The Lamin-Like LITTLE NUCLEI 1 (LINC1) Regulates Pattern-Triggered Immunity and Jasmonic Acid Signaling

Pathogen-associated molecular pattern (PAMP) recognition occurs by plasma membrane located receptors that induce among other processes nuclear gene expression. However, signaling to the nuclear compartment is restricted by the nuclear envelope and nuclear pore complexes. We show here that among the...

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Main Authors: Mai Jarad, Kiruthiga Mariappan, Marilia Almeida-Trapp, Michael Florian Mette, Axel Mithöfer, Naganand Rayapuram, Heribert Hirt
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-01-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fpls.2019.01639/full
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author Mai Jarad
Kiruthiga Mariappan
Marilia Almeida-Trapp
Michael Florian Mette
Axel Mithöfer
Naganand Rayapuram
Heribert Hirt
author_facet Mai Jarad
Kiruthiga Mariappan
Marilia Almeida-Trapp
Michael Florian Mette
Axel Mithöfer
Naganand Rayapuram
Heribert Hirt
author_sort Mai Jarad
collection DOAJ
description Pathogen-associated molecular pattern (PAMP) recognition occurs by plasma membrane located receptors that induce among other processes nuclear gene expression. However, signaling to the nuclear compartment is restricted by the nuclear envelope and nuclear pore complexes. We show here that among the four Arabidopsis lamin homologs LITTLE NUCLEI/CROWDED NUCLEI (LINC/CRWN), LINC1 plays an important role in PTI and jasmonic acid (JA) signaling. We show that linc1 knock out mutants affect PAMP-triggered MAPK activation and growth inhibition, but not reactive oxygen species or callose accumulation. We also demonstrate that linc1 mutants are compromised in regulating PAMP-triggered pathogen-related genes, in particular encoding factors involved in JA signaling and responses. Expression of a number of JAZ domain proteins, the key JA-related transcription factor MYC2 as well as key MYB transcription factors and biosynthesis genes of both the indole and aliphatic glucosinolate pathways are changed in linc1 mutants. Moreover, PAMP triggers JA and JA-Ile accumulation in linc1 mutants, whereas salicylic acid levels are unchanged. Despite impairment in PAMP-triggered immunity, linc1 mutants still show basal immunity towards Pseudomonas syringae DC3000 strains. High JA levels usually render plants resistant to necrotrophic pathogen. Thus, linc1 mutants show enhanced resistance to Botrytis cinerea infection. In accordance with a general role of LINC1 in JA signaling, linc1 mutants are hypersensitive to growth inhibition to external JA. In summary, our findings show that the lamin-like LINC1 protein plays a key role in JA signaling and regulation of PTI responses in Arabidopsis.
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spelling doaj.art-5e82d01aea314c1abe96eb3a32998c682022-12-21T19:18:12ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2020-01-011010.3389/fpls.2019.01639492411The Lamin-Like LITTLE NUCLEI 1 (LINC1) Regulates Pattern-Triggered Immunity and Jasmonic Acid SignalingMai Jarad0Kiruthiga Mariappan1Marilia Almeida-Trapp2Michael Florian Mette3Axel Mithöfer4Naganand Rayapuram5Heribert Hirt6DARWIN21, Biological and Environmental Sciences and Engineering Division (BESE), King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi ArabiaDARWIN21, Biological and Environmental Sciences and Engineering Division (BESE), King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi ArabiaDARWIN21, Biological and Environmental Sciences and Engineering Division (BESE), King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi ArabiaDARWIN21, Biological and Environmental Sciences and Engineering Division (BESE), King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi ArabiaResearch Group Plant Defense Physiology, Max Planck Institute for Chemical Ecology, Jena, GermanyDARWIN21, Biological and Environmental Sciences and Engineering Division (BESE), King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi ArabiaDARWIN21, Biological and Environmental Sciences and Engineering Division (BESE), King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi ArabiaPathogen-associated molecular pattern (PAMP) recognition occurs by plasma membrane located receptors that induce among other processes nuclear gene expression. However, signaling to the nuclear compartment is restricted by the nuclear envelope and nuclear pore complexes. We show here that among the four Arabidopsis lamin homologs LITTLE NUCLEI/CROWDED NUCLEI (LINC/CRWN), LINC1 plays an important role in PTI and jasmonic acid (JA) signaling. We show that linc1 knock out mutants affect PAMP-triggered MAPK activation and growth inhibition, but not reactive oxygen species or callose accumulation. We also demonstrate that linc1 mutants are compromised in regulating PAMP-triggered pathogen-related genes, in particular encoding factors involved in JA signaling and responses. Expression of a number of JAZ domain proteins, the key JA-related transcription factor MYC2 as well as key MYB transcription factors and biosynthesis genes of both the indole and aliphatic glucosinolate pathways are changed in linc1 mutants. Moreover, PAMP triggers JA and JA-Ile accumulation in linc1 mutants, whereas salicylic acid levels are unchanged. Despite impairment in PAMP-triggered immunity, linc1 mutants still show basal immunity towards Pseudomonas syringae DC3000 strains. High JA levels usually render plants resistant to necrotrophic pathogen. Thus, linc1 mutants show enhanced resistance to Botrytis cinerea infection. In accordance with a general role of LINC1 in JA signaling, linc1 mutants are hypersensitive to growth inhibition to external JA. In summary, our findings show that the lamin-like LINC1 protein plays a key role in JA signaling and regulation of PTI responses in Arabidopsis.https://www.frontiersin.org/article/10.3389/fpls.2019.01639/fullnuclear envelopelaminpathogen-associated molecular patterninnate immunityjasmonic acidglucosinolate biosynthesis
spellingShingle Mai Jarad
Kiruthiga Mariappan
Marilia Almeida-Trapp
Michael Florian Mette
Axel Mithöfer
Naganand Rayapuram
Heribert Hirt
The Lamin-Like LITTLE NUCLEI 1 (LINC1) Regulates Pattern-Triggered Immunity and Jasmonic Acid Signaling
Frontiers in Plant Science
nuclear envelope
lamin
pathogen-associated molecular pattern
innate immunity
jasmonic acid
glucosinolate biosynthesis
title The Lamin-Like LITTLE NUCLEI 1 (LINC1) Regulates Pattern-Triggered Immunity and Jasmonic Acid Signaling
title_full The Lamin-Like LITTLE NUCLEI 1 (LINC1) Regulates Pattern-Triggered Immunity and Jasmonic Acid Signaling
title_fullStr The Lamin-Like LITTLE NUCLEI 1 (LINC1) Regulates Pattern-Triggered Immunity and Jasmonic Acid Signaling
title_full_unstemmed The Lamin-Like LITTLE NUCLEI 1 (LINC1) Regulates Pattern-Triggered Immunity and Jasmonic Acid Signaling
title_short The Lamin-Like LITTLE NUCLEI 1 (LINC1) Regulates Pattern-Triggered Immunity and Jasmonic Acid Signaling
title_sort lamin like little nuclei 1 linc1 regulates pattern triggered immunity and jasmonic acid signaling
topic nuclear envelope
lamin
pathogen-associated molecular pattern
innate immunity
jasmonic acid
glucosinolate biosynthesis
url https://www.frontiersin.org/article/10.3389/fpls.2019.01639/full
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