A cellular outlook of galls induced by root-knot nematodes in the model host Arabidopsis thaliana

Engler, Janice de Almeida; Siqueira, Kércya Maria Simões de; Nascimento, Danila Cabral do; Costa, Tiago Gonçalves da; Engler, Gilbert

doi:10.4322/nematoda.00616

Cited by 9 publications

(8 citation statements)

References 47 publications

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“…G. m. = Gigaspora margarita. New Phytologist targeted sampling: selecting sub-hyphopodial segments may in fact have reduced the dilution of fewer populated high ploidy classes and possibly also improved the overall quality of nuclear extracts (de Almeida- Engler et al, 2016). Furthermore, our detailed analysis of nuclear size distribution in longitudinal root sections and its correlation with ploidy revealed additional details.…”

Section: Am Colonization and Local Increases In Ploidymentioning

confidence: 87%

Local endoreduplication as a feature of intracellular fungal accommodation in arbuscular mycorrhizas

et al. 2019

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Summary The intracellular accommodation of arbuscular mycorrhizal (AM) fungi is a paradigmatic feature of this plant symbiosis that depends on the activation of a dedicated signaling pathway and the extensive reprogramming of host cells, including striking changes in nuclear size and transcriptional activity. By combining targeted sampling of early root colonization sites, detailed confocal imaging, flow cytometry and gene expression analyses, we demonstrate that local, recursive events of endoreduplication are triggered in the Medicago truncatula root cortex during AM colonization. AM colonization induces an increase in ploidy levels and the activation of endocycle specific markers. This response anticipates the progression of fungal colonization and is limited to arbusculated and neighboring cells in the cortical tissue. Furthermore, endoreduplication is not induced in M. truncatula mutants for symbiotic signaling pathway genes. On this basis, we propose endoreduplication as part of the host cell prepenetration responses that anticipate AM fungal accommodation in the root cortex.

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Section: Am Colonization and Local Increases In Ploidymentioning

confidence: 87%

Local endoreduplication as a feature of intracellular fungal accommodation in arbuscular mycorrhizas

et al. 2019

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“…After 4 weeks, Arabidopsis seedlings wild-type and healthy green plantlets of transgenic lines were placed in soil containing 30% of sand and were kept in a growth chamber in with 8-h light/16-h dark photoperiod at 21 • C/18 • C for growth for approximately 20 days. Each plant was then infected with 300 freshly hatched pre-parasitic stage 2 juvenile nematodes according to de Almeida-Engler et al (2016).…”

Section: Plant Material Growth Conditions and Nematode Infectionmentioning

confidence: 99%

“…For nematode infection tests and histological analysis, plantlets from Arabidopsis wild-type (cv. Col-0 and LER) and transgenic lines (ABAP1/abap1 and ABAP1 OE ) germinated in soil were infected with 300 juvenile nematodes (J2) of M. incognita per plant (de Almeida-Engler et al, 2016). Plantlets were then kept in a growth chamber (8-h light/16-h darkness) during 6-7 weeks after nematode inoculation.…”

Section: Histological Analysis and Nematode Infection Assaysmentioning

confidence: 99%

“…Acid fuchsin staining was performed in infected roots of ABAP1/abap1, ABAP1 OE , and wild-type seedlings as described by de Almeida-Engler et al (2016), to track nematode development within the roots. The whole infected roots (40 DAI) were fixed and stained for 5 h in a solution of equal parts of 95% ethanol and glacial acetic acid, containing 17.5 mg/L acid fuchsin.…”

Section: Acid Fuchsin Staining Of Abap1 Transgenic Lines Infected Rootsmentioning

confidence: 99%

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The Armadillo BTB Protein ABAP1 Is a Crucial Player in DNA Replication and Transcription of Nematode-Induced Galls

et al. 2021

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The biogenesis of root-knot nematode (Meloidogyne spp.)-induced galls requires the hyperactivation of the cell cycle with controlled balance of mitotic and endocycle programs to keep its homeostasis. To better understand gall functioning and to develop new control strategies for this pest, it is essential to find out how the plant host cell cycle programs are responding and integrated during the nematode-induced gall formation. This work investigated the spatial localization of a number of gene transcripts involved in the pre-replication complex during DNA replication in galls and report their akin colocation with the cell cycle S-phase regulator Armadillo BTB Arabidopsis Protein 1 (ABAP1). ABAP1 is a negative regulator of pre-replication complex controlling DNA replication of genes involved in control of cell division and proliferation; therefore, its function has been investigated during gall ontogenesis. Functional analysis was performed upon ABAP1 knockdown and overexpression in Arabidopsis thaliana. We detected ABAP1 promoter activity and localized ABAP1 protein in galls during development, and its overexpression displayed significantly reduced gall sizes containing atypical giant cells. Profuse ABAP1 expression also impaired gall induction and hindered nematode reproduction. Remarkably, ABAP1 knockdown likewise negatively affected gall and nematode development, suggesting its involvement in the feeding site homeostasis. Microscopy analysis of cleared and nuclei-stained whole galls revealed that ABAP1 accumulation resulted in aberrant giant cells displaying interconnected nuclei filled with enlarged heterochromatic regions. Also, imbalanced ABAP1 expression caused changes in expression patterns of genes involved in the cell division control as demonstrated by qRT-PCR. CDT1a, CDT1b, CDKA;1, and CYCB1;1 mRNA levels were significantly increased in galls upon ABAP1 overexpression, possibly contributing to the structural changes in galls during nematode infection. Overall, data obtained in galls reinforced the role of ABAP1 controlling DNA replication and mitosis and, consequently, cell proliferation. ABAP1 expression might likely take part of a highly ordered mechanism balancing of cell cycle control to prevent gall expansion. ABAP1 expression might prevent galls to further expand, limiting excessive mitotic activity. Our data strongly suggest that ABAP1 as a unique plant gene is an essential component for cell cycle regulation throughout gall development during nematode infection and is required for feeding site homeostasis.

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“…Sijmons first established culture conditions to successfully establish a new model system for studying the infection and development of M. incognita in Arabidopsis thaliana ( Sijmons et al., 1991 ). The infection of A. thaliana with M. incognita is a well-suited model system for studying the molecular interactions between nematodes and their hosts ( Engler et al., 2016 ; Singh et al., 2016 ; Teixeira et al., 2016 ; Warmerdam et al., 2018 ; Warmerdam et al., 2020 ). Teixeira and Warmerdam studied early defense responses against M. incognita in A. thaliana .…”

Section: Introductionmentioning

confidence: 99%

AtSWEET1 negatively regulates plant susceptibility to root-knot nematode disease

et al. 2023

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The root-knot nematode Meloidogyne incognita is a pathogenic pest that causes severe economic loss to agricultural production by forming a parasitic relationship with its hosts. During the development of M. incognita in the host plant roots, giant cells are formed as a nutrient sink. However, the roles of sugar transporters during the giant cells gain sugar from the plant cells are needed to improve. Meanwhile, the eventual function of sugars will eventually be exported transporters (SWEETs) in nematode-plant interactions remains unclear. In this study, the expression patterns of Arabidopsis thaliana SWEETs were examined by inoculation with M. incognita at 3 days post inoculation (dpi) (penetration stage) and 18 dpi (developing stage). We found that few AtSWEETs responded sensitively to M. incognita inoculation, with the highest induction of AtSWEET1 (AT1G21460), a glucose transporter gene. Histological analyses indicated that the β-glucuronidase (GUS) and green fluorescent protein (GFP) signals were observed specifically in the galls of AtSWEET1-GUS and AtSWEET1-GFP transgenic plant roots, suggesting that AtSWEET1 was induced specifically in the galls. Genetic studies have shown that parasitism of M. incognita was significantly affected in atsweet1 compared to wild-type and complementation plants. In addition, parasitism of M. incognita was significantly affected in atsweet10 but not in atsweet13 and atsweet14, expression of which was induced by inoculation with M. incognita. Taken together, these data prove that SWEETs play important roles in plant and nematode interactions.

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A cellular outlook of galls induced by root-knot nematodes in the model host Arabidopsis thaliana

Cited by 9 publications

References 47 publications

Local endoreduplication as a feature of intracellular fungal accommodation in arbuscular mycorrhizas

Local endoreduplication as a feature of intracellular fungal accommodation in arbuscular mycorrhizas

The Armadillo BTB Protein ABAP1 Is a Crucial Player in DNA Replication and Transcription of Nematode-Induced Galls

AtSWEET1 negatively regulates plant susceptibility to root-knot nematode disease

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