Time-dependent effects of Pochonia chlamydosporia endophytism on gene expression profiles of colonized tomato roots

Pentimone, Isabella; Colagiero, Mariantonietta; Ferrara, Massimo; Nigro, Franco; Rosso, Laura Cristina; Ciancio, Aurelio

doi:10.1007/s00253-019-10058-z

Cited by 16 publications

(25 citation statements)

References 57 publications

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“…The interaction between the virulence of M. incognita and the microbial diversity in the various niches M. incognita occupy has been studied in the context of biological control, revealing complex relationships, which efficacy diminishes with the transfer from lab to field ( 20 ). In this field of research, common themes include the isolation of Meloidogyne pathogens from the cuticles of J2s ( 21 – 23 ) and the identification of soil microbes and bacterial volatile compounds with antagonistic effects ( 24 , 25 ) from key taxa, including Rhizobia ( 26 ), Trichoderma and Pseudomonas ( 27 , 28 ), Pasteuria ( 29 ), Pochonia ( 30 , 31 ), and some mycorrhiza ( 31 – 33 ).…”

Section: Introductionmentioning

confidence: 99%

Bacterial Community Structure Dynamics in Meloidogyne incognita -Infected Roots and Its Role in Worm-Microbiome Interactions

Yergaliyev

Alexander-Shani

Dimerets

et al. 2020

mSphere

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Plant parasitic nematodes such as Meloidogyne incognita have a complex life cycle, occurring sequentially in various niches of the root and rhizosphere. They are known to form a range of interactions with bacteria and other microorganisms that can affect their densities and virulence. High-throughput sequencing can reveal these interactions in high temporal and geographic resolutions, although thus far we have only scratched the surface. In this study, we have carried out a longitudinal sampling scheme, repeatedly collecting rhizosphere soil, roots, galls, and second-stage juveniles from 20 plants to provide a high-resolution view of bacterial succession in these niches, using 16S rRNA metabarcoding. Our findings indicate that a structured community develops in the root, in which gall communities diverge from root segments lacking a gall, and that this structure is maintained throughout the crop season. We describe the successional process leading toward this structure, which is driven by interactions with the nematode and later by an increase in bacteria often found in hypoxic and anaerobic environments. We present evidence that this structure may play a role in the nematode’s chemotaxis toward uninfected root segments. Finally, we describe the J2 epibiotic microenvironment as ecologically deterministic, in part, due to the active bacterial attraction of second-stage juveniles. IMPORTANCE The study of high-resolution successional processes within tightly linked microniches is rare. Using the power and relatively low cost of metabarcoding, we describe the bacterial succession and community structure in roots infected with root-knot nematodes and in the nematodes themselves. We reveal separate successional processes in galls and adjacent non-gall root sections, which are driven by the nematode’s life cycle and the progression of the crop season. With their relatively low genetic diversity, large geographic range, spatially complex life cycle, and the simplified agricultural ecosystems they occupy, root-knot nematodes can serve as a model organism for terrestrial holobiont ecology. This perspective can improve our understanding of the temporal and spatial aspects of biological control efficacy.

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Section: Introductionmentioning

confidence: 99%

Bacterial Community Structure Dynamics in Meloidogyne incognita -Infected Roots and Its Role in Worm-Microbiome Interactions

Yergaliyev

Alexander-Shani

Dimerets

et al. 2020

mSphere

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“…Endophyte colonization can activate defense responses at the molecular level, upon additional biotic or abiotic stresses including root-associated microorganisms or pathogens, with an increase of the defense-related gene expression [6,7]. In the case of P. chlamydosporia, roots of monocot and dicot host plants showed that the endophyte colonization induced the expression of several defense genes in roots, eliciting an early host defense response, which is effective in the presence of pests such as endoparasitic nematodes [8][9][10][11]. Endophytic P. chlamydosporia induced changes in the transcriptome of tomato roots, highlighting a specific modulation of stress-responsive transcripts related to a selective activation of defense pathways [11].…”

Section: Introductionmentioning

confidence: 99%

“…In the case of P. chlamydosporia, roots of monocot and dicot host plants showed that the endophyte colonization induced the expression of several defense genes in roots, eliciting an early host defense response, which is effective in the presence of pests such as endoparasitic nematodes [8][9][10][11]. Endophytic P. chlamydosporia induced changes in the transcriptome of tomato roots, highlighting a specific modulation of stress-responsive transcripts related to a selective activation of defense pathways [11]. The endophyte affected the root expression of key genes of the jasmonic acid (JA) pathway, such as lipoxygenases.…”

Section: Introductionmentioning

confidence: 99%

“…This pathway has also been associated with systemically induced defense against nematode invasion [12,13], suggesting a beneficial effect of P. chlamydosporia. Also, groups of well-known salicylic acid (SA)-responsive genes, such as phenylalanine ammonia lyase (PAL) were clearly affected by the fungus 21 days after infection (dai) [11]. Interestingly, the tomato genes not expressed in the presence of P. chlamydosporia, at the early stage of interaction, included several glutaredoxins (GRXs).…”

Section: Introductionmentioning

confidence: 99%

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Root Endophytism by Pochonia chlamydosporia Affects Defense-Gene Expression in Leaves of Monocot and Dicot Hosts under Multiple Biotic Interactions

Tolba

Rosso

Pentimone

et al. 2021

Plants

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A study was carried out on the effect of the root endophytic fungus Pochonia chlamydosporia on plant systemic signal of defense related genes during fungal or nematode parasitism. Different biotic stress factors were examined, inoculating roots of dicot and monocot hosts with the endophyte, and measuring the expression of defense genes in leaves. A first greenhouse assay was carried out on expression of PAL, PIN II, PR1 and LOX D in leaves of tomato cv Tondino inoculated with Phytophthora infestans (CBS 120920), inoculating or not the roots of infected plants with P. chlamydosporia DSM 26985. In a second assay, plants of banana (Musa acuminata cv Grand Naine) were artificially infected with Fusarium oxysporum f. sp. cubense Tropical race 4 (TR4) and inoculated or not with DSM 26985. In a further experiment, banana plants were inoculated or not with P. chlamydosporia plus juveniles of the root knot nematode (RKN) Meloidogyne incognita. A similar assay was also carried out in vitro with adults and juveniles of the lesion nematode Pratylenchus goodeyi. Differential expression of the defense genes examined was observed for all plant-stress associations, indicative of early, upward systemic signals induced by the endophyte. Changes in expression profiles included a 5-fold down-regulation of PIN II at 2 dai in leaves of tomato plants treated with P. infestans and/or P. chlamydosporia, and the up-regulation of PAL by the endophyte alone, at 2 and 7 dai. In the TR4 assay, PR1 was significantly up-regulated at 7 dai in banana leaves, but only in the P. chlamydosporia treated plants. At 10 dai, PIN II expression was significantly higher in leaves of plants inoculated only with TR4. The banana-RKN assay showed a PR1 expression significantly higher than controls at 4 and 7 dai in plants inoculated with P. chlamydosporia alone, and a down-regulation at 4 dai in leaves of plants also inoculated with RKN, with a PR1 differential up-regulation at 10 dai. Pratylenchus goodeyi down-regulated PIN at 21 dai, with or without the endophyte, as well as PAL but only in presence of P. chlamydosporia. When inoculated alone, the endophyte up-regulated PR1 and LOX. The gene expression patterns observed in leaves suggest specific and time-dependent relationships linking host plants and P. chlamydosporia in presence of biotic stress factors, functional to a systemic, although complex, activation of defense genes.

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“…The interaction of M. incognita virulence and microbial taxa in the various niches they occupy, have been studied in the context of biological control, revealing complex relationships, which efficacy diminishes with the transfer from lab to field [20] . Common themes in this line of research include the isolation of Meloidogyne pathogens from the cuticle of second stage juveniles (J2) [21][22][23] , or the identification of soil microbes and bacterial volatile compounds with antagonistic effects [24,25] , key taxa including Rhizobia [26] , Trichoderma and Pseudomonas [27,28] , Pasteuria [29] , Pochonia [30,31] and some mycorrhiza [31][32][33] .…”

Section: Introductionmentioning

confidence: 99%

The bacterial community structure dynamics inMeloidogyne incognitainfected roots and its role in worm-microbiome interactions

Yergaliyev

Alexander-Shani

Dimeretz

et al. 2020

Preprint

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BackgroundPlant parasitic nematodes such as Meloidogyne incognita have a complex life cycle, occurring sequentially in various niches of the root and rhizosphere. They are known to form a range of interactions with bacteria and other microorganisms, that can affect their densities and virulence. High throughput sequencing can reveal these interactions in high temporal, and geographic resolutions, although thus far we have only scratched the surface. We have carried out a longitudinal sampling scheme, repeatedly collecting rhizosphere soil, roots, galls and second stage juveniles from 20 plants to provide a high resolution view of bacterial succession in these niches, using 16S rRNA metabarcoding. ResultsWe find that a structured community develops in the root, in which gall communities diverge from root segments lacking a gall, and that this structure is maintained throughout the crop season. We detail the successional process leading toward this structure, which is driven by interactions with the nematode and later by an increase in bacteria often found in hypoxic and anaerobic environments.We show evidence that this structure may play a role in the nematode's chemotaxis towards 1 uninfected root segments. Finally, we describe the J2 epibiotic microenvironment as ecologically deterministic, in part, due to active bacterial attraction of second stage juveniles. ConclusionsHigh density sampling, both temporally and across adjacent microniches, coupled with the power and relative low cost of metabarcoding, has provided us with a high resolution description of our study system. Such an approach can advance our understanding of holobiont ecology. Meloidogyne spp., with their relatively low genetic diversity, large geographic range and the simplified agricultural ecosystems they occupy, can serve as a model organism. Additionally, the perspective this approach provides could promote the efforts toward biological control efficacy.

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Time-dependent effects of Pochonia chlamydosporia endophytism on gene expression profiles of colonized tomato roots

Cited by 16 publications

References 57 publications

Bacterial Community Structure Dynamics in Meloidogyne incognita -Infected Roots and Its Role in Worm-Microbiome Interactions

Bacterial Community Structure Dynamics in Meloidogyne incognita -Infected Roots and Its Role in Worm-Microbiome Interactions

Root Endophytism by Pochonia chlamydosporia Affects Defense-Gene Expression in Leaves of Monocot and Dicot Hosts under Multiple Biotic Interactions

The bacterial community structure dynamics inMeloidogyne incognitainfected roots and its role in worm-microbiome interactions

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