Drought shifts sorghum root metabolite and microbiome profiles and enriches the stress response factor pipecolic acid

Caddell, Daniel; Louie, Katherine; Bowen, Benjamin P.; Sievert, Julie; Hollingsworth, Joy; Dahlberg, Jeff; Purdom, Elizabeth; Northen, Trent; Coleman‐Derr, Devin

doi:10.1101/2020.11.08.373399

Cited by 8 publications

(5 citation statements)

References 99 publications

(138 reference statements)

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“…However few studies have identified changes of rhizosphere metabolites in soil in response to abiotic stressors. For example, Caddell et al 2021 investigated the dynamics of sorghum rhizosphere metabolites during drought (87), and Mavrodi et al (2012) established that phenazines accumulate in the rhizosphere of dryland cereals (88), but responses to nutrient limitation, in particular, have been understudied in rhizosphere soil. Here, we demonstrate that metabolites recovered from the rhizosphere soil of switchgrass shifted in response to nutrient (N, P) and water-limited conditions.…”

Section: Discussionmentioning

confidence: 99%

Nutrient and moisture limitation reveal keystone metabolites that link switchgrass rhizosphere metabolome and microbiome dynamics

Baker¹,

Zhalnina

Yuan³

et al. 2022

Preprint

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Plants exude large quantities of rhizosphere metabolites that can modulate composition and activity of microbial communities in response to environmental stress. While rhizodeposition dynamics have been associated with rhizosphere microbiome succession, and may be particularly impactful in stressful conditions, specific evidence of these connections has rarely been documented. Here, we grew the bioenergy crop switchgrass (Panicum virgatum) in a marginal soil, under nutrient limited, moisture limited, +nitrogen (N), and +phosphorus (P) conditions, to identify links between rhizosphere chemistry, microbiome dynamics, and abiotic stressors. To characterize links between rhizosphere microbial communities and metabolites, we used 16S rRNA amplicon sequencing and LC-MS/MS-based metabolomics. We measured significant changes in rhizosphere metabolite profiles in response to abiotic stress and linked them to changes in microbial communities using network analysis. N-limitation amplified the abundance of aromatic acids, pentoses, and their derivatives in the rhizosphere, and their enhanced availability was linked to the abundance of diverse bacterial lineages from Acidobacteria, Verrucomicrobia, Planctomycetes, and Alphaproteobacteria. Conversely, N-amended conditions enhanced the availability of N-rich rhizosphere compounds, which coincided with proliferation of Actinobacteria. Treatments with contrasting N availability differed greatly in the abundance of potential keystone metabolites; serotonin, ectoine, and acetylcholine were particularly abundant in N-replete soils, while chlorogenic, cinnamic, and glucuronic acids were found in N-limited soils. Serotonin, the keystone metabolite we identified with the largest number of links to microbial taxa, significantly affected root architecture and growth of rhizosphere microorganisms, highlighting its potential to shape microbial community and mediate rhizosphere plant-microbe interactions.

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Section: Discussionmentioning

confidence: 99%

Nutrient and moisture limitation reveal keystone metabolites that link switchgrass rhizosphere metabolome and microbiome dynamics

Baker¹,

Zhalnina

Yuan³

et al. 2022

Preprint

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“…To simulate the carbon sources available in the sorghum rhizosphere, a new media recipe was designed based on previously reported metabolomics analysis of the rhizosphere soil of sorghum grown plants (Caddell et al, 2020). The base formula represents a MOPS Media Enhanced (MME) solution, to which a select group of carbon and nitrogen sources were added.…”

Section: Ssm Media Formulationmentioning

confidence: 99%

Defined synthetic microbial communities colonize and benefit field-grown sorghum

Fonseca-García,

Wilson,

Elmore

et al. 2023

Preprint

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The rhizosphere represents a dynamic and complex interface between plant hosts and the microbial community found in the surrounding soil. While it is recognized that manipulating the rhizosphere has the potential to improve plant fitness and health, engineering the rhizosphere microbiome through inoculation has often proved challenging. This is in large part due to the competitive microbial ecosystem in which the added microbes must survive, and lack of adaptation of these added microbes to the specific metabolic and environmental pressures of the rhizosphere. Here, we constructed an inoculation formula using a defined synthetic community (dSynCom) approach that we hypothesized would improve engraftment efficiency and potentially the relationship with the host plant, Sorghum bicolor. The dSynCom was assembled from bacterial isolates that were either: 1) identified to potentially play a role in community cohesion through network analysis, or 2) identified to benefit from host-specific exudate compounds. Growth of the dSynCom was first evaluated in vitro on solid media, secondly in planta under gnotobiotic laboratory conditions, and finally using sorghum plants grown in the field. We demonstrate that the dSynCom performs best in terms of maintaining diversity when grown in the presence of the plant host in lab conditions, and that many lineages are lost from the community when grown either in vitro or in a native field setting. Finally, we demonstrate that the dSynCom is able to promote growth of above- and below-ground plant phenotypes compared to uninoculated controls, both in the lab and when applied to plants grown in the field. These results demonstrate the potential utility of SynComs for supporting crop performance even in the absence of persistence, and the need for a deeper mechanistic understanding of community control of host fitness in agricultural contexts.

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“…These processes are orchestrated by multilayer components involving plants, microorganisms, soil, and environmental traits that shape the final result. The accumulation of stress-related factors in plant roots during drought, including G3P and pipecolic acid, has been linked to actinobacteria enrichment in the rhizosphere (Knight et al, 2018;Caddell et al, 2020; Table 2).…”

Section: Plant-mediated Reshaping Of Microbiota Composition In Respon...mentioning

confidence: 99%

Plant-microbiome interactions under drought—insights from the molecular machinist’s toolbox

Ait-El-Mokhtar,

Meddich,

Baslam

2023

Front. Sustain. Food Syst.

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Plants face numerous challenges in novel and harsh environments, including altered precipitation regimes, salinity, extreme temperatures, increased atmospheric CO2, nutrient deficiency, heavy metals, and oxygen. Drought remains a major constraint to crop productivity and meeting food demand, with the frequency, intensity, and duration of drought expected to raise in the coming century. The “cry for help” hypothesis proposes that timely recruiting of the microbiome by plants may confer benefits in stress alleviation, plant growth, fitness, and health. The root-associated microbiome harbors 10–100 times more functional genes than the host, which can significantly stimulate the metabolic and genetic potential of plant–microbiome assembly. However, cross-talk among drought and the root-associated microbes, and among the root-associated microbiome and the host-plant, is less well understood. Understanding the molecular aspect of multiple mechanisms by which microbes associate with plants during drought stress is of fundamental importance in plant biology and agriculture. In this review, we examine the progress in research on the response of plant and its microbiome assemblages and interactions to drought stress, including the impact of drought and root exudates on host resilience. We delve into the potential of ‘omics’ technologies to unravel the signaling networks underlying these interactions and the multiway interactions that occur among the host and its associated microbiome. We then discuss the shortfalls, challenges, and future research directions in this field. Overall, we argue that harnessing/manipulating the crop microbiome presents a promising strategy for improving agricultural systems in the face of global climate change.

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Drought shifts sorghum root metabolite and microbiome profiles and enriches the stress response factor pipecolic acid

Cited by 8 publications

References 99 publications

Nutrient and moisture limitation reveal keystone metabolites that link switchgrass rhizosphere metabolome and microbiome dynamics

Nutrient and moisture limitation reveal keystone metabolites that link switchgrass rhizosphere metabolome and microbiome dynamics

Defined synthetic microbial communities colonize and benefit field-grown sorghum

Plant-microbiome interactions under drought—insights from the molecular machinist’s toolbox

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