Interaction of Medicago truncatula lysin motif receptor-like kinases, NFP and LYK3, produced in Nicotiana benthamiana induces defence-like responses.

Receptor(-like) kinases with Lysin Motif (LysM) domains in their extracellular region play crucial roles during plant interactions with microorganisms; e.g. Arabidopsis thaliana CERK1 activates innate immunity upon perception of fungal chitin/chitooligosaccharides, whereas Medicago truncatula NFP an...

Full description

Bibliographic Details
Main Authors: Anna Pietraszewska-Bogiel, Benoit Lefebvre, Maria A Koini, Dörte Klaus-Heisen, Frank L W Takken, René Geurts, Julie V Cullimore, Theodorus W J Gadella
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2013-01-01
Series:PLoS ONE
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23750228/?tool=EBI
_version_ 1818426529355399168
author Anna Pietraszewska-Bogiel
Benoit Lefebvre
Maria A Koini
Dörte Klaus-Heisen
Frank L W Takken
René Geurts
Julie V Cullimore
Theodorus W J Gadella
author_facet Anna Pietraszewska-Bogiel
Benoit Lefebvre
Maria A Koini
Dörte Klaus-Heisen
Frank L W Takken
René Geurts
Julie V Cullimore
Theodorus W J Gadella
author_sort Anna Pietraszewska-Bogiel
collection DOAJ
description Receptor(-like) kinases with Lysin Motif (LysM) domains in their extracellular region play crucial roles during plant interactions with microorganisms; e.g. Arabidopsis thaliana CERK1 activates innate immunity upon perception of fungal chitin/chitooligosaccharides, whereas Medicago truncatula NFP and LYK3 mediate signalling upon perception of bacterial lipo-chitooligosaccharides, termed Nod factors, during the establishment of mutualism with nitrogen-fixing rhizobia. However, little is still known about the exact activation and signalling mechanisms of MtNFP and MtLYK3. We aimed at investigating putative molecular interactions of MtNFP and MtLYK3 produced in Nicotiana benthamiana. Surprisingly, heterologous co-production of these proteins resulted in an induction of defence-like responses, which included defence-related gene expression, accumulation of phenolic compounds, and cell death. Similar defence-like responses were observed upon production of AtCERK1 in N. benthamiana leaves. Production of either MtNFP or MtLYK3 alone or their co-production with other unrelated receptor(-like) kinases did not induce cell death in N. benthamiana, indicating that a functional interaction between these LysM receptor-like kinases is required for triggering this response. Importantly, structure-function studies revealed that the MtNFP intracellular region, specific features of the MtLYK3 intracellular region (including several putative phosphorylation sites), and MtLYK3 and AtCERK1 kinase activity were indispensable for cell death induction, thereby mimicking the structural requirements of nodulation or chitin-induced signalling. The observed similarity of N. benthamiana response to MtNFP and MtLYK3 co-production and AtCERK1 production suggests the existence of parallels between Nod factor-induced and chitin-induced signalling mediated by the respective LysM receptor(-like) kinases. Notably, the conserved structural requirements for MtNFP and MtLYK3 biological activity in M. truncatula (nodulation) and in N. benthamiana (cell death induction) indicates the relevance of the latter system for studies on these, and potentially other symbiotic LysM receptor-like kinases.
first_indexed 2024-12-14T14:31:17Z
format Article
id doaj.art-c7d32d86c6b343cba029c5f331db8511
institution Directory Open Access Journal
issn 1932-6203
language English
last_indexed 2024-12-14T14:31:17Z
publishDate 2013-01-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS ONE
spelling doaj.art-c7d32d86c6b343cba029c5f331db85112022-12-21T22:57:48ZengPublic Library of Science (PLoS)PLoS ONE1932-62032013-01-0186e6505510.1371/journal.pone.0065055Interaction of Medicago truncatula lysin motif receptor-like kinases, NFP and LYK3, produced in Nicotiana benthamiana induces defence-like responses.Anna Pietraszewska-BogielBenoit LefebvreMaria A KoiniDörte Klaus-HeisenFrank L W TakkenRené GeurtsJulie V CullimoreTheodorus W J GadellaReceptor(-like) kinases with Lysin Motif (LysM) domains in their extracellular region play crucial roles during plant interactions with microorganisms; e.g. Arabidopsis thaliana CERK1 activates innate immunity upon perception of fungal chitin/chitooligosaccharides, whereas Medicago truncatula NFP and LYK3 mediate signalling upon perception of bacterial lipo-chitooligosaccharides, termed Nod factors, during the establishment of mutualism with nitrogen-fixing rhizobia. However, little is still known about the exact activation and signalling mechanisms of MtNFP and MtLYK3. We aimed at investigating putative molecular interactions of MtNFP and MtLYK3 produced in Nicotiana benthamiana. Surprisingly, heterologous co-production of these proteins resulted in an induction of defence-like responses, which included defence-related gene expression, accumulation of phenolic compounds, and cell death. Similar defence-like responses were observed upon production of AtCERK1 in N. benthamiana leaves. Production of either MtNFP or MtLYK3 alone or their co-production with other unrelated receptor(-like) kinases did not induce cell death in N. benthamiana, indicating that a functional interaction between these LysM receptor-like kinases is required for triggering this response. Importantly, structure-function studies revealed that the MtNFP intracellular region, specific features of the MtLYK3 intracellular region (including several putative phosphorylation sites), and MtLYK3 and AtCERK1 kinase activity were indispensable for cell death induction, thereby mimicking the structural requirements of nodulation or chitin-induced signalling. The observed similarity of N. benthamiana response to MtNFP and MtLYK3 co-production and AtCERK1 production suggests the existence of parallels between Nod factor-induced and chitin-induced signalling mediated by the respective LysM receptor(-like) kinases. Notably, the conserved structural requirements for MtNFP and MtLYK3 biological activity in M. truncatula (nodulation) and in N. benthamiana (cell death induction) indicates the relevance of the latter system for studies on these, and potentially other symbiotic LysM receptor-like kinases.https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23750228/?tool=EBI
spellingShingle Anna Pietraszewska-Bogiel
Benoit Lefebvre
Maria A Koini
Dörte Klaus-Heisen
Frank L W Takken
René Geurts
Julie V Cullimore
Theodorus W J Gadella
Interaction of Medicago truncatula lysin motif receptor-like kinases, NFP and LYK3, produced in Nicotiana benthamiana induces defence-like responses.
PLoS ONE
title Interaction of Medicago truncatula lysin motif receptor-like kinases, NFP and LYK3, produced in Nicotiana benthamiana induces defence-like responses.
title_full Interaction of Medicago truncatula lysin motif receptor-like kinases, NFP and LYK3, produced in Nicotiana benthamiana induces defence-like responses.
title_fullStr Interaction of Medicago truncatula lysin motif receptor-like kinases, NFP and LYK3, produced in Nicotiana benthamiana induces defence-like responses.
title_full_unstemmed Interaction of Medicago truncatula lysin motif receptor-like kinases, NFP and LYK3, produced in Nicotiana benthamiana induces defence-like responses.
title_short Interaction of Medicago truncatula lysin motif receptor-like kinases, NFP and LYK3, produced in Nicotiana benthamiana induces defence-like responses.
title_sort interaction of medicago truncatula lysin motif receptor like kinases nfp and lyk3 produced in nicotiana benthamiana induces defence like responses
url https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23750228/?tool=EBI
work_keys_str_mv AT annapietraszewskabogiel interactionofmedicagotruncatulalysinmotifreceptorlikekinasesnfpandlyk3producedinnicotianabenthamianainducesdefencelikeresponses
AT benoitlefebvre interactionofmedicagotruncatulalysinmotifreceptorlikekinasesnfpandlyk3producedinnicotianabenthamianainducesdefencelikeresponses
AT mariaakoini interactionofmedicagotruncatulalysinmotifreceptorlikekinasesnfpandlyk3producedinnicotianabenthamianainducesdefencelikeresponses
AT dorteklausheisen interactionofmedicagotruncatulalysinmotifreceptorlikekinasesnfpandlyk3producedinnicotianabenthamianainducesdefencelikeresponses
AT franklwtakken interactionofmedicagotruncatulalysinmotifreceptorlikekinasesnfpandlyk3producedinnicotianabenthamianainducesdefencelikeresponses
AT renegeurts interactionofmedicagotruncatulalysinmotifreceptorlikekinasesnfpandlyk3producedinnicotianabenthamianainducesdefencelikeresponses
AT julievcullimore interactionofmedicagotruncatulalysinmotifreceptorlikekinasesnfpandlyk3producedinnicotianabenthamianainducesdefencelikeresponses
AT theodoruswjgadella interactionofmedicagotruncatulalysinmotifreceptorlikekinasesnfpandlyk3producedinnicotianabenthamianainducesdefencelikeresponses