Hox genes limit germ cell formation in the short germ insect Gryllus bimaculatus

Hox genes are conserved transcription factor-encoding genes that specify the identity of body regions in bilaterally symmetrical animals. In the cricket Gryllus bimaculatus, a member of the hemimetabolous insect group Orthoptera, the induction of a subset of mesodermal cells to form the primordial germ cells (PGCs) is restricted to the second through the fourth abdominal segments (A2 to A4). In numerous insect species, the Hox genes Sex-combs reduced (Scr), Antennapedia (Antp), Ultrabithorax (Ubx), and abdominal-A (abd-A) jointly regulate the identities of middle and posterior body segments, suggesting that these genes may restrict PGC formation to specific abdominal segments in G. bimaculatus. Here we show that reducing transcript levels of some or all of these Hox genes results in supernumerary and/or ectopic PGCs, either individually or in segment-specific combinations, suggesting that the role of these Hox genes is to limit PGC development with respect to their number, segmental location, or both. These data provide evidence of a role for this ancient group of genes in PGC development.

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Hox genes limit germ cell formation in the short germ insect Gryllus bimaculatus

10.1101/419119 ◽

2018 ◽

Author(s):

Austen A. Barnett ◽

Taro Nakamura ◽

Cassandra G. Extavour

Keyword(s):

Hox Genes ◽

Primordial Germ Cells ◽

Cell Formation ◽

Gryllus Bimaculatus ◽

Sex Combs Reduced ◽

Body Regions ◽

Sex Combs ◽

Hemimetabolous Insect ◽

Encoding Genes ◽

Germ Cell Formation

AbstractHox genes are conserved transcription factor-encoding genes that specify the identity of body regions in bilaterally symmetrical animals. In the cricket Gryllus bimaculatus, a member of the hemimetabolous insect group Orthoptera, the induction of a subset of mesodermal cells to form the primordial germ cells (PGCs) is restricted to the second through the fourth abdominal segments (A2-A4). In numerous insect species, the Hox genes Sex-combs reduced (Scr), Antennapedia (Antp), Ultrabithorax (Ubx) and abdominal-A (abd-A) jointly regulate the identities of middle and posterior body segments, suggesting that these genes may restrict PGC formation to specific abdominal segments in G. bimaculatus. Here we show that all of these Hox genes, either individually or in segment-specific combinations, restrict PGC formation. Our data provides evidence for a segmental Hox code used to regulate the placement of PGC formation, reminiscent of the segmental Hox codes used in other arthropod groups to establish other aspects of segmental identity. These data also provide, to our knowledge, the first evidence for this ancient group of genes in determining PGC placement within the context of axial patterning in any animal studied thus far.

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Sequence of the Tribolium castaneum Homeotic Complex: The Region Corresponding to the Drosophila melanogaster Antennapedia Complex

Genetics ◽

10.1093/genetics/160.3.1067 ◽

2002 ◽

Vol 160 (3) ◽

pp. 1067-1074

Author(s):

Susan J Brown ◽

John P Fellers ◽

Teresa D Shippy ◽

Elizabeth A Richardson ◽

Mark Maxwell ◽

...

Keyword(s):

Tribolium Castaneum ◽

Hox Genes ◽

Transcription Unit ◽

Sex Combs Reduced ◽

Sex Combs ◽

Selector Genes ◽

Homeotic Selector Genes ◽

Encoding Genes ◽

Single Cluster ◽

Homeotic Selector

Abstract The homeotic selector genes of the red flour beetle, Tribolium castaneum, are located in a single cluster. We have sequenced the region containing the homeotic selector genes required for proper development of the head and anterior thorax, which is the counterpart of the ANTC in Drosophila. This 280-kb interval contains eight homeodomain-encoding genes, including single orthologs of the Drosophila genes labial, proboscipedia, Deformed, Sex combs reduced, fushi tarazu, and Antennapedia, as well as two orthologs of zerknüllt. These genes are all oriented in the same direction, as are the Hox genes of amphioxus, mice, and humans. Although each transcription unit is similar to its Drosophila counterpart in size, the Tribolium genes contain fewer introns (with the exception of the two zerknüllt genes), produce shorter mRNAs, and encode smaller proteins. Unlike the ANTC, this region of the Tribolium HOMC contains no additional genes.

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Interactions of the TriboliumSex combs reducedandproboscipediaOrthologs in Embryonic Labial Development

Genetics ◽

10.1093/genetics/159.4.1643 ◽

2001 ◽

Vol 159 (4) ◽

pp. 1643-1648 ◽

Cited By ~ 1

Author(s):

Mark A DeCamillis ◽

David L Lewis ◽

Susan J Brown ◽

Richard W Beeman ◽

Robin E Denell

Keyword(s):

Hox Genes ◽

Oncopeltus Fasciatus ◽

Red Flour Beetle ◽

Homeotic Genes ◽

Wild Type ◽

Sex Combs Reduced ◽

Drosophila Embryogenesis ◽

Sex Combs ◽

In The Wild

AbstractThe role of Hox genes in the development of insect gnathal appendages has been examined in three insects: the fruitfly, Drosophila melanogaster; the milkweed bug, Oncopeltus fasciatus; and the red flour beetle, Tribolium castaneum. In each of these organisms, the identity of the labium depends on the homeotic genes Sex combs reduced (Scr) and proboscipedia (pb). Loss of pb function in each of the three insects results in homeotic transformation of the labial appendages to legs. In contrast, loss of Scr function yields a different transformation in each species. Interestingly, mutations in Cephalothorax (Cx), the Tribolium ortholog of Scr, transform the labial appendages to antennae, a result seen in the other insects only when both pb and Scr are removed. We show here that the Tribolium labial appendages also develop as antennae in double mutants. Further, we demonstrate that expression of the Tribolium proboscipedia ortholog maxillopedia (mxp) is greatly reduced or absent in the labium of Cx mutant larvae. Thus, in the wild-type labial segment, Cx function is required (directly or indirectly) for mxp transcription. A similar interaction between Scr and pb during Drosophila embryogenesis has been described recently. Thus, this regulatory paradigm appears to be conserved at least within the Holometabola.

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Functional requirement of gp130-mediated signaling for growth and survival of mouse primordial germ cells in vitro and derivation of embryonic germ (EG) cells

Development ◽

10.1242/dev.122.4.1235 ◽

1996 ◽

Vol 122 (4) ◽

pp. 1235-1242 ◽

Cited By ~ 3

Author(s):

U. Koshimizu ◽

T. Taga ◽

M. Watanabe ◽

M. Saito ◽

Y. Shirayoshi ◽

...

Keyword(s):

Germ Cells ◽

Intracellular Signaling ◽

Primordial Germ Cells ◽

Cell Formation ◽

Embryonic Stem ◽

Oncostatin M ◽

Receptor Complexes ◽

Binding Subunit

Leukemia inhibitory factor (LIF) is a cytokine known to influence proliferation and/or survival of mouse primordial germ cells (PGC) in culture. The receptor complex for LIF comprises LIF-binding subunit and non-binding signal transducer, gp130. The gp130 was originally identified as a signal-transducing subunit of interleukin (IL)-6 and later also found to be a functional component of receptor complexes for other LIF-related cytokines (oncostatin M [OSM], ciliary neurotrophic factor [CNTF] and IL-11). In this study, we have analyzed the functional role of gp130-mediated signaling in PGC growth in vitro. OSM was able to fully substitute for LIF; both cytokines promoted the proliferation of migratory PGC (mPGC) and enhanced the viability of postmigratory (colonizing) PGC (cPGC) when cultured on SI/SI4-m220 cells. Interestingly, IL-11 stimulated mPGC growth comparable to LIF and OSM, but did not affect cPGC survival. IL-6 and CNTF did not affect PGC. In addition, a combination of IL-6 and soluble IL-6 binding subunit (sIL-6R), which is known to activate intracellular signaling via gp130, fully reproduced the LIF action of PGC. Both in the presence and absence of LIF, addition of neutralizing antibody against gp130 in culture remarkably blocked cPGC survival. These results suggest a pivotal role of gp130 in PGC development, especially that it is indispensable for cPGC survival as comparable to the c-KIT-mediated action. We have further demonstrated that a combination of LIF with forskolin or retinoic acid, a potent mitogen for PGC, supported the proliferation of PGC, leading to propagation of the embryonic stem cell-like cells, termed embryonic germ (EG) cells. Since EG cells were also obtained by using OSM or the IL-6/sIL-6R complex in place of LIF, a significant contribution of gp130-mediated signaling in EG cell formation was further suggested.

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Role of the esc+ gene product in ensuring the selective expression of segment-specific homeotic genes in Drosophila

Development ◽

10.1242/dev.76.1.297 ◽

1983 ◽

Vol 76 (1) ◽

pp. 297-331

Author(s):

Gary Struhl

Keyword(s):

Gene Product ◽

The Body ◽

Homeotic Genes ◽

Bithorax Complex ◽

Sex Combs Reduced ◽

Sex Combs ◽

Correct Determination ◽

Correct Expression

The product of the extra sex combs+ (esc+) gene is required during embryogenesis for the correct determination of segments in Drosophila. If this product is absent, most segments develop like the normal eighth abdominal segment. Here, I extend previous results (Struhl, 1981a) showing that this phenotype results in large part from indiscriminate expression of the bithorax-complex genes which are normally active only in particular segments of the thorax and abdomen. In addition, I test whether the esc+ gene product is required for the correct expression of other homeotic genes. First, I have examined two genes of the Antennapedia-complex (Sex combs reduced+ and Antennapedia+): I find that both genes are normally required in only some of the body segments, but that in the absence of the esc+ gene product, both appear to function adventitiously in other segments. Second, comparing esc+ and esc− embryos lacking both these genes as well as the bithorax-complex, I find that additional homeotic genes (possibly those normally involved in specifying head segments) appear to be expressed indiscriminately when the esc+ gene product is absent. Finally, I present evidence that the products of the esc+ gene and the Polycomb+ gene (a second gene required for the correct regulation of the bithorax-complex) act independently. On the basis of these results, I propose a tentative outline of the roles and realms of action of all of these genes.

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Analysis of Drosophila proboscipedia mutant alleles

Genome ◽

10.1139/g03-133 ◽

2004 ◽

Vol 47 (3) ◽

pp. 600-609 ◽

Cited By ~ 6

Author(s):

I Tayyab ◽

H M Hallahan ◽

A Percival-Smith

Keyword(s):

Dna Sequence ◽

Hox Genes ◽

Genetic Interaction ◽

Direct Interaction ◽

Protein Product ◽

Maxillary Palp ◽

Phenotypic Analysis ◽

Sex Combs Reduced ◽

Important Region ◽

Sex Combs

Proboscipedia (PB) is a HOX protein required for adult maxillary palp and proboscis formation. To identify domains of PB important for function, 21 pb point mutant alleles were sequenced. Twelve pb alleles had DNA sequence changes that encode an altered PB protein product. The DNA sequence changes of these 12 alleles fell into 2 categories: missense alleles that effect the PB homeodomain (HD), and nonsense or frameshift alleles that result in C-terminal truncations of the PB protein. The phenotypic analysis of the pb homeobox missense alleles suggests that the PB HD is required for maxillary palp and proboscis development and pb – Sex combs reduced (Scr) genetic interaction. The phenotypic analysis of the pb nonsense or frameshift alleles suggests that the C-terminus is an important region required for maxillary palp and proboscis development and pb–Scr genetic interaction. PB and SCR do not interact directly with one another in a co-immunoprecipitation assay and in a yeast two-hybrid analysis, which suggests the pb–Scr genetic interaction is not mediated by a direct interaction between PB and SCR.Key words: proboscipedia, Sex combs reduced, Hox genes, mutant analysis, Drosophila body plan, appendage development.

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Hox genes mediate the escalation of sexually antagonistic traits in water striders

Biology Letters ◽

10.1098/rsbl.2018.0720 ◽

2019 ◽

Vol 15 (2) ◽

pp. 20180720 ◽

Cited By ~ 2

Author(s):

Antonin Jean Johan Crumière ◽

Abderrahman Khila

Keyword(s):

Sexual Conflict ◽

Hox Genes ◽

Complete Loss ◽

Water Strider ◽

Fitness Costs ◽

Sex Combs Reduced ◽

Hox Gene ◽

Water Striders ◽

Sex Combs ◽

Sex Comb

Sexual conflict occurs when traits favoured in one sex impose fitness costs on the other sex. In the case of sexual conflict over mating rate, the sexes often undergo antagonistic coevolution and escalation of traits that enhance females' resistance to superfluous mating and traits that increase males' persistence. How this escalation in sexually antagonistic traits is established during ontogeny remains unclear. In the water strider Rhagovelia antilleana, male persistence traits consist of sex combs on the forelegs and multiple rows of spines and a thick femur in the rear legs. Female resistance traits consist of a prominent spike-like projection of the pronotum. RNAi knockdown against the Hox gene Sex Combs Reduced resulted in the reduction in both the sex comb in males and the pronotum projection in females. RNAi against the Hox gene Ultrabithorax resulted in the complete loss or reduction of all persistence traits in male rear legs. These results demonstrate that Hox genes can be involved in intra- and inter-locus sexual conflict and mediate escalation of sexually antagonistic traits.

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TheDrosophilaproboscis is specified by two Hox genes,proboscipediaandSex combs reduced, via repression of leg and antennal appendage genes

Development ◽

10.1242/dev.128.14.2803 ◽

2001 ◽

Vol 128 (14) ◽

pp. 2803-2814 ◽

Cited By ~ 1

Author(s):

Arhat Abzhanov ◽

Stacy Holtzman ◽

Thomas C. Kaufman

Keyword(s):

Limb Development ◽

Hox Genes ◽

Distinct Type ◽

Wild Type ◽

Fate Map ◽

Genetic Studies ◽

Unique Type ◽

Sex Combs Reduced ◽

Sex Combs ◽

Labial Disc

The proboscis is one of the most highly modified appendages in Drosophila melanogaster. However, the phenotypes of proboscipedia (pb) mutants, which transform the proboscis into leg or antenna, indicate a basic homology among these limbs. Recent genetic studies have revealed a developmental system for patterning appendages and identified several genes required for limb development. Among these are: extradenticle (exd), homothorax (hth), dachshund (dac), Distal-less (Dll) and spalt (sal). These limb genes have not been well studied in wild-type mouthparts and their role if any in this appendage is not well understood. Here we demonstrate that the homeotic gene products Proboscipedia (Pb) and Sex combs reduced (Scr) regulate the limb genes in the labial disc to give rise to a unique type of appendage, the proboscis. Pb inhibits exd, dac and sal expression and downregulates Dll. This observation explains the ability of Pb to inhibit the effects of ectopically expressed trunk Hox genes in the proboscis, to suppress leg identity in the trunk and to transform antenna to maxillary palp. Scr suppresses sal expression and also downregulates Dll in the labial discs; discs mutant for both pb and Scr give rise to complete antennae, further demonstrating appendage homology. In the labial disc, Pb positively regulates transcription of Scr, whereas in the embryo, Scr positively regulates pb. Additionally, our results suggests a revised fate map of the labial disc. We conclude that the proboscis constitutes a genetically distinct type of appendage whose morphogenesis does not require several important components of leg and/or antennal patterning systems, but retains distal segmental homology with these appendages.

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A novel post-developmental role of the Hox genes underlies normal adult behaviour

10.1101/2021.08.29.458086 ◽

2021 ◽

Author(s):

A. Raouf Issa ◽

Claudio R. Alonso

Keyword(s):

Flight Control ◽

Dopaminergic Neurons ◽

Molecular Mechanisms ◽

Hox Genes ◽

Neural Function ◽

Mature Neurons ◽

The Stability ◽

Encoding Genes ◽

Control Functional

The molecular mechanisms underlying the stability of mature neurons and neural circuits are poorly understood. Here we explore this problem and discover that the Hox genes are a component of the genetic programme that maintains normal neural function in adult Drosophila. We show that post-developmental downregulation of the Hox gene Ultrabithorax (Ubx) in adult neurons leads to substantial anomalies in flight. Mapping the cellular basis of these effects reveals that Ubx is required within a subset of dopaminergic neurons, and cell circuitry analyses and optogenetics allow us to link these dopaminergic neurons to flight control. Functional imaging experiments show that Ubx is necessary for normal dopaminergic activity, and neuron-specific RNA-sequencing defines two previously uncharacterised ion channel-encoding genes as potential mediators of Ubx behavioural roles. Our study thus reveals a novel role of the Hox system in controlling adult behaviour and neural function.

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The genome of a daddy-long-legs (Opiliones) illuminates the evolution of arachnid appendages

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2021.1168 ◽

2021 ◽

Vol 288 (1956) ◽

pp. 20211168

Author(s):

Guilherme Gainett ◽

Vanessa L. González ◽

Jesús A. Ballesteros ◽

Emily V. W. Setton ◽

Caitlin M. Baker ◽

...

Keyword(s):

Genetic Basis ◽

Hox Genes ◽

Genome Duplication ◽

Draft Genome ◽

Growth Factor Receptor ◽

Loss Of Function ◽

Sex Combs Reduced ◽

Sex Combs ◽

Dynamic Genome ◽

Epidermal Growth

Chelicerate arthropods exhibit dynamic genome evolution, with ancient whole-genome duplication (WGD) events affecting several orders. Yet, genomes remain unavailable for a number of poorly studied orders, such as Opiliones (daddy-long-legs), which has hindered comparative study. We assembled the first harvestman draft genome for the species Phalangium opilio , which bears elongate, prehensile appendages, made possible by numerous distal articles called tarsomeres. Here, we show that the genome of P. opilio exhibits a single Hox cluster and no evidence of WGD. To investigate the developmental genetic basis for the quintessential trait of this group—the elongate legs—we interrogated the function of the Hox genes Deformed ( Dfd ) and Sex combs reduced ( Scr ), and a homologue of Epidermal growth factor receptor ( Egfr ). Knockdown of Dfd incurred homeotic transformation of two pairs of legs into pedipalps, with dramatic shortening of leg segments in the longest leg pair, whereas homeosis in L3 is only achieved upon double Dfd + Scr knockdown. Knockdown of Egfr incurred shortened appendages and the loss of tarsomeres. The similarity of Egfr loss-of-function phenotypic spectra in insects and this arachnid suggest that repeated cooption of EGFR signalling underlies the independent gains of supernumerary tarsomeres across the arthropod tree of life.

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