Microbe-dependent heterosis in maize

Abstract

Hybrids account for nearly all commercially planted varieties of maize and many other crop plants, because crosses between inbred lines of these species produce F1 offspring that greatly outperform their parents. The mechanisms underlying this phenomenon, called heterosis or hybrid vigor, are not well understood despite over a century of intensive research (1). The leading hypotheses--which focus on quantitative genetic mechanisms (dominance, overdominance, and epistasis) and molecular mechanisms (gene dosage and transcriptional regulation)--have been able to explain some but not all of the observed patterns of heterosis (2, 3). However, possible ecological drivers of heterosis have largely been ignored. Here we show that heterosis of root biomass and germination in maize is strongly dependent on the belowground microbial environment. We found that, in some cases, inbred lines perform as well by these criteria as their F1 offspring under sterile conditions, but that heterosis can be restored by inoculation with a simple community of seven bacterial strains. We observed the same pattern for seedlings inoculated with autoclaved vs. live soil slurries in a growth chamber, and for plants grown in fumigated vs. untreated soil in the field. Together, our results demonstrate a novel, ecological mechanism for heterosis whereby soil microbes generally impair the germination and early growth of inbred but not hybrid maize.