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The endobacterium of an arbuscular mycorrhizal fungus modulates the expression of its toxin-antitoxin systems during the life cycle of its host.

ABSTRACT: Arbuscular mycorrhizal fungi (AMF) are widespread root symbionts that perform important ecological services, such as improving plant nutrient and water acquisition. Some AMF from the Gigasporaceae family host a population of endobacteria, Candidatus Glomeribacter gigasporarum (Cagg). The analysis of the Cagg genome identified six putative toxin-antitoxin modules (TAs), consisting of pairs of stable toxins and unstable antitoxins that affect diverse physiological functions. Sequence analysis suggested that these TA modules were acquired by horizontal transfer. Gene expression patterns of two TAs (yoeB/yefM and chpB/chpS) changed during the fungal life cycle, with the expression during the pre-symbiotic phase higher than during the symbiosis with the plant host. The heterologous expression in Escherichia coli demonstrated the functionality only for the YoeB-YefM pair. On the basis of these observations, we speculate that TA modules might help Cagg adapt to its intracellular habitat, coordinating its proliferation with the physiological state of the AMF host.

SUBMITTER: Salvioli di Fossalunga A

PROVIDER: S-EPMC5607366 | biostudies-literature | 2017 Oct

REPOSITORIES: biostudies-literature

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The endobacterium of an arbuscular mycorrhizal fungus modulates the expression of its toxin-antitoxin systems during the life cycle of its host.

Salvioli di Fossalunga Alessandra A Lipuma Justine J Venice Francesco F Dupont Laurence L Bonfante Paola P

The ISME journal 20170526 10

Arbuscular mycorrhizal fungi (AMF) are widespread root symbionts that perform important ecological services, such as improving plant nutrient and water acquisition. Some AMF from the Gigasporaceae family host a population of endobacteria, Candidatus Glomeribacter gigasporarum (Cagg). The analysis of the Cagg genome identified six putative toxin-antitoxin modules (TAs), consisting of pairs of stable toxins and unstable antitoxins that affect diverse physiological functions. Sequence analysis sugg ...[more]

PMID: 28548657

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Project description:Roots of most terrestrial plants form symbiotic associations (mycorrhiza) with soil- borne arbuscular mycorrhizal fungi (AMF). Many studies show that mycorrhizal colonization enhances plant resistance against pathogenic fungi. However, the mechanism of mycorrhiza-induced disease resistance remains equivocal. In this study, we found that mycorrhizal inoculation with AMF Funneliformis mosseae significantly alleviated tomato (Solanum lycopersicum Mill.) early blight disease caused by Alternaria solani Sorauer. AMF pre-inoculation led to significant increases in activities of β-1,3-glucanase, chitinase, phenylalanine ammonia-lyase (PAL) and lipoxygenase (LOX) in tomato leaves upon pathogen inoculation. Mycorrhizal inoculation alone did not influence the transcripts of most genes tested. However, pathogen attack on AMF-inoculated plants provoked strong defense responses of three genes encoding pathogenesis-related proteins, PR1, PR2, and PR3, as well as defense-related genes LOX, AOC, and PAL, in tomato leaves. The induction of defense responses in AMF pre-inoculated plants was much higher and more rapid than that in un-inoculated plants in present of pathogen infection. Three tomato genotypes: a Castlemart wild-type (WT) plant, a jasmonate (JA) biosynthesis mutant (spr2), and a prosystemin-overexpressing 35S::PS plant were used to examine the role of the JA signaling pathway in AMF-primed disease defense. Pathogen infection on mycorrhizal 35S::PS plants led to higher induction of defense-related genes and enzymes relative to WT plants. However, pathogen infection did not induce these genes and enzymes in mycorrhizal spr2 mutant plants. Bioassays showed that 35S::PS plants were more resistant and spr2 plants were more susceptible to early blight compared with WT plants. Our finding indicates that mycorrhizal colonization enhances tomato resistance to early blight by priming systemic defense response, and the JA signaling pathway is essential for mycorrhiza-primed disease resistance.

Project description:Tea has been gaining increasing popularity all over the world in recent years, and its yield and quality depend on the growth and development of tea plants [Camellia sinensis (L.) Kuntze] in various environments. Nowadays, biotic stress and extreme weather, such as high temperature, drought, waterlogging, pests, and diseases, bring about much pressure on the production of tea with high quality. Wherein anthracnose, which is the most common and serious disease of tea plants, has earned more and more attention, as its control mainly relies on chemical pesticides. Arbuscular mycorrhizal fungi (AMF), forming symbiosis with most terrestrial plants, participate in plant resistance against the anthracnose disease, which was found by previous studies in a few herbaceous plants. However, there are a few studies about arbuscular mycorrhizal (AM) fungal regulation of the resistance to the anthracnose pathogen in woody plants so far. In this paper, we investigated the effect of AMF on the development of anthracnose caused by Colletotrichum camelliae and tried to decipher the pertinent mechanism through transcriptome analysis. Results showed that inoculating AMF significantly reduced the damage of anthracnose on tea seedlings by reducing the lesion area by 35.29% compared to that of the control. The content of superoxide anion and activities of catalase and peroxidase significantly increased (P < 0.05) in mycorrhizal treatment in response to the pathogen with 1.23, 2.00, and 1.39 times higher, respectively, than those in the control. Pathways of plant hormone signal transduction, mitogen-activated protein kinase (MAPK) signaling, and phenylpropanoid biosynthesis might play roles in this regulation according to the transcriptomic results. Further redundancy analysis (RDA) and partial least squares structural equation modeling (PLS-SEM) analysis found that plant hormones, such as auxin and ethylene, and the antioxidant system (especially peroxidase) were of great importance in the AM fungal alleviation of anthracnose. Our results preliminarily indicated the mechanisms of enhanced resistance in mycorrhizal tea seedlings to the anthracnose pathogen and provided a theoretical foundation for the application of AMF as one of the biological control methods in tea plantations.

Dataset Information

The endobacterium of an arbuscular mycorrhizal fungus modulates the expression of its toxin-antitoxin systems during the life cycle of its host.

Publications

The endobacterium of an arbuscular mycorrhizal fungus modulates the expression of its toxin-antitoxin systems during the life cycle of its host.

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