Troponin I controls ovulatory contraction of non-striated actomyosin networks in the C. elegans somatic gonad

Abstract The tra-1 gene is a terminal regulator of somatic sex in Caenorhabditis elegans: high tra-1 activity elicits female development, low tra-1 activity elicits male development. To investigate the function and evolution of tra-1, we examined the tra-1 gene from the closely related nematode C. briggsae. Ce-tra-1 and Cb-tra-1 are unusually divergent. Each gene generates two transcripts, but only one of these is present in both species. This common transcript encodes TRA-1A, which shows only 44% amino acid identity between the species, a figure much lower than that for previously compared genes. A Cb-tra-1 transgene rescues many tissues of tra-1(nul1) mutants of C. elegans but not the somatic gonad or germ line. This transgene also causes nongonadal feminization of XO animals, indicating incorrect sexual regulation. Alignment of Ce-TRA-1A and Cb-TRA-1A defines several conserved regions likely to be important for tra-1 function. The phenotypic differences between Ce-tra-1(null) mutants rescued by Cb-tra-1 transgenes and wild-type C. elegans indicate significant divergence of regulatory regions. These molecular and functional studies suggest that evolution of sex determination in nematodes is rapid and genetically complex.

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lin-35/Rb and xnp-1/ATR-X function redundantly to control somatic gonad development in C. elegans

Developmental Biology ◽

10.1016/j.ydbio.2004.06.009 ◽

2004 ◽

Vol 273 (2) ◽

pp. 335-349 ◽

Cited By ~ 23

Author(s):

Aaron M. Bender ◽

Orion Wells ◽

David S. Fay

Keyword(s):

Gonad Development ◽

C Elegans ◽

Somatic Gonad

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hlh-12, a gene that is necessary and sufficient to promote migration of gonadal regulatory cells in C. elegans, evolved within the Caenorhabditis clade

Genetics ◽

10.1093/genetics/iyab127 ◽

2021 ◽

Author(s):

Hana E Littleford ◽

Karin Kiontke ◽

David H A Fitch ◽

Iva Greenwald

Keyword(s):

Ectopic Expression ◽

Morphological Diversity ◽

Nematode Species ◽

Bhlh Protein ◽

Vulval Development ◽

C Elegans ◽

Form And Function ◽

Somatic Gonad ◽

And Function ◽

Necessary And Sufficient

Abstract Specialized cells of the somatic gonad primordium of nematodes play important roles in the final form and function of the mature gonad. C. elegans hermaphrodites are somatic females that have a two-armed, U-shaped gonad that connects to the vulva at the midbody. The outgrowth of each gonad arm from the somatic gonad primordium is led by two female Distal Tip Cells (fDTC), while the Anchor Cell (AC) remains stationary and central to coordinate uterine and vulval development. The bHLH protein HLH-2 and its dimerization partners LIN-32 and HLH-12 had previously been shown to be required for fDTC specification. Here, we show that ectopic expression of both HLH-12 and LIN-32 in cells with AC potential transiently transforms them into fDTC-like cells. Furthermore, hlh-12 was known to be required for the fDTCs to sustain gonad arm outgrowth. Here, we show that ectopic expression of HLH-12 in the normally stationary AC causes displacement from its normal position, and that displacement likely results from activation of the leader program of fDTCs because it requires genes necessary for gonad arm outgrowth. Thus, HLH-12 is both necessary and sufficient to promote gonadal regulatory cell migration. As differences in female gonadal morphology of different nematode species reflect differences in the fate or migratory properties of the fDTCs or of the AC, we hypothesized that evolutionary changes in the expression of hlh-12 may underlie evolution of such morphological diversity. However, we were unable to identify an hlh-12 ortholog outside of Caenorhabditis. Instead, by performing a comprehensive phylogenetic analysis of all Class II bHLH proteins in multiple nematode species, we found that HLH-12 evolved within the Caenorhabditis clade, possibly by duplicative transposition of hlh-10. Our analysis suggests that control of gene regulatory hierarchies for gonadogenesis can be remarkably plastic during evolution without adverse phenotypic consequence.

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Mutations that Affect Channel Opening of Innexin Hemichannels in the C. elegans Gonad

10.20944/preprints202011.0151.v1 ◽

2020 ◽

Author(s):

Todd Starich ◽

David Greenstein

Keyword(s):

Cell Proliferation ◽

Gap Junctions ◽

Germ Cell ◽

Structural Model ◽

Loss Of Function ◽

C Elegans ◽

Somatic Gonad ◽

Channel Opening ◽

Germline Proliferation ◽

Germ Cell Proliferation

In C. elegans, gap junctions couple cells of the somatic gonad with the germline to support germ cell proliferation and gametogenesis. We previously characterized a strong loss-of-function mutation (T239I) affecting the second extracellular loop (EL2) of the somatic INX-8 hemichannel subunit. These mutant hemichannels form non-functional gap junctions with germline-expressed innexins. Here we describe the characterization of mutations that restore germ cell proliferation in the T239I EL2 mutant background. We recovered seven intragenic mutations located in diverse domains of INX-8 but not the EL domains. These second-site mutations compensate for the original channel defect to varying degrees, from nearly complete wild-type rescue, to partial rescue of germline proliferation. One suppressor mutation (E350K) supports the innexin cryo-EM structural model that the channel pore opening is surrounded by a cytoplasmic dome. Two suppressor mutations (S9L and I36N) may form leaky hemichannels that support germline proliferation but cause the demise of somatic sheath cells. Phenotypic analyses of three other suppressors reveal an equivalency in the rescue of germline proliferation and comparable delays in gametogenesis but a graded rescue of fertility. These latter mutations may be useful to probe interactions with the biochemical pathways that produce the molecules transiting through soma-germline gap junctions.

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A normally attractive cell interaction is repulsive in two C. elegans mesodermal cell migration mutants

Development ◽

10.1242/dev.113.3.797 ◽

1991 ◽

Vol 113 (3) ◽

pp. 797-803 ◽

Cited By ~ 4

Author(s):

M.J. Stern ◽

H.R. Horvitz

Keyword(s):

Cell Migration ◽

Caenorhabditis Elegans ◽

Premature Termination ◽

Cell Interaction ◽

Egg Laying ◽

Wild Type ◽

Mesodermal Cell ◽

C Elegans ◽

Somatic Gonad ◽

Sex Myoblasts

In wild-type Caenorhabditis elegans hermaphrodites, two bilaterally symmetric sex myoblasts (SMs) migrate anteriorly to flank the precise center of the gonad, where they divide to generate the muscles required for egg laying (J. E. Sulston and H. R. Horvitz (1977) Devl Biol. 56, 110–156). Although this migration is largely independent of the gonad, a signal from the gonad attracts the SMs to their precise final positions (J. H. Thomas, M. J. Stern and H. R. Horvitz (1990) Cell 62, 1041–1052). Here we show that mutations in either of two genes, egl-15 and egl-17, cause the premature termination of the migrations of the SMs. This incomplete migration is caused by the repulsion of the SMs by the same cells in the somatic gonad that are the source of the attractive signal in wild-type animals.

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The evolution of cell lineage in nematodes

Development ◽

10.1242/dev.1994.supplement.85 ◽

1994 ◽

Vol 1994 (Supplement) ◽

pp. 85-95

Author(s):

Ralf J. Sommer ◽

Lynn K. Carta ◽

Paul W. Sternberg

Keyword(s):

Cell Lineage ◽

Experimental System ◽

Nematode Species ◽

Cell Fates ◽

Equivalence Group ◽

Vulval Development ◽

C Elegans ◽

Somatic Gonad ◽

Vulval Precursor Cell ◽

P Cells

The invariant development of free-living nematodes combined with the extensive knowledge of Caenorhabditis elegans developmental biology provides an experimental system for an analysis of the evolution of developmental mechanisms. We have collected a number of new nematode species from soil samples. Most are easily cultured and their development can be analyzed at the level of individual cells using techniques standard to Caenorhabditis. So far, we have focused on differences in the development of the vulva among species of the families Rhabditidae and Panagrolaimidae. Preceding vulval development, twelve Pn cells migrate into the ventral cord and divide to produce posterior daughters [Pn.p cells] whose fates vary in a position specific manner [from P1.p anterior to P12.p posterior]. In C. elegans hermaphrodites, P(3-8).p are tripotent and form an equivalence group. These cells can express either of two vulval fates (1° or 2°) in response to a signal from the anchor cell of the somatic gonad, or a non-vulval fate (3°), resulting in a 3°-3°-2°-1°-2°-3° pattern of cell fates. Evolutionary differences in vulval development include the number of cells in the vulval equivalence group, the number of 1° cells, the number of progeny generated by each vulval precursor cell, and the position of VPCs before morphogenesis. Examples of three Rhabditidae genera have a posterior vulva in the position of P9-P11 ectoblasts. In Cruznema tripartitum, P(5-7).p form the vulva as in Caenorhabditis, but they migrate posteriorly before dividing. Induction occurs after the gonad grows posteriorly to the position of P(5-7).p cells. In two other species, Mesorhabditis sp. PS 1179 and Teratorhabditis palmarum, we have found changes in induction and competence with respect to their presumably more C. elegans-like ancestor. In Mesorhabditis, P(5-7).p form the vulva after migrating to a posterior position. However, the gonad is not required to specify the pattern of cell fates 3°-2°-1°-2°-3°. Moreover, the Pn.p cells are not equivalent in their potentials to form the vulva. A regulatory constraint in this family thus forces the same set of precursors to generate the vulva, rather than more appropriately positioned Pn.p cells.

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Regulation of Actin Dynamics in the C. elegans Somatic Gonad

Journal of Developmental Biology ◽

10.3390/jdb7010006 ◽

2019 ◽

Vol 7 (1) ◽

pp. 6 ◽

Cited By ~ 5

Author(s):

Charlotte Kelley ◽

Erin Cram

Keyword(s):

Reproductive System ◽

Cell Types ◽

Actin Dynamics ◽

Entry And Exit ◽

Cell Type ◽

C Elegans ◽

Type Study ◽

Somatic Gonad ◽

Uterus Contraction

The reproductive system of the hermaphroditic nematode C. elegans consists of a series of contractile cell types—including the gonadal sheath cells, the spermathecal cells and the spermatheca–uterine valve—that contract in a coordinated manner to regulate oocyte entry and exit of the fertilized embryo into the uterus. Contraction is driven by acto-myosin contraction and relies on the development and maintenance of specialized acto-myosin networks in each cell type. Study of this system has revealed insights into the regulation of acto-myosin network assembly and contractility in vivo.

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INF2- and FHOD-related formins promote ovulation in the somatic gonad of C. elegans

Cytoskeleton ◽

10.1002/cm.21345 ◽

2016 ◽

Vol 73 (12) ◽

pp. Spc1-Spc1

Author(s):

Anna Hegsted ◽

Forrest A. Wright ◽

SarahBeth Votra ◽

David Pruyne

Keyword(s):

C Elegans ◽

Somatic Gonad

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hecd-1 Modulates Notch Activity in Caenorhabditis elegans

G3 Genes|Genome|Genetics ◽

10.1534/g3.114.015321 ◽

2015 ◽

Vol 5 (3) ◽

pp. 353-359 ◽

Cited By ~ 3

Author(s):

Yunting Chen ◽

Iva Greenwald

Keyword(s):

Quality Control ◽

Caenorhabditis Elegans ◽

Cell Fate ◽

Germ Line ◽

Notch Pathway ◽

Cell Fate Decisions ◽

Notch Activity ◽

C Elegans ◽

Somatic Gonad ◽

Constitutively Active

Abstract Notch is a receptor that mediates cell–cell interactions that specify binary cell fate decisions in development and tissue homeostasis. Inappropriate Notch signaling is associated with cancer, and mutations in Notch pathway components have been associated with developmental diseases and syndromes. In Caenorhabditis elegans, suppressors of phenotypes associated with constitutively active LIN-12/Notch have identified many conserved core components and direct or indirect modulators. Here, we molecularly identify sel(ar584), originally isolated as a suppressor of a constitutively active allele of lin-12. We show that sel(ar584) is an allele of hecd-1, the ortholog of human HECDT1, a ubiquitin ligase that has been implicated in several different mammalian developmental events. We studied interactions of hecd-1 with lin-12 in the somatic gonad and with the other C. elegans Notch gene, glp-1, in the germ line. We found that hecd-1 acts as a positive modulator of lin-12/Notch activity in a somatic gonad context—the original basis for its isolation—but acts autonomously as a negative modulator of glp-1/Notch activity in the germ line. As the yeast ortholog of HECD-1, Ufd4p, has been shown to function in quality control, and C. elegans HECD-1 has been shown to affect mitochondrial maintenance, we propose that the different genetic interactions between hecd-1 and Notch genes we observed in different cell contexts may reflect differences in quality control regulatory mechanisms or in cellular metabolism.

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