Transcriptomic analysis ofUstilago maydisinfectingArabidopsisreveals important aspects of the fungus pathogenic mechanisms

Martínez‐Soto, Domingo; Robledo-Briones, Angélica M.; Estrada-Luna, Andrés Adolfo; Ruíz-Herrera, José

doi:10.4161/psb.25059

Cited by 31 publications

(23 citation statements)

References 84 publications

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“…If chitin is sufficient to induce resistance against T. ni and susceptibility against Pto , treatment of Col-0 roots with Paxillus involutus , another ECM fungus or a pathogen like Ustilago maydis should also result in ISS against Pto . However, U. maydis can cause necrosis and stunting of Arabidopsis 48 . To avoid fungal pathogenicity confounding the data interpretation, Arabidopsis roots were treated with heat-killed U. maydis D132.…”

Section: Resultsmentioning

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

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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%

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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“…The sample was passed through SEP‐PAK C18 filters (Waters Associates Inc., Milford, MA, USA) and subjected to HPLC (Shimadzu class 10A series, Kyoto, Japan) with two LC‐10AT pumps and equipped with the software Class LC‐10At series, version 5.03 (Shimadzu, Kyoto, Japan) using a Zorbax C‐18 column (Agilent Technologies, Wilmington, DE, USA) (Martinez‐Soto et al . ).…”

Section: Methodsmentioning

confidence: 97%

Plant volatiles cause direct, induced and associational resistance in common bean to the fungal pathogen Colletotrichum lindemuthianum

Morales-Vargas²,

et al. 2014

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Experimental Baj ıo, INIFAP-Celaya, Km 6.5 Carr. Celaya-San Miguel de Allende 38810, Guanajuato, M exico Summary 1. Plants that express resistance to herbivores emit volatile organic compounds (VOCs) that can trigger resistance responses in undamaged neighbours. Recent reports indicate that VOCs can also trigger the resistance to pathogens, an effect that might be due to different mechanisms: the priming of an induced expression of resistance genes in the receiver or direct inhibitory effects on microbial pathogens that cause a passive 'associational' resistance in the VOC-exposed plant. 2. We investigated whether VOCs emitted from a resistant common bean (Phaseolus vulgaris) cultivar enhance the resistance to the fungus Colletotrichum lindemuthianum in a susceptible cultivar and analysed whether specific VOCs are likely to directly affect the pathogen. 3. We found that susceptible plants exposed to the headspace of resistance-expressing plants over 6 h became phenotypically as resistant as the resistant cultivar. Several resistance marker genes (PATHOGENESIS-RELATED [PR] 1, 2 and 4) were primed in VOC-exposed susceptible plants. After challenging, these genes reached expression levels at least as high as in the resistant cultivar. Additionally, individual VOCs such as limonene, linalool, nonanal, methyl salicylate and methyl jasmonate at natural concentrations directly inhibited the germination of conidia as did also the headspace of a resistance-expressing plant. This inhibition of conidial germination was dosagedependent and irreversible. 4. Synthesis. We conclude that VOCs are involved in the resistance of bean to fungal pathogens. They can contribute to the direct resistance in the emitter itself, and resistance phenotypes of neighbouring receiver plants can result from induced as well as associational resistance. Plant VOCs play multiple roles in the resistance of plants to microbial pathogens.

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“…Almost all of the well-studied Ustilago maydis virulence factors conserved among Ustilaginales were found conserved in the four Pseudozyma genomes (Table 1). The conservation of the Pit cluster (Doehlemann et al , 2011) Cmu1 (Djamei et al , 2011), Cwh41 (Martínez-Soto et al , 2013), and Hum3 (Muller et al , 2008) was found in all four Pseudozyma genomes (Table 1). Tin2 (Tanaka et al , 2014) was also found conserved, but the P. hubeiensis ortholog was lacking a strong secretion signal (Table 1).…”

Section: Resultsmentioning

confidence: 96%

Pseudozyma saprotrophic yeasts have retained a large effector arsenal, including functional Pep1 orthologs

Sharma

Ökmen

Doehlemann

et al. 2018

Preprint

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SummaryThe basidiomycete smut fungi are predominantly plant parasitic, causing severe losses in some crops. Most species feature a saprotrophic haploid yeast stage, and several smut fungi are only known from this stage, with some isolated from habitats without suitable hosts, e.g. from Antarctica. Thus, these species are generally believed to be apathogenic, but recent findings that some of these might have a plant pathogenic sexual counterpart, casts doubts on the validity of this hypothesis. Here, four Pseudozyma genomes were re-annotated and compared to published smut pathogens and the well-characterised effector gene Pep1 from these species was checked for its ability to complement a Pep1 deletion strain of Ustilago maydis. It was found that 113 high-confidence putative effector proteins were conserved among smut and Pseudozyma genomes. Among these were several validated effector proteins, including Pep1. By genetic complementation we show that Pep1 homologs from the supposedly apathogenic yeasts restore virulence in Pep1-deficient mutants Ustilago maydis. Thus, it is concluded that Pseudozyma species have retained a suite of effectors. This hints at the possibility that Pseudozyma species have kept an unknown plant pathogenic stage for sexual recombination or that these effectors have positive effects when colonising plant surfaces.

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Transcriptomic analysis ofUstilago maydisinfectingArabidopsisreveals important aspects of the fungus pathogenic mechanisms

Cited by 31 publications

References 84 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

Plant volatiles cause direct, induced and associational resistance in common bean to the fungal pathogen Colletotrichum lindemuthianum

Pseudozyma saprotrophic yeasts have retained a large effector arsenal, including functional Pep1 orthologs

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