Sorghum Root Flavonoid Chemistry, Cultivar, and Frost Stress Effects on Rhizosphere Bacteria and Fungi

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Abstract

Biotic stresses, including fungal infections, result in increased production of flavonoid compounds, including 3-deoxyanthocyanidins (3-DAs), in the leaf tissues of Sorghum bicolor. Our objectives were to determine whether sorghum genotypic variation influenced root flavonoid and 3-DA concentrations and rhizosphere microbial communities and to identify how these relationships were affected by abiotic stress. We evaluated root chemicals and rhizosphere microbiomes of five near-isogenic lines of sorghum before and after a late-season frost. Roots were analyzed for total flavonoids, total phenolics, 3-DA concentrations, and antioxidant activity. Amplicon sequencing of 16S ribosomal RNA genes and internal transcribed spacer regions was performed on rhizosphere soils. Concentrations of luteolinidin (a 3-DA) and total flavonoids differed between several lines before frost; however, these relationships changed after frost. Luteolinidin increased in three lines after frost, whereas total flavonoids decreased in all the lines after frost. Lines that differed in luteolinidin and total flavonoid concentrations before frost were different from those after frost. Rhizosphere community compositions also differed before and after frost but only fungal community compositions differed among sorghum lines. Bacterial community compositions were highly correlated with total flavonoid and luteolinidin concentrations. Furthermore, a greater number of bacterial taxa were correlated with total flavonoids and luteolinidin compared with fungal taxa. Collectively, this study provides evidence that plant genotypic variation influences root flavonoids and rhizosphere community composition and that these relationships are affected by frost. Plant–microbe interactions and secondary metabolite production may be important components to include for selective breeding of sorghum for frost stress tolerance.

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Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota

Lingfei Hu, Christelle A M Robert, Selma Cadot … (2018)

By changing soil properties, plants can modify their growth environment. Although the soil microbiota is known to play a key role in the resulting plant-soil feedbacks, the proximal mechanisms underlying this phenomenon remain unknown. We found that benzoxazinoids, a class of defensive secondary metabolites that are released by roots of cereals such as wheat and maize, alter root-associated fungal and bacterial communities, decrease plant growth, increase jasmonate signaling and plant defenses, and suppress herbivore performance in the next plant generation. Complementation experiments demonstrate that the benzoxazinoid breakdown product 6-methoxy-benzoxazolin-2-one (MBOA), which accumulates in the soil during the conditioning phase, is both sufficient and necessary to trigger the observed phenotypic changes. Sterilization, fungal and bacterial profiling and complementation experiments reveal that MBOA acts indirectly by altering root-associated microbiota. Our results reveal a mechanism by which plants determine the composition of rhizosphere microbiota, plant performance and plant-herbivore interactions of the next generation.

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Root Exudation of Primary Metabolites: Mechanisms and Their Roles in Plant Responses to Environmental Stimuli

Alberto Canarini, Christina Kaiser, Andrew Merchant … (2019)

Root exudation is an important process determining plant interactions with the soil environment. Many studies have linked this process to soil nutrient mobilization. Yet, it remains unresolved how exudation is controlled and how exactly and under what circumstances plants benefit from exudation. The majority of root exudates including primary metabolites (sugars, amino acids, and organic acids) are believed to be passively lost from the root and used by rhizosphere-dwelling microbes. In this review, we synthetize recent advances in ecology and plant biology to explain and propose mechanisms by which root exudation of primary metabolites is controlled, and what role their exudation plays in plant nutrient acquisition strategies. Specifically, we propose a novel conceptual framework for root exudates. This framework is built upon two main concepts: (1) root exudation of primary metabolites is driven by diffusion, with plants and microbes both modulating concentration gradients and therefore diffusion rates to soil depending on their nutritional status; (2) exuded metabolite concentrations can be sensed at the root tip and signals are translated to modify root architecture. The flux of primary metabolites through root exudation is mostly located at the root tip, where the lack of cell differentiation favors diffusion of metabolites to the soil. We show examples of how the root tip senses concentration changes of exuded metabolites and translates that into signals to modify root growth. Plants can modify the concentration of metabolites either by controlling source/sink processes or by expressing and regulating efflux carriers, therefore challenging the idea of root exudation as a purely unregulated passive process. Through root exudate flux, plants can locally enhance concentrations of many common metabolites, which can serve as sensors and integrators of the plant nutritional status and of the nutrient availability in the surrounding environment. Plant-associated micro-organisms also constitute a strong sink for plant carbon, thereby increasing concentration gradients of metabolites and affecting root exudation. Understanding the mechanisms of and the effects that environmental stimuli have on the magnitude and type of root exudation will ultimately improve our knowledge of processes determining soil CO2 emissions, ecosystem functioning, and how to improve the sustainability of agricultural production.

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Root exudates regulate soil fungal community composition and diversity.

Corey D. Broeckling, Amanda K Broz, Joy Bergelson … (2008)

Plants are in constant contact with a community of soil biota that contains fungi ranging from pathogenic to symbiotic. A few studies have demonstrated a critical role of chemical communication in establishing highly specialized relationships, but the general role for root exudates in structuring the soil fungal community is poorly described. This study demonstrates that two model plant species (Arabidopsis thaliana and Medicago truncatula) are able to maintain resident soil fungal populations but unable to maintain nonresident soil fungal populations. This is mediated largely through root exudates: the effects of adding in vitro-generated root exudates to the soil fungal community were qualitatively and quantitatively similar to the results observed for plants grown in those same soils. This effect is observed for total fungal biomass, phylotype diversity, and overall community similarity to the starting community. Nonresident plants and root exudates influenced the fungal community by both positively and negatively impacting the relative abundance of individual phylotypes. A net increase in fungal biomass was observed when nonresident root exudates were added to resident plant treatments, suggesting that increases in specific carbon substrates and/or signaling compounds support an increased soil fungal population load. This study establishes root exudates as a mechanism through which a plant is able to regulate soil fungal community composition.