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. 2024 Apr 3;226(4):iyae014.
doi: 10.1093/genetics/iyae014.

Maternal mitochondrial function affects paternal mitochondrial inheritance in Drosophila

Jinguo Cao  1   2 , Yuying Luo  1 , Yonghe Chen  3 , Zhaoqi Wu  1 , Jiting Zhang  1 , Yi Wu  4   5 , Wen Hu  4
Affiliations

Maternal mitochondrial function affects paternal mitochondrial inheritance in Drosophila

Jinguo Cao et al. Genetics. .

Abstract

The maternal inheritance of mitochondria is a widely accepted paradigm, and mechanisms that prevent paternal mitochondria transmission to offspring during spermatogenesis and postfertilization have been described. Although certain species do retain paternal mitochondria, the factors affecting paternal mitochondria inheritance in these cases are unclear. More importantly, the evolutionary benefit of retaining paternal mitochondria and their ultimate fate are unknown. Here we show that transplanted exogenous paternal D. yakuba mitochondria can be transmitted to offspring when maternal mitochondria are dysfunctional in D. melanogaster. Furthermore, we show that the preserved paternal mitochondria are functional, and can be stably inherited, such that the proportion of paternal mitochondria increases gradually in subsequent generations. Our work has important implications that paternal mitochondria inheritance should not be overlooked as a genetic phenomenon in evolution, especially when paternal mitochondria are of significant differences from the maternal mitochondria or the maternal mitochondria are functionally abnormal. Our results improve the understanding of mitochondrial inheritance and provide a new model system for its study.

Keywords: Drosophila; mt:CoⅠ; mitochondria transmission; mtDNA; paternal mitochondria inheritance.

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Conflict of interest statement

Conflicts of interest The authors declare that they have no conflict of interest.

Figures

Fig. 1.
Fig. 1.
The pupal eclosion rate from the cross mt: CoⅠts females with Het males correlates with the age of female flies. a) Schematics of the mitochondrial genome and the D loop regions of D. yakuba and D. melanogaster. PCR primers specifically targeting the unique regions of D. yakuba and D. melanogaster mtDNA sequences are shown. b) The pupal eclosion rates of w1118, mt: CoⅠts, and the Het flies. The results shown are mean ± SE. c) The pupal eclosion rate of F1 flies from the cross of mt: CoⅠts females (ages, 1–15 days) with Het males. The results shown are mean ± SE.
Fig. 2.
Fig. 2.
Detection of paternal mtDNA in F1 flies from the cross mt: CoⅠts females with Het males. a) Paternal D. yakuba mtDNA can be detected in F1 flies from the cross mt: CoⅠts females with Het males. Amplified DNA fragments from mtDNA of mt: CoⅠts and Het are used as negative and positive controls. b) Amplified DNA fragments of F1 flies from the cross mt: CoⅠts females with Het males are shown aligned with D. yakuba mtDNA sequence. c) Mitochondrial and nuclear extracts from mt: CoⅠts, Het, and F1 flies were separated and amplified with D. yakuba specific primers. Amplified fragments can be detected in the mitochondrial extracts from Het and F1 flies, but not in the nuclear extracts. d) Real-time RT–PCR analysis of mtDNA content. d) yakuba mtDNA in F1 flies is about 5.85% and in Fn (n > 30) is about 103.76% of Het flies. Four data sets were averaged. The content of D. yakuba mtDNA in F1 (*P < 0.05) and Fn (****P < 0.0001) flies is significantly different from that in mt: CoⅠts flies. e) Mitochondrial Respiratory Chain Complex Ⅳ Activity of Het, mt: CoⅠts and F1 flies at 29°C. F1 flies acquire about 45.67% complex Ⅳ activity of wild-type flies. The results shown are mean ± SE. Six data sets were averaged. The complex Ⅳ Activity in F1 flies is significantly different from that in mt: CoⅠts flies (***P < 0.001).
Fig. 3.
Fig. 3.
Detection of paternal mtDNA in F1 flies from control crosses. a) Detection of paternal D. yakuba mtDNA in F1 flies from the cross mt: CoⅠts females with Het males at 18°C. Amplified DNA fragments from mtDNA of mt: CoⅠts and Het flies are used as negative and positive controls. No amplified bands could be detected from mt: CoⅠts × Het F1 flies cultured at 18°C. b) Detection of paternal D. yakuba mtDNA in F1 flies from the cross w1118 females with Het males at 29°C. Amplified DNA fragments from mtDNA of mt: CoⅠts and Het flies are used as negative and positive controls. c) Real-time RT–PCR analysis of mtDNA content. The content of D. yakuba mtDNA in F1 flies from mt: Colts females ×Het males at 18℃ and w1118 females ×Het males at 29℃ has no significant difference to that in mt: Colts flies. Three data sets were averaged.
Fig. 4.
Fig. 4.
Detection of paternal mtDNA in the F3, F4 generations and the bodies/ovaries of F3 flies. a) Detection of paternal D. yakuba mtDNA in F3 flies. Amplified D. yakuba DNA fragments from mt:CoⅠts and Het flies were used as negative and positive controls. b) Detection of paternal D. yakuba mtDNA in F4 flies. Amplified DNA fragments from mt:CoⅠts and Het flies were used as negative and positive controls. c) Detection of D. yakuba mtDNA in the bodies and ovaries of F3 flies. Dissected ovaries and bodies from F3 flies were separately subjected to DNA extraction. Amplified D. yakuba DNA fragments were detected in F3 ovaries and bodies.
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