Transcriptomic analysis of growth heterosis in larval Pacific oysters ( Crassostrea gigas )

Abstract

Compared with understanding of biological shape and form, knowledge is sparse regarding what regulates growth and body size of a species. For example, the genetic and physiological causes of heterosis (hybrid vigor) have remained elusive for nearly a century. Here, we investigate gene-expression patterns underlying growth heterosis in the Pacific oyster (Crassostrea gigas) in two partially inbred (f ‫؍‬ 0.375) and two hybrid larval populations produced by a reciprocal cross between the two inbred families. We cloned cDNA and generated 4.5 M sequence tags with massively parallel signature sequencing. The sequences contain 23,274 distinct signatures that are expressed at statistically nonzero levels and show a highly positively skewed distribution with median and modal counts of 9.25 million and 3 transcripts per million, respectively. For nearly half of these signatures, expression level depends on genotype and is predominantly nonadditive (hybrids deviate from the inbred average). Statistical contrasts suggest Ϸ350 candidate genes for growth heterosis that exhibit concordant nonadditive expression in reciprocal hybrids; this represents only Ϸ1.5% of the >20,000 transcripts. Patterns of gene expression, which include dominance for low expression and even underdominance of expression, are more complex than predicted from classical dominant or overdominant explanations of heterosis. Preliminary identification of ribosomal proteins among candidate genes supports the suggestion from previous studies that efficiency of protein metabolism plays a role in growth heterosis.MPSS ͉ nonadditive expression ͉ factorial cross of partially inbred lines ͉ potence ͉ protein metabolism W hole-genome sequencing has yielded rich insights into the number of genes required to make complex eukaryotic animals (1-4). Surprisingly few genes, however, can effect major changes in body design and shape. For example, elaboration and mutation of a fairly small number of developmentally important regulatory genes, such as the Hox gene cluster, appear to have driven the evolution of the major metazoan body plans (5). Profound changes in shape or morphology, underlying adaptive differences among closely related species, also can be caused by mutations in a very few genes (6-8).Compared with our growing understanding of the evolution of biological shape and form, our understanding of what regulates body size and the rates and efficiencies of physiological functions is much less developed. For example, the genetic and physiological causes of heterosis (hybrid vigor) and its converse, inbreeding depression, have remained elusive for nearly a century, despite the economic and scientific significance of these phenomena (9-12). Major genetic explanations for heterosis are overdominance, the superiority of heterozygotes at genes affecting fitness or economic traits, dominance, the masking, in hybrids, of deleterious recessive mutations by dominant alleles inherited from one or the other inbred parent, and epistasis, the interaction of alleles at differe...

The Transcriptional Landscape of Cross-Specific Hybrids and Its Possible Link With Growth in Brook Charr (Salvelinus fontinalis Mitchill)

“…Among the most common hypotheses regarding the mechanisms underlying heterosis are: (i) dominance, which explains heterosis by masking the effect of deleterious alleles by superior alleles from the parents; (ii) overdominance, for which allelic interactions at heterozygous locus result in positive effect superior to homozygote; (iii) pseudo-overdominance, which is a positive dominance complementation of linked alleles (Lippman and Zamir 2007). Moreover, dominant patterns of expression regulation have been proposed to result from allelic dosage effects (Auger et al 2005), monoallelic expression (Birchler et al 2003), or epistatic gene interactions (Hedgecock et al 2007). The main differences observed between LD and RL hybrids lie in the proportions of maternal/paternal dominant transcripts and over-/underdominance (Table 1).…”

“…Other studies have also focused on elucidating the genomic basis of heterosis of mollusc production (Hedgecock et al 2007) and plant production (Auger et al 2005;Swanson-Wagner et al 2006;Lippman and Zamir 2007;Ge et al 2008;Stupar et al 2008). Comparative studies of genome-wide transcriptomes of parental and hybrid crosses also revealed that hybrids tended to express numerous genes at a level outside the range observed in their parental lines Ranz et al 2004;Auger et al 2005;Cui et al 2006;Hughes et al 2006;Stupar and Springer 2006;Swanson-Wagner et al 2006;Hedgecock et al 2007;Rottscheidt and Harr 2007;Ge et al 2008;Roberge et al 2008;Stupar et al 2008;Normandeau et al 2009;Renaut et al 2009). Thus, divergent lineages can accumulate divergences in gene regulation networks through time and these divergences often result in misexpressed genes (reviewed by Landry et al 2007), which could affect the viability or fitness of individuals.…”

Interpreting physiological responses to environmental change through gene expression profiling

“…In model organisms, the short signature sequences can then be mapped onto the genomic sequence, but in unsequenced organisms the genes must still be identified on a gene-by-gene basis using PCR primers based on the signature sequences. Despite this shortcoming, MPSS was used to investigate gene expression patterns underlying growth heterosis in oysters whose genome has not been sequenced, revealing that ribosomal proteins are differentially expressed, and suggesting an important role for protein metabolism in heterosis (Hedgecock et al, 2007). Finally, access to most of these technologies is only available through commercial companies, meaning that it may prove financially restrictive to use them for gene expression profiling.…”

Extensive heterosis in growth of yeast hybrids is explained by a combination of genetic models

“…Furthermore, several research approaches, such as functional genomics, transcriptomics, metabolomics and proteomics, have been applied to investigate the basis of heterosis. Such studies have tested the hypothesis that due to the genetic differences among the parental genomes, cumulative positive effects of differential gene expression in the hybrid improve the function of metabolic pathways, energy production and energetic efficiency of cellular processes in ways that lead to heterosis (Hedgecock et al, 2007;Goff, 2011;Baranwal et al, 2012;Schnable and Springer, 2013).…”