scholarly journals Systematic comparison of developmental GRNs explains how novelty is incorporated in early development

2020 ◽  
Author(s):  
Gregory A. Cary ◽  
Brenna S. McCauley ◽  
Olga Zueva ◽  
Joseph Pattinato ◽  
William Longabaugh ◽  
...  
Keyword(s):  
Early Development ◽  
Regulatory Networks ◽  
Morphological Diversity ◽  
Sea Star ◽  
Animal Diversity ◽  
Evolutionarily Conserved ◽  
Overall Stability ◽  
Gene Regulatory ◽  
Embryonic Viability ◽  
Viable Embryo

SUMMARYThe impressive array of morphological diversity among animal taxa represents the product of millions of years of evolution. Morphology is the output of development, therefore phenotypic evolution arises from changes to the topology of the gene regulatory networks (GRNs) that control the highly coordinated process of embryogenesis1. While genetic variation can arise anywhere in the genome and affect any part of an individual GRN, the need to form a viable embryo provides a constraint on the types of variation that pass the filter of selection. A particular challenge in understanding the origins of animal diversity lies in determining how GRNs incorporate novelty while preserving the overall stability of the network, and hence, embryonic viability. Here we assemble a comprehensive GRN, consisting of 42 genes (nodes) and 84 interactions (edges), for the model of endomesoderm specification in the sea star from zygote through gastrulation that corresponds to the GRN for sea urchin development of equivalent territories and stages2. Using these detailed models we make the first systems-level comparison of early development and examine how novelty is incorporated into GRNs. We show how the GRN is resilient to the introduction of a transcription factor, pmar1, the inclusion of which leads to a switch between two stable modes of Delta-Notch signaling. Signaling pathways can function in multiple modes and we propose that GRN changes that lead to switches between modes may be a common evolutionary mechanism for changes in embryogenesis. Our data additionally proposes a model in which evolutionarily conserved network motifs, or kernels, may function throughout development to stabilize these signaling transitions.

scholarly journals Systematic comparison of sea urchin and sea star developmental gene regulatory networks explains how novelty is incorporated in early development

2020 ◽  
Vol 11 (1) ◽  
Author(s):  
Gregory A. Cary ◽  
Brenna S. McCauley ◽  
Olga Zueva ◽  
Joseph Pattinato ◽  
William Longabaugh ◽  
...  
Keyword(s):  
Early Development ◽  
Sea Urchin ◽  
Gene Regulatory Networks ◽  
Regulatory Networks ◽  
Morphological Diversity ◽  
Sea Star ◽  
Animal Diversity ◽  
Evolutionarily Conserved ◽  
Overall Stability ◽  
Gene Regulatory

AbstractThe extensive array of morphological diversity among animal taxa represents the product of millions of years of evolution. Morphology is the output of development, therefore phenotypic evolution arises from changes to the topology of the gene regulatory networks (GRNs) that control the highly coordinated process of embryogenesis. A particular challenge in understanding the origins of animal diversity lies in determining how GRNs incorporate novelty while preserving the overall stability of the network, and hence, embryonic viability. Here we assemble a comprehensive GRN for endomesoderm specification in the sea star from zygote through gastrulation that corresponds to the GRN for sea urchin development of equivalent territories and stages. Comparison of the GRNs identifies how novelty is incorporated in early development. We show how the GRN is resilient to the introduction of a transcription factor, pmar1, the inclusion of which leads to a switch between two stable modes of Delta-Notch signaling. Signaling pathways can function in multiple modes and we propose that GRN changes that lead to switches between modes may be a common evolutionary mechanism for changes in embryogenesis. Our data additionally proposes a model in which evolutionarily conserved network motifs, or kernels, may function throughout development to stabilize these signaling transitions.

scholarly journals Divergence of gene regulatory network linkages during specification of ectoderm and mesoderm in early development of sea urchins

2016 ◽  
Author(s):  
Eric M. Erkenbrack ◽  
Eric H. Davidson
Keyword(s):  
Early Development ◽  
Regulatory Networks ◽  
Evolutionary Dynamics ◽  
Sea Urchins ◽  
Regulatory Genes ◽  
Geological Time ◽  
Appreciable Change ◽  
Comparative Analyses ◽  
Temporal Gene Expression ◽  
Gene Regulatory

AbstractDevelopmental gene regulatory networks (GRNs) are assemblages of gene regulatory interactions that direct ontogeny of animal body plans. Studies of GRNs operating in early development of euechinoid sea urchins has revealed that little appreciable change has occurred since their divergence approximately 90 million years ago (mya). These observations suggest that strong conservation of GRN architecture has been maintained in early development of the sea urchin lineage. To test whether this is true for all sea urchins, comparative analyses of echinoid taxa that diverged deeper in geological time must be conducted. Recent studies highlighted extensive divergence of skeletogenic mesoderm specification in the sister clade of euechinoids, the cidaroids, suggesting that comparative analyses of cidaroid GRN architecture may confer a greater understanding of the evolutionary dynamics of developmental GRNs. Here, we report spatiotemporal patterning of 55 regulatory genes and perturbation analyses of key regulatory genes involved in euechinoid oral-aboral patterning of non-skeletogenic mesodermal and ectodermal domains in early development of the cidaroid Eucidaris tribuloides. Our results indicate that developmental GRNs directing mesodermal and ectodermal specification have undergone marked alterations since the divergence of cidaroids and euechinoids. Notably, statistical and clustering analyses of echinoid temporal gene expression datasets indicate that regulation of mesodermal genes has diverged more markedly than regulation of ectodermal genes. Although research on indirect-developing euechinoid sea urchins suggests strong conservation of GRN circuitry during early embryogenesis, this study indicates that since the divergence of cidaroids and euechinoids developmental GRNs have undergone significant divergence.

scholarly journals Evolution of abbreviated development in Heliocidaris erythrogramma dramatically re-wired the highly conserved sea urchin developmental gene regulatory network to decouple signaling center function from ultimate fate

2019 ◽  
Author(s):  
Allison Edgar ◽  
Maria Byrne ◽  
David R. McClay ◽  
Gregory A. Wray
Keyword(s):  
Early Development ◽  
Regulatory Networks ◽  
Molecular Mechanisms ◽  
Sea Urchins ◽  
Stabilizing Selection ◽  
Developmental Gene ◽  
Heliocidaris Erythrogramma ◽  
Signaling Center ◽  
Gene Regulatory ◽  
Ultimate Fate

AbstractDevelopmental gene regulatory networks (GRNs) describe the interactions among gene products that drive the differential transcriptional and cell regulatory states that pattern the embryo and specify distinct cell fates. GRNs are often deeply conserved, but whether this is the product of constraint inherent to the network structure or stabilizing selection remains unclear. We have constructed the first formal GRN for early development in Heliocidaris erythrogramma, a species with dramatically accelerated, direct development. This life history switch has important ecological consequences, arose rapidly, and has evolved independently many times in echinoderms, suggesting it is a product of selection. We find that H. erythrogramma exhibits dramatic differences in GRN topology compared with ancestral, indirect-developing sea urchins. In particular, the GRN sub-circuit that directs the early and autonomous commitment of skeletogenic cell precursors in indirect developers appears to be absent in H. erythrogramma, a particularly striking change in relation to both the prior conservation of this sub-circuit and the key role that these cells play ancestrally in early development as the embryonic signaling center. These results show that even highly conserved molecular mechanisms of early development can be substantially reconfigured in a relatively short evolutionary time span, suggesting that selection rather than constraint is responsible for the striking conservation of the GRN among other sea urchins.

scholarly journals TBX5 drives Aldh1a2 expression to regulate a RA-Hedgehog-Wnt gene regulatory network coordinating cardiopulmonary development

2021 ◽  
Author(s):  
Scott A rankin ◽  
Jeffery D Steimle ◽  
Xinan Yang ◽  
Ariel B Rydeen ◽  
Kunal Agarwal ◽  
...  
Keyword(s):  
Heart Development ◽  
Regulatory Networks ◽  
Lateral Plate ◽  
T Box ◽  
Terrestrial Vertebrates ◽  
Regulatory Module ◽  
Evolutionarily Conserved ◽  
Terrestrial Life ◽  
Gene Regulatory ◽  
Foregut Endoderm

The gene regulatory networks that coordinate the development of the cardiac and pulmonary systems are essential for terrestrial life but poorly understood. The T-box transcription factor Tbx5 is critical for both pulmonary specification and heart development, but how these activities are mechanistically integrated remains unclear. We show that Tbx5 regulates an evolutionarily conserved retinoic acid (RA)-Hedgehog-Wnt signaling cascade coordinating cardiopulmonary development. We demonstrate that Tbx5 directly maintains expression of the RA-synthesizing enzyme Aldh1a2 in the foregut lateral plate mesoderm via an intronic enhancer that is evolutionarily conserved among terrestrial vertebrates. Tbx5 promotes posterior second heart field identity in a positive feedback loop with RA, antagonizing a Fgf8-Cyp regulatory module and restricting FGF activity to the anterior. Tbx5/Aldh1a2-dependent RA signaling also directly activates Shh transcription in the adjacent foregut endoderm through the conserved MACS1 enhancer. Epithelial Hedgehog then signals back to the mesoderm, where together with Tbx5 it activates expression of Wnt2/2b that ultimately induce pulmonary fate in the foregut endoderm. These results provide mechanistic insight into the interrelationship between heart and lung development informing cardiopulmonary evolution and birth defects.

Evolutionarily conserved hierarchical gene regulatory networks for plant salt stress response

Nature Plants ◽  
2021 ◽  
Author(s):  
Ting-Ying Wu ◽  
HonZhen Goh ◽  
Christina B. Azodi ◽  
Shalini Krishnamoorthi ◽  
Ming-Jung Liu ◽  
...  
Keyword(s):  
Salt Stress ◽  
Stress Response ◽  
Gene Regulatory Networks ◽  
Regulatory Networks ◽  
Salt Stress Response ◽  
Evolutionarily Conserved ◽  
Gene Regulatory

scholarly journals Divergence of ectodermal and mesodermal gene regulatory network linkages in early development of sea urchins

2016 ◽  
Vol 113 (46) ◽  
pp. E7202-E7211 ◽  
Author(s):  
Eric M. Erkenbrack
Keyword(s):  
Early Development ◽  
Regulatory Networks ◽  
Evolutionary Dynamics ◽  
Sea Urchins ◽  
Regulatory Genes ◽  
Geological Time ◽  
Appreciable Change ◽  
Comparative Analyses ◽  
Temporal Gene Expression ◽  
Gene Regulatory

Developmental gene regulatory networks (GRNs) are assemblages of gene regulatory interactions that direct ontogeny of animal body plans. Studies of GRNs operating in the early development of euechinoid sea urchins have revealed that little appreciable change has occurred since their divergence ∼90 million years ago (mya). These observations suggest that strong conservation of GRN architecture was maintained in early development of the sea urchin lineage. Testing whether this holds for all sea urchins necessitates comparative analyses of echinoid taxa that diverged deeper in geological time. Recent studies highlighted extensive divergence of skeletogenic mesoderm specification in the sister clade of euechinoids, the cidaroids, suggesting that comparative analyses of cidaroid GRN architecture may confer a greater understanding of the evolutionary dynamics of developmental GRNs. Here I report spatiotemporal patterning of 55 regulatory genes and perturbation analyses of key regulatory genes involved in euechinoid oral–aboral patterning of nonskeletogenic mesodermal and ectodermal domains in early development of the cidaroid Eucidaris tribuloides. These results indicate that developmental GRNs directing mesodermal and ectodermal specification have undergone marked alterations since the divergence of cidaroids and euechinoids. Notably, statistical and clustering analyses of echinoid temporal gene expression datasets indicate that regulation of mesodermal genes has diverged more markedly than regulation of ectodermal genes. Although research on indirect-developing euechinoid sea urchins suggests strong conservation of GRN circuitry during early embryogenesis, this study indicates that since the divergence of cidaroids and euechinoids, developmental GRNs have undergone significant, cell type–biased alterations.

scholarly journals Waiting in the wings: what can we learn about gene co-option from the diversification of butterfly wing patterns?

2017 ◽  
Vol 372 (1713) ◽  
pp. 20150485 ◽  
Author(s):  
Chris D. Jiggins ◽  
Richard W. R. Wallbank ◽  
Joseph J. Hanly
Keyword(s):  
Gene Regulatory Networks ◽  
Regulatory Networks ◽  
Spatial Information ◽  
Morphological Diversity ◽  
Regulatory Elements ◽  
Evolutionary Change ◽  
Divergent Evolution ◽  
Butterfly Wing ◽  
Wing Patterns ◽  
Gene Regulatory

A major challenge is to understand how conserved gene regulatory networks control the wonderful diversity of form that we see among animals and plants. Butterfly wing patterns are an excellent example of this diversity. Butterfly wings form as imaginal discs in the caterpillar and are constructed by a gene regulatory network, much of which is conserved across the holometabolous insects. Recent work in Heliconius butterflies takes advantage of genomic approaches and offers insights into how the diversification of wing patterns is overlaid onto this conserved network. WntA is a patterning morphogen that alters spatial information in the wing. Optix is a transcription factor that acts later in development to paint specific wing regions red. Both of these loci fit the paradigm of conserved protein-coding loci with diverse regulatory elements and developmental roles that have taken on novel derived functions in patterning wings. These discoveries offer insights into the ‘Nymphalid Ground Plan’, which offers a unifying hypothesis for pattern formation across nymphalid butterflies. These loci also represent ‘hotspots’ for morphological change that have been targeted repeatedly during evolution. Both convergent and divergent evolution of a great diversity of patterns is controlled by complex alleles at just a few genes. We suggest that evolutionary change has become focused on one or a few genetic loci for two reasons. First, pre-existing complex cis -regulatory loci that already interact with potentially relevant transcription factors are more likely to acquire novel functions in wing patterning. Second, the shape of wing regulatory networks may constrain evolutionary change to one or a few loci. Overall, genomic approaches that have identified wing patterning loci in these butterflies offer broad insight into how gene regulatory networks evolve to produce diversity. This article is part of the themed issue ‘Evo-devo in the genomics era, and the origins of morphological diversity’.

scholarly journals Molecular patterning during the development of Phoronopsis harmeri reveals similarities to rhynchonelliform brachiopods

2019 ◽  
Author(s):  
Carmen Andrikou ◽  
Yale J. Passamaneck ◽  
Chris J. Lowe ◽  
Mark Q. Martindale ◽  
Andreas Hejnol
Keyword(s):  
Cell Fate ◽  
Regulatory Networks ◽  
Expression Patterns ◽  
Dynamic Expression ◽  
Evolutionarily Conserved ◽  
Oral Ectoderm ◽  
Gene Regulatory ◽  
Phoronopsis Harmeri ◽  
Evolutionary Lineages ◽  
Germ Layer Formation

AbstractBackgroundAnswering the question how conserved patterning systems are across evolutionary lineages requires a broad taxon sampling. Phoronid development has previously been studied using fate mapping and morphogenesis, yet molecular descriptions are missing. Here we report the expression patterns of the evolutionarily conserved anterior (otx, gsc, six3/6, nk2.1), posterior (cdx, bra) and endomesodermal (foxA, gata4/5/6, twist) markers in the phoronid Phoronopsis harmeri.ResultsThe transcription factors foxA, gata4/5/6 and cdx show conserved expression in patterning the development and regionalization of the phoronid embryonic gut, with foxA expressed in the presumptive foregut, gata4/5/6 demarcating the midgut and cdx confined to the hindgut. Surprisingly, brachyury, an evolutionary conserved transcription factor often associated with gastrulation movements and patterning of the mouth and hindgut, seems to be unrelated with gastrulation and mouth patterning in phoronids. Furthermore, six3/6, a well-conserved anterior marker, shows a remarkably dynamic expression, demarcating not only the apical organ and the oral ectoderm, but also clusters of cells of the developing midgut and the anterior mesoderm, similar to what has been reported for brachiopods, bryozoans and some deuterostome Bilateria.ConclusionsOur comparison of gene expression patterns with other studied Bilateria reveals that the timing of axis determination and cell fate distribution of the phoronid shows highest similarities to rhynchonelliform brachiopods. Despite these similarities, the phoronid P. harmeri shows also particularities in its development, which hint to divergences in the arrangement of gene regulatory networks responsible for germ layer formation and axis specification.

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