Climate change 2014 - Synthesis Report

Healthy plants host diverse but taxonomically structured communities of microorganisms, the plant microbiota, that colonize every accessible plant tissue. Plant-associated microbiomes confer fitness advantages to the plant host, including growth promotion, nutrient uptake, stress tolerance and resistance to pathogens. In this Review, we explore how plant microbiome research has unravelled the complex network of genetic, biochemical, physical and metabolic interactions among the plant, the associated microbial communities and the environment. We also discuss how those interactions shape the assembly of plant-associated microbiomes and modulate their beneficial traits, such as nutrient acquisition and plant health, in addition to highlighting knowledge gaps and future directions. In this Review, Trivedi and colleagues explore the interactions between plants, their associated microbial communities and the environment, and also discuss how those interactions shape the assembly of plant-associated microbiomes and modulate their beneficial traits.

Plant–microbiome interactions: from community assembly to plant health

Across plants and animals, host-associated microbial communities play fundamental roles in host nutrition, development, and immunity. The factors that shape host–microbiome interactions are poorly understood, yet essential for understanding the evolution and ecology of these symbioses. Plant roots assemble two distinct microbial compartments from surrounding soil: the rhizosphere (microbes surrounding roots) and the endosphere (microbes within roots). Root-associated microbes were key for the evolution of land plants and underlie fundamental ecosystem processes. However, it is largely unknown how plant evolution has shaped root microbial communities, and in turn, how these microbes affect plant ecology, such as the ability to mitigate biotic and abiotic stressors. Here we show that variation among 30 angiosperm species, which have diverged for up to 140 million years, affects root bacterial diversity and composition. Greater similarity in root microbiomes between hosts leads to negative effects on plant performance through soil feedback, with specific microbial taxa in the endosphere and rhizosphere potentially affecting competitive interactions among plant species. Drought also shifts the composition of root microbiomes, most notably by increasing the relative abundance of the Actinobacteria. However, this drought response varies across host plant species, and host-specific changes in the relative abundance of endosphere Streptomyces are associated with host drought tolerance. Our results emphasize the causes of variation in root microbiomes and their ecological importance for plant performance in response to biotic and abiotic stressors.

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Assembly and ecological function of the root microbiome across angiosperm plant species.

The soil microbiome governs biogeochemical cycling of macronutrients, micronutrients and other elements vital for the growth of plants and animal life. Understanding and predicting the impact of climate change on soil microbiomes and the ecosystem services they provide present a grand challenge and major opportunity as we direct our research efforts towards one of the most pressing problems facing our planet. In this Review, we explore the current state of knowledge about the impacts of climate change on soil microorganisms in different climate-sensitive soil ecosystems, as well as potential ways that soil microorganisms can be harnessed to help mitigate the negative consequences of climate change. In this Review, Jansson and Hofmockel explore the impacts of climate change on soil microorganisms in different climate-sensitive soil ecosystems and the potential ways that soil microorganisms can be harnessed to help mitigate the negative consequences of climate change.

Soil microbiomes and climate change

Root-associated microbes can improve plant growth, and they offer the potential to increase crop resilience to future drought. Although our understanding of the complex feedbacks between plant and microbial responses to drought is advancing, most of our knowledge comes from non-crop plants in controlled experiments. We propose that future research efforts should attempt to quantify relationships between plant and microbial traits, explicitly focus on food crops, and include longer-term experiments under field conditions. Overall, we highlight the need for improved mechanistic understanding of the complex feedbacks between plants and microbes during, and particularly after, drought. This requires integrating ecology with plant, microbiome, and molecular approaches and is central to making crop production more resilient to our future climate.

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Harnessing rhizosphere microbiomes for drought-resilient crop production

Root endophytes have been shown to have important roles in determining host fitness under periods of drought stress, and yet the effect of drought on the broader root endosphere bacterial community remains largely uncharacterized. In this study, we present phylogenetic profiles of bacterial communities associated with drought-treated root and rhizosphere tissues of 18 species of plants with varying degrees of drought tolerance belonging to the Poaceae family, including important crop plants. Through 16S rRNA gene profiling across two distinct watering regimes and two developmental time points, we demonstrate that there is a strong correlation between host phylogenetic distance and the microbiome dissimilarity within root tissues, and that drought weakens this correlation by inducing conserved shifts in bacterial community composition. We identify a significant enrichment in a wide variety of Actinobacteria during drought within the roots of all hosts, and demonstrate that this enrichment is higher within the root than it is in the surrounding environments. Furthermore, we show that this observed enrichment is the result of an absolute increase in Actinobacterial abundance and that previously hypothesized mechanisms for observed enrichments in Actinobacteria in drought-treated soils are unlikely to fully account for the phenomena observed here within the plant root.

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Drought and host selection influence bacterial community dynamics in the grass root microbiome.

Drought stress is a major obstacle to crop productivity, and the severity and frequency of drought are expected to increase in the coming century. Certain root-associated bacteria have been shown to mitigate the negative effects of drought stress on plant growth, and manipulation of the crop microbiome is an emerging strategy for overcoming drought stress in agricultural systems, yet the effect of drought on the development of the root microbiome is poorly understood. Through 16S rRNA amplicon and metatranscriptome sequencing, as well as root metabolomics, we demonstrate that drought delays the development of the early sorghum root microbiome and causes increased abundance and activity of monoderm bacteria, which lack an outer cell membrane and contain thick cell walls. Our data suggest that altered plant metabolism and increased activity of bacterial ATP-binding cassette (ABC) transporter genes are correlated with these shifts in community composition. Finally, inoculation experiments with monoderm isolates indicate that increased colonization of the root during drought can positively impact plant growth. Collectively, these results demonstrate the role that drought plays in restructuring the root microbiome and highlight the importance of temporal sampling when studying plant-associated microbiomes.

https://www.pnas.org/content/pnas/115/18/E4284.full.pdf

Drought delays development of the sorghum root microbiome and enriches for monoderm bacteria

Drought is the most important environmental stress limiting crop yields. The C4 cereal sorghum [Sorghum bicolor (L.) Moench] is a critical food, forage, and emerging bioenergy crop that is notably drought-tolerant. We conducted a large-scale field experiment, imposing preflowering and postflowering drought stress on 2 genotypes of sorghum across a tightly resolved time series, from plant emergence to postanthesis, resulting in a dataset of nearly 400 transcriptomes. We observed a fast and global transcriptomic response in leaf and root tissues with clear temporal patterns, including modulation of well-known drought pathways. We also identified genotypic differences in core photosynthesis and reactive oxygen species scavenging pathways, highlighting possible mechanisms of drought tolerance and of the delayed senescence, characteristic of the stay-green phenotype. Finally, we discovered a large-scale depletion in the expression of genes critical to arbuscular mycorrhizal (AM) symbiosis, with a corresponding drop in AM fungal mass in the plants' roots.

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Stephanie DeGraaf

Papers

Drought and host selection influence bacterial community dynamics in the grass root microbiome.

Drought delays development of the sorghum root microbiome and enriches for monoderm bacteria

Transcriptomic analysis of field-droughted sorghum from seedling to maturity reveals biotic and metabolic responses.