Quantitative system drift compensates for altered maternal inputs to the gap gene network of the scuttle fly Megaselia abdita
The segmentation gene network in insects can produce equivalent phenotypic outputs despite differences in upstream regulatory inputs between species. We investigate the mechanistic basis of this phenomenon through a systems-level analysis of the gap gene network in the scuttle fly Megaselia abdita (...
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Abstract | The segmentation gene network in insects can produce equivalent phenotypic outputs despite differences in upstream regulatory inputs between species. We investigate the mechanistic basis of this phenomenon through a systems-level analysis of the gap gene network in the scuttle fly Megaselia abdita (Phoridae). It combines quantification of gene expression at high spatio-temporal resolution with systematic knock-downs by RNA interference (RNAi). Initiation and dynamics of gap gene expression differ markedly between M. abdita and Drosophila melanogaster, while the output of the system converges to equivalent patterns at the end of the blastoderm stage. Although the qualitative structure of the gap gene network is conserved, there are differences in the strength of regulatory interactions between species. We term such network rewiring 'quantitative system drift'. It provides a mechanistic explanation for the developmental hourglass model in the dipteran lineage. Quantitative system drift is likely to be a widespread mechanism for developmental evolution. |
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AbstractList | The segmentation gene network in insects can produce equivalent phenotypic outputs despite differences in upstream regulatory inputs between species. We investigate the mechanistic basis of this phenomenon through a systems-level analysis of the gap gene network in the scuttle fly Megaselia abdita (Phoridae). It combines quantification of gene expression at high spatio-temporal resolution with systematic knock-downs by RNA interference (RNAi). Initiation and dynamics of gap gene expression differ markedly between M. abdita and Drosophila melanogaster, while the output of the system converges to equivalent patterns at the end of the blastoderm stage. Although the qualitative structure of the gap gene network is conserved, there are differences in the strength of regulatory interactions between species. We term such network rewiring 'quantitative system drift'. It provides a mechanistic explanation for the developmental hourglass model in the dipteran lineage. Quantitative system drift is likely to be a widespread mechanism for developmental evolution. The segmentation gene network in insects can produce equivalent phenotypic outputs despite differences in upstream regulatory inputs between species. We investigate the mechanistic basis of this phenomenon through a systems-level analysis of the gap gene network in the scuttle fly Megaselia abdita (Phoridae). It combines quantification of gene expression at high spatio-temporal resolution with systematic knock-downs by RNA interference (RNAi). Initiation and dynamics of gap gene expression differ markedly between M. abdita and Drosophila melanogaster, while the output of the system converges to equivalent patterns at the end of the blastoderm stage. Although the qualitative structure of the gap gene network is conserved, there are differences in the strength of regulatory interactions between species. We term such network rewiring ‘quantitative system drift’. It provides a mechanistic explanation for the developmental hourglass model in the dipteran lineage. Quantitative system drift is likely to be a widespread mechanism for developmental evolution.DOI: http://dx.doi.org/10.7554/eLife.04785.001 The segmentation gene network in insects can produce equivalent phenotypic outputs despite differences in upstream regulatory inputs between species. We investigate the mechanistic basis of this phenomenon through a systems-level analysis of the gap gene network in the scuttle fly Megaselia abdita (Phoridae). It combines quantification of gene expression at high spatio-temporal resolution with systematic knock-downs by RNA interference (RNAi). Initiation and dynamics of gap gene expression differ markedly between M. abdita and Drosophila melanogaster , while the output of the system converges to equivalent patterns at the end of the blastoderm stage. Although the qualitative structure of the gap gene network is conserved, there are differences in the strength of regulatory interactions between species. We term such network rewiring ‘quantitative system drift’. It provides a mechanistic explanation for the developmental hourglass model in the dipteran lineage. Quantitative system drift is likely to be a widespread mechanism for developmental evolution. DOI: http://dx.doi.org/10.7554/eLife.04785.001 Similar biological phenomena can result from different processes occurring in different organisms. For example, the early stages of how an insect develops from an egg can vary substantially between different species. Nonetheless, all insects have a body plan that develops in segments. The same outcome occurring as a result of different developmental steps is known as ‘system drift’, but the mechanisms underlying this phenomenon are largely unknown. How the body segments of the fruit fly Drosophila develop has been extensively studied. First, a female fruit fly adds messenger RNA (or mRNA) molecules copied from a number of genes into her egg cells. These mRNA molecules are then used to produce proteins whose concentration varies along the length of each egg. These proteins in turn switch on so-called ‘gap genes’ in differing amounts in different locations throughout the fruit fly embryo. The activity of these genes goes on to define the position and extent of specific segments along the fruit fly's body. Like the fruit fly, the scuttle fly Megaselia abdita has a segmented body. However, mothers of this species deposit somewhat different protein gradients into their eggs. How the regulation of development differs in the scuttle fly to compensate for this change is unknown. Now, Wotton et al. have studied, in detail, how gap genes are regulated in this less well-understood fly species to understand the mechanisms responsible for a specific example of system drift. In the fruit fly, gap genes normally switch-off (or reduce the expression of) other gap genes within the same developing body segment, and Wotton et al. found that the same kind of interactions tended to occur in the scuttle fly. As such, the overall structure of the gap gene network was fairly similar between scuttle and fruit flies. There were, however, differences in the strength of these interactions in the two fly species. These quantitative differences result in a different way of making the same segmental pattern in the embryo. In this way, Wotton et al. show how tinkering with the strength of specific gene interactions can provide an explanation for system drift. DOI: http://dx.doi.org/10.7554/eLife.04785.002 The segmentation gene network in insects can produce equivalent phenotypic outputs despite differences in upstream regulatory inputs between species. We investigate the mechanistic basis of this phenomenon through a systems-level analysis of the gap gene network in the scuttle fly Megaselia abdita (Phoridae). It combines quantification of gene expression at high spatio-temporal resolution with systematic knock-downs by RNA interference (RNAi). Initiation and dynamics of gap gene expression differ markedly between M. abdita and Drosophila melanogaster, while the output of the system converges to equivalent patterns at the end of the blastoderm stage. Although the qualitative structure of the gap gene network is conserved, there are differences in the strength of regulatory interactions between species. We term such network rewiring ‘quantitative system drift’. It provides a mechanistic explanation for the developmental hourglass model in the dipteran lineage. Quantitative system drift is likely to be a widespread mechanism for developmental evolution. Similar biological phenomena can result from different processes occurring in different organisms. For example, the early stages of how an insect develops from an egg can vary substantially between different species. Nonetheless, all insects have a body plan that develops in segments. The same outcome occurring as a result of different developmental steps is known as ‘system drift’, but the mechanisms underlying this phenomenon are largely unknown. How the body segments of the fruit fly Drosophila develop has been extensively studied. First, a female fruit fly adds messenger RNA (or mRNA) molecules copied from a number of genes into her egg cells. These mRNA molecules are then used to produce proteins whose concentration varies along the length of each egg. These proteins in turn switch on so-called ‘gap genes’ in differing amounts in different locations throughout the fruit fly embryo. The activity of these genes goes on to define the position and extent of specific segments along the fruit fly's body. Like the fruit fly, the scuttle fly Megaselia abdita has a segmented body. However, mothers of this species deposit somewhat different protein gradients into their eggs. How the regulation of development differs in the scuttle fly to compensate for this change is unknown. Now, Wotton et al. have studied, in detail, how gap genes are regulated in this less well-understood fly species to understand the mechanisms responsible for a specific example of system drift. In the fruit fly, gap genes normally switch-off (or reduce the expression of) other gap genes within the same developing body segment, and Wotton et al. found that the same kind of interactions tended to occur in the scuttle fly. As such, the overall structure of the gap gene network was fairly similar between scuttle and fruit flies. There were, however, differences in the strength of these interactions in the two fly species. These quantitative differences result in a different way of making the same segmental pattern in the embryo. In this way, Wotton et al. show how tinkering with the strength of specific gene interactions can provide an explanation for system drift. |
Author | Alcaine-Colet, Anna Jiménez-Guri, Eva Lemke, Steffen Crombach, Anton Schmidt-Ott, Urs Jaeger, Johannes Wotton, Karl R Janssens, Hilde |
Author_xml | – sequence: 1 givenname: Karl R surname: Wotton fullname: Wotton, Karl R organization: European Molecular Biology Laboratory, CRG Systems Biology Research Unit, Centre for Genomic Regulation, Barcelona, Spain – sequence: 2 givenname: Eva surname: Jiménez-Guri fullname: Jiménez-Guri, Eva organization: European Molecular Biology Laboratory, CRG Systems Biology Research Unit, Centre for Genomic Regulation, Barcelona, Spain – sequence: 3 givenname: Anton surname: Crombach fullname: Crombach, Anton organization: European Molecular Biology Laboratory, CRG Systems Biology Research Unit, Centre for Genomic Regulation, Barcelona, Spain – sequence: 4 givenname: Hilde surname: Janssens fullname: Janssens, Hilde organization: European Molecular Biology Laboratory, CRG Systems Biology Research Unit, Centre for Genomic Regulation, Barcelona, Spain – sequence: 5 givenname: Anna surname: Alcaine-Colet fullname: Alcaine-Colet, Anna organization: European Molecular Biology Laboratory, CRG Systems Biology Research Unit, Centre for Genomic Regulation, Barcelona, Spain – sequence: 6 givenname: Steffen surname: Lemke fullname: Lemke, Steffen organization: Department of Organismal Biology and Anatomy, University of Chicago, Chicago, United States – sequence: 7 givenname: Urs surname: Schmidt-Ott fullname: Schmidt-Ott, Urs organization: Department of Organismal Biology and Anatomy, University of Chicago, Chicago, United States – sequence: 8 givenname: Johannes surname: Jaeger fullname: Jaeger, Johannes organization: European Molecular Biology Laboratory, CRG Systems Biology Research Unit, Centre for Genomic Regulation, Barcelona, Spain |
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Keywords | stem cells RNA interference developmental system drift evolutionary biology developmental biology evolutionary developmental biology (evo-devo) gap gene network Megaselia abdita data quantification genomics D. melanogaster |
Language | English |
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SubjectTerms | Abdomen Animals Biology Blastoderm Body Patterning - genetics Chironomidae Culicidae data quantification Databases, Genetic Developmental Biology and Stem Cells developmental system drift Diptera - embryology Diptera - genetics Drift Drosophila melanogaster Drosophila melanogaster - embryology Drosophila melanogaster - genetics Drosophila Proteins - genetics Drosophila Proteins - metabolism Drosophilidae Embryo, Nonmammalian - metabolism Evolution Evolution, Molecular evolutionary developmental biology Female gap gene network Gene expression Gene Expression Regulation, Developmental Gene Regulatory Networks Genes, Insect Genomics and Evolutionary Biology Megaselia abdita Mosquitoes Phylogenetics Psychodidae RNA Interference RNA, Messenger - genetics RNA, Messenger - metabolism RNA-mediated interference Segmentation |
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Title | Quantitative system drift compensates for altered maternal inputs to the gap gene network of the scuttle fly Megaselia abdita |
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