An official website of the United States government
Summary Macroorganisms’ genotypes shape their phenotypes, which in turn shape the habitat available to potential microbial symbionts. This influence of host genotype on microbiome composition has been demonstrated in many systems; however, most previous studies have either compared unrelated genotypes or delved into molecular mechanisms. As a result, it is currently unclear whether the heritability of host‐associated microbiomes follows similar patterns to the heritability of other complex traits.We take a new approach to this question by comparing the microbiomes of diverse maize inbred lines and their F1hybrid offspring, which we quantified in both rhizosphere and leaves of field‐grown plants using 16S‐v4 and ITS1 amplicon sequencing.We show that inbred lines and hybrids differ consistently in the composition of bacterial and fungal rhizosphere communities, as well as leaf‐associated fungal communities. A wide range of microbiome features display heterosis within individual crosses, consistent with patterns for nonmicrobial maize phenotypes. For leaf microbiomes, these results were supported by the observation that broad‐sense heritability in hybrids was substantially higher than narrow‐sense heritability.Our results support our hypothesis that at least some heterotic host traits affect microbiome composition in maize.
more »
« less
Microbe-dependent heterosis in maize
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 F1offspring 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.
more »
« less
- PAR ID:
- 10277456
- Publisher / Repository:
- Proceedings of the National Academy of Sciences
- Date Published:
- Journal Name:
- Proceedings of the National Academy of Sciences
- Volume:
- 118
- Issue:
- 30
- ISSN:
- 0027-8424
- Page Range / eLocation ID:
- Article No. e2021965118
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Yuan, Y (Ed.)Abstract Disease resistance in plants can be conferred by single genes of large effect or by multiple genes each conferring incomplete resistance. The latter case, termed quantitative resistance, may be difficult for pathogens to overcome through evolution due to the low selection pressures exerted by the actions of any single gene and, for some diseases, is the only identified source of genetic resistance. We evaluated quantitative resistance to 2 diseases of maize in a biparental mapping population as well as backcrosses to both parents. Quantitative trait locus analysis shows that the genetic architecture of resistance to these diseases is characterized by several modes of gene action including additivity as well as dominance, overdominance, and epistasis. Heterosis or hybrid vigor, the improved performance of a hybrid compared with its parents, can be caused by nonadditive gene action and is fundamental to the breeding of several crops including maize. In the backcross populations and a diverse set of maize hybrids, we find heterosis for resistance in many cases and that the degree of heterosis appears to be dependent on both hybrid genotype and disease.more » « less
-
The hybrid between female channel catfish (Ictalurus punctatus) and male blue catfish (Ictalurus furcatus) is superior in feed conversion, disease resistance, carcass yield, and harvestability compared to both parental species. However, heterosis and heterobeltiosis only occur in pond culture, and channel catfish grow much faster than the other genetic types in small culture units. This environment-dependent heterosis is intriguing, but the underlying genetic mechanisms are not well understood. In this study, phenotypic characterization and transcriptomic analyses were performed in the channel catfish, blue catfish, and their reciprocal F1s reared in tanks. The results showed that the channel catfish is superior in growth-related morphometrics, presumably due to significantly lower innate immune function, as investigated by reduced lysozyme activity and alternative complement activity. RNA-seq analysis revealed that genes involved in fatty acid metabolism/transport are significantly upregulated in channel catfish compared to blue catfish and hybrids, which also contributes to the growth phenotype. Interestingly, hybrids have a 40–80% elevation in blood glucose than the parental species, which can be explained by a phenomenon called transgressive expression (overexpression/underexpression in F1s than the parental species). A total of 1140 transgressive genes were identified in F1 hybrids, indicating that 8.5% of the transcriptome displayed transgressive expression. Transgressive genes upregulated in F1s are enriched for glycan degradation function, directly related to the increase in blood glucose level. This study is the first to explore molecular mechanisms of environment-dependent heterosis/heterobeltiosis in a vertebrate species and sheds light on the regulation and evolution of heterosis vs. hybrid incompatibility.more » « less
-
Abstract Although the importance of the soil microbiome in mediating plant community structures and functions has been increasingly emphasized in ecological studies, the biological processes driving crop diversity overyielding remain unexplained in agriculture. Based on the plant–soil feedback (PSF) theory and method, we quantified to what extent and how soil microbes contributed to intercropping overyielding.Soils were collected as inocula and sequenced from a unique 10‐year field experiment, consisting of monoculture, intercropping and rotation planted with wheat (Triticum aestivum), maize (Zea mays)or faba bean (Vicia faba). A PSF greenhouse study was conducted to test microbial effects on three crops' growth in monoculture or intercropping.In wheat & faba bean (W&F) and maize & faba bean (M&F) systems, soil microbes drove intercropping overyielding compared to monoculture, with 28%–51% of the overyielding contributed by microbial legacies. The overyielding effects resulted from negative PSFs in both systems, as crops, in particular faba bean grew better in soils conditioned by other crops than itself. Moreover, faba bean grew better in soils from intercropping or rotation than from the average of monocultures, indicating a strong positive legacy effect of multispecies cropping systems. However, with positive PSF and negative legacy benefit effect of intercropping/rotation, we did not observe significant overyielding in the W&M system.With more bacterial and fungal dissimilarities by metabarcoding in heterospecific than its own soil, the better it improved faba bean growth. More detailed analysis showed faba bean monoculture soil accumulated more putative pathogens with higherFusariumrelative abundance and moreFusarium oxysporumgene copies by qPCR, while in heterospecific soils, there were less pathogenic effects when cereals were engaged. Further analysis in maize/faba bean intercropping also showed an increase of rhizobia relative abundance.Synthesis and applications. Our results demonstrate a soil microbiome‐mediated advantage in intercropping through suppression of the negative PSF of pathogens and increasing beneficial microbes. As microbial mediation of overyielding is context‐dependent, we conclude that the dynamics of both beneficial and pathogenic microbes should be considered in designing cropping systems for sustainable agriculture, particularly including combinations of legumes and cereals.more » « less
-
A biphasic trajectory for maize stalk mechanics shaped by genetic, environmental, and biotic factorsSUMMARY Stalk mechanical properties impact plant stability and interactions with pathogenic microorganisms. The evaluation of stalk mechanics has focused primarily on the end‐of‐season outcomes and defined differences among inbred and hybrid maize genotypes. However, there is a gap in understanding how these different end‐of‐season outcomes are achieved. This study measured stalk flexural stiffness in maize inbred genotypes across multiple environments and in maize commercial hybrid genotypes under different disease states. Under all conditions, stalk flexural stiffness followed a biphasic trajectory, characterized by a linear increase phase and a sustained phase. Within a genotype, the environment or disease state altered the rate of increase in the linear phase but did not impact the timing of transition to the sustained phase. Whereas between genotypes, the timing of transition between phases varied. Destructive 3‐point bend tests of inbred stalks showed that the trajectory of stalk mechanics is defined by the bending modulus, not the geometry. Together, these results define a biphasic trajectory of maize stalk mechanics that can be modulated by internal and external factors. This work provides a foundation for breeding programs to make informed decisions when selecting for optimized stalk mechanical trajectories, which are necessary for enhancing resilience to environmental stresses.more » « less
