Host-pathogen interaction between pitaya and Neoscytalidium dimidiatum reveals the mechanisms of immune response associated with defense regulators and metabolic pathways

Abstract Background Understanding how plants and pathogens regulate each other's gene expression during their interactions is key to revealing the mechanisms of disease resistance and controlling the development of pathogens. Despite extensive studies on the molecular and genetic basis of plant...

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Main Authors: Meng Wang, Zhouwen Wang, Yi Ding, Shaoling Kang, Senrong Jiang, Zhuangjia Yang, Zhan Xie, Jialin Wang, Shuangshuang Wei, Jiaquan Huang, Dongdong Li, Xingyu Jiang, Hua Tang
Format: Article
Language:English
Published: BMC 2024-01-01
Series:BMC Plant Biology
Subjects:
Online Access:https://doi.org/10.1186/s12870-023-04685-y
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author Meng Wang
Zhouwen Wang
Yi Ding
Shaoling Kang
Senrong Jiang
Zhuangjia Yang
Zhan Xie
Jialin Wang
Shuangshuang Wei
Jiaquan Huang
Dongdong Li
Xingyu Jiang
Hua Tang
author_facet Meng Wang
Zhouwen Wang
Yi Ding
Shaoling Kang
Senrong Jiang
Zhuangjia Yang
Zhan Xie
Jialin Wang
Shuangshuang Wei
Jiaquan Huang
Dongdong Li
Xingyu Jiang
Hua Tang
author_sort Meng Wang
collection DOAJ
description Abstract Background Understanding how plants and pathogens regulate each other's gene expression during their interactions is key to revealing the mechanisms of disease resistance and controlling the development of pathogens. Despite extensive studies on the molecular and genetic basis of plant immunity against pathogens, the influence of pitaya immunity on N. dimidiatum metabolism to restrict pathogen growth is poorly understood, and how N. dimidiatum breaks through pitaya defenses. In this study, we used the RNA-seq method to assess the expression profiles of pitaya and N. dimidiatum at 4 time periods after interactions to capture the early effects of N. dimidiatum on pitaya processes. Results The study defined the establishment of an effective method for analyzing transcriptome interactions between pitaya and N. dimidiatum and to obtain global expression profiles. We identified gene expression clusters in both the host pitaya and the pathogen N. dimidiatum. The analysis showed that numerous differentially expressed genes (DEGs) involved in the recognition and defense of pitaya against N. dimidiatum, as well as N. dimidiatum’s evasion of recognition and inhibition of pitaya. The major functional groups identified by GO and KEGG enrichment were responsible for plant and pathogen recognition, phytohormone signaling (such as salicylic acid, abscisic acid). Furthermore, the gene expression of 13 candidate genes involved in phytopathogen recognition, phytohormone receptors, and the plant resistance gene (PG), as well as 7 effector genes of N. dimidiatum, including glycoside hydrolases, pectinase, and putative genes, were validated by qPCR. By focusing on gene expression changes during interactions between pitaya and N. dimidiatum, we were able to observe the infection of N. dimidiatum and its effects on the expression of various defense components and host immune receptors. Conclusion Our data show that various regulators of the immune response are modified during interactions between pitaya and N. dimidiatum. Furthermore, the activation and repression of these genes are temporally coordinated. These findings provide a framework for better understanding the pathogenicity of N. dimidiatum and its role as an opportunistic pathogen. This offers the potential for a more effective defense against N. dimidiatum.
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spelling doaj.art-cbc70bede62d4565b4e3b9e673fd12a92024-01-07T12:18:57ZengBMCBMC Plant Biology1471-22292024-01-0124111910.1186/s12870-023-04685-yHost-pathogen interaction between pitaya and Neoscytalidium dimidiatum reveals the mechanisms of immune response associated with defense regulators and metabolic pathwaysMeng Wang0Zhouwen Wang1Yi Ding2Shaoling Kang3Senrong Jiang4Zhuangjia Yang5Zhan Xie6Jialin Wang7Shuangshuang Wei8Jiaquan Huang9Dongdong Li10Xingyu Jiang11Hua Tang12School of Breeding and Multiplication, Hainan UniversitySchool of Tropical Agriculture and Forestry, Hainan UniversitySchool of Breeding and Multiplication, Hainan UniversitySchool of Breeding and Multiplication, Hainan UniversitySchool of Breeding and Multiplication, Hainan UniversitySchool of Breeding and Multiplication, Hainan UniversitySchool of Breeding and Multiplication, Hainan UniversityCollege of Life Sciences, Hainan UniversityCollege of Life Sciences, Hainan UniversitySchool of Breeding and Multiplication, Hainan UniversitySchool of Breeding and Multiplication, Hainan UniversitySchool of Tropical Agriculture and Forestry, Hainan UniversitySchool of Breeding and Multiplication, Hainan UniversityAbstract Background Understanding how plants and pathogens regulate each other's gene expression during their interactions is key to revealing the mechanisms of disease resistance and controlling the development of pathogens. Despite extensive studies on the molecular and genetic basis of plant immunity against pathogens, the influence of pitaya immunity on N. dimidiatum metabolism to restrict pathogen growth is poorly understood, and how N. dimidiatum breaks through pitaya defenses. In this study, we used the RNA-seq method to assess the expression profiles of pitaya and N. dimidiatum at 4 time periods after interactions to capture the early effects of N. dimidiatum on pitaya processes. Results The study defined the establishment of an effective method for analyzing transcriptome interactions between pitaya and N. dimidiatum and to obtain global expression profiles. We identified gene expression clusters in both the host pitaya and the pathogen N. dimidiatum. The analysis showed that numerous differentially expressed genes (DEGs) involved in the recognition and defense of pitaya against N. dimidiatum, as well as N. dimidiatum’s evasion of recognition and inhibition of pitaya. The major functional groups identified by GO and KEGG enrichment were responsible for plant and pathogen recognition, phytohormone signaling (such as salicylic acid, abscisic acid). Furthermore, the gene expression of 13 candidate genes involved in phytopathogen recognition, phytohormone receptors, and the plant resistance gene (PG), as well as 7 effector genes of N. dimidiatum, including glycoside hydrolases, pectinase, and putative genes, were validated by qPCR. By focusing on gene expression changes during interactions between pitaya and N. dimidiatum, we were able to observe the infection of N. dimidiatum and its effects on the expression of various defense components and host immune receptors. Conclusion Our data show that various regulators of the immune response are modified during interactions between pitaya and N. dimidiatum. Furthermore, the activation and repression of these genes are temporally coordinated. These findings provide a framework for better understanding the pathogenicity of N. dimidiatum and its role as an opportunistic pathogen. This offers the potential for a more effective defense against N. dimidiatum.https://doi.org/10.1186/s12870-023-04685-yHost–pathogen interactionPitaya cankerN.dimidiatumTranscriptomics
spellingShingle Meng Wang
Zhouwen Wang
Yi Ding
Shaoling Kang
Senrong Jiang
Zhuangjia Yang
Zhan Xie
Jialin Wang
Shuangshuang Wei
Jiaquan Huang
Dongdong Li
Xingyu Jiang
Hua Tang
Host-pathogen interaction between pitaya and Neoscytalidium dimidiatum reveals the mechanisms of immune response associated with defense regulators and metabolic pathways
BMC Plant Biology
Host–pathogen interaction
Pitaya canker
N.dimidiatum
Transcriptomics
title Host-pathogen interaction between pitaya and Neoscytalidium dimidiatum reveals the mechanisms of immune response associated with defense regulators and metabolic pathways
title_full Host-pathogen interaction between pitaya and Neoscytalidium dimidiatum reveals the mechanisms of immune response associated with defense regulators and metabolic pathways
title_fullStr Host-pathogen interaction between pitaya and Neoscytalidium dimidiatum reveals the mechanisms of immune response associated with defense regulators and metabolic pathways
title_full_unstemmed Host-pathogen interaction between pitaya and Neoscytalidium dimidiatum reveals the mechanisms of immune response associated with defense regulators and metabolic pathways
title_short Host-pathogen interaction between pitaya and Neoscytalidium dimidiatum reveals the mechanisms of immune response associated with defense regulators and metabolic pathways
title_sort host pathogen interaction between pitaya and neoscytalidium dimidiatum reveals the mechanisms of immune response associated with defense regulators and metabolic pathways
topic Host–pathogen interaction
Pitaya canker
N.dimidiatum
Transcriptomics
url https://doi.org/10.1186/s12870-023-04685-y
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