Epistatic QTL for yield heterosis in tomato

Controlled population development and genome-wide association studies have
proven powerful in uncovering genes and alleles underlying complex traits.
An underexplored dimension of such studies is the phenotypic contribution
of non-additive interactions between quantitative trait loci (QTL).
Capturing such epistasis in a genome-wide manner requires very large
populations to represent replicated combinations of loci whose
interactions determine phenotypic outcomes. Here, we dissect epistasis
using a densely genotyped population of 1400 backcross-inbred lines (BILs)
between a modern processing tomato inbred (Solanum lycopersicum) and the
Lost Accession of a distant, green-fruited, drought-tolerant wild species,
Solanum pennellii. The homozygous BILs, each representing an average of 11
introgressions, and their hybrids with the recurrent parents were
phenotyped for tomato yield components. Population-wide mean yield of the
BILs was less than 50% of that of their hybrids (BILH), and
correspondingly, homozygous introgressions across the genome reduced yield
relative to recurrent parent while several QTL of the BILHs independently
improved productivity. Analysis of two QTL scans showed 32 cases of less
than additive and 48 cases of more than additive interactions. Strikingly,
one epistatic interaction involving S. pennellii QTL on
chromosomes 1 and 7, which independently did not affect yield, increased
fruit yield by 20-50% in the double introgression hybrid grown in
irrigated and dry fields over a period of three years and varied genetic
backgrounds. Our work demonstrates the power of large, interspecific
controlled population development to uncover hidden QTL phenotypes, and
how rare epistatic interactions can improve crop productivity via
heterosis.