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

doi:10.1073/pnas.0610880104

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

*Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089-0371; and
^‡Solexa, Inc., 25861 Industrial Boulevard, Hayward, CA 94545

Communicated by George N. Somero, Stanford University, Pacific Grove, CA, December 8, 2006 (received for review May 6, 2006)

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 ≈350 candidate genes for growth heterosis that exhibit concordant nonadditive expression in reciprocal hybrids; this represents only ≈1.5% 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.

Footnotes

^†To whom correspondence should be addressed. E-mail: dhedge{at}usc.edu
Author contributions: D.H., D.T.M., and B.B. designed the project, C.D.H. and E.M. performed research; C.D.H. contributed new bioinformatic tools; D.H., J.-Z.L., S.D., and C.D.H. analyzed MPSS data; and D.H., S.D., C.D.H., E.M., and D.T.M. wrote the paper.
↵ ^§Present address: Forestgenix, LLC, 5566 San Juan Way, Pleasanton, CA 94566.
↵ ^¶Present address: Gene-fx, Inc., Berkeley, CA 94705.
Conflict of interest statement: J.-Z.L., S.D., C.D.H., and B.B. were employees of Lynx Therapeutics, Inc., at the time this work was done. C.D.H. remains an employee of Solexa, Inc., which merged with Lynx Therapuetics in 2005.
Data deposition: The data reported in this paper have been deposited in the Gene Expression Omnibus (GEO) database, www.ncbi.nlm.nih.gov/geo (series GSE3596, platform GPL3062, and samples GSM83048–GSM83051). The sequences from the Megaclone libraries have been deposited in the GenBank database (accession nos. DV736295–DV736964).
Abbreviations:

D,

dominance;

FS,

four-stepper;

MPSS,

massively parallel signature sequencing;

OD,

overdominance;

PD,

partial dominance;

SNP,

single-nucleotide polymorphism;

tpm,

transcripts per million;

TS,

two-stepper;

UD,

underdominance.
Freely available online through the PNAS open access option.