Expression of PmACRE1 in Arabidopsis thaliana enables host defence against Bursaphelenchus xylophilus infection

Abstract Background Pine wilt disease (PWD) is a destructive disease that endangers pine trees, resulting in the wilting, with yellowing and browning of the needles, and eventually the death of the trees. Previous studies showed that the Avr9/Cf-9 rapidly elicited (PmACRE1) gene was downregulated by...

Full description

Bibliographic Details
Main Authors: Wanfeng Xie, Xiaomei Xu, Wenjing Qiu, Xiaolin Lai, Mengxia Liu, Feiping Zhang
Format: Article
Language:English
Published: BMC 2022-11-01
Series:BMC Plant Biology
Subjects:
Online Access:https://doi.org/10.1186/s12870-022-03929-7
_version_ 1811211010902589440
author Wanfeng Xie
Xiaomei Xu
Wenjing Qiu
Xiaolin Lai
Mengxia Liu
Feiping Zhang
author_facet Wanfeng Xie
Xiaomei Xu
Wenjing Qiu
Xiaolin Lai
Mengxia Liu
Feiping Zhang
author_sort Wanfeng Xie
collection DOAJ
description Abstract Background Pine wilt disease (PWD) is a destructive disease that endangers pine trees, resulting in the wilting, with yellowing and browning of the needles, and eventually the death of the trees. Previous studies showed that the Avr9/Cf-9 rapidly elicited (PmACRE1) gene was downregulated by Bursaphelenchus xylophilus infection, suggesting a correlation between PmACRE1 expression and pine tolerance. Here, we used the expression of PmACRE1 in Arabidopsis thaliana to evaluate the role of PmACRE1 in the regulation of host defence against B. xylophilus infection. Results Our results showed that the transformation of PmACRE1 into A. thaliana enhanced plant resistance to the pine wood nematode (PWN); that is, the leaves of the transgenic line remained healthy for a longer period than those of the blank vector group. Ascorbate peroxidase (APX) activity and total phenolic acid and total flavonoid contents were higher in the transgenic line than in the control line. Widely targeted metabolomics analysis of the global secondary metabolites in the transgenic line and the vector control line showed that the contents of 30 compounds were significantly different between these two lines; specifically, the levels of crotaline, neohesperidin, nobiletin, vestitol, and 11 other compounds were significantly increased in the transgenic line. The studies also showed that the ACRE1 protein interacted with serine hydroxymethyltransferase, catalase domain-containing protein, myrosinase, dihydrolipoyl dehydrogenase, ketol-acid reductoisomerase, geranylgeranyl diphosphate reductase, S-adenosylmethionine synthase, glutamine synthetase, and others to comprehensively regulate plant resistance. Conclusions Taken together, these results indicate that PmACRE1 has a potential role in the regulation of plant defence against PWNs.
first_indexed 2024-04-12T05:05:46Z
format Article
id doaj.art-265d116511c54baf8df5a3abc882779e
institution Directory Open Access Journal
issn 1471-2229
language English
last_indexed 2024-04-12T05:05:46Z
publishDate 2022-11-01
publisher BMC
record_format Article
series BMC Plant Biology
spelling doaj.art-265d116511c54baf8df5a3abc882779e2022-12-22T03:46:52ZengBMCBMC Plant Biology1471-22292022-11-0122111410.1186/s12870-022-03929-7Expression of PmACRE1 in Arabidopsis thaliana enables host defence against Bursaphelenchus xylophilus infectionWanfeng Xie0Xiaomei Xu1Wenjing Qiu2Xiaolin Lai3Mengxia Liu4Feiping Zhang5Jinshan College, Fujian Agriculture and Forestry UniversityKey Laboratory of Integrated Pest Management in Ecological Forests, Fujian Province University, Fujian Agriculture and Forestry UniversityKey Laboratory of Integrated Pest Management in Ecological Forests, Fujian Province University, Fujian Agriculture and Forestry UniversityKey Laboratory of Integrated Pest Management in Ecological Forests, Fujian Province University, Fujian Agriculture and Forestry UniversityKey Laboratory of Integrated Pest Management in Ecological Forests, Fujian Province University, Fujian Agriculture and Forestry UniversityKey Laboratory of Integrated Pest Management in Ecological Forests, Fujian Province University, Fujian Agriculture and Forestry UniversityAbstract Background Pine wilt disease (PWD) is a destructive disease that endangers pine trees, resulting in the wilting, with yellowing and browning of the needles, and eventually the death of the trees. Previous studies showed that the Avr9/Cf-9 rapidly elicited (PmACRE1) gene was downregulated by Bursaphelenchus xylophilus infection, suggesting a correlation between PmACRE1 expression and pine tolerance. Here, we used the expression of PmACRE1 in Arabidopsis thaliana to evaluate the role of PmACRE1 in the regulation of host defence against B. xylophilus infection. Results Our results showed that the transformation of PmACRE1 into A. thaliana enhanced plant resistance to the pine wood nematode (PWN); that is, the leaves of the transgenic line remained healthy for a longer period than those of the blank vector group. Ascorbate peroxidase (APX) activity and total phenolic acid and total flavonoid contents were higher in the transgenic line than in the control line. Widely targeted metabolomics analysis of the global secondary metabolites in the transgenic line and the vector control line showed that the contents of 30 compounds were significantly different between these two lines; specifically, the levels of crotaline, neohesperidin, nobiletin, vestitol, and 11 other compounds were significantly increased in the transgenic line. The studies also showed that the ACRE1 protein interacted with serine hydroxymethyltransferase, catalase domain-containing protein, myrosinase, dihydrolipoyl dehydrogenase, ketol-acid reductoisomerase, geranylgeranyl diphosphate reductase, S-adenosylmethionine synthase, glutamine synthetase, and others to comprehensively regulate plant resistance. Conclusions Taken together, these results indicate that PmACRE1 has a potential role in the regulation of plant defence against PWNs.https://doi.org/10.1186/s12870-022-03929-7Pine wilt diseasePmACRE1MetabolitesDisease resistanceProtein interactions
spellingShingle Wanfeng Xie
Xiaomei Xu
Wenjing Qiu
Xiaolin Lai
Mengxia Liu
Feiping Zhang
Expression of PmACRE1 in Arabidopsis thaliana enables host defence against Bursaphelenchus xylophilus infection
BMC Plant Biology
Pine wilt disease
PmACRE1
Metabolites
Disease resistance
Protein interactions
title Expression of PmACRE1 in Arabidopsis thaliana enables host defence against Bursaphelenchus xylophilus infection
title_full Expression of PmACRE1 in Arabidopsis thaliana enables host defence against Bursaphelenchus xylophilus infection
title_fullStr Expression of PmACRE1 in Arabidopsis thaliana enables host defence against Bursaphelenchus xylophilus infection
title_full_unstemmed Expression of PmACRE1 in Arabidopsis thaliana enables host defence against Bursaphelenchus xylophilus infection
title_short Expression of PmACRE1 in Arabidopsis thaliana enables host defence against Bursaphelenchus xylophilus infection
title_sort expression of pmacre1 in arabidopsis thaliana enables host defence against bursaphelenchus xylophilus infection
topic Pine wilt disease
PmACRE1
Metabolites
Disease resistance
Protein interactions
url https://doi.org/10.1186/s12870-022-03929-7
work_keys_str_mv AT wanfengxie expressionofpmacre1inarabidopsisthalianaenableshostdefenceagainstbursaphelenchusxylophilusinfection
AT xiaomeixu expressionofpmacre1inarabidopsisthalianaenableshostdefenceagainstbursaphelenchusxylophilusinfection
AT wenjingqiu expressionofpmacre1inarabidopsisthalianaenableshostdefenceagainstbursaphelenchusxylophilusinfection
AT xiaolinlai expressionofpmacre1inarabidopsisthalianaenableshostdefenceagainstbursaphelenchusxylophilusinfection
AT mengxialiu expressionofpmacre1inarabidopsisthalianaenableshostdefenceagainstbursaphelenchusxylophilusinfection
AT feipingzhang expressionofpmacre1inarabidopsisthalianaenableshostdefenceagainstbursaphelenchusxylophilusinfection