Systemic changes in photosynthesis and reactive oxygen species homeostasis in shoots of <i>Arabidopsis thaliana</i> infected with the beet cyst nematode <i>Heterodera schachtii</i>

Labudda, Mateusz; Różańska, Elżbieta; Czarnocka, Weronika; Sobczak, Mirosław; Dzik, Jolanta M.

doi:10.1111/mpp.12652

Cited by 38 publications

(34 citation statements)

References 82 publications

(110 reference statements)

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“…This would be consistent with the fact that often in the first phase (an alarm phase) of the plant stress response (3 dpi) there is a rapid production of reactive oxygen and nitrogen species. We showed this in earlier studies, where H. schachtii parasitism on A. thaliana roots caused an accumulation of superoxide and hydrogen peroxide molecules in the shoots of infected plants at 3 dpi, probably as a result of the observed down‐regulation of antioxidant enzymes (Labudda et al , ). Melillo et al .…”

Section: Discussionsupporting

confidence: 70%

“…This could also be one of the reasons for the reduced nitrate levels observed in the present study at 7 dpi in the roots of A. thaliana infected with H. schachtii . Another explanation may be as a result from their intensive root‐to‐shoot transport, where carbon skeletons, energy, and reducing power derived from photosynthesis are easily available and allow the conversion of inorganic N to the organic form (Labudda et al , ; Zhang et al , ). Indeed, their increased content in shoots of infected plants was only recorded at this time point.…”

Section: Discussionmentioning

confidence: 99%

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Heterodera schachtii infection affects nitrogen metabolism in Arabidopsis thaliana

et al. 2020

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Nitrogen metabolism is important for physiological processes during normal growth and development, as well as plant defence responses. Second‐stage juveniles of the cyst nematode Heterodera schachtii penetrate into the root and initiate permanent feeding sites called syncytia, from which they draw all necessary nutrients. To unravel whether the cyst nematode infestation changes nitrogen metabolism, the enzymatic activity and gene expression of nitrate (NIA) and nitrite (NIR) reductases and glutamate dehydrogenase (GDH), as well as levels of the metabolites nitrates, nitrites, and ammonium ions were estimated both locally in inoculated roots and systemically in shoots of inoculated Arabidopsis thaliana plants at 3, 7, and 15 days post‐inoculation (dpi). Moreover, gene expression of long hypocotyle 5 (HY5), a basic‐region leucine zipper (bZIP) transcription factor, was also determined, to learn more about the potential transcriptional regulation of the analysed enzymes. It was shown that the activity of nitrogen‐related enzymes and the content of metabolites fluctuated during the whole period of infection. These results were accompanied by organ‐specific and dpi‐dependent gene expression patterns. The high gene expression level of HY5 in infected roots at 7 and 15 dpi coexisted with enhanced expression of NIA1 and NIR1 at 7 dpi and NIA2 at 15 dpi. Enhanced HY5 expression level in shoots of infected plants at 15 dpi was followed by up‐regulation of NIA1 expression, suggesting that HY5 may regulate the gene expression of NIA and NIR during nematode infection. Our results indicate that changes in plant nitrogen metabolism occur during cyst nematode infection.

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Section: Discussionsupporting

confidence: 70%

Section: Discussionmentioning

confidence: 99%

Heterodera schachtii infection affects nitrogen metabolism in Arabidopsis thaliana

et al. 2020

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“…Although the whole life cycle of endoparasitic nematodes is linked with the host roots, these parasites induce strong systemic responses in the aerial parts of the plants (Labudda, Rózanska, Czarnocka, Sobczak, & Dzik, 2018). Then, monitoring the physiological processes that occur in the shoot provides indications of how nematodes affect plant physiology (Lu, Davis, Kemerait, Iersel, & Scherm, 2014).…”

Section: Introductionmentioning

confidence: 99%

Root morphology, gas exchange and chlorophyll fluorescence of coffee cultivars and progenies are altered by Meloidogyne paranaensis infestation and water deficit

Pasqualotto

Salgado

Terra

et al. 2020

Journal of Phytopathology

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Climate change greatly influences coffee production, especially in areas infested with plant‐parasitic nematodes. In this study, coffee genotypes showed differences in their morphological and physiological characteristics when subjected to a water deficit and parasitism by Meloidogyne paranaensis. The cultivar IPR 100 had the largest superficial and volumetric root system area, even when parasitized. The two progenies (MG 0179‐1 and MG 0179‐3) and the cultivar Catuaí IAC 62 had a similar surface area (p < .05) when parasitized. However, the root surface area and volume of MG 0179‐3 increased by 96% and 400%, respectively, when parasitized by M. paranaensis. On the other hand, Catuaí IAC 62 had a 31% reduction in root surface area. Catuai 62 and IPR 100 showed higher sensitivity to drought when parasitized because of the increased photochemical sensitivity and reduction in photochemical quenching. In MG 0179‐1 and MG 0179‐3, an increase in non‐photochemical quenching occurred in response to stress, indicating that these progenies use a photochemical response to protect photosystem II. In this work, MG 0179‐3, which is resistant to M. paranaensis, was remarkable because, interestingly, the infestation caused an increase in its root surface area. In addition, MG 0179‐3 had relatively good photochemical performance under water deficit and M. paranaensis parasitism.

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“…For this reason, tissue damage in hosts must be limited until reproduction of nematodes has finished. The content and composition of photosynthetic pigments are effective markers of the physiological status of infected plants (Labudda et al , ). Our results indicate that H. filipjevi causes only moderate alterations in content and composition of photosynthetic pigments in infected barley.…”

Section: Discussionmentioning

confidence: 99%

“…Nematode feeding inside the roots causes dramatic reorganization of the metabolism in all plant organs. Induced changes encompass activation of local (in roots) and systemic (in shoots) defence responses, among which proteolysis is an extremely important housekeeping process that must be mentioned (Labudda et al , ,b, ).…”

Section: Introductionmentioning

confidence: 99%

Activity profiling of barley vacuolar processing enzymes provides new insights into the plant and cyst nematode interaction

Labudda

Różańska

Prabucka

et al. 2019

Molecular Plant Pathology

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Summary Vacuolar processing enzymes (VPEs) play an important role during regular growth and development and defence responses. Despite substantial attempts to understand the molecular basis of plant–cyst nematode interaction, the mechanism of VPEs functioning during this interaction remains unknown. The second‐stage Heterodera filipjevi juvenile penetrates host roots and induces the formation of a permanent feeding site called a syncytium. To investigate whether infection with H. filipjevi alters plant host VPEs, the studies were performed in Hordeum vulgare roots and leaves on the day of inoculation and at 7, 14 and 21 days post‐inoculation (dpi). Implementing molecular, biochemical and microscopic methods we identified reasons for modulation of barley VPE activity during interaction with H. filipjevi. Heterodera filipjevi parasitism caused a general decrease of VPE activity in infected roots, but live imaging of VPEs showed that their activity is up‐regulated in syncytia at 7 and 14 dpi and down‐regulated at 21 dpi. These findings were accompanied by tissue‐specific VPE gene expression patterns. Expression of the barley cystatin HvCPI‐4 gene was stimulated in leaves but diminished in roots upon infestation. External application of cyclotides that can be produced naturally by VPEs elicits in pre‐parasitic juveniles vesiculation of their body, enhanced formation of granules, induction of exploratory behaviour (stylet thrusts and head movements), production of reactive oxygen species (ROS) and final death by methuosis. Taken together, down‐regulation of VPE activity through nematode effectors promotes the nematode invasion rates and leads to avoidance of the induction of the plant proteolytic response and death of the invading juveniles.

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Systemic changes in photosynthesis and reactive oxygen species homeostasis in shoots of Arabidopsis thaliana infected with the beet cyst nematode Heterodera schachtii

Cited by 38 publications

References 82 publications

Heterodera schachtii infection affects nitrogen metabolism in Arabidopsis thaliana

Heterodera schachtii infection affects nitrogen metabolism in Arabidopsis thaliana

Root morphology, gas exchange and chlorophyll fluorescence of coffee cultivars and progenies are altered by Meloidogyne paranaensis infestation and water deficit

Activity profiling of barley vacuolar processing enzymes provides new insights into the plant and cyst nematode interaction

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