Role of stress‐related hormones in plant defence during early infection of the cyst nematode <i>Heterodera schachtii</i> in Arabidopsis

Kammerhofer, Nina; Radakovic, Zoran S.; Regis, Jully M. A.; Dobrev, Petre I.; Vaňková, Radomı́ra; Grundler, Florian M. W.; Siddique, Shahid; Hofmann, Julia; Wieczorek, Krzysztof

doi:10.1111/nph.13395

Cited by 107 publications

(132 citation statements)

References 65 publications

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“…However, a picture emerges showing that root feeding by nematodes activates an integrated signaling network, which is highly regulated by plant hormones. Root feeding by sedentary endoparasitic nematodes results in the production and accumulation of SA, JA, and ET at the site of infection (67). Subsequently, transcriptional reprogramming results in the activation of the core defense system involving SA/JA/ET-mediated pathways (80,93,168).…”

Section: Nematode-induced Systemic Defense Pathwaysmentioning

confidence: 99%

Plant-Mediated Systemic Interactions Between Pathogens, Parasitic Nematodes, and Herbivores Above- and Belowground

Biere

Goverse

2016

Annu. Rev. Phytopathol.

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Plants are important mediators of interactions between aboveground (AG) and belowground (BG) pathogens, arthropod herbivores, and nematodes (phytophages). We highlight recent progress in our understanding of within- and cross-compartment plant responses to these groups of phytophages in terms of altered resource dynamics and defense signaling and activation. We review studies documenting the outcome of cross-compartment interactions between these phytophage groups and show patterns of cross-compartment facilitation as well as cross-compartment induced resistance. Studies involving soilborne pathogens and foliar nematodes are scant. We further highlight the important role of defense signaling loops between shoots and roots to activate a full resistance complement. Moreover, manipulation of such loops by phytophages affects systemic interactions with other plant feeders. Finally, cross-compartment-induced changes in root defenses and root exudates extend systemic defense loops into the rhizosphere, enhancing or reducing recruitment of microbes that induce systemic resistance but also affecting interactions with root-feeding phytophages.

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Section: Nematode-induced Systemic Defense Pathwaysmentioning

confidence: 99%

Plant-Mediated Systemic Interactions Between Pathogens, Parasitic Nematodes, and Herbivores Above- and Belowground

Biere

Goverse

2016

Annu. Rev. Phytopathol.

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“…Auxin, ET and GA have also been reported to play a positive role in the early stages of development of nematode feeding cells313233. ET is recognized to play a role in nematode attraction, migration, feeding site formation, and host defense during early stages of nematode infection32343536, but the role may differ for the interaction of plants with cyst nematode and RKN. For example, an intact ET pathway is prerequisite for plant defense to RKN2737.…”

mentioning

confidence: 99%

Ethylene response pathway modulates attractiveness of plant roots to soybean cyst nematode Heterodera glycines

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et al. 2017

Sci Rep

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Plant parasitic nematodes respond to root exudates to locate their host roots. In our studies second stage juveniles of Heterodera glycines, the soybean cyst nematode (SCN), quickly migrated to soybean roots in Pluronic F-127 gel. Roots of soybean and non-host Arabidopsis treated with the ethylene (ET)-synthesis inhibitor aminoethoxyvinylglycine (AVG) were more attractive to SCN than untreated roots, and significantly more nematodes penetrated into roots. Moreover, Arabidopsis ET insensitive mutants (ein2, ein2-1, ein2-5, ein3-1, ein5-1, and ein6) were more attractive than wild-type plants. Conversely, the constitutive triple-response mutant ctr1-1, was less attractive to SCN. While ET receptor gain-of-function mutant ein4-1 attracted more SCN than the wild-type, there were no significant differences in attractiveness between another gain-of-function ET receptor mutant, etr1-3, or the loss-of-function mutants etr1-7 and ers1-3 and the wild type. Expression of the reporter construct EBS: β-glucuronidase (GUS) was detected in Arabidopsis root tips as early as 6 h post infection, indicating that ET signaling was activated in Arabidopsis early by SCN infection. These results suggest that an active ET signaling pathway reduces root attractiveness to SCN in a way similar to that reported for root-knot nematodes, but opposite to that suggested for the sugar beet cyst nematode Heterodera schachtii.

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“…Together, these results indicate that MYB83 regulates auxin and cytokinin responses at various levels of biosynthesis, signal transduction, and downstream responses. Also, ethylene has been shown to play contrasting dual functions during various nematode parasitic stages (Wubben et al, 2001;Kammerhofer et al, 2015). Notably, numerous ethylene response factors (ERFs), which control the downstream signaling of ethylene response, were also identified among the MYB83-indcued genes overlapping with the syncytium DEGs (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…We therefore focused our discussion on the potential importance of these genes for syncytium formation and nematode parasitism. Levels and signaling of phytohormones play fundamental roles in determining syncytium cell fate reprogramming and differentiation (Grunewald et al, 2009b;Gheysen and Mitchum, 2011;Goverse and Bird, 2011;Cabrera et al, 2015;Kammerhofer et al, 2015). In particular, auxin signaling has been shown to be rapidly activated upon nematode infection leading to syncytium differentiation and development (Goverse et al, 2000;Karczmarek et al, 2004;Grunewald et al, 2009a;Absmanner et al, 2013;Hewezi et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

“…7A). While the function of jasmonic acid and abscisic acid signaling in directing plant response to cyst nematodes is not fully understood (Kammerhofer et al, 2015), it has been recently demonstrated that these pathways regulate defense responses and basal immunity against sedentary and migratory nematodes (Nahar et al, 2011(Nahar et al, , 2012Ozalvo et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

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Cooperative Regulatory Functions of miR858 and MYB83 during Cyst Nematode Parasitism

et al. 2017

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ORCID IDs: 0000-0003-4046-1672 (J.H.R.); 0000-0001-5256-8878 (T.H.).MicroRNAs (miRNAs) recently have been established as key regulators of transcriptome reprogramming that define cell function and identity. Nevertheless, the molecular functions of the greatest number of miRNA genes remain to be determined. Here, we report cooperative regulatory functions of miR858 and its MYB83 transcription factor target gene in transcriptome reprogramming during Heterodera cyst nematode parasitism of Arabidopsis (Arabidopsis thaliana). Gene expression analyses and promoter-GUS fusion assays documented a role of miR858 in posttranscriptional regulation of MYB83 in the Heterodera schachtii-induced feeding sites, the syncytia. Constitutive overexpression of miR858 interfered with H. schachtii parasitism of Arabidopsis, leading to reduced susceptibility, while reduced miR858 abundance enhanced plant susceptibility. Similarly, MYB83 expression increases were conducive to nematode infection because overexpression of a noncleavable coding sequence of MYB83 significantly increased plant susceptibility, whereas a myb83 mutation rendered the plants less susceptible. In addition, RNA-seq analysis revealed that genes involved in hormone signaling pathways, defense response, glucosinolate biosynthesis, cell wall modification, sugar transport, and transcriptional control are the key etiological factors by which MYB83 facilitates nematode parasitism of Arabidopsis. Furthermore, we discovered that miR858-mediated silencing of MYB83 is tightly regulated through a feedback loop that might contribute to fine-tuning the expression of more than a thousand of MYB83-regulated genes in the H. schachtii-induced syncytium. Together, our results suggest a role of the miR858-MYB83 regulatory system in finely balancing gene expression patterns during H. schachtii parasitism of Arabidopsis to ensure optimal cellular function.

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Role of stress‐related hormones in plant defence during early infection of the cyst nematode Heterodera schachtii in Arabidopsis

Cited by 107 publications

References 65 publications

Plant-Mediated Systemic Interactions Between Pathogens, Parasitic Nematodes, and Herbivores Above- and Belowground

Plant-Mediated Systemic Interactions Between Pathogens, Parasitic Nematodes, and Herbivores Above- and Belowground

Ethylene response pathway modulates attractiveness of plant roots to soybean cyst nematode Heterodera glycines

Cooperative Regulatory Functions of miR858 and MYB83 during Cyst Nematode Parasitism

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