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 (Birchler et al. 2003). 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 (Stuber et al. 1992;Birchler 2015). 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.

Plant Breeding and Microbiome

“…To increase the level of sustainability, various agroecological management strategies of agricultural production systems have been reviewed, including the use of microorganisms in the process of plant domestication, genetic improvement, and the production of improved varieties. According to the references presented in the scientific literature, to increase agricultural production and the sustainability of production systems, future research should develop breeding methods that optimize symbiosis in crops [9], since the interactions with soil microorganisms could be important for the expression of heterosis in some species [20], proposing an alternative framework to produce new phenotypes by modifying genomic information and the microbiota associated with plants [3]; efficient interaction with certain beneficial microorganisms is expected to be an additional factor in plant production. These new agricultural practices can include the reproduction of the microbiome, the transplantation and engineering of specific microbiomes [30] and their transfer through seeds [3,43] or in vitro culture [46].…”

“…These results suggest that advances in the development of maize hybrids have had a significant impact on the microbial communities of the rhizosphere and on the assembly of their interaction networks. Wagner et al [20] found that interactions with soil microorganisms are important for the expression of heterosis in corn and Zambonin et al [21], found no significant interaction between corn hybrids and inoculation with Azospirillum sp. for the variables studied including grain yield, and the specificity between maize hybrids and inoculation was not verified.…”

Grain Yield of Maize Hybrids in Response to Inoculation with Azospirillum sp. under Nitrogen Limiting Conditions in Huaura, Peru

“…The significance of the variance components show in this case that the effect of treatments was similar to or greater than the effect of the corn hybrids per se, which suggests that the response in grain yield in the corn cultivars may be balanced with nitrogen fertilization and inoculation with Azospirillum sp. ; this aspect has been studied by Wagner et al (2020) who demostrated that interactions with soil microorganisms are important for the expression of heterosis in corn.…”

“…Correa-Galeote et al (2016) suggested that the genotype of Andean starchy maize could be the main factor in controlling bacterial diversity in its rhizosphere, either in monoculture or in association with other plants. The results of Wagner et al (2020) show that interactions with soil microorganisms are important for the expression of heterosis in corn. Recently, SCAR-type molecular markers have been developed for the identification of A. brasilense (Coniglio et al 2020).…”

Genetic basis of a spontaneous mutation’s expressivity

“…A commonly observed form of background effect among individuals carrying the same mutation is different degrees of response to that mutation (or ‘variable expressivity’) (4). Variable expressivity can arise due to a myriad of reasons, including genetic interactions (or epistasis) between a mutation and segregating loci (1), dominance (1), stochastic noise (5), the microbiome (6), and the environment (1).…”