Heterosis of leaf and rhizosphere microbiomes in field-grown maize

Abstract

Word count (Total): 6693 Word count (Introduction): 818 Word count (Methods): 3241 Word count (Results): 1859 Word count (Discussion): 783 Number of figures: 6 (all in color) Number of tables: 1 Supporting Information: 4 tables + 7 figures (all in color) Word count (Acknowledgements): 105 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 F1 hybrid 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 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 non-microbial 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.

Phyllosphere microbiota: Community dynamics and its interaction with plant hosts

“…The host plant is Arabidopsis thaliana, unless otherwise stated. Less is known about fungi and oomycetes, although there have been studies profiling the fungal or oomycete communities in the phyllosphere of different plant species (e.g., Arabidopsis, rice, maize, and tropical mangrove) (Horton et al, 2014;Agler et al, 2016;Yao et al, 2019;Wagner et al, 2020). Studies using fluorescence-based approaches have also demonstrated the diversity and spatial distribution patterns of different bacterial taxa on the leaf surface of Arabidopsis and bean plants (Remus-Emsermann et al, 2014;Esser et al, 2015).…”

“…Various studies in different plant species, including Arabidopsis , grapevine, and the perennial mustard plant Boechera stricta , have shown that the leaf and root microbiotas can overlap substantially in key community members, although the overall community structure and composition can differ (Bai et al, 2015; Zarraonaindia et al, 2015; Wagner et al, 2016). These studies suggest that the leaf and root microbiotas may be derived from a similar source (i.e., soil) and/or that the two communities may interact with each other in natural environments (e.g., through wind, rain splashing, or insect movement) (Vogel et al, 2016; Tkacz et al, 2020; Liu et al, 2020a). The soil origin of the phyllosphere microbiota is supported by reports showing that both root and leaf microbiotas depend on the soil community (Zarraonaindia et al, 2015; Finkel et al, 2019) and that some endophytic rhizobia bacteria inoculated in soil can migrate to rice leaves through vascular tissue (Chi et al, 2005).…”

“…The phyllosphere microbiota is quite diverse and changeable. Many environmental and ecological factors, such as climate (sunlight, ultraviolet irradiation, and precipitation), insect/pathogen infection, field management (e.g., fertilizer), and soil type, greatly influence assembly of the microbiota (Vogel et al, 2016; Tkacz et al, 2020; Liu et al, 2020a). Within the holobiont, plant genotype, microbe–microbe interaction, and metabolites (e.g., sugar, other carbon sources, or leaf exudates) together shape the microbiota community, and there can be cross‐talk between the three (e.g., plant genetics can mediate and determine the specific types of microbe–microbe interactions or metabolite production).…”

“…A number of studies have shown that the phyllosphere microbiota, at the community‐ or individual‐strain level, can enhance the disease resistance of plants to pathogens, which could be mediated by the production of antimicrobial compounds, microbe–microbe competition or activation of plant defense (Lindow and Suslow, 2003; Vogel et al, 2016; Preininger et al, 2018). For instance, Berg and colleagues showed that a phyllosphere community derived from the “leaf wash” of tomato leaves or a SynCom of 12 bacterial strains protects tomato plants from infection by Pseudomonas syringae pathogen, and the level of protection is associated with the initial dose and community composition (Berg and Koskella, 2018).…”

Water Stress and Disruption of Mycorrhizae Induce Parallel Shifts in Phyllosphere Microbiome Composition

“…In contrast to previous work in the rhizosphere microbiome (Carrión et al 2019; H. Liu et al 2021), transplanting microbial communities from stressful conditions onto plants in the growth chamber did not improve disease resistance, so we cannot conclude whether stress-induced compositional shifts in phyllosphere microbiota are adaptive for the host plant. While it is always possible that other, unmeasured traits were improved by microbiome transplant, our results may reflect growing evidence that host selection is weaker in the phyllosphere than the rhizosphere (Wagner et al 2020).…”