Mycorrhiza-Triggered Transcriptomic and Metabolomic Networks Impinge on Herbivore Fitness

Kaling, Moritz; Schmidt, Anna Mareike; Moritz, Franco; Rosenkranz, Maaria; Witting, Michael; Kasper, Karl; Janz, Dennis; Schmitt‐Kopplin, Philippe; Schnitzler, Jörg‐Peter; Polle, Andrea

doi:10.1104/pp.17.01810

Cited by 74 publications

(106 citation statements)

References 94 publications

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“…Low-molecular weight secondary metabolites contribute to plant defence and to systemic resistance against invading pathogens and other threats 29,35,42 . Our RNAseq data showed that L. bicolor treatment resulted in significant upregulation of the camalexin biosynthesis genes PAD3 and CYP71A13 (Figure 2 and Supplementary Table 1).…”

Section: Resultsmentioning

confidence: 99%

“…In addition to interactions with rhizobacteria, most vascular plants (>90%) form beneficial symbioses with arbuscular mycorrhizal (AM) fungi or ectomycorrhizal (ECM) fungi 24 . Both AM and ECM fungi can induce ISR on their host plants against foliar pests and pathogens 25–29 . AM symbiosis requires the Common Symbiotic Pathway (CSP) for initiation of successful symbiosis 30 ; recent evidence suggests that ECM symbiosis may also depend on the CSP 31 .…”

Section: Introductionmentioning

confidence: 99%

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Ectomycorrhizal fungi induce systemic resistance against insects on a non-mycorrhizal plant in a CERK1-dependent manner

Vishwanathan

Zienkiewicz²,

Liu

et al. 2019

Preprint

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20Below-ground microbes can induce systemic resistance (ISR) against foliar pests and 21 pathogens on diverse plant hosts. The prevalence of ISR among plant-microbe-pest systems 22 raises the question of host specificity in microbial induction of ISR. To test whether ISR is 23 limited by plant host range, we tested the ISR-inducing ectomycorrhizal (ECM) fungus 24 Laccaria bicolor on the non-mycorrhizal plant Arabidopsis. We found that root inoculation 25 with L. bicolor triggered ISR against the insect herbivore Trichoplusia ni and induced systemic 26 susceptibility (ISS) against the bacterial pathogen Pseudomonas syringae pv. tomato DC3000 27 (Pto). We found that L. bicolor-triggered ISR against T. ni was dependent on jasmonic acid 28 (JA) signaling and salicylic acid (SA) biosynthesis and signaling. We found that heat killed L. 29 bicolor and chitin are sufficient to trigger ISR against T. ni and ISS against Pto and that the 30 chitin receptor CERK1 is necessary for L. bicolor-mediated effects on systemic immunity. 31Collectively our findings suggest that some ISR responses might not require intimate co-32 evolution of host and microbe, but rather might be the result of root perception of conserved 33 microbial signals. 34 35 Plants associate with complex communities of microorganisms. Interplay of host and 36 microbial genotype determine whether the outcome of specific plant-microbe interactions is 37 beneficial or detrimental to plant health 1-3 . Plants possess receptors to sense potential 38 pathogens including transmembrane pattern-recognition receptors that recognize conserved 39 microbe-associated molecular patterns (MAMPs), and intracellular receptors that directly or 40 indirectly recognize effectors to help limit pathogen growth 4,5 . MAMP perception by plant 41 receptors triggers pattern-triggered immunity (PTI) responses including a reactive oxygen 42 species (ROS) burst, Mitogen-Activated Protein Kinase (MAPK) signaling, ion influx and 43 callose deposition 6-9 . In addition to local immune mechanisms, root-associated microbes can 44 induce systemic resistance (ISR) against a diverse spectrum of above-ground threats 2,10 . While 45 the mechanisms by which plants perceive MAMPs and effectors are well understood, there is 46 a more limited understanding of the mechanisms by which plant perceive the microbes that 47 trigger ISR. 48 In response to perception of microbes or pathogens, plants activate systemic defense 49 mechanisms including commensal-triggered ISR and pathogen-triggered systemic acquired 50 resistance (SAR) 11,12 . While both SAR and ISR confer resistance to pests and pathogens, they 51 promote resistance through distinct mechanisms 2 . SAR occurs upon local perception of a 52 pathogen, MAMP, or effector and results in systemic induction of SA-dependent gene 53 expression and accumulation of secondary metabolites 13,14 . Unlike SAR, ISR is associated with 54 small or no changes in systemic gene expression and phytohormone levels 15,16 . Additionally, 55while SAR is dependent...

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Ectomycorrhizal fungi induce systemic resistance against insects on a non-mycorrhizal plant in a CERK1-dependent manner

Vishwanathan

Zienkiewicz²,

Liu

et al. 2019

Preprint

Self Cite

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“…Biochemical transformations were inferred by calculating all possible pairwise mass differences within a sample’s spectrum and matching differences (within 1□ppm) to a list of common biochemical transformations 50 . Biochemical transformations were identified following the procedures described by Breitling et al 50 and previously employed by Bailey et al 34 , Graham et al 10,11 , Moritz et al 36 , Kaling et al 35 , and Stegen et al 12 . Briefly, pairwise mass differences between all m/z peaks in a sample were compared with a reference list of 1298 commonly observed biochemical reactions of organic matter (Supplementary Table 2).…”

Section: Methodsmentioning

confidence: 99%

Carbon limitation leads to thermodynamic regulation of aerobic metabolism

Garayburu‐Caruso

Stegen

Song

et al. 2020

Preprint

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13Organic matter (OM) metabolism in freshwater ecosystems is a critical source of uncertainty in 14 global biogeochemical cycles, yet aquatic OM cycling remains poorly understood. Here, we 15 present the first work to explicitly test OM thermodynamics as a key regulator of aerobic 16 respiration, challenging long-held beliefs that organic carbon and oxygen concentrations are the 17 primary determinants of respiration rates. We pair controlled microcosm experiments with 18 ultrahigh-resolution OM characterization to demonstrate a clear relationship between OM 19 thermodynamic favorability and aerobic respiration under carbon limitation. We also 20 demonstrate a shift in the regulation of aerobic respiration from OM thermodynamics to nitrogen 21 content when carbon is in excess, highlighting a central role for OM thermodynamics in aquatic 22 biogeochemical cycling particularly in carbon-limited ecosystems. Our work therefore 23 illuminates a structural gap in aquatic biogeochemical models and presents a new paradigm in 24 which OM thermodynamics and nitrogen content interactively govern aerobic respiration. 25 26 27 3 Metabolism of organic matter (OM) in freshwater ecosystems plays a large role in global 28 biogeochemical cycles 1-3 , as freshwater ecosystems emit more than 2 Pg C yr -1 into the 29 atmosphere 4,5 . These emissions are largely dominated by contributions from river corridors 1,5,6 , 30 and within the river corridor, areas of groundwater-surface water mixing (hyporheic zones) have 31 a disproportionate impact on aerobic respiration 7-9 . Recent field observations have suggested that 32 OM chemistry, and in particular OM thermodynamics, are key to predicting aerobic respiration 33 in hyporheic zones 10-12 . If supported, these observations challenge a widespread paradigm that 34 organic carbon and oxygen concentrations are the primary determinants of aerobic respiration 35 rates and highlight a key source of model uncertainty. Yet, no work has provided direct evidence 36 for OM thermodynamics as a regulator of aerobic respiration in a controlled laboratory 37 environment. Demonstrating this behavior would identify mechanisms that drive field-based 38 phenomena and would enable key properties of OM to be represented in predictive models, 39 thereby contributing to reducing the uncertainty in modeling river corridor biogeochemical 40 cycling 13,14 . 41We use highly controlled aerobic microcosms, non-invasive dissolved oxygen consumption 42 rates, and ultrahigh-resolution OM characterization to investigate the role of OM chemistry in 43 determining aerobic respiration in hyporheic zone sediments. Based on field observations 10-12 , 44 we hypothesized that OM chemistry, including thermodynamic favorability and nitrogen (N) 45 content, would regulate aerobic respiration. Historically, investigations of thermodynamic 46 constraints on microbial metabolism have primarily focused on oxidation-reduction reactions 47 premise that using oxygen as the terminal electron acceptor provides sufficient energy ...

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“…Fungal symbionts use their BVOCs to induce mycorrhiza formation (Ditengou et al 2015), and rhizobacteria of several bacterial genera use their BVOCs to protect roots against fungal pathogens (Mendez-Bravo et al 2018). Ectomycorrhiza formation may activate jasmonic acid signalling, alter BVOC profiles and reduce herbivory in foliage of Populus × canescens (Kaling et al 2018). MTs released from tree leaf litter may also have important allelopathic effects in soil e.g.…”

Section: Bvocs Of Rhizosphere Litter and Understorymentioning

confidence: 99%

Unravelling the functions of biogenic volatiles in boreal and temperate forest ecosystems

et al. 2019

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Living trees are the main source of biogenic volatile organic compounds (BVOCs) in forest ecosystems, but substantial emissions originate from leaf and wood litter, the rhizosphere and from microorganisms. This review focuses on temperate and boreal forest ecosystems and the roles of BVOCs in ecosystem function, from the leaf to the forest canopy and from the forest soil to the atmosphere level. Moreover, emphasis is given to the question of how BVOCs will help forests adapt to environmental stress, particularly biotic stress related to climate change. Trees use their vascular system and emissions of BVOCs in internal communication, but emitted BVOCs have extended the communication to tree population and whole community levels and beyond. Future forestry practices should consider the importance of BVOCs in attraction and repulsion of attacking bark beetles, but also take an advantage of herbivore-induced BVOCs to improve the efficiency of natural enemies of herbivores. BVOCs are extensively involved in ecosystem services provided by forests including the positive effects on human health. BVOCs have a key role in ozone formation but also in ozone quenching. Oxidation products form secondary organic aerosols that disperse sunlight deeper into the forest canopy, and affect cloud formation and ultimately the climate. We also discuss the technical side of reliable BVOC sampling of forest trees for future interdisciplinary studies that should bridge the gaps between the forest sciences, health sciences, chemical ecology, conservation biology, tree physiology and atmospheric science.

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Mycorrhiza-Triggered Transcriptomic and Metabolomic Networks Impinge on Herbivore Fitness

Cited by 74 publications

References 94 publications

Ectomycorrhizal fungi induce systemic resistance against insects on a non-mycorrhizal plant in a CERK1-dependent manner

Ectomycorrhizal fungi induce systemic resistance against insects on a non-mycorrhizal plant in a CERK1-dependent manner

Carbon limitation leads to thermodynamic regulation of aerobic metabolism

Unravelling the functions of biogenic volatiles in boreal and temperate forest ecosystems

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