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 first-generation [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. 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. Abiotic stressors are known to impact the expression of heterosis; however, the potential role of microbes in heterosis has largely been ignored. Here, we show that heterosis of root biomass and other traits 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 versus live soil slurries in a growth chamber and for plants grown in steamed or fumigated versus untreated soil in the field. In a different field site, however, soil steaming increased rather than decreased heterosis, indicating that the direction of the effect depends on community composition, environment, or both. Together, our results demonstrate an ecological phenomenon whereby soil microbes differentially impact the early growth of inbred and hybrid maize.

Heterosis counteracts hybrid breakdown to forestall speciation by parallel natural selection

“…In spite of F 2 hybrid breakdown, we detected no postzygotic isolation in ponds because of counteracting heterosis. We detected heterosis in aquarium-raised limnetic F 1 hybrids but not in benthic F 1 hybrids, which is consistent with previous findings that features of the environment can underlie heterosis [64]. F 1 heterosis (and F 2 breakdown) is regularly observed in plants [65][66][67][68], but is not as common in outbred wild animal species.…”

The diverse effects of phenotypic dominance on hybrid fitness

“…How common, then, is this pattern? While there are many excellent examples of environment‐dependent heterosis, they rarely match the pattern described exactly—either because F1 fitness is intermediate in one of the environments (e.g., Crespel et al., 2012 , 2012 ; Martins et al., 2019 ; Munaro et al., 2011 ; Vetukhiv & Beardmore, 1959 ; Walter et al., 2020 ; Wu & Campbell, 2006 ; Wang et al., 2022 ), or because F1 fitness was not available for the individual cross directions (e.g., Benyi & Gall, 1981 ; Dittrich‐Reed, 2013 ; Domgínguez & Albornoz, 1987 ; Harrison, 1962 ; Maynard Smith, 1956 ; Stojanova et al., 2021 ; Wagner et al., 2021 ). As such we have found only two possible examples of the complete pattern.…”

Litterbag-NIRS to Forecast Yield: a Horticultural Case with Biofertilizer Effectors

“…The importance of the soil microbes in heterosis has largely been ignored. A first study by Wagner et al (2021) has shown that the heterosis of the root biomass and other traits in maize depends to a great extent on the belowground microbial environmental, although the intrinsic profile of the natural soil can drive the responses in different ways. All this underlines the importance of microbiologically defining the soil that acts as a control group in each experiment that involves microbial effectors.…”