Genetic Variation for Ontogenetic Shifts in Metabolism Underlies Physiological Homeostasis in <i>Drosophila</i>

Matoo, Omera B.; Julick, Cole R.; Montooth, Kristi L.

doi:10.1534/genetics.119.302052

Cited by 28 publications

(39 citation statements)

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“…For example, mutations in the Drosophila mitochondrial pyruvate carrier MPC1, which render cells unable to transport pyruvate into the mitochondria, elicit no obvious phenotypes when mutant larvae are raised under standard growth conditions (Bricker et al, 2012). Moreover, natural populations of Drosophila can buffer larval development against significant variations in mitochondrial oxidative capacity and the scaling relationship between mass and metabolic rate (Matoo et al, 2019). A similar phenomenon is also observed in Caenorhabditis elegans, where entire metabolic pathways are rewired in response to dietary stress or genetic mutations (MacNeil et al, 2013;Watson et al, 2014Watson et al, , 2016.…”

Section: Drosophila As a Model For Studying Metabolic Plasticitymentioning

confidence: 99%

Lactate dehydrogenase and glycerol-3-phosphate dehydrogenase cooperatively regulate growth and carbohydrate metabolism during Drosophila melanogaster larval development

Rai

Buddika

et al. 2019

Development

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The dramatic growth that occurs during Drosophila larval development requires rapid conversion of nutrients into biomass. Many larval tissues respond to these biosynthetic demands by increasing carbohydrate metabolism and lactate dehydrogenase (LDH) activity. The resulting metabolic program is ideally suited for synthesis of macromolecules and mimics the manner by which cancer cells rely on aerobic glycolysis. To explore the potential role of Drosophila LDH in promoting biosynthesis, we examined how Ldh mutations influence larval development. Our studies unexpectedly found that Ldh mutants grow at a normal rate, indicating that LDH is dispensable for larval biomass production. However, subsequent metabolomic analyses suggested that Ldh mutants compensate for the inability to produce lactate by generating excess glycerol-3phosphate (G3P), the production of which also influences larval redox balance. Consistent with this possibility, larvae lacking both LDH and G3P dehydrogenase (GPDH1) exhibit growth defects, synthetic lethality and decreased glycolytic flux. Considering that human cells also generate G3P upon inhibition of lactate dehydrogenase A (LDHA), our findings hint at a conserved mechanism in which the coordinate regulation of lactate and G3P synthesis imparts metabolic robustness to growing animal tissues.

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Section: Drosophila As a Model For Studying Metabolic Plasticitymentioning

confidence: 99%

Lactate dehydrogenase and glycerol-3-phosphate dehydrogenase cooperatively regulate growth and carbohydrate metabolism during Drosophila melanogaster larval development

Rai

Buddika

et al. 2019

Development

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“…This high-throughput method enables larger, more efficient experiments and can be applied to a wide array of aquatic taxa and experimental designs. Due to its ability to quantify fine-scale differences in a relatively short amount of time, the high-throughput fluorometry technique is common in, for example, water quality management (Carstea, Bridgeman, Baker, & Reynolds, 2016;Gregor & Maršálek, 2005), agriculture (Kalaji et al, 2014(Kalaji et al, , 2018, physiology (Bergman Filho, Soares, & Loureiro, 2011;Matoo, Julick, & Montooth, 2019), and medical microbiology (Chinen et al, 2015). To date, these methods and practical tools remain relatively underutilized in aquatic ecology, disease ecology, and evolutionary epidemiology.…”

Section: Discussionmentioning

confidence: 99%

A high‐throughput method to quantify feeding rates in aquatic organisms: A case study with Daphnia

Hite

Pfenning-Butterworth

Vetter

et al. 2020

Ecology and Evolution

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Food ingestion is one of the most basic features of all organisms. However, obtaining precise—and high‐throughput—estimates of feeding rates remains challenging, particularly for small, aquatic herbivores such as zooplankton, snails, and tadpoles. These animals typically consume low volumes of food that are time‐consuming to accurately measure. We extend a standard high‐throughput fluorometry technique, which uses a microplate reader and 96‐well plates, as a practical tool for studies in ecology, evolution, and disease biology. We outline technical and methodological details to optimize quantification of individual feeding rates, improve accuracy, and minimize sampling error. This high‐throughput assay offers several advantages over previous methods, including i) substantially reduced time allotments per sample to facilitate larger, more efficient experiments; ii) technical replicates; and iii) conversion of in vivo measurements to units (mL‐1 hr‐1 ind‐1) which enables broad‐scale comparisons across an array of taxa and studies. To evaluate the accuracy and feasibility of our approach, we use the zooplankton, Daphnia dentifera, as a case study. Our results indicate that this procedure accurately quantifies feeding rates and highlights differences among seven genotypes. The method detailed here has broad applicability to a diverse array of aquatic taxa, their resources, environmental contaminants (e.g., plastics), and infectious agents. We discuss simple extensions to quantify epidemiologically relevant traits, such as pathogen exposure and transmission rates, for infectious agents with oral or trophic transmission.

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“…This compensation 332 could be through mechanisms of physiological homeostasis (see e.g. 94 ) or through clonal 333 selection favoring lineages with mito-nuclear genotypes in which mutations in the nuclear 334 genome compensate for the deleterious mutations in the mitochondrial genome. One potentially 335 important source for genetic and/or physiological compensation might be polyploidy, as sexual 336 P. antipodarum are all diploid and asexual P. antipodarum are all polyploid 55 .…”

Section: Discussion 312mentioning

confidence: 99%

Phenotypic variation in mitochondrial function across New Zealand snail populations

Greimann

Fahrner

Woodell

et al. 2017

Preprint

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1Mitochondrial function is critical for energy homeostasis and should shape how genetic variation 2 in metabolism is transmitted through levels of biological organization to generate stability in 3 organismal performance. Mitochondrial function is encoded by genes in two distinct and 4 separately inherited genomes -the mitochondrial genome and the nuclear genome -and selection 5 is expected to maintain functional mito-nuclear interactions. Nevertheless, high levels of 6 polymorphism in genes involved in these mito-nuclear interactions and variation for 7 mitochondrial function are nevertheless frequently observed, demanding an explanation for how 8 and why variability in such a fundamental trait is maintained. Potamopyrgus antipodarum is a 9New Zealand freshwater snail with coexisting sexual and asexual individuals and, accordingly, 10 contrasting systems of separate vs. co-inheritance of nuclear and mitochondrial genomes. As 11 such, this snail provides a powerful means to dissect the evolutionary and functional 12 consequences of mito-nuclear variation. The lakes inhabited by P. antipodarum span wide 13 environmental gradients, with substantial across-lake genetic structure and mito-nuclear 14 discordance. This situation allows us to use comparisons across reproductive modes and lakes to 15 partition variation in cellular respiration across genetic and environmental axes. Here, we 16 integrated cellular, physiological, and behavioral approaches to quantify variation in 17 mitochondrial function across a diverse set of wild P. antipodarum lineages. We found 18 extensive across-lake variation in organismal oxygen consumption, mitochondrial membrane 19 potential, and behavioral response to heat stress, but few global effects of reproductive mode or 20 sex. Taken together, our data set the stage for applying this important model system for sexual 21 reproduction and polyploidy to dissecting the complex relationships between mito-nuclear 22 variation, performance, plasticity, and fitness in natural populations. 23 3 24 KEYWORDS 25 asexual reproduction, JC-1, mitochondria, oxygen consumption, Potamopyrgus antipodarum, 26 sexual reproduction 27

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Genetic Variation for Ontogenetic Shifts in Metabolism Underlies Physiological Homeostasis in Drosophila

Abstract: Organismal physiology emerges from metabolic pathways and structures that can vary across development and among individuals. Matoo, Julick, and Montooth found significant variation, both genetic and ontogenetic, in mitochondrial physiology in wild-type and mitochondrial-nuclear...

Cited by 28 publications

References 93 publications

Lactate dehydrogenase and glycerol-3-phosphate dehydrogenase cooperatively regulate growth and carbohydrate metabolism during Drosophila melanogaster larval development

Lactate dehydrogenase and glycerol-3-phosphate dehydrogenase cooperatively regulate growth and carbohydrate metabolism during Drosophila melanogaster larval development

A high‐throughput method to quantify feeding rates in aquatic organisms: A case study with Daphnia

Phenotypic variation in mitochondrial function across New Zealand snail populations

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