Unequal and Genotype-Dependent Expression of Mitochondrial Genes in Larvae of the Pacific Oyster Crassostrea gigas

• Published in: The Biological bulletin (Lancaster) 2010-04, Vol.218 (2), p.122-131
• Main Authors: CUROLE, JASON P., MEYER, ELI, MANAHAN, DONAL T., HEDGECOCK, DENNIS
• Format: Article
• Language: English
• Subjects: Animals; Crassostrea; Crassostrea - genetics; Crassostrea gigas; Crosses, Genetic; DNA sequencing; DNA, Mitochondrial - chemistry; DNA, Mitochondrial - genetics; Gene Expression; Genes; Genes, Mitochondrial; Genetic aspects; Genetic loci; Genomes; Genomics; Genotype; Genotype & phenotype; Genotypes; Hybridity; Inbreeding; Larva - genetics; Larvae; Marine; Metabolism; Mitochondria; Mitochondrial DNA; Mitochondrial genes; Mitochondrial Proteins - biosynthesis; Molecular Sequence Data; Nucleotide sequencing; Oysters; Physiological aspects; PHYSIOLOGY & BIOMECHANICS; RNA; RNA, Untranslated - biosynthesis; Sequence Analysis, DNA; Signatures
• ISSN: 0006-3185; 1939-8697
• DOI: 10.1086/BBLv218n2p122

Mitochondria are essential for regulation of energy metabolism, but little is known about patterns of mitochondrial genome expression in invertebrates. To explore the association of mitochondrial expression with differential growth of Crassostrea gigas, the Pacific oyster, we crossed two inbred lines to produce inbred and hybrid larvae, which grew at different rates under the same environmental conditions. Using high-throughput cloning and sequencing methods, we identified 1.1 million expressed sequence tags from the mitochondrial genome, 96.7% of which were perfect matches to genes targeted by the method. Expression varied significantly among genes, ranging over nearly four orders of magnitude, from mt:lRNA, which constituted 21% of all transcripts, to mt:CoII, which constituted less than 0.02% of all transcripts. Variable expression of genes coding for subunits of macro-molecular complexes (e.g., mt:CoI and mt:CoII) implies that stoichiometry in these complexes must be regulated post-transcriptionally. Surprisingly, the mitochondrial transcriptome contained non-coding transcripts, which may play a role in the regulation of mitochondrial function. Finally, mitochondrial expression depended strongly on maternal factors and nuclear-cytoplasmic interactions, which may explain previously observed growth differences between reciprocal hybrids. Differences in mitochondrial gene expression could provide a biochemical index for the metabolic basis of genetically determined differences in larval growth.