Hybrid vigor in Drosophila: Respiration and mitochondrial energy conservation

McDaniel, Robert G.; Grimwood, Brian G.

doi:10.1016/0305-0491(71)90009-5

Cited by 13 publications

(4 citation statements)

References 14 publications

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“…This association was also reported in animals. McDaniel and Grimwood [ 51 ] demonstrated that heterosis of body weight in Drosophila melanogaster was correlated with oxidative phosphorylation efficiency. To validate the role of oxidative phosphorylation in negative heterosis of muscle yield in chickens, we further detected the ATP content and ATPase activity of breast muscle tissues for reciprocal crosses and parental lines.…”

Section: Discussionmentioning

confidence: 99%

Genetic basis of negative heterosis for growth traits in chickens revealed by genome-wide gene expression pattern analysis

Mai

Wen

et al. 2021

J Animal Sci Biotechnol

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Background Heterosis is an important biological phenomenon that has been extensively utilized in agricultural breeding. However, negative heterosis is also pervasively observed in nature, which can cause unfavorable impacts on production performance. Compared with systematic studies of positive heterosis, the phenomenon of negative heterosis has been largely ignored in genetic studies and breeding programs, and the genetic mechanism of this phenomenon has not been thoroughly elucidated to date. Here, we used chickens, the most common agricultural animals worldwide, to determine the genetic and molecular mechanisms of negative heterosis. Results We performed reciprocal crossing experiments with two distinct chicken lines and found that the body weight presented widely negative heterosis in the early growth of chickens. Negative heterosis of carcass traits was more common than positive heterosis, especially breast muscle mass, which was over − 40% in reciprocal progenies. Genome-wide gene expression pattern analyses of breast muscle tissues revealed that nonadditivity, including dominance and overdominace, was the major gene inheritance pattern. Nonadditive genes, including a substantial number of genes encoding ATPase and NADH dehydrogenase, accounted for more than 68% of differentially expressed genes in reciprocal crosses (4257 of 5587 and 3617 of 5243, respectively). Moreover, nonadditive genes were significantly associated with the biological process of oxidative phosphorylation, which is the major metabolic pathway for energy release and animal growth and development. The detection of ATP content and ATPase activity for purebred and crossbred progenies further confirmed that chickens with lower muscle yield had lower ATP concentrations but higher hydrolysis activity, which supported the important role of oxidative phosphorylation in negative heterosis for growth traits in chickens. Conclusions These findings revealed that nonadditive genes and their related oxidative phosphorylation were the major genetic and molecular factors in the negative heterosis of growth in chickens, which would be beneficial to future breeding strategies.

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Section: Discussionmentioning

confidence: 99%

Genetic basis of negative heterosis for growth traits in chickens revealed by genome-wide gene expression pattern analysis

Mai

Wen

et al. 2021

J Animal Sci Biotechnol

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“…In addition, oxidative phosphorylation forms adenosine triphosphate (ATP) as a result of the transfer of electrons from NADH or FADH2 to O 2 by a series of electron carriers related to six genes namely ATP6V1A, UQCRQ, NDUFA8, NDUFV3, NDUFB3, and UQCRC2. This pathway is also correlated with body weight in Drosophila, and is associated with heterosis in plants (Mcdaniel and Grimwood, 1971; Katara (Mai et al, 2021). The liver is the major site of amino acid metabolism and fat deposition in the body, and 37 non-conserved AS genes are significantly enriched in metabolic pathways, amino acid metabolism, and glycerolipid metabolism.…”

Section: Discussionmentioning

confidence: 99%

“…In addition, oxidative phosphorylation forms adenosine triphosphate (ATP) as a result of the transfer of electrons from NADH or FADH2 to O 2 by a series of electron carriers related to six genes namely ATP6V1A , UQCRQ , NDUFA8 , NDUFV3 , NDUFB3 , and UQCRC2 . This pathway is also correlated with body weight in Drosophila, and is associated with heterosis in plants ( Mcdaniel and Grimwood, 1971 ; Katara et al, 2020 ). By detecting ATP content and ATPase activity in reciprocal cross chickens, Mai et al validated that oxidative phosphorylation is the major genetic and molecular factor in growth ( Mai et al, 2021 ).…”

Section: Discussionmentioning

confidence: 99%

Transcriptome-Wide Analyses Identify Dominant as the Predominantly Non-Conservative Alternative Splicing Inheritance Patterns in F1 Chickens

2021

Front. Genet.

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Transcriptome analysis has been used to investigate many economically traits in chickens; however, alternative splicing still lacks a systematic method of study that is able to promote proteome diversity, and fine-tune expression dynamics. Hybridization has been widely utilized in chicken breeding due to the resulting heterosis, but the dynamic changes in alternative splicing during this process are significant yet unclear. In this study, we performed a reciprocal crossing experiment involving the White Leghorn and Cornish Game chicken breeds which exhibit major differences in body size and reproductive traits, and conducted RNA sequencing of the brain, muscle, and liver tissues to identify the inheritance patterns. A total of 40 515 and 42 612 events were respectively detected in the brain and muscle tissues, with 39 843 observed in the liver; 2807, 4242, and 4538 events significantly different between two breeds were identified in the brain, muscle, and liver tissues, respectively. The hierarchical cluster of tissues from different tissues from all crosses, based on the alternative splicing profiles, suggests high tissue and strain specificity. Furthermore, a comparison between parental strains and hybrid crosses indicated that over one third of alternative splicing genes showed conserved patterns in all three tissues, while the second prevalent pattern was non-additive, which included both dominant and transgressive patterns; this meant that the dominant pattern plays a more important role than suppression. Our study provides an overview of the inheritance patterns of alternative splicing in layer and broiler chickens, to better understand post-transcriptional regulation during hybridization.

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“…The effect of this unique evolutionary strategy on intracellular bioenergetics is unclear, but examining the effect of heterozygosity on mitochondrial function and overall fitness can inform predictions. Higher rates of coupled mitochondrial respiration and increased fitness (interpreted as heterosis) have been observed in F1 hybrids from inbred Drosophila melanogaster lines (McDaniel and Grimwood 1971;Martinez and McDaniel 1979) and natural Tigriopus californicus populations (Ellison and Burton 2008) compared to their parental lineages, whereas lower values for these traits have been observed when backcrosses lead to mismatched mitochondrial and introgressed nuclear genomes in natural populations of Tigriopus californicus (Ellison and Burton 2008) and Urosaurus (Haenel and Moore 2018). High heterozygosity of asexual vertebrates led numerous researchers to predict an increase in performance compared to sexual parental species (White 1970;Schultz 1971;Cole 1975;Mitton and Grant 1984;Bullini 1994;Cullum 1997), yet the results from several studies have contradicted these predictions by showing reduced aerobic performance in asexual lineages (Cullum 1997;Mee et al 2011;Denton et al 2017).…”

Section: Introductionmentioning

confidence: 99%

Reduced Mitochondrial Respiration in Hybrid Asexual Lizards

Klabacka

Parry

Yap

et al. 2022

The American Naturalist

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The scarcity of asexual reproduction in vertebrates alludes to an inherent cost. Several groups of asexual vertebrates exhibit lower endurance capacity (a trait predominantly sourced by mitochondrial respiration) compared to congeneric sexual species. Here we measure endurance capacity in five species of Aspidoscelis lizards and examine mitochondrial respiration between sexual and asexual species using mitochondrial respirometry. Our results show reduced endurance capacity, mitochondrial respiration, and phenotypic variability in asexual species compared to parental sexual species along with a positive relationship between endurance capacity and mitochondrial respiration. Results of lower endurance capacity and lower mitochondrial respiration in asexualAspidoscelis are consistent with hypotheses involving mitonuclear incompatibility.

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Hybrid vigor in Drosophila: Respiration and mitochondrial energy conservation

Cited by 13 publications

References 14 publications

Genetic basis of negative heterosis for growth traits in chickens revealed by genome-wide gene expression pattern analysis

Genetic basis of negative heterosis for growth traits in chickens revealed by genome-wide gene expression pattern analysis

Transcriptome-Wide Analyses Identify Dominant as the Predominantly Non-Conservative Alternative Splicing Inheritance Patterns in F1 Chickens

Reduced Mitochondrial Respiration in Hybrid Asexual Lizards

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