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

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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Main Authors: Labudda, M., Rozanska, E., Prabucka, B., Muszynska, E., Marecka, D., Kozak, M., Dababat, A.A., Sobczak, M.
Format: Article biblioteca
Language:English
Published: British Society for Plant Pathology 2020
Subjects:HORDEUM VULGARE, HETERODERA, PLANT NEMATODES, ENZYMES,
Online Access:https://hdl.handle.net/10883/20625
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spelling dig-cimmyt-10883-206252021-07-30T14:28:03Z Activity profiling of barley vacuolar processing enzymes provides new insights into the plant and cyst nematode interaction Labudda, M. Rozanska, E. Prabucka, B. Muszynska, E. Marecka, D. Kozak, M. Dababat, A.A. Sobczak, M. HORDEUM VULGARE HETERODERA PLANT NEMATODES ENZYMES 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. 38-52 2020-01-28T01:20:18Z 2020-01-28T01:20:18Z 2020 Article Published Version 1464-6722 (Print) https://hdl.handle.net/10883/20625 10.1111/mpp.12878 English https://bsppjournals.onlinelibrary.wiley.com/doi/full/10.1111/mpp.12878#support-information-section CIMMYT manages Intellectual Assets as International Public Goods. The user is free to download, print, store and share this work. In case you want to translate or create any other derivative work and share or distribute such translation/derivative work, please contact CIMMYT-Knowledge-Center@cgiar.org indicating the work you want to use and the kind of use you intend; CIMMYT will contact you with the suitable license for that purpose. Open Access PDF United Kingdom British Society for Plant Pathology Wiley 1 21 Molecular Plant Pathology
institution CIMMYT
collection DSpace
country México
countrycode MX
component Bibliográfico
access En linea
databasecode dig-cimmyt
tag biblioteca
region America del Norte
libraryname CIMMYT Library
language English
topic HORDEUM VULGARE
HETERODERA
PLANT NEMATODES
ENZYMES
HORDEUM VULGARE
HETERODERA
PLANT NEMATODES
ENZYMES
spellingShingle HORDEUM VULGARE
HETERODERA
PLANT NEMATODES
ENZYMES
HORDEUM VULGARE
HETERODERA
PLANT NEMATODES
ENZYMES
Labudda, M.
Rozanska, E.
Prabucka, B.
Muszynska, E.
Marecka, D.
Kozak, M.
Dababat, A.A.
Sobczak, M.
Activity profiling of barley vacuolar processing enzymes provides new insights into the plant and cyst nematode interaction
description 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.
format Article
topic_facet HORDEUM VULGARE
HETERODERA
PLANT NEMATODES
ENZYMES
author Labudda, M.
Rozanska, E.
Prabucka, B.
Muszynska, E.
Marecka, D.
Kozak, M.
Dababat, A.A.
Sobczak, M.
author_facet Labudda, M.
Rozanska, E.
Prabucka, B.
Muszynska, E.
Marecka, D.
Kozak, M.
Dababat, A.A.
Sobczak, M.
author_sort Labudda, M.
title Activity profiling of barley vacuolar processing enzymes provides new insights into the plant and cyst nematode interaction
title_short Activity profiling of barley vacuolar processing enzymes provides new insights into the plant and cyst nematode interaction
title_full Activity profiling of barley vacuolar processing enzymes provides new insights into the plant and cyst nematode interaction
title_fullStr Activity profiling of barley vacuolar processing enzymes provides new insights into the plant and cyst nematode interaction
title_full_unstemmed Activity profiling of barley vacuolar processing enzymes provides new insights into the plant and cyst nematode interaction
title_sort activity profiling of barley vacuolar processing enzymes provides new insights into the plant and cyst nematode interaction
publisher British Society for Plant Pathology
publishDate 2020
url https://hdl.handle.net/10883/20625
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