Abstract
The cladoceran crustacean Daphnia has long been a model of energy allocation studies due to its important position in the trophic cascade of freshwater ecosystems. However, the loci for controlling energy allocation between life history traits still remain unknown. Here, we report CRISPR/Cas-mediated target mutagenesis of DNA methyltransferase 3.1 (DNMT3.1) that is upregulated in response to caloric restriction in Daphnia magna. The resulting biallelic mutant is viable and did not show any change in growth rate, reproduction, and longevity under nutrient rich conditions. In contrast, under starved conditions, the growth rate of this DNMT3.1 mutant was increased but its reproduction was reciprocally reduced compared to the wild type when the growth and reproduction activities competed during a period from instar 4 to 8. The life span of this mutant was significantly shorter than that of the wild type. We also compared transcriptomes between DNMT3.1 mutant and wild type under nutrient-rich and starved conditions. Consistent with the DNMT3.1 mutant phenotypes, the starved condition led to changes in the transcriptomes of the mutant including differential expression of vitellogenin genes. In addition, we found upregulation of the I am not dead yet (INDY) ortholog, which has been known to shorten the life span in Drosophila, explaining the shorter life span of the DNMT3.1 mutant. These results establish DNMT3.1 as a key regulator for life span and energy allocation between growth and reproduction during caloric restriction. Our findings reveal how energy allocation is implemented by selective expression of a DNMT3 ortholog that is widely distributed among animals. We also infer a previously unidentified adaptation of Daphnia that invests more energy for reproduction than growth under starved conditions.
Highlights
The cladoceran crustacean Daphnia has long been a model of energy allocation studies due to its important position in the trophic cascade of freshwater ecosystems
We have previously shown that Daphnia DNMT3.1 was upregulated in response to starvation, suggesting a potential function of this gene for energy allocation
We introduced a mutation into DNMT3.1 and analyzed phenotypes of its mutant under caloric restriction
Summary
The cladoceran crustacean Daphnia has long been a model of energy allocation studies due to its important position in the trophic cascade of freshwater ecosystems. We found upregulation of the I am not dead yet (INDY) ortholog, which has been known to shorten the life span in Drosophila, explaining the shorter life span of the DNMT3.1 mutant These results establish DNMT3.1 as a key regulator for life span and energy allocation between growth and reproduction during caloric restriction. Based on energy utilization at an individual level, a theory called the Dynamic Energy budget, which can predict population dynamics, has been proposed[17] In addition to those studies at the individual and population levels, genes affecting life history traits have been investigated in model organisms including Drosophila melanogaster, which led to the identification of genetic factors controlling lifespan and fecundity such as Insulin-like receptor[18, 19], Forkhead box O (Foxo)[20], and I am not dead yet (Indy)[21]. In the honeybee (Apis mellifera), silencing of DNMT3 altered the developmental fate of workers-destined larvae towards queen-like t raits[33]
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