundary of TP; arrow marks Y-system beside the granular junction of arms of putative V-filaments (compare with V,W). a,Trichomympha TS at TZ/centriole junction showing asymmetric acorn-like complex. b.Trichomympha more distal TS; cb crescentic body. N, Q, S from Lange and Olsen (1976 figs 4, 13, 15), T-Z, a, b from Gibbons and Grimstone ( Fig. 8 figs 56, 32, 23/4) by permission)
Fig. 16.
Fig. 16.
Eozoan TZs compared with green algae. A, B. Stigeoclonium sp. (Plantae: Chlorophyta, Chaetophorales). In A The acorn-V filament system (aV) is joined by slanting linker (L) directly to a central axial filament (arrow) stemming from the less dense lower part of TP; this proximal stellate structure and its central filament (f) are shown in TS in B); distal and proximal 'basal cylinders' (c) have a fluted wall, seen in TS as 18-gonal stars with 18 dense granules at each vertex, so are not literally cylinders. They are really two concentric 9-pointed stars, mutually rotated by 20°, the inner more obtuse star points being attached to the inner vertices of the outer, whose vertices join to the A-tubule feet. The central pair enters the upper cylinder and is joined to TP by a central fibre (f) resembling a distal hub-spoke structure, less obvious than cartwheel (cw) hub-spokes. C-F. Rhynchomonas nasuta (Eozoa: Euglenozoa: Kinetoplastea: Bodonida: Neobodonina) from Swale ( figs 2D, 3B, D, 4A). C-E. In LS a sleeve-like basal cylinder (c) surrounds cp and TP level with the base of the paraxonemal rod (PR); a putative acorn complex. F. The basal cylinder (c) surrounds both cp mts (arrow);vC ventral cilium; dC dorsal cilium. G. Azumiobodo hoyamushi (Neobodonina) from Hirose et al. ( fig. 2A) by permission; the proximal TZ, longer than in Rhynchomonas, has a central filament, F. H. I. Trypanosoma brucei brucei (Kinetoplastea: Trypanosomida).H. LS showing very short basal cylinder (c) surrounding cp (asterisk) distal to TP and putative acorn-V (aV) at TF level. I. TS of acorn (a) and TFs (arrowheads); numberd after Geimer and Melkonian (2004). J. Jakoba libera (Eozoa: Jakobea: Jakobina) anterior cilium from Patterson ( fig. 1E) by permission; short type I TZ with TP possibly directly overlying acorn complex (arrow); these structures are less fuzzy in Reclinomonas (O,P). K. Chlamydomonas reinhardtii detergent-extracted TZ in LS showing slanting linker between acorn and proximal stellate structure. From Geimer and Melkonian (2004) by permission. L. Procryptobia sorokini (Bodonida, Parabodonina) from Frolov et al. ( fig. 17) by permission; type II TZ with putative acorn complex (arrow) at TF level. M, N. Trypanosoma bruceiM. Sum of five tomographic slices (total thickness 8.5 nm) showing cp termination of cp at TP and surrounding basal cylinder. N. 1.6 nm thick tomographic slice through junctional complex between cp, basal cylinder (c), and TP, and acorn complexes (aV) of ciliated and barren (posterior) centriole (pc); cw cartwheels. O, P. Reclinomonas americana (Eozoa: Jakobea; Jakobina) consecutive LSs of posterior cilium through cp/TP junctional complex. O. section though axosome (ax) around putative shorter mt apparently ending just above TP (arrowhead; arrows mark position where TP joins doublets), through similar plane to J, but sharper). P. section through slightly longer cp mt joined to TP; axosomal plate with slender laminae (asterisks) to doublets; the asymmetric acorn complex (a and arrowhead) appears to be directly attached beneath TP; arrows mark putative end of C tubules; left doublet ? broken at long arrow. Q-T. Andalucia godoyi (Jakobea: Andalucina) from Lara et al. ( figs 6, 7, 12, 16). Q, R anterior cilium in oblique and LS. S. posterior cilium TS embracing superimposed cp base and TP lattice. T. U-W. Stygiella incarcerata (Jakobea: Andalucina) consecutive sections of anterior cilium from Simpson and Patterson (, then Jakoba incarcerata) fig 3h-j by permission. U. immediately above cp base doublets, five filaments (partial-nonagonal) link A-tubule feet of doublets 2-7 only. V. immediately proximal to U a dense semicircular sheet stretches between doublet 2-7 and four filaments (partial nonagonal) link A-tubule feet of doublets 7-9, 1, 2 W. Top of centriole with filled C tubules (c) and acorn filaments. X, Y consecutive sections of Reclinomonas americana anterior cilium TP (X) and top of centriole (Y) with nonagonal fibre linking A-tubule feet. Reclinomonas americana TS of centriole Z. Stephanopogon pattersoni (Eozoa: Percolozoa) arrow centriolar cup. a. Creneis carolina (Eozoa: Percolozoa) from Pánek et al. ( fig. 5E) by permission; TP overlies asymmetric dense acorn complex (aV); arrow marks end of C tubule. b. Pleurostomum flabellatum (Eozoa: Percolozoa) possible acorn-V structure from Park et al. ( fig. 3C) by permission; numbering follows Geimer and Melkonian (2004). c. Pharyngomonas kirbyi (Eozoa: Percolozoa) TP in TS TP in TS from Park and Simpson ( fig. 4H) by permission. d. e. Stephanopogon minuta TZ from Yubuki and Leander ( 5A, 5B) by permission. d. TS showing dense hub and asymmetric acorn (at level of aY in Z). e. LS showing axosomal thickening of TP (large arrow) and acorn complex (small arrow). f. cilium 1, g. cilium 2 of ' Percolomonas' sulcatus showing putative acorn-V complex (Eozoa: Percolozoa) from Brugerolle and Simpson ( fig. 4c). h. Stephanopogon pattersoni TS showing TP with radial links to doublets and A-B links. i. Pleurostomum flabellatum TZ in LS from Park et al. ( fig. 3A) by permission. j. Percolomonas cosmopolitus (Eozoa: Percolozoa) from Fenchel and Patterson ( fig 6c) by permission. k. Tetramitus rostratus (Eozoa: Percolozoa) cilium 3 Balamuth et al. ( fig. 12) by permission. A, from Manton ( figs 1, 20); H, I, M, N from Lacomble et al. ( figs 1C, 3E, 4A, D); O, P, X, Y from O'Kelly ( figs 8, 9, 12, 13); Z, h from Lee et al. ( figs 4D,F) by permission.
Fig. 17.
Fig. 17.
Six filamentary patterns in immensely stretched TZ of the postgaardiid Calkinsia(Euglenozoa)A-H; short TZ/centrioles of Hemimastigophora (L-P), and other comparisons. A. Calkinsia aureus dorsal cilium LS showing levels represented in TS by B-H; PR paraxonemal rod; paraxial plate (PP) is opposite TP; PH proximal hub; TF transition fibres; white arrow marks end of C tubules. B. 9+2 axoneme; doublets with arms and spokes. C. doublets unchanged, cp replaced by axosomal filament. D. distal hub-spoke structure; the diamond-shaped densities beside the doublets (long white arrow) have two distinct parts (white arrowheads) lesser densities (asterisks) between them and the hub (H) and the spoke filaments are also double; the diamonds are linked by V-shaped filaments like star points directed towards the centres of the A-B links (black arrowheads). E-G. successive levels of proximal hub-spoke structure, spokes more clearly double, showing Y-links, (Y, arrowhead). H. acorn V at the TF/triplet start level; two longest thin arrows mark peripheral acorn and fat arrows lumenal acorn filament; other arrows explained in text I. Postgaardi mariagerensis(Euglenozoa, Postgaardea) from Simpson et al. ( fig. 17) by permission; Y Y-links. J. K. Calkinsia diagrams from Yubuki et al. (2009) interpreting hub-spoke structures: J level D, M level F. L-P Hemimastigophora TZs from Foissner and Foissner ( figs 44, 45, 49, 51) by permission: L-P. Stereonema geiseri.L. Slightly oblique TS of putative acorn complex. M. Median LS of TP (arrowhead) with faint central projecting filament (small arrow) and thin basal cylinder (larger arrow) r long 2-mt root.N. TS of distal TZ with slender nonagonal fibre (arrows) attached to A-tubule feet and thicker A-B links (arrowhead. O. TS of centriole/TZ junction embracing central part of T with irregular lattice superimposed on underlying acorn filaments. P. Tangential LS of TP and underlying acorn filaments (arrow); very short centriole with basal cup (c). Q. Hemimastix amphikineta LS of TP, separate ac (asterisks), and long and short 2-mt roots (r) from Foissner and Foissner ( fig. 58) by permission. R. Sainouron acronematica (Cercozoa) distal hub-spoke complex, from Cavalier-Smith et al. ( fig. 4e) by permission. S, T. Viridiraptor invadens (Cercozoa): S. TZ at level of proximal hub (='central ring') and its spokes; Y Y-links. T. TZ at level of axosome (ax) and inner cylinder (ic); the 'outer cylinder' (ic) is just the extra dense arms of the Y-links. U. Collodictyon triciliatum(Sulcozoa) TS of cp within sleeve and surrounding stellate structure and Y-links(Y) from Brugerolle et al. (2002) by permission. A-H, J, K from Yubuki et al. ( fig. 6); S, T from Hess and Melkonian ( fig. 5C2, E) by permission.
Fig. 18.
Fig. 18.
Opisthokont transition zones: comparison of Fungi (A-I, M), Choanozoa (N, R, U, X, Y) and sponges (J, K, O-Q). A-C. Polychytrium aggregatum Chytridiomycetes (Polychytriales) zoospores.A. Tangential LS through cilium-bearing centriole (K = kinetosome) and barren centriole (nfc =non-flagellate centriole; distally capped by acorn-like structure a) showing endpoints of C tubules (C) and lattice substructure of transition cylinder/helix (TH). TF transition fibres, TP transition plate, asterisk putative acorn-homologue, Y Y-links. d doublets. B. Median LS showing central pair mts apparently passing through the strongly stained TZ 'plug' zone (cp?) to top of centriole. C. TS through fibrous connective linking centrioles. D, E. Neokarlingia chitinophila (Polychytriales) zoospore cilium consecutive serial sections just distal to (D) and at (E) the TZ acorn-homologue (fig 4a, b). F, I. Karlingiomyces asterocystis (Polychytriales); LS (F) and TS through centrioles; cp penetrates through entire TH (F, note radial linkers from TH to cp), its base being below TH proximal end, in same section as distal end of triplets (I; at this level nfc lumen has a fuzzy acorn-homologue). G. Stephanoeca diplocostata (Choanoflagellatea: Acanthoecida) from Leadbeater ( fig. 5); a acorn; bc barren centriole; c constriction; sd striated disc mts; asterisk plug proximal to TP; arrows ciliary hairs. H. Maunachytrium keaense (Chytridiomycota: Lobulomycetales) from Simmons et al. ( fig. 6A) by permission. J, K. Demosponge Sigmadocia caerulea (Haplosclerida) larval epithelial cilium from Maldonado ( fig. 4J, G) by permission. c = transitional cylinder linked to A tubule feet of doublets (db) and by thin radial links to central sheath (cs) around cp; Y = Y-links, AB =A-B linker. L. Volkanus costatus (Choanoflagellatea: Acanthoecida) from Leadbeater ( fig. 25); a acorn; bc barren centriole; dc daughter centrioles; sd striated disc mts; asterisk plug proximal to TP. M. Monoblepharis polymorpha (Chytridiomycota: Monoblepharidales) semicircular striated disc (sd), from which microtubules (mt) radiate, surrounds ciliated centriole (k);ac annular cisterna of Golgi. N. Codonosiga (=Codosiga) botrytis (Choanoflagellatea: Craspedida) TS of radiating mts around anterior centriole, with circumferential dense arcs shown in LS in Y, Z. O. Demosponge Halisarca dujardini (Halisarcida) from Gonobobleva and Maldonado ( fig. 3C) by permission; c = transitional cylinder. a = putative acorn-homologue;ac accessory centriole, ce ciliated centriole, r =rootlet. P. Demosponge Sigmadocia caerulea (Haplosclerida) larval epithelial cilium from Maldonado ( fig. 4H); as/ap =TF; bf basal foot from which mts (m) radiate into cytoplasm. Q. Demosponge Halichondria melanodocia (Halichondrida) larval epithelial cilium from Woollacott and Pinto ( fig. 2) AS =alar sheet (= TF), FR = fibrous rootlet. AP = R. Choanoflagellate Codonosiga (=Codosiga) botrytis TZ/centriole junctions showing acorn homologue with peripheral filaments linking A-tubule feet of five doublets (7-9, 1, 2); arrowheads mark possible homologues of the more distinct central elements in Chlamydomonas in S; arrow marks densities absent in Chlamydomonas but present in Phalansterium (Fig. 19C,D). S. Chlamydomonas reinhardtii (Chlorophyta)acorn-V complex proximal to filaments with acorn shape; arrowheads mark similar elements at centre of standard arc-like acorn lumenal filament between doublets 2 and 7 and subsidiary filament arcing from 1 and 8) from Geimer and Melkonian ( fig. 4.38) by permission.T. Malawimonad Gefionella okellyi acorn-homologue(not acorn-shaped) without V-filaments. U. Codonosiga (=Codosiga) botrytis TS through ciliary bulge showing central fibre (cf) and radial links to doublets fig. 30 V. Choanoflagellate Monosiga ovata (Craspedida) TS of barren basal body showing unique lumenal lattice. W. Desmarella moniliformis (Choanoflagellatea: Craspedida); cf central filament connecting cp to dense plug at and below constriction; fr fibrillar rootlet, c ciliary constriction. X. Monosiga ovata showing wide constriction with central plug (p) so densely stained as to obscure details visible in Y. Y. Choanoflagellate Monosiga ovata showing central filament linking cp (c) and a secondary plate just distal to TP; nb aciliate centriole; mt fans (f) surround centriolar base. Z, a. Codonosiga (=Codosiga) botrytis fig. 21 fig. 27. Codonosiga (=Codosiga) botrytis LS showing variable length of central fibre connecting cp axosomal plate to TP; al putative cross section of acorn-like lumenal filament. b. Monoblepharis polymorpha (Chytridiomycota) striated disc (sd) level with top of cartwheel (cw) (which protrudes from centriole base) associates with a smooth annular cisterna (ac); a acorn filaments, seen in TS in Fig. 20A. A-F from Longcore and Simmons ( fig. 3c, d, e, 4a, b, 6a, d); N, R, U, V, Z, a from Hibberd ( figs 15, 19, 27, 29, 30), M, b from Mollicone and Longcore ( figs 18, 20) by permission V, X, Y. from Karpov and Leadbeater ( figs 3, 5, 6) by permission
Fig. 19.
Fig. 19.
Early torcid transition zones: Amoebozoa and Apusozoa. A, D, E, H-L. Phalansterium digitatum (Amoebozoa:) from Hibberd ( figs 9, 10, 13-17) by permission. B, C, F, G. Phalansterium arcticum from Shmakova et al. ( figs 19A-C, E) by permission. M, O, P, Q, R, S. Thecamonas trahens(Apusozoa: Thecomonadea) from Heiss et al. figs 2A 3D, F, C, 4A, 7B by permission. T. Mastigella rubiformis (Amoebozoa: Archamoebae) from Zadrobílková et al. (2015) fig. 7F by permission. A. P. digitatum swollen proximal TZ region without cp, showing plug (P), nonagonal tube NT (=TC), putative TP and acorn (a) plus linker between them (small arrowhead); open arrows indicate striated TF, double arrowheads concentric dense bands linking radiating mts. B. P. arcticum TS above TZ base showing 18-gonal/nonagonal tube (arrows)C. P. arcticum acorn complex at TZ base (proximal to B, in TF zone). D. P. digiataumacorn-V complex at doublet/ytiplet junction.C, D doublet numbering after Geimer and Melkonian 2004). E. enlargement of A at centriole/TZ junction. F. P. arcticum TZ in LS showing central structure (originally identified as a mt), which might be a mt as in H, L or instead the central filament as in I. G. P. arcticum TZ LS. H, L. P. digitatum TSs in distal Y-link zone showing single central mt. I-K successively more proximal TSs of P. digitatum TZ showing central filament (I), plug (P in J) and nonagonal tube/'transition cylinder' (TC in K). M. Thecamonas trahens posterior cilium LS near base of highly asymmetric centriole and TZ. Zig-zagnonagonal/18-gonal tube (Z); ce centriole elongation on inner side; cw cartwheel. N. Pygsuia biforma (Apusozoa: Breviatea) oblique LS of TZ showing TP and axosomal plate (asterisk); from Brown et al. ( fig. 1h). O. Thecamonas trahens LS of anterior ciliary base linked directly to mitochondrion (m) and to posterior centriole (pc) by striated connector (sc); posterior centriole closely linked to cell surface (asterisk);z zigzag nonagonal/18-gonal tube. P. T. trahens LS of both centrioles showing large offset and thin connector (arrow); base of anterior centriole is linked to a mitochondrion (m); base of posterior (AF) beveled, at cell surface; a putative acorn. Q. Thecamonas trahens posterior centriole TS near base showing triplet, doublet and singlet mts. R. Thecamonas trahens anterior cilium at cp base showing peripheral 18-gonal star (arrows), central axosomal densities and faint radial linkers between them. S. Thecamonas trahens anterior cilium with nonagonal tube (arrows) around cp.T. Tangential LS of Mastigella rubiformis (Amoebozoa: Archamoebea) ciliary base showing two-tiered circumferential centriolar root radiating from distal centriole with upper fibrillar sheet and lower radiating mts (Black arrow). Asterisk is dense cylinder outside the doublets similar to that of Viridiraptor. White arrow marks possible TZ basal cylinder.
Fig. 20.
Fig. 20.
Fungal transition zones. A-C. Monoblepharis polymorpha (Chytridiomycota: Parachytriomycetes). A. TS of TZ/centriole junction showing central acorn complex (doublets numbered after Geimer and Melkonian 2004) and the striated disc (sd) of radiating mts linked by circumferential filaments attached (arrow) distally to triplets. B. LS showing TP at constriction well separated from acorn complex at TZ base (level with TF bases); c centriolar connector. C. Monoblepharis polymorpha spiral fibre (arrow) in proximal TZ; Y Y-links. D. Codonosiga (=Codosiga) botrytis (Choanoflagellatea). Distal TS of non-ciliate centriole with putative acorn complex (triplets numbered after Geimer and Melkonian , often with faint C tubules implying they end within this section) from Hibberd ( fig 29) by permission. E. Gonapodya polymorpha (Parachytriomycetes); LS showing annular cisternae linked to striated disc, putative acorn complex (a) and spiral fibre (sf) proximal to TP; F lateral flanges. F. Chlamydomonas reinhardtii (Chlorophyta)acorn-V complex proximal to filaments with acorn shape from Geimer and Melkonian (2005) by permission. G. Phalansterium arcticum (Amoebozoa) from Shmakova et al. (2018) by permission. H. Gonapodya polymorpha LS showing central filament (arrows) supporting ciliary flanges.I. Harpochytrium hedynii (Parachytriomycetes: Monoblepharidales) from Travland and Whisler ( fig. 2) by permission; K TZ proximal to TP; arrow marks top of centriole; cf central filament linking cp to TP; open arrow striated disc. J. Coelomomyces punctatus (Allomycetes: Blastocladiales) from Martin ( fig. 11); arrow dense sleeve around centriole (ce); centriole attached basally to nucleus (N) nestles in indentation of mitochondrion m); central pair mts (A) with projections extend greatly below TFs; a putative acorn lumenal filament; arrowhead putative link between cp and acorn. J*. Coelomomyces intractyoplasmic axoneme (A) doublets with arms and spokes and cp. K. Catenochytridium hemicysti (Chytridiomycetes: Cladochytriales) from Barr et al. ( fig. 24). Type Ia TZ with TP/axosome (ax/TP) close to acorn) and distal TH with central pair (cp) within it; Y dense Y-link zone extended as distal sleeve around doublets; if arrows mark ends of C-tubules old TP label marks a distal centriolar plate. L. Phalansterium digitatum (Amoebozoa) from Hibberd ( Fig. 12) by permission; concentric rings X, Y, Z link pericentriolar fan mts. L' Olpidium brassicae slender ring linked to A-tubule feet proximal to TP; from Lange and Olson ( fig. 14).M. Caulochytrium protostelioides (Chytridiomycetes) TS through dense distal part of TFs including acorn-V and probably also upper part of underlying centriolar (not TZ) 'terminal plate'; from Powell ( fig. 13) by permission. N. Monosiga ovata (Choanoflagellatea) TS of proximal end of anterior ciliated centriole with radiating mts; arrows show circumferential linkers; from Karpov ( fig. 5a) by permission. O. P. Caulochytrium protostelioides (Chytridiomycetes) from Powell ( figs 11, 14) by permission. O. LS of centriole and proximal type II TZ showing spiral fibre (arrows) and acorn-complex overlying dense centriolar 'terminal' plate ('TP'; the more distal TZ TP is not shown). P. TS of proximal TZ with spiral fibre and dense A-tubule feet. Q. Olpidium brassicae ciliated centriole LS from Lange and Olson ( fig. 1) by permission; sf level of spiral fibre/circular filament in L'; a level of acorn TS in Fig. 15Q; arrow distal end of C tubule. R, S, U-V. Polyphlyctis willoughbyi (Chytridiomycetes) from Letcher and Powell ( figs 5A, L-N, 6A). R, S. Type Ib TZ; LSs through ciliary plug (FP) and centriole (K). T-V. consecutive sections through TZ base (right) and barren centriole (left). T. base of plug (p). U. right centriole TP with dense central zone (arrow) and top of barren centriole (bc). V. bc (cartwheel zone); right centriole with acorn lumenal filament between doublets 2, 7. W, X. Allochytridium luteum (Chytridiomycetes) from Barr and Désaulniers ( figs 22, 23) by permission. W. arrows mark rods supporting sleeve around doublets distal to TZ. X. arrows mark basal sleeve around doublets, arrowhead TH. Y. Allochytridium expandens from Barr ( fig. 33) by permission; short arrow marks Y-link zone sleeve around doublets, long arrow basal cylinder/TH. Z-c. Paramecium tetraurelia (Alveolata: Ciliophora) from Dute and Kung ( figs 2, 3, 10, by permission. Z. TZ fixed directly in glutaraldehyde, then OsO4, in LS shows one mt of cp attached to curved thin axosomal plate (thin arrow) connected by granules to thick central zone of curved TP. Paired arrows mark plaque and bracket necklace zones; asterisks mark loose ring linked to doublets distal to TP. a. TS at level of single mt attached to axosome. b. TS at TP level showing its outer ring attached to doublets, dense central thickening (A), and thinner intermediate lattice. c. incubation in polycationic ferritin solution before fixation (to label surface anionic sites: arrowheads) breaks cp from axosome, allowing TP to flatten in LS. d. Hemimastix amphikineta (Hemimastigophora) from Foissner and Foissner ( fig. 58) by permission. e. Putative acorn lumenal filament in Rhesus monkey oviduct centriole from Anderson ( fig. 1c) by permission. f. Coelomomyces punctatus (Allomycetes: Blastocladiales) from Martin ( fig. 12) by permission; zoospore centriole (K) attached basally to nucleus (N) and laterally to mitochondrial envelope (m); cartwheel hub (H) extends throughout centriole to putative acorn (a); arrowhead marks granule at base of one cp mt that may be part of connector to acorn complex; short arrow marks possible tenuous relics of TP linking cp base to doublets; asterisks mark A-tubule feet on doublets opposite cp base
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