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Loss of egg yolk genes in mammals and the origin of lactation and placentation.

ABSTRACT: Embryonic development in nonmammalian vertebrates depends entirely on nutritional reserves that are predominantly derived from vitellogenin proteins and stored in egg yolk. Mammals have evolved new resources, such as lactation and placentation, to nourish their developing and early offspring. However, the evolutionary timing and molecular events associated with this major phenotypic transition are not known. By means of sensitive comparative genomics analyses and evolutionary simulations, we here show that the three ancestral vitellogenin-encoding genes were progressively lost during mammalian evolution (until around 30-70 million years ago, Mya) in all but the egg-laying monotremes, which have retained a functional vitellogenin gene. Our analyses also provide evidence that the major milk resource genes, caseins, which have similar functional properties as vitellogenins, appeared in the common mammalian ancestor approximately 200-310 Mya. Together, our data are compatible with the hypothesis that the emergence of lactation in the common mammalian ancestor and the development of placentation in eutherian and marsupial mammals allowed for the gradual loss of yolk-dependent nourishment during mammalian evolution.

SUBMITTER: Brawand D

PROVIDER: S-EPMC2267819 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Eggs with the same total weight may have considerable differences in yolk weight. Eggs with a high percentage of yolk have a higher nutritional value, more flavor, and are more desirable to consumers. However, a large yolk proportion means more dry matter in the eggs, which reduces the feed efficiency. The elucidation of the genetic factors of yolk quantity in eggs is of scientific and practical significance. Through RNA sequencing, we explored the transcriptome of ovarian tissue from 12 Wenchang chickens, including 6 chickens that laid eggs with a high yolk percentage (32%) and 6 that laid low yolk percentage eggs (25%). We identified a total of 362 differentially expressed genes (P-value < 0.01, log2 fold change < -1, log2 fold change > 1), of which 220 were upregulated and 142 were downregulated in high yolk percentage hens. According to the Gene Ontology terms annotation and Kyoto Encyclopedia of Genes and Genomes enrichment analysis, the differentially expressed genes were associated with the regulation of various cell functions, cell differentiation and development, neuroactive ligand-receptor interactions, and calcium and ubiquitin-mediated proteolysis signaling pathways. To further filter for genes that were directly involved in yolk accumulation, the chicken quantitative trait loci database, genes within 100 kb upstream and downstream of the yolk weight trait SNP, and intersection genes in protein-protein interaction network diagrams were used to detect genes that overlapped with the differentially expressed genes. We found 7 candidate genes in total, MNR2, AOX1, ANTXRL, GRAMD1C, EEF2, COMP, and JUND, which affect female reproductive performance and the growth and development of follicles, supporting cell transport, cell proliferation, and differentiation. All candidate genes and several randomly selected genes were verified by quantitative real time PCR, and the results were consistent with the RNA sequencing. In conclusion, investigating the molecular mechanisms of high yolk percentage traits will allow breeding strategies to be optimized to alter the percentage of yolk in chicken eggs.

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Loss of egg yolk genes in mammals and the origin of lactation and placentation.

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