Functional morphology and evolutionary origin of the three-part pharynx in nematodes

Lieven, Alexander Fürst von

doi:10.1078/0944-2006-00115

Cited by 22 publications

(22 citation statements)

References 11 publications

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“…We attempted laser ablations in T. lirellus, but were unsuccessful due to technical problems (see Materials and methods). Further, other species that are closely related to the free-living soil nematodes, such as the Plectidae (Blaxter et al, 1998), do not have peristalsis and do not have three-part pharynxes (von Lieven, 2003;J.-T. A. Chiang, unpublished), and were therefore not useful as outgroups. Thus, determination of the ancestral functions of pharyngeal neurons await the availability of more favorable outgroup species.…”

Section: Discussionmentioning

confidence: 99%

“…Additionally, to help determine the ancestral pattern of pharyngeal behaviors, we observed a close relative, Teratocephalus lirellus, as the outgroup species (Blaxter et al, 1998). Anatomically, the pharynxes in all of these species were similarly divided into the corpus, isthmus and terminal bulb (albeit with minor anatomical variations; see Chitwood and Chitwood, 1974;Maggenti, 1981;von Lieven, 2003;von Lieven and Sudhaus, 2000;Zhang and Baldwin, 1999). Yet behaviorally, each family, as well as T. lirellus, exhibited significant differences.…”

Section: The Isthmus and Terminal Bulb Evolved Differences In Their Smentioning

confidence: 99%

“…In particular, C. elegans is a free-living soil nematode (nematodes can be classified ecologically as free-living or parasitic, and soil-dwelling or aquatic). Characterization of pharyngeal behaviors in other freeliving soil nematodes has been rather limited, and generally did not examine the regulatory functions of pharyngeal neurons (Doncaster, 1962;Mapes, 1965;von Lieven, 2003).…”

Section: Introductionmentioning

confidence: 99%

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Evolution of pharyngeal behaviors and neuronal functions in free-living soil nematodes

Chiang

Steciuk

Shtonda

et al. 2006

Journal of Experimental Biology

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SUMMARY To explore the use of Caenorhabditis elegans and related nematodes for studying behavioral evolution, we conducted a comparative study of pharyngeal behaviors and neuronal regulation in free-living soil nematodes. The pharynx is divided into three parts: corpus, isthmus and terminal bulb,and pharyngeal behaviors consist of stereotyped patterns of two motions:pumping and peristalsis. Based on an outgroup species, Teratocephalus lirellus, the ancestral pattern of pharyngeal behaviors consisted of corpus pumping, isthmus peristalsis and terminal bulb pumping, each occurring independently. Whereas corpus pumping remained largely conserved, isthmus and terminal bulb behaviors evolved extensively from the ancestral pattern in the four major free-living soil nematode families. In the Rhabditidae family,which includes Caenorhabditis elegans, the anterior isthmus switched from peristalsis to pumping, and anterior isthmus and terminal bulb pumping became coupled to corpus pumping. In the Diplogasteridae family, the terminal bulb switched from pumping to peristalsis, and isthmus and terminal bulb became coupled for peristalsis. In the Cephalobidae family, isthmus peristalsis and terminal bulb pumping became coupled. And in the Panagrolaimidae family, the posterior isthmus switched from peristalsis to pumping. Along with these behavioral changes, we also found differences in the neuronal regulation of isthmus and terminal bulb behaviors. M2, a neuron that has no detectable function in C. elegans, stimulated anterior isthmus peristalsis in the Panagrolaimidae. Further, M4 was an important excitatory neuron in each family, but its exact downstream function varied between stimulation of posterior isthmus peristalsis in the Rhabditidae,isthmus/terminal bulb peristalsis in the Diplogasteridae, isthmus peristalsis and terminal bulb pumping in the Cephalobidae, and posterior isthmus/terminal bulb pumping in the Panagrolaimidae. In the Rhabditidae family, although M4 normally has no effect on the terminal bulb, we found that M4 can stimulate the terminal bulb in C. elegans if the Ca2+-activated K+ channel SLO-1 is inactivated. C. elegans slo-1 mutants have generally increased neurotransmission, and in slo-1 mutants we found novel electropharyngeogram signals and increased pumping rates that suggested activation of M4-terminal bulb synapses. Thus, we suggest that the lack of M4-terminal bulb stimulations in C. elegans and the Rhabditidae family evolved by changes in synaptic transmission. Altogether, we found behavioral and neuronal differences in the isthmus and terminal bulb of free-living soil nematodes, and we examined potential underlying mechanisms of one aspect of M4 evolution. Our results suggest the utility of Caenorhabditis elegans and related nematodes for studying behavioral evolution.

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Section: Discussionmentioning

confidence: 99%

Section: The Isthmus and Terminal Bulb Evolved Differences In Their Smentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Evolution of pharyngeal behaviors and neuronal functions in free-living soil nematodes

Chiang

Steciuk

Shtonda

et al. 2006

Journal of Experimental Biology

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“…These ridges are completely disorganized in eat-17 mutants ( Figure 1B). In wild-type worms, the grinder is composed of three separate plates that are arranged in approximate triradial symmetry (Albertson and Thomson 1976;von Lieven 2003). These plates are secreted from the apical surfaces of pharyngeal muscle cells pm6 and pm7 in the terminal bulb (Albertson and Thomson 1976).…”

Section: Eat-17 Mutants Are Eat Due To Defects In Grinder Formationmentioning

confidence: 99%

The Jaw of the Worm: GTPase-activating Protein EAT-17 Regulates Grinder Formation in Caenorhabditis elegans

et al. 2013

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Constitutive transport of cellular materials is essential for cell survival. Although multiple small GTPase Rab proteins are required for the process, few regulators of Rabs are known. Here we report that EAT-17, a novel GTPase-activating protein (GAP), regulates RAB-6.2 function in grinder formation in Caenorhabditis elegans. We identified EAT-17 as a novel RabGAP that interacts with RAB-6.2, a protein that presumably regulates vesicle trafficking between Golgi, the endoplasmic reticulum, and plasma membrane to form a functional grinder. EAT-17 has a canonical GAP domain that is critical for its function. RNA interference against 25 confirmed and/or predicted RABs in C. elegans shows that RNAi against rab-6.2 produces a phenotype identical to eat-17. A directed yeast twohybrid screen using EAT-17 as bait and each of the 25 RAB proteins as prey identifies RAB-6.2 as the interacting partner of EAT-17, confirming that RAB-6.2 is a specific substrate of EAT-17. Additionally, deletion mutants of rab-6.2 show grinder defects identical to those of eat-17 loss-of-function mutants, and both RAB-6.2 and EAT-17 are expressed in the terminal bulb of the pharynx where the grinder is located. Collectively, these results suggest that EAT-17 is a specific GTPase-activating protein for RAB-6.2. Based on the conserved function of Rab6 in vesicular transport, we propose that EAT-17 regulates the turnover rate of RAB-6.2 activity in cargo trafficking for grinder formation. C ELLS constitutively transport newly synthesized proteins, lipids, and other molecules to their periphery through vesicle trafficking. As the process is conserved from yeast to humans, it is essential for the function and survival of cells. Rab GTPases are small GTP binding proteins that regulate the transport of vesicles between different compartments of the cell (Zerial and McBride 2001;Jordens et al. 2005;Grosshans et al. 2006). Rab6's are localized to Golgi membranes to mark and target both anterograde cargos from Golgi to post-Golgi compartments (such as the plasma membrane) and retrograde cargos from early/recycling endosomes to Golgi and the endoplasmic reticulum (Jasmin et al. 1992;Martinez et al. 1994Martinez et al. , 1997Girod et al. 1999;Opdam et al. 2000;Del Nery et al. 2006). For fast turnover, Rabs require guanine nucleotide exchange factors (Rab GEFs) for activation and GTPase-activating proteins (Rab GAPs) to turn off activity (Grosshans et al. 2006). While the role of Rab6 in membrane trafficking is well established, very few GAPs or GEFs for Rab6 have been identified; thus their physiological importance is largely unknown. The physiological roles of RabGAPs were addressed only recently in flies (Houalla et al. 2010;Uytterhoeven et al. 2011) and worms (Chotard et al. 2010). In those cases, removing the function of the RabGAPs produced phenotypes almost identical to those of removing the relevant Rabs, showing the fundamental roles of RabGAPs in modulating Rab functions. Currently, the only identified GAP for Rab6 is GAPCenA in humans,...

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“…On such occasions it could be observed that O. attenuata n. sp. lacks the pharyngeal pocket valve described in Acrobeles and Poikilolaimus by Fürst von Lieven (2003b). Kinetoplastid protists of the same kind as observed in Oigolaimella also occurred in the guts of specimens of Diplogasteroides spengelii isolated from sap flux of an elm tree in Berlin, Germany.…”

Section: Flagellatesmentioning

confidence: 80%

Description of Oigolaimella attenuata n. sp. (Diplogastridae) associated with termites (Reticulitermes) and remarks on life cycle, giant spermatozoa, gut-inhabiting flagellates and other associates

Lieven

Sudhaus

2008

Nematol

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A new species of the diplogastrid genus Oigolaimella is described in colonies of termites belonging to the genus Reticulitermes from Corsica (France) and USA. Oigolaimella attenuata n. sp. males can be recognised by the conspicuous length of the ventral unkeeled part of the otherwise keeled gubernaculum and, in contrast to the other members of the genus, the fact that the lateral field of both adult stages is marked by a single line. A diagnostic key for the five species of Oigolaimella is presented. Life cycle and development, including spermiogenesis, sperm transfer, sperm competition and fertilisation are described in detail. Some interesting aberrations of the reproductive system are documented. The new species uses the preoral cavities of the termites for internal phoresis and is associated with non-pathogenic gut-inhabiting flagellates of the taxon Kinetoplastida. The heads of 76 of 117 examined termites were infested with dauer juveniles of O. attenuata n. sp. with an average of 6.4 nematodes per termite. Six additional nematode species were isolated from the bodies of the termites, particularly a species of Pristionchus and, for the first time, Halicephalobus sp., Mesorhabditis spiculigera and Rhabditella axei. Rhabpanus ossiculum was isolated from termite-inhabited wood from Corsica, the first such detection in Europe. In the course of our discussion of the literature on termite-associated nematodes, we propose the new combination Pristionchus formosianus (Poinar, Meikle & Mercadier, 2006) n. comb. (= Chroniodiplogaster formosiana).

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Functional morphology and evolutionary origin of the three-part pharynx in nematodes

Cited by 22 publications

References 11 publications

Evolution of pharyngeal behaviors and neuronal functions in free-living soil nematodes

Evolution of pharyngeal behaviors and neuronal functions in free-living soil nematodes

The Jaw of the Worm: GTPase-activating Protein EAT-17 Regulates Grinder Formation in Caenorhabditis elegans

Description of Oigolaimella attenuata n. sp. (Diplogastridae) associated with termites (Reticulitermes) and remarks on life cycle, giant spermatozoa, gut-inhabiting flagellates and other associates

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