Compatibility between mitochondrial and nuclear genomes correlates with the quantitative trait of lifespan in Caenorhabditis elegans

Abstract

Mutations in mitochondrial genome have epistatic effects on organisms depending on the nuclear background, but a role for the compatibility of mitochondrial-nuclear genomes (mit-n) in the quantitative nature of a complex trait remains unexplored. We studied a panel of recombinant inbred advanced intercrossed lines (RIAILs) of C. elegans that were established from a cross between the N2 and HW strains. We determined the HW nuclear genome content and the mitochondrial type (HW or N2) of each RIAIL strain. We found that the degree of mit-n compatibility was correlated with the lifespans but not the foraging behaviors of RIAILs. Several known aging-associated QTLs individually showed no relationship with mitotypes but collectively a weak trend consistent with a role in mit-n compatibility. By association mapping, we identified 293 SNPs that showed linkage with lifespan and a relationship with mitotypes consistent with a role in mit-n compatibility. We further found an association between mit-n compatibility and several functional characteristics of mitochondria as well as the expressions of genes involved in the respiratory oxidation pathway. The results provide the first evidence implicating mit-n compatibility in the quantitative nature of a complex trait, and may be informative to certain evolutionary puzzles on hybrids.

Modern human origins: multiregional evolution of autosomes and East Asia origin of Y and mtDNA

“…Sharing of physiology should be informative for a phonetic approach of phylogeny. Coevolution of mtDNA, Y, and autosomes has been found by many previous studies (25,(65)(66)(67)(68), which may play a key role in the diversification into multiple haplotypes during AMH radiation from its place of origin to other regions by hybridization with archaic humans. People who have stayed relatively unchanged in physiology and living environments from the ancestor would be expected to have few deviations from the ancestor haplotype and their present day living place would indicate place of origin for the ancestor.…”

“…Seemingly unexpectedly, certain Neanderthals found in Europe is most closely related to Asians (Vi33. 25) or Americans (Vi33.26), and one of the three Neanderthals closest to Africans was closer to East Asians than to Europeans. However, this would be expected if Africans associated with the Neanderthal exit had entered Asia or South Asia via the Northern route from Siberia or possibly a Southern route.…”

“…Most SNPs in these DNAs can be proven to be under selection, e.g. certain SNPs or haplotypes of mtDNA or Y chr are known to be related to human diseases or compatibility with nuclear genomes (25,(61)(62)(63)(64)(65). Sharing of alleles of mtDNA or Y chr should mean similar selection, reflecting both environments and physiology or primarily physiology when saturation has been reached.…”

“…In recent years, a more complete molecular evolutionary theory, the maximum genetic distance or diversity (MGD) hypothesis, has been making steady progress in solving both evolutionary and contemporary biomedical problems (20)(21)(22)(23)(24)(25)(26)(27). The core concept of the MGD theory, maximum genetic diversity, is a priori expected and supported by numerous facts (20,28,29).…”

MOTS‐c: A Mitochondrial‐Encoded Regulator of the Nucleus

“…Further, polymorphisms in a mitochondrial‐encoded tRNA and a nuclear‐encoded tRNA synthetase, which are independently silent, cause significant developmental and reproductive defects in flies when combined . In worms, association mapping in a panel of hybrids, generated by a cross between C. elegans strains (N2 and HW), indicated that the quantitative trait of aging may depend on genome‐wide quantitative variations in mitonuclear genomic compatibility . Interspecies cytoplasmic–nuclear hybrids (cybrids) within Caenorhabditis briggsae showed that mitonuclear discord can reduce fecundity, increase adiposity, and elevate ROS levels .…”