Evolution of insect development: to the hemimetabolous paradigm

Mito, Taro; Nakamura, Taro; Noji, Sumihare

doi:10.1016/j.gde.2010.04.005

Cited by 22 publications

(13 citation statements)

References 60 publications

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“…The fruit fly Drosophila melanogaster has been used as the main model organism for understanding the mechanisms of segmentation. However, with all of its advantages, Drosophila exhibits a derived form of embryonic development, making it a poor representative of more common and widespread types of arthropod segmentation (Davis and Patel, 2002; Mito et al, 2010; Peel et al, 2005). …”

Section: Introductionmentioning

confidence: 99%

Dynamics of growth zone patterning in the milkweed bug Oncopeltus fasciatus

et al. 2017

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We describe the dynamic process of abdominal segment generation in the milkweed bug Oncopeltus fasciatus. We present detailed morphological measurements of the growing germband throughout segmentation. Our data are complemented by cell division profiles and expression patterns of key genes, including invected and even-skipped as markers for different stages of segment formation. We describe morphological and mechanistic changes in the growth zone and in nascent segments during the generation of individual segments and throughout segmentation, and examine the relative contribution of newly formed versus existing tissue to segment formation. Although abdominal segment addition is primarily generated through the rearrangement of a pool of undifferentiated cells, there is nonetheless proliferation in the posterior. By correlating proliferation with gene expression in the growth zone, we propose a model for growth zone dynamics during segmentation in which the growth zone is functionally subdivided into two distinct regions: a posterior region devoted to a slow rate of growth among undifferentiated cells, and an anterior region in which segmental differentiation is initiated and proliferation inhibited.

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Section: Introductionmentioning

confidence: 99%

Dynamics of growth zone patterning in the milkweed bug Oncopeltus fasciatus

et al. 2017

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“…Drosophila development follows the so-called ‘long germband’ developmental mode, which is derived and found only in a subset of holometabolous insect lineages (Peel 2008; Mito et al 2010). The most common, and likely ancestral, mode of arthropod pre-segmentation developmental is short germband embryogenesis (Peel 2008; Mito et al 2010) In short germband embryogenesis, a small number of cells in the blastoderm embryo form the most anterior segments (called the germ anlage), while more posterior segments arise after gastrulation by growth and cell division (reviewed in Davis and Patel 2002). Whereas long germ development often occurs in a syncytium, short germ segmental patterning occurs in a cellularized environment via an oscillatory mechanism (Sarrazin et al 2012).…”

Section: Introductionmentioning

confidence: 99%

Tribolium castaneumas a model for microRNA evolution, expression and function during short germband development

Ninova

Ronshaugen

Griffiths-Jones

2015

Preprint

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MicroRNAs are well-established players in the development of multicellular animals. Most of our understanding of microRNA function in arthropod development comes from studies in Drosophila. Despite their advantages as model systems, the long germband embryogenesis of fruit flies is an evolutionary derived state restricted to several holometabolous insect lineages. MicroRNA evolution and expression across development in animals exhibiting the ancestral and more widespread short germband mode of embryogenesis has not been characterized. We sequenced small RNA libraries of oocytes and successive time intervals covering the embryonic development of the short germband model organism, the red flour beetle Tribolium castaneum. We analysed the evolution and temporal expression of the microRNA complement, and sequenced libraries of total RNA to investigate the relationships with microRNA target expression. We show microRNA maternal loading and sequence-specific 3'-end non-template oligoadenylation of maternally deposited microRNAs that is conserved between Tribolium and Drosophila. We further uncover large clusters encoding multiple paralogs from several Tribolium-specific microRNA families expressed during a narrow interval of time immediately after the activation of zygotic transcription. These novel microRNAs, together with several early expressed conserved microRNAs, target a significant number of maternally deposited transcripts. Comparison with Drosophila shows that microRNA-mediated maternal transcript targeting is a conserved phenomenon in insects, but the number and sequences of microRNAs involved in this process have diverged. The expression of fast-evolving and species-specific microRNAs in the early blastoderm of T.castaneum is consistent with previous findings in Drosophila and shows that the unique permissiveness for microRNA innovation at this stage is a conserved phenomenon.

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mentioning

confidence: 99%

“…Fruit flies follow the so-called "long germband" developmental mode, which is derived and found only in a subset of holometabolous insect lineages (Peel 2008;Mito et al 2010). The most common, and likely ancestral, mode of arthropod presegmentation development is short germband embryogenesis (Peel 2008;Mito et al 2010). In short germband embryogenesis, a small number of cells in the blastoderm (called the germ anlage) form the most anterior embryonic segments, and the remaining portion gives rise to the extraembryonic serosal membrane (Handel et al 2000).…”

mentioning

confidence: 99%

MicroRNA evolution, expression, and function during short germband development in Tribolium castaneum

2015

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MicroRNAs are well-established players in the development of multicellular animals. Most of our understanding of microRNA function in arthropod development comes from studies in Drosophila. Despite their advantages as model systems, the long germband embryogenesis of fruit flies is an evolutionary derived state restricted to several holometabolous insect lineages. MicroRNA evolution and expression across development in animals exhibiting the ancestral and more widespread short germband mode of embryogenesis has not been characterized. We sequenced small RNA libraries of oocytes and successive intervals covering the embryonic development of the short germband model organism, Tribolium castaneum. We analyzed the evolution and temporal expression of the microRNA complement and sequenced libraries of total RNA to investigate the relationships with microRNA target expression. We show microRNA maternal loading and sequence-specific 3 ′ end nontemplate oligoadenylation of maternally deposited microRNAs that is conserved between Tribolium and Drosophila. We further uncover large clusters encoding multiple paralogs from several Tribolium-specific microRNA families expressed during a narrow interval of time immediately after the activation of zygotic transcription. These novel microRNAs, together with several early expressed conserved microRNAs, target a significant number of maternally deposited transcripts. Comparison with Drosophila shows that microRNA-mediated maternal transcript targeting is a conserved process in insects, but the number and sequences of microRNAs involved have diverged. The expression of fast-evolving and species-specific microRNAs in the early blastoderm of T. castaneum is consistent with previous findings in Drosophila and shows that the unique permissiveness for microRNA innovation at this stage is a conserved phenomenon.

show abstract

Evolution of insect development: to the hemimetabolous paradigm

Cited by 22 publications

References 60 publications

Dynamics of growth zone patterning in the milkweed bug Oncopeltus fasciatus

Dynamics of growth zone patterning in the milkweed bug Oncopeltus fasciatus

Tribolium castaneumas a model for microRNA evolution, expression and function during short germband development

MicroRNA evolution, expression, and function during short germband development in Tribolium castaneum

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