Dual mode of embryonic development is highlighted by expression and function of Nasonia pair-rule genes

Rosenberg, Miriam; Brent, Ava E.; Payre, François; Desplan, Claude

doi:10.7554/elife.01440

Cited by 63 publications

(96 citation statements)

References 85 publications

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“…In contrast to this long-germ mode of segmentation, most insects and other arthropods exhibit a short-germ mode of segmentation, during which only a few anterior segments are generated simultaneously and subsequently a speciesspecific number of posterior segments are added sequentially from a posterior growth zone or segment addition zone (SAZ) (Davis and Patel, 2002;Tautz, 2004;Peel et al, 2005;McGregor et al, 2009). Note, however, that these modes of segmentation may not always be discrete because a mixed mode of segmentation has recently been proposed for Nasonia vitripennis (Rosenberg et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

The Wnt and Delta-Notch signalling pathways interact to direct pair-rule gene expression via caudal during segment addition in the spider Parasteatoda tepidariorum

et al. 2016

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In short-germ arthropods, posterior segments are added sequentially from a segment addition zone (SAZ) during embryogenesis. Studies in spiders such as Parasteatoda tepidariorum have provided insights into the gene regulatory network (GRN) underlying segment addition, and revealed that Wnt8 is required for dynamic Delta (Dl) expression associated with the formation of new segments. However, it remains unclear how these pathways interact during SAZ formation and segment addition. Here, we show that Delta-Notch signalling is required for Wnt8 expression in posterior SAZ cells, but represses the expression of this Wnt gene in anterior SAZ cells. We also found that these two signalling pathways are required for the expression of the spider orthologues of even-skipped (eve) and runt-1 (run-1), at least in part via caudal (cad). Moreover, it appears that dynamic expression of eve in this spider does not require a feedback loop with run-1, as is found in the pair-rule circuit of the beetle Tribolium. Taken together, our results suggest that the development of posterior segments in Parasteatoda is directed by dynamic interactions between Wnt8 and Delta-Notch signalling that are read out by cad, which is necessary but probably not sufficient to regulate the expression of eve and run-1. Our study therefore provides new insights towards better understanding the evolution and developmental regulation of segmentation in other arthropods, including insects.

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Section: Introductionmentioning

confidence: 99%

The Wnt and Delta-Notch signalling pathways interact to direct pair-rule gene expression via caudal during segment addition in the spider Parasteatoda tepidariorum

et al. 2016

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“…Over the past decade or so, several important genetic, genomic, and cell biological studies have been conducted in the jewel wasp N. vitripennis 19,[32][33][34][35] . These studies have been facilitated by the development of several important sgRNA #Injected (31) 62 (17) 659 (100) 271 (100) C 12 (7) 0 (0) 93 (35) 57 (22) 1318 (100) Table 3.…”

Section: Discussionmentioning

confidence: 99%

Generation of heritable germline mutations in the jewel waspNasonia vitripennisusing CRISPR/Cas9

Li¹,

Cook

Douglah

et al. 2016

Preprint

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The revolutionary RNA-guided endonuclease CRISPR/Cas9 system has proven to be a powerful tool for gene editing in a plethora of organisms. Here, utilizing this system we developed an efficient protocol for the generation of heritable germline mutations in the parasitoid jewel wasp, Nasonia vitripennis, a rising insect model organism for the study of evolution, development of axis pattern formation, venom production, haplo-diploid sex determination, and host-symbiont interactions. To establish CRISPRdirected gene editing in N. vitripennis, we targeted a conserved eye pigmentation gene cinnabar, generating several independent heritable germline mutations in this gene. Briefly, to generate these mutants, we developed a protocol to efficiently collect N. vitripennis eggs from a parasitized flesh fly pupa, Sarcophaga bullata, inject these eggs with Cas9/guide RNA mixtures, and transfer injected eggs back into the host to continue development. We also describe a flow for screening mutants and establishing stable mutant strains through genetic crosses. Overall, our results demonstrate that the CRISPR/Cas9 system is a powerful tool for genome manipulation in N. vitripennis, with strong potential for expansion to target critical genes, thus allowing for the investigation of several important biological phenomena in this organism.Hymenopteran insects, including all ants, bees, and wasps, represent one of the most prominent insect orders, occupying roughly 8% of all described species on earth 1 . The parasitoid wasp Nasonia vitripennis is one of the most tractable and comprehensively studied hymenopterans genetically 2 , owing to its overall ease of laboratory use, its short generation time (roughly ~2 weeks), tolerance for inbreeding, and straightforward rearing. Like all other hymenopterans, N. vitripennis utilizes a haplodiploid sex determination system by which haploid males develop parthenogenetically from unfertilized eggs while diploid females develop from fertilized eggs 2 . Interestingly, this mode of sex determination makes N. vitripennis and other members of the clade vulnerable to manipulation by microbial and genetic parasites. For example, Arsenophonus nasoniae, a natural bacterial endosymbiont of N. vitripennis, effectively kills male progeny by manipulating key components of the mitotic machinery required specifically for early male embryonic development 3 . This male-killing results in significantly biased sex ratios favoring females, thereby benefiting the bacteria as they are transmitted solely from infected mother to offspring 4 . In addition to sex ratio-distorting bacteria, other genetic agents can influence the sex ratios of hymenopteran insects. For example, although the genome of N. vitripennis naturally harbors five chromosomes, some individuals have been discovered to also contain a sixth, supernumerary (B) chromosome termed paternal sex ratio (PSR) 5 . PSR is paternally transmitted through the sperm and acts by eliminating the haploid genome, thereby converting what should be diploid females i...

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“…Recently, a study of pair-rule gene expression and function was performed in Nasonia; the results suggested that, in fact, the species exhibits dual modes of embryogenesis, a Drosophila-like mode at the anterior region and a Tribolium-like mode at the posterior region. Knockdown of Nasonia pair-rule genes, Nveve, odd and h (a hairy homolog), results in a loss of alternate anterior segments and a loss of posterior segments, and also Nvodd is expressed in waves (Rosenberg et al, 2014).…”

Section: Evolution and A Model Of Bombyx Segmentation Mechanismsmentioning

confidence: 99%

Analyses of interactions among pair-rule genes and the gap gene Krüppel in Bombyx segmentation

Nakao

2015

Developmental Biology

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In the short-germ insect Tribolium, a pair-rule gene circuit consisting of the Tribolium homologs of even-skipped, runt, and odd-skipped (Tc-eve, Tc-run and Tc-odd, respectively) has been implicated in segment formation. To examine the application of the model to other taxa, I studied the expression and function of pair-rule genes in Bombyx mori, together with a Bombyx homolog of Krüppel (Bm-Kr), a known gap gene. Knockdown embryos of Bombyx homologs of eve, run and odd (Bm-eve, Bm-run and Bm-odd) exhibited asegmental phenotypes similar to those of Tribolium knockdowns. However, pair-rule gene interactions were similar to those of both Tribolium and Drosophila, which, different from Tribolium, shows a hierarchical segmentation mode. Additionally, the Bm-odd expression pattern shares characteristics with those of Drosophila pair-rule genes that receive upstream regulatory input. On the other hand, Bm-Kr knockdowns exhibited a large posterior segment deletion as observed in short-germ insects. However, a detailed analysis of these embryos indicated that Bm-Kr modulates expression of pair-rule genes like in Drosophila, although the mechanisms appear to be different. This suggested hierarchical interactions between Bm-Kr and pair-rule genes. Based on these results, I concluded that the pair-rule gene circuit model that describes Tribolium development is not applicable to Bombyx.

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Dual mode of embryonic development is highlighted by expression and function of Nasonia pair-rule genes

Cited by 63 publications

References 85 publications

The Wnt and Delta-Notch signalling pathways interact to direct pair-rule gene expression via caudal during segment addition in the spider Parasteatoda tepidariorum

The Wnt and Delta-Notch signalling pathways interact to direct pair-rule gene expression via caudal during segment addition in the spider Parasteatoda tepidariorum

Generation of heritable germline mutations in the jewel waspNasonia vitripennisusing CRISPR/Cas9

Analyses of interactions among pair-rule genes and the gap gene Krüppel in Bombyx segmentation

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