Maternal loading of a small heat shock protein increases embryo thermal tolerance in<i>Drosophila melanogaster</i>

Lockwood, Brent L.; Julick, Cole R.; Montooth, Kristi L.

doi:10.1101/150102

Cited by 11 publications

(16 citation statements)

References 84 publications

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“…Also, overexpression of Hsp23 muscle‐specific has been suggested to promote proteostasis and protect muscle from heat stress (Kawasaki et al, ). Moreover, the overexpression of muscle‐specific Hsp23 gene in female ovaries produced offspring embryos with increased thermal tolerance (Lockwood, Julick, & Montooth, ). In other species such as Leishmania donovani, the scuttle fly Megaselia scalaris and the whitefly Bemisia tabaci, Hsp23 expression is required for surviving extreme temperature treatments (Díaz et al, ; Hombach, Ommen, MacDonald, & Clos, ; Malewski et al, ).…”

Section: Discussionmentioning

confidence: 99%

A transcriptional and functional analysis of heat hardening in two invasive fruit fly species, Bactrocera dorsalis and Bactrocera correcta

Zhao

et al. 2019

Evolutionary Applications

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Many insects have the capacity to increase their resistance to high temperatures by undergoing heat hardening at nonlethal temperatures. Although this response is well established, its molecular underpinnings have only been investigated in a few species where it seems to relate at least partly to the expression of heat shock protein (Hsp) genes. Here, we studied the mechanism of hardening and associated transcription responses in larvae of two invasive fruit fly species in China, Bactrocera dorsalis and Bactrocera correcta. Both species showed hardening which increased resistance to 45°C, although the more widespread B. dorsalis hardened better at higher temperatures compared to B. correcta which hardened better at lower temperatures. Transcriptional analyses highlighted expression changes in a number of genes representing different biochemical pathways, but these changes and pathways were inconsistent between the two species. Overall B. dorsalis showed expression changes in more genes than B. correcta. Hsp genes tended to be upregulated at a hardening temperature of 38°C in both species, while at 35°C many Hsp genes tended to be upregulated in B. correcta but not B. dorsalis. One candidate gene (the small heat shock protein gene, Hsp23) with a particularly high level of upregulation was investigated functionally using RNA interference (RNAi). We found that RNAi may be more efficient in B. dorsalis, in which suppression of the expression of this gene removed the hardening response, whereas in B. correcta RNAi did not decrease the hardening response. The different patterns of gene expression in these two species at the two hardening temperatures highlight the diverse mechanisms underlying hardening even in closely related species. These results may provide target genes for future control efforts against such pest species.

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Section: Discussionmentioning

confidence: 99%

A transcriptional and functional analysis of heat hardening in two invasive fruit fly species, Bactrocera dorsalis and Bactrocera correcta

Zhao

et al. 2019

Evolutionary Applications

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“…Data availability modENCODE transcript data are publicly available online at flybase.org (Gramates et al, 2017). Phenotypic data reported herein are available from the Dryad digital repository (Lockwood et al, 2017): https://doi.org/10.5061/dryad.55cc1.…”

Section: Competing Interestsmentioning

confidence: 99%

Maternal loading of a small heat shock protein increases embryo thermal tolerance inDrosophila melanogaster

Lockwood

Julick

Montooth

2017

Journal of Experimental Biology

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Maternal investment is likely to have direct effects on offspring survival. In oviparous animals whose embryos are exposed to the external environment, maternal provisioning of molecular factors like mRNAs and proteins may help embryos cope with sudden changes in the environment. Here, we sought to modify the maternal mRNA contribution to offspring embryos and test for maternal effects on acute thermal tolerance in early embryos of We drove overexpression of a small heat shock protein gene () in female ovaries and measured the effects of acute thermal stress on offspring embryonic survival and larval development. We report that overexpression of the gene in female ovaries produced offspring embryos with increased thermal tolerance. We also found that brief heat stress in the early embryonic stage (0-1 h old) caused decreased larval performance later in life (5-10 days old), as indexed by pupation height. Maternal overexpression of protected embryos against this heat-induced defect in larval performance. Our data demonstrate that transient products of single genes have large and lasting effects on whole-organism environmental tolerance. Further, our results suggest that maternal effects have a profound impact on offspring survival in the context of thermal variability.

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“…), as well as the composition of maternally deposited mRNAs and proteins in eggs (Tadros and Lipshitz ; Lockwood et al. ; Crofton et al. ).…”

Section: Discussionmentioning

confidence: 99%

“…The composition of these maternal contributions therefore play a critical role in early development and can act as a mode of parental investment in offspring fitness, with mothers experiencing poor nutrition having more limited resources to devote to offspring fitness (Mousseau and Fox 1998). To confirm whether such effects were involved here, it would be useful to test in future studies to compare treatments for differences in egg size (Vijendravarma et al 2010), as well as the composition of maternally deposited mRNAs and proteins in eggs (Tadros and Lipshitz 2009;Lockwood et al 2017;Crofton et al 2018).…”

Section: Mechanisms Of Maternal Effect Variationmentioning

confidence: 99%

Contribution of maternal effects to dietary selection in Mediterranean fruit flies

et al. 2019

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Individual responses to dietary variation represent a fundamental component of fitness, and nutritional adaptation can occur over just a few generations. Maternal effects can show marked proximate responses to nutrition, but whether they contribute to longer term dietary adaptation is unclear. Here, we tested the hypotheses that maternal effects: (i) contribute to dietary adaptation, (ii) diminish when dietary conditions are constant between generations, (iii) are trait‐specific and (iv) interact with high‐ and low‐quality food. We used experimental evolution regimes in the medfly ( Ceratitis capitata ) to test these predictions by subjecting an outbred laboratory‐adapted population to replicated experimental evolution on either constant high calorie sugar (‘A’) or low‐calorie starch (‘S’) larval diets, with a standard adult diet across both regimes. We measured the contribution of maternal effects by comparing developmental and adult phenotypes of individuals reared on their own diet with those swapped onto the opposite diet for either one or two generations (high and low maternal effect conditions, respectively), both at the start and after 30 generations of selection. Initially, there were strong maternal effects on female body mass and male mating success but not larval survival. Interestingly, the initial maternal effects observed in female body mass and male mating success showed sex‐specific interactions when individuals from high calorie regimes were tested on low calorie diets. However, as populations responded to selection, the effects of maternal provisioning on all traits diminished. The results broadly supported the predictions. They show how the contribution of maternal effects to dietary responses evolves in a context‐dependent manner, with significant variation across different fitness‐related traits. We conclude that maternal effects can evolve during nutritional adaptation and hence may be an important life history trait to measure, rather than to routinely minimize.

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Maternal loading of a small heat shock protein increases embryo thermal tolerance inDrosophila melanogaster

Cited by 11 publications

References 84 publications

A transcriptional and functional analysis of heat hardening in two invasive fruit fly species, Bactrocera dorsalis and Bactrocera correcta

A transcriptional and functional analysis of heat hardening in two invasive fruit fly species, Bactrocera dorsalis and Bactrocera correcta

Maternal loading of a small heat shock protein increases embryo thermal tolerance inDrosophila melanogaster

Contribution of maternal effects to dietary selection in Mediterranean fruit flies

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