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 ◽  
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.

The evolution of cell lineage in nematodes

Development ◽  
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.

scholarly journals A bHLH Code for Sexually Dimorphic Form and Function of the C. elegans Somatic Gonad

2017 ◽  
Vol 27 (12) ◽  
pp. 1853-1860.e5 ◽  
Author(s):  
Maria D. Sallee ◽  
Hana E. Littleford ◽  
Iva Greenwald
Keyword(s):  
Sexually Dimorphic ◽  
C Elegans ◽  
Form And Function ◽  
Somatic Gonad ◽  
And Function

scholarly journals Mitochondrial translation and dynamics synergistically extend lifespan in C. elegans through HLH-30

2019 ◽  
Author(s):  
Yasmine J. Liu ◽  
Rebecca L. McIntyre ◽  
Georges E. Janssens ◽  
Evan G. Williams ◽  
Jiayi Lan ◽  
...  
Keyword(s):  
Synergistic Effect ◽  
Mitochondrial Network ◽  
Mitochondrial Translation ◽  
C Elegans ◽  
Form And Function ◽  
Unfolded Protein ◽  
Lysosome Biogenesis ◽  
And Function ◽  
Protein Response ◽  
Mitochondrial Unfolded Protein Response

AbstractMitochondrial form and function, such as translation, are closely interlinked in homeostasis and aging. Inhibiting mitochondrial translation is known to increase lifespan in C. elegans, which is accompanied by a fragmented mitochondrial network. However, the causality between mitochondrial translation and morphology in longevity remains uncharacterized. Here, we show in C. elegans that disrupting mitochondrial network homeostasis by either blocking fission or fusion synergizes with the reduced mitochondrial translation to substantially prolong lifespan and stimulate stress response such as the mitochondrial unfolded protein response, UPRMT. Conversely, immobilizing the mitochondrial network through a simultaneous abrogation of fission and fusion reverses the lifespan increase induced by mitochondrial translation inhibition. Furthermore, we find that the synergistic effect of inhibiting both mitochondrial translation and dynamics on lifespan, despite stimulating UPRMT, does not require it. Instead, this lifespan-extending synergy is exclusively dependent on the lysosome biogenesis and autophagy transcription factor HLH-30/TFEB. Altogether, our study reveals the mechanistic connections between mitochondrial translation and dynamics in regulating longevity.SUMMARYMitochondrial form and function are intimately intertwined. Liu et al. find the synergistic effect of inhibiting both mitochondrial translation and dynamics on lifespan. This synergy is dependent on the induction of lysosome biogenesis through the nuclear localization of HLH-30.

scholarly journals Mitochondrial translation and dynamics synergistically extend lifespan in C. elegans through HLH-30

2020 ◽  
Vol 219 (6) ◽  
Author(s):  
Yasmine J. Liu ◽  
Rebecca L. McIntyre ◽  
Georges E. Janssens ◽  
Evan G. Williams ◽  
Jiayi Lan ◽  
...  
Keyword(s):  
Mitochondrial Dynamics ◽  
Mitochondrial Network ◽  
Mitochondrial Translation ◽  
C Elegans ◽  
Form And Function ◽  
Unfolded Protein ◽  
Lysosome Biogenesis ◽  
And Function ◽  
Protein Response ◽  
Mitochondrial Unfolded Protein Response

Mitochondrial form and function are closely interlinked in homeostasis and aging. Inhibiting mitochondrial translation is known to increase lifespan in C. elegans, and is accompanied by a fragmented mitochondrial network. However, whether this link between mitochondrial translation and morphology is causal in longevity remains uncharacterized. Here, we show in C. elegans that disrupting mitochondrial network homeostasis by blocking fission or fusion synergizes with reduced mitochondrial translation to prolong lifespan and stimulate stress response such as the mitochondrial unfolded protein response, UPRMT. Conversely, immobilizing the mitochondrial network through a simultaneous disruption of fission and fusion abrogates the lifespan increase induced by mitochondrial translation inhibition. Furthermore, we find that the synergistic effect of inhibiting both mitochondrial translation and dynamics on lifespan, despite stimulating UPRMT, does not require it. Instead, this lifespan-extending synergy is exclusively dependent on the lysosome biogenesis and autophagy transcription factor HLH-30/TFEB. Altogether, our study reveals the mechanistic crosstalk between mitochondrial translation, mitochondrial dynamics, and lysosomal signaling in regulating longevity.

scholarly journals Reproductive Ontogeny and the Evolution of Morphological Diversity in Conifers and Other Plants

2019 ◽  
Vol 59 (3) ◽  
pp. 548-558 ◽  
Author(s):  
A B Leslie ◽  
J M Losada
Keyword(s):  
Morphological Evolution ◽  
Morphological Diversity ◽  
Developmental Rate ◽  
Reproductive Organs ◽  
Developmental Trajectory ◽  
Evolutionary Significance ◽  
Developmental Patterns ◽  
Functional Roles ◽  
Form And Function ◽  
And Function

Abstract Biologists often study morphological evolution through form and function relationships. But biological structures can perform multiple functional roles, complicating efforts to understand the evolutionary significance of any one relationship. Plant reproductive organs perform multiple roles in a sequence, however, which provides a unique opportunity to understand how structures evolve to meet multiple functional demands. Using conifers as a study group, we discuss how a shared developmental trajectory links the performance of sequential functional roles. Variation in development among lineages can underlie morphological diversity; pollination-stage seed cones in Pinaceae conifers function similarly but show diverse forms reflecting differences in developmental rate. As cones develop further, the morphologies that they use to perform later functional roles are influenced by the specific developmental patterns used to meet earlier demands, which may ultimately limit morphological diversity. However, we also show how selective pressures relating to the final functional stage (seed dispersal) may influence cone anatomy and morphology over all previous stages, highlighting the complex linkages among form, function, and development. We end by discussing the potential relationships between functional ontogeny and morphological disparity in plant reproductive structures more broadly, suggesting that the complex functional roles associated with seed plant reproduction probably underlie the high disparity in this group.

Form and function: structural analysis in evolutionary morphology

Paleobiology ◽  
1981 ◽  
Vol 7 (4) ◽  
pp. 430-442 ◽  
Author(s):  
George V. Lauder
Keyword(s):  
Structural Complexity ◽  
Morphological Diversity ◽  
Structural Features ◽  
Constrained Systems ◽  
Hierarchical Organization ◽  
Evolutionary Morphology ◽  
Form And Function ◽  
Historical Factors ◽  
Functional Patterns ◽  
And Function

A theoretical approach to the analysis of historical factors (Raup 1972) in evolutionary morphology is presented which addresses transformational hypotheses about structural systems. This (structural) approach to testing historical hypotheses about phylogenetic constraints on form and function and structural and functional versatility involves (1) the reconstruction of nested sets of structural features in monophyletic taxa, (2) the use of general or emergent organizational properties of structural and functional systems (as opposed to uniquely derived morphological features), and (3) the comparative examination of the consequences for structural and functional diversity of these general features in related monophyletic taxa.Three examples of emergent organizational properties are considered: structural complexity, repetition of parts, and the decoupling of primitively constrained systems. Two classes of hypotheses about the evolution of design are proposed. Transformational hypotheses concern historical pathways of change in form as a consequence of general organizational features which are primitive for a lineage. Relational hypotheses involve correlations between structure-function networks primitive for a clade and morphological diversity both between and within terminal taxa. To the extent that transformational and relational hypotheses about form are corroborated, they provide evidence of underlying regularity in the transformation of organic design that may be a consequence of the hierarchical organization of structural and functional patterns in organisms.

scholarly journals The C. elegans even-skipped homologue, vab-7, specifies DB motoneurone identity and axon trajectory

Development ◽  
2002 ◽  
Vol 129 (4) ◽  
pp. 853-862 ◽  
Author(s):  
Behrooz Esmaeili ◽  
Jennifer M. Ross ◽  
Cara Neades ◽  
David M. Miller ◽  
Julie Ahringer
Keyword(s):  
Ectopic Expression ◽  
Specific Gene ◽  
Locomotory Activity ◽  
Homeodomain Protein ◽  
Independent Manner ◽  
C Elegans ◽  
Parallel Pathway ◽  
And Function ◽  
Work Supports ◽  
Repressor Activity

Locomotory activity is defined by the specification of motoneurone subtypes. In the nematode, C. elegans, DA and DB motoneurones innervate dorsal muscles and function to induce movement in the backwards or forwards direction, respectively. These two neurone classes express separate sets of genes and extend axons with oppositely directed trajectories; anterior (DA) versus posterior (DB). The DA-specific homeoprotein UNC-4 interacts with UNC-37/Groucho to repress the DB gene, acr-5 (nicotinic acetylcholine receptor subunit). We show that the C. elegans even-skipped-like homoedomain protein, VAB-7, coordinately regulates different aspects of the DB motoneurone fate, in part by repressing unc-4. Wild-type DB motoneurones express VAB-7, have posteriorly directed axons, express ACR-5 and lack expression of the homeodomain protein UNC-4. In a vab-7 mutant, ectopic UNC-4 represses acr-5 and induces an anteriorly directed DB axon trajectory. Thus, vab-7 indirectly promotes DB-specific gene expression and posteriorly directed axon outgrowth by preventing UNC-4 repression of DB differentiation. Ectopic expression of VAB-7 also induces DB traits in an unc-4-independent manner, suggesting that VAB-7 can act through a parallel pathway. This work supports a model in which a complementary pair of homeodomain transcription factors (VAB-7 and UNC-4) specifies differences between DA and DB neurones through inhibition of the alternative fates. The recent findings that Even-skipped transcriptional repressor activity specifies neurone identity and axon guidance in the mouse and Drosophila motoneurone circuit points to an ancient origin for homeoprotein-dependent mechanisms of neuronal differentiation in the metazoan nerve cord.

LIN-12 protein expression and localization during vulval development in C. elegans

Development ◽  
1998 ◽  
Vol 125 (16) ◽  
pp. 3101-3109 ◽  
Author(s):  
D. Levitan ◽  
I. Greenwald
Keyword(s):  
Cell Fate ◽  
Feedback Mechanism ◽  
Precursor Cell ◽  
Vulval Development ◽  
Ras Pathway ◽  
Cell Fate Decisions ◽  
C Elegans ◽  
Somatic Gonad ◽  
Multiple Cell ◽  
Vulval Precursor Cell

We have used a LIN-12::GFP fusion protein to examine LIN-12 accumulation during cell fate decisions important for vulval development. During the naturally variable anchor cell (AC)/ventral uterine precursor cell (VU) decision of the somatic gonad, a transcription-based feedback mechanism biases two equivalent cells so that one becomes the AC while the other becomes a VU. LIN-12::GFP accumulation reflects lin-12 transcription: LIN-12::GFP is initially present in both cells, but disappears from the presumptive AC and becomes restricted to the presumptive VU. During vulval precursor cell (VPC) fate determination, six equipotential cells uniformly transcribe lin-12 and have invariant fates that are specified by multiple cell-cell interactions. The pattern of LIN-12::GFP accumulation in VPCs and in the VPC lineages is dynamic and does not always reflect lin-12 transcription. In particular, LIN-12::GFP is expressed initially in all six VPCs, but appears to be reduced specifically in P6.p as a consequence of the activation of the Ras pathway by an EGF-like inductive signal from the AC. We propose that downregulation of LIN-12 stability or translation in response to inductive signalling helps impose a bias on lateral signalling and contributes to the invariant pattern of VPC fates.

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