The Glutamate Receptor Plays a Role in Defense against <i>Botrytis cinerea</i> through Electrical Signaling in Tomato

Plant <i>glutamate-like receptor</i> genes (<i>GLRs</i>) are homologous to mammalian <i>ionotropic glutamate receptors</i> genes (<i>iGluRs</i>). Although GLRs have been implicated in plant defenses to biotic stress, the relationship between GLR-mediat...

Full description

Bibliographic Details
Main Authors: Shuxian Feng, Caizhe Pan, Shuting Ding, Qiaomei Ma, Chaoyi Hu, Ping Wang, Kai Shi
Format: Article
Language:English
Published: MDPI AG 2021-11-01
Series:Applied Sciences
Subjects:
Online Access:https://www.mdpi.com/2076-3417/11/23/11217
_version_ 1827675191452368896
author Shuxian Feng
Caizhe Pan
Shuting Ding
Qiaomei Ma
Chaoyi Hu
Ping Wang
Kai Shi
author_facet Shuxian Feng
Caizhe Pan
Shuting Ding
Qiaomei Ma
Chaoyi Hu
Ping Wang
Kai Shi
author_sort Shuxian Feng
collection DOAJ
description Plant <i>glutamate-like receptor</i> genes (<i>GLRs</i>) are homologous to mammalian <i>ionotropic glutamate receptors</i> genes (<i>iGluRs</i>). Although GLRs have been implicated in plant defenses to biotic stress, the relationship between GLR-mediated plant immunity against fungal pathogens and electrical signals remains poorly understood. Here, we found that pretreatment with a GLR inhibitor, 6,7-dinitriquinoxaline-2,3-dione (DNQX), increased the susceptibility of tomato plants to the necrotrophic fungal pathogen <i>Botrytis cinerea</i>. Assessment of the <i>glr3.3</i>, <i>glr3.5</i> and <i>glr3.3/glr3.5</i> double-mutants upon <i>B. cinerea</i> infection showed that tomato GLR3.3 and GLR3.5 are essential for plant immunity against <i>B. cinerea</i>, wherein GLR3.3 plays the main role. Analysis of the membrane potential changes induced by glutamate (Glu) or glycine (Gly) revealed that amplitude was significantly reduced by knocking out <i>GLR3.3</i> in tomato. While treatment with Glu or Gly significantly increased immunity against <i>B. cinerea</i> in wild-type plants, this effect was significantly attenuated in <i>glr3.3</i> mutants. Thus, our data demonstrate that GLR3.3- and GLR3.5-mediated plant immunity against <i>B. cinerea</i> is associated with electrical signals in tomato plants.
first_indexed 2024-03-10T04:57:43Z
format Article
id doaj.art-e5d957a0728443edb7e9a7d09907f14d
institution Directory Open Access Journal
issn 2076-3417
language English
last_indexed 2024-03-10T04:57:43Z
publishDate 2021-11-01
publisher MDPI AG
record_format Article
series Applied Sciences
spelling doaj.art-e5d957a0728443edb7e9a7d09907f14d2023-11-23T02:04:27ZengMDPI AGApplied Sciences2076-34172021-11-0111231121710.3390/app112311217The Glutamate Receptor Plays a Role in Defense against <i>Botrytis cinerea</i> through Electrical Signaling in TomatoShuxian Feng0Caizhe Pan1Shuting Ding2Qiaomei Ma3Chaoyi Hu4Ping Wang5Kai Shi6The Department of Horticulture, Zhejiang University, Hangzhou 310058, ChinaThe Department of Horticulture, Zhejiang University, Hangzhou 310058, ChinaThe Department of Horticulture, Zhejiang University, Hangzhou 310058, ChinaThe Department of Horticulture, Zhejiang University, Hangzhou 310058, ChinaThe Department of Horticulture, Zhejiang University, Hangzhou 310058, ChinaThe Department of Horticulture, Zhejiang University, Hangzhou 310058, ChinaThe Department of Horticulture, Zhejiang University, Hangzhou 310058, ChinaPlant <i>glutamate-like receptor</i> genes (<i>GLRs</i>) are homologous to mammalian <i>ionotropic glutamate receptors</i> genes (<i>iGluRs</i>). Although GLRs have been implicated in plant defenses to biotic stress, the relationship between GLR-mediated plant immunity against fungal pathogens and electrical signals remains poorly understood. Here, we found that pretreatment with a GLR inhibitor, 6,7-dinitriquinoxaline-2,3-dione (DNQX), increased the susceptibility of tomato plants to the necrotrophic fungal pathogen <i>Botrytis cinerea</i>. Assessment of the <i>glr3.3</i>, <i>glr3.5</i> and <i>glr3.3/glr3.5</i> double-mutants upon <i>B. cinerea</i> infection showed that tomato GLR3.3 and GLR3.5 are essential for plant immunity against <i>B. cinerea</i>, wherein GLR3.3 plays the main role. Analysis of the membrane potential changes induced by glutamate (Glu) or glycine (Gly) revealed that amplitude was significantly reduced by knocking out <i>GLR3.3</i> in tomato. While treatment with Glu or Gly significantly increased immunity against <i>B. cinerea</i> in wild-type plants, this effect was significantly attenuated in <i>glr3.3</i> mutants. Thus, our data demonstrate that GLR3.3- and GLR3.5-mediated plant immunity against <i>B. cinerea</i> is associated with electrical signals in tomato plants.https://www.mdpi.com/2076-3417/11/23/11217glutamate receptor-likenecrotrophic pathogenselectrical signal<i>Botrytis cinerea</i><i>Solanum lycopersicum</i>
spellingShingle Shuxian Feng
Caizhe Pan
Shuting Ding
Qiaomei Ma
Chaoyi Hu
Ping Wang
Kai Shi
The Glutamate Receptor Plays a Role in Defense against <i>Botrytis cinerea</i> through Electrical Signaling in Tomato
Applied Sciences
glutamate receptor-like
necrotrophic pathogens
electrical signal
<i>Botrytis cinerea</i>
<i>Solanum lycopersicum</i>
title The Glutamate Receptor Plays a Role in Defense against <i>Botrytis cinerea</i> through Electrical Signaling in Tomato
title_full The Glutamate Receptor Plays a Role in Defense against <i>Botrytis cinerea</i> through Electrical Signaling in Tomato
title_fullStr The Glutamate Receptor Plays a Role in Defense against <i>Botrytis cinerea</i> through Electrical Signaling in Tomato
title_full_unstemmed The Glutamate Receptor Plays a Role in Defense against <i>Botrytis cinerea</i> through Electrical Signaling in Tomato
title_short The Glutamate Receptor Plays a Role in Defense against <i>Botrytis cinerea</i> through Electrical Signaling in Tomato
title_sort glutamate receptor plays a role in defense against i botrytis cinerea i through electrical signaling in tomato
topic glutamate receptor-like
necrotrophic pathogens
electrical signal
<i>Botrytis cinerea</i>
<i>Solanum lycopersicum</i>
url https://www.mdpi.com/2076-3417/11/23/11217
work_keys_str_mv AT shuxianfeng theglutamatereceptorplaysaroleindefenseagainstibotrytiscinereaithroughelectricalsignalingintomato
AT caizhepan theglutamatereceptorplaysaroleindefenseagainstibotrytiscinereaithroughelectricalsignalingintomato
AT shutingding theglutamatereceptorplaysaroleindefenseagainstibotrytiscinereaithroughelectricalsignalingintomato
AT qiaomeima theglutamatereceptorplaysaroleindefenseagainstibotrytiscinereaithroughelectricalsignalingintomato
AT chaoyihu theglutamatereceptorplaysaroleindefenseagainstibotrytiscinereaithroughelectricalsignalingintomato
AT pingwang theglutamatereceptorplaysaroleindefenseagainstibotrytiscinereaithroughelectricalsignalingintomato
AT kaishi theglutamatereceptorplaysaroleindefenseagainstibotrytiscinereaithroughelectricalsignalingintomato
AT shuxianfeng glutamatereceptorplaysaroleindefenseagainstibotrytiscinereaithroughelectricalsignalingintomato
AT caizhepan glutamatereceptorplaysaroleindefenseagainstibotrytiscinereaithroughelectricalsignalingintomato
AT shutingding glutamatereceptorplaysaroleindefenseagainstibotrytiscinereaithroughelectricalsignalingintomato
AT qiaomeima glutamatereceptorplaysaroleindefenseagainstibotrytiscinereaithroughelectricalsignalingintomato
AT chaoyihu glutamatereceptorplaysaroleindefenseagainstibotrytiscinereaithroughelectricalsignalingintomato
AT pingwang glutamatereceptorplaysaroleindefenseagainstibotrytiscinereaithroughelectricalsignalingintomato
AT kaishi glutamatereceptorplaysaroleindefenseagainstibotrytiscinereaithroughelectricalsignalingintomato