Tall fescue cultivar and fungal endophyte combinations influence plant growth and root exudate composition

Guo, Jing; McCulley, Rebecca L.; McNear, David H.

doi:10.3389/fpls.2015.00183

Cited by 83 publications

(67 citation statements)

References 108 publications

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“…Stands with higher endophyte-infection frequencies contain more soil C and N than E-stands or stands with low frequencies of infected tall fescue, presumably due to decreased microbial activity or altered plant inputs (Franzluebbers et al 1999;Guo et al 2015;Iqbal et al 2012). Therefore, because factors such as nutrient availability have been shown to influence nonsymbiotic N fixation in grassland soils (ZechmeisterBoltenstern and Kinzel 1990), non-symbiotic N fixing soil microorganisms may also be affected by CTE+ tall fescue, which has further implications for altered Npools and dynamics in pastures.…”

Section: Introductionmentioning

confidence: 99%

Fungal endophyte symbiosis alters nitrogen source of tall fescue host, but not nitrogen fixation in co-occurring red clover

et al. 2015

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Background and aims Infection of tall fescue with the common toxic fungal endophyte Epichloë coenophiala harms livestock via toxic alkaloid production; therefore, non-toxic 'novel' strains of the endophyte have been developed and released. How different endophyte strains impact biological nitrogen fixation (BNF) in mixed species pastures is unknown. We asked whether novel endophyte or common toxic endophyte-infected (NE+; CTE+) tall fescue affects symbiotic and nonsymbiotic BNF, and utilization of biologically-fixed nitrogen in tall fescue. Methods Tall fescue was planted either endophyte-free (E-), infected with CTE, two non-toxic strains AR542 NE, AR584 NE, or a blend of endophyte treatments. We measured natural abundance of 15 N in plant and soil samples, and conducted soil acetylene reduction assays. Results Endophyte presence and strain significantly affected the δ 15 N of tall fescue. Near red clover, CTE+ and AR584 NE+ tall fescue were most 15 N-depleted; but away, E-tall fescue was most 15 N-depleted. Endophyte strain significantly influenced N concentration in red clover, but not symbiotic or non-symbiotic BNF.Conclusions Endophyte strains produce different effects on tall fescue's competitive ability and nitrogen utilization. In mixed pastures, deployment of NE strains for decreased alkaloid toxicity will differentially impact use of biologically fixed nitrogen in tall fescue and nitrogen concentration in red clover. Abbreviations CTE+common toxic endophyte-infected Eendophyte-free BNF biological nitrogen fixation NE+ novel endophyte-infected EMix equal mix of E-, CTE+, AR542 NE+, and AR584 NE+ treatments within plot PDF pasture demonstration farm RC red clover TF(+RC) tall fescue plant located close to red clover TF(-RC) tall fescue plant located away from red clover CF-IRMS continuous flow isotope ratio mass spectrometer ARA acetylene reduction assay Plant Soil

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Section: Introductionmentioning

confidence: 99%

Fungal endophyte symbiosis alters nitrogen source of tall fescue host, but not nitrogen fixation in co-occurring red clover

et al. 2015

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“…Previous studies have suggested that the alteration of plant metabolic responses during this stage correspond to the lifestyles of the microbe attempting to infect the plant tissues. For example, root exudate composition was found to vary with the type of endophytes colonizing tall fescue (Guo et al, 2015). Sugar and amino acid content in tomato root exudates have been shown to be differentially impacted by the application of biocontrol Fusarium sp.…”

Section: Introductionmentioning

confidence: 99%

The Influence of Contrasting Microbial Lifestyles on the Pre-symbiotic Metabolite Responses of Eucalyptus grandis Roots

et al. 2019

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Plant roots co-inhabit the soil with a diverse consortium of microbes of which a number attempt to enter symbiosis with the plant. These microbes may be pathogenic, mutualistic, or commensal. Hence, the health and survival of plants is heavily reliant on their ability to perceive different microbial lifestyles and respond appropriately. Emerging research suggests that there is a pivotal role for plant root secondary metabolites in responding to microbial colonization. However, it is largely unknown if plants are able to differentiate between microbes of different lifestyles and respond differently during the earliest stages of pre-symbiosis (i.e., prior to physical contact). In studying plant responses to a range of microbial isolates, we questioned: (1) if individual microbes of different lifestyles and species caused alterations to the plant root metabolome during pre-symbiosis, and (2) if these early metabolite responses correlate with the outcome of the symbiotic interaction in later phases of colonization. We compared the changes of the root tip metabolite profile of the model tree Eucalyptus grandis during pre-symbiosis with two isolates of a pathogenic fungus (Armillaria luteobubalina), one isolate of a pathogenic oomycete (Phytophthora cinnamomi), two isolates of an incompatible mutualistic fungus (Suillus granulatus), and six isolates of a compatible mutualistic fungus (Pisolithus microcarpus). Untargeted metabolite profiling revealed predominantly positive root metabolite responses at the pre-symbiosis stage, prior to any observable phenotypical changes of the root tips. Metabolite responses in the host tissue that were specific to each microbial species were identified. A deeper analysis of the root metabolomic profiles during pre-symbiotic contact with six strains of P. microcarpus showed a connection between these early metabolite responses in the root with later colonization success. Further investigation using isotopic tracing revealed a portion of metabolites found in root tips originated from the fungus. RNA-sequencing also showed that the plant roots undergo complementary transcriptomic reprogramming in response to the fungal stimuli. Taken together, our results demonstrate that the early metabolite responses of plant roots are partially selective toward the lifestyle of the interacting microbe, and that these responses can be crucial in determining the outcome of the interaction.

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“…Whereas the majority of metabolites used as signals between organisms in plant-microbe interactions are common to both mutualistic and pathogenic symbioses (Wong et al, 2019;Xu et al, 2015), there are also examples in the literature where either soil microbes or their plant hosts release genusor species-specific metabolites that facilitate their interaction. For example, root exudate contents of tomato and tall fescue vary based on the type of soil-microbes with which they were interacting (Guo, McCulley, & McNear, 2015;Kamilova, Kravchenko, Shaposhnikov, Makarova, & Lugtenberg, 2006). Similarly, soil-microbes can produce specific metabolites to facilitate root colonization on host plants; the secretion of hypaphorine by the ectomycorrhizal fungus Pisolithus tinctorius is related to colonization (Beguiristain & Lapeyrie, 1997).…”

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Comparative metabolomics implicates threitol as a fungal signal supporting colonization of Armillaria luteobubalina on eucalypt roots

Wong-Bajracharya

Plett

Natera

et al. 2019

Plant Cell & Environment

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Armillaria root rot is a fungal disease that affects a wide range of trees and crops around the world. Despite being a widespread disease, little is known about the plant molecular responses towards the pathogenic fungi at the early phase of their interaction. With recent research highlighting the vital roles of metabolites in plant root–microbe interactions, we sought to explore the presymbiotic metabolite responses of Eucalyptus grandis seedlings towards Armillaria luteobuablina, a necrotrophic pathogen native to Australia. Using a metabolite profiling approach, we have identified threitol as one of the key metabolite responses in E. grandis root tips specific to A. luteobubalina that were not induced by three other species of soil‐borne microbes of different lifestyle strategies (a mutualist, a commensalist, and a hemi‐biotrophic pathogen). Using isotope labelling, threitol detected in the Armillaria‐treated root tips was found to be largely derived from the fungal pathogen. Exogenous application of d‐threitol promoted microbial colonization of E. grandis and triggered hormonal responses in root cells. Together, our results support a role of threitol as an important metabolite signal during eucalypt‐Armillaria interaction prior to infection thus advancing our mechanistic understanding on the earliest stage of Armillaria disease development. Comparative metabolomics of eucalypt roots interacting with a range of fungal lifestyles identified threitol enrichment as a specific characteristic of Armillaria pathogenesis. Our findings suggest that threitol acts as one of the earliest fungal signals promoting Armillaria colonization of roots.

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Tall fescue cultivar and fungal endophyte combinations influence plant growth and root exudate composition

Cited by 83 publications

References 108 publications

Fungal endophyte symbiosis alters nitrogen source of tall fescue host, but not nitrogen fixation in co-occurring red clover

Fungal endophyte symbiosis alters nitrogen source of tall fescue host, but not nitrogen fixation in co-occurring red clover

The Influence of Contrasting Microbial Lifestyles on the Pre-symbiotic Metabolite Responses of Eucalyptus grandis Roots

Comparative metabolomics implicates threitol as a fungal signal supporting colonization of Armillaria luteobubalina on eucalypt roots

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