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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.

SUBMITTER: Wagner MR

PROVIDER: S-EPMC8325155 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Heterosis, which has greatly increased maize yields, is associated with gene expression patterns during key developmental stages that enhance hybrid phenotypes relative to parental phenotypes. Before heterosis can be more effectively used for crop improvement, hybrid maize developmental gene expression patterns must be better understood. Here, six maize hybrids, including the popular hybrid Zhengdan958 (ZC) from China, were studied. Maize hybrids created in-house were generated using an incomplete diallel cross (NCII)-based strategy from four elite inbred parental lines. Differential gene expression (DEG) profiles corresponding to three developmental stages revealed that hybrid partial expression patterns exhibited complementarity of expression of certain parental genes, with parental allelic expression patterns varying both qualitatively and quantitatively in hybrids. Single-parent expression (SPE) and parent-specific expression (PSE) types of qualitative variation were most prevalent, 43.73 and 41.07% of variation, respectively. Meanwhile, negative super-dominance (NSD) and positive super-dominance (PSD) types of quantitative variation were most prevalent, 31.06 and 24.30% of variation, respectively. During the early reproductive growth stage, the gene expression pattern differed markedly from other developmental stage patterns, with allelic expression patterns during seed development skewed toward low-value parental alleles in hybrid seeds exhibiting significant quantitative variation-associated superiority. Comparisons of qualitative gene expression variation rates between ZC and other hybrids revealed proportions of SPE-DEGs (41.36%) in ZC seed DEGs that significantly exceeded the average proportion of SPE-DEGs found in seeds of other hybrids (28.36%). Importantly, quantitative gene expression variation rate comparisons between ZC and hybrids, except for transgressive expression, revealed that the ZC rate exceeded the average rate for other hybrids, highlighting the importance of partial gene expression in heterosis. Moreover, enriched ZC DEGs exhibiting distinct tissue-specific expression patterns belonged to four biological pathways, including photosynthesis, plant hormone signal transduction, biology metabolism and biosynthesis. These results provide valuable technical insights for creating hybrids exhibiting strong heterosis.

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Microbe-dependent heterosis in maize.

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