Discovery of a novel nucleoside immune signaling molecule 2′-deoxyguanosine in microbes and plants

Introduction: Beneficial microorganisms play essential roles in plant growth and induced systemic resistance (ISR) by releasing signaling molecules. Our previous study obtained the crude extract from beneficial endophyte Paecilomyces variotii, termed ZNC (ZhiNengCong), which significantly enhanced p...

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Main Authors: Chongchong Lu, Qingbin Wang, Yanke Jiang, Min Zhang, Xuanlin Meng, Yang Li, Baoyou Liu, Ziyi Yin, Haifeng Liu, Chune Peng, Fuchuan Li, Yingzhe Yue, Mingxia Hao, Yurong Sui, Lulu Wang, Guodong Cheng, Jianzhu Liu, Zhaohui Chu, Changxiang Zhu, Hansong Dong, Xinhua Ding
Format: Article
Language:English
Published: Elsevier 2023-04-01
Series:Journal of Advanced Research
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2090123222001539
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author Chongchong Lu
Qingbin Wang
Yanke Jiang
Min Zhang
Xuanlin Meng
Yang Li
Baoyou Liu
Ziyi Yin
Haifeng Liu
Chune Peng
Fuchuan Li
Yingzhe Yue
Mingxia Hao
Yurong Sui
Lulu Wang
Guodong Cheng
Jianzhu Liu
Zhaohui Chu
Changxiang Zhu
Hansong Dong
Xinhua Ding
author_facet Chongchong Lu
Qingbin Wang
Yanke Jiang
Min Zhang
Xuanlin Meng
Yang Li
Baoyou Liu
Ziyi Yin
Haifeng Liu
Chune Peng
Fuchuan Li
Yingzhe Yue
Mingxia Hao
Yurong Sui
Lulu Wang
Guodong Cheng
Jianzhu Liu
Zhaohui Chu
Changxiang Zhu
Hansong Dong
Xinhua Ding
author_sort Chongchong Lu
collection DOAJ
description Introduction: Beneficial microorganisms play essential roles in plant growth and induced systemic resistance (ISR) by releasing signaling molecules. Our previous study obtained the crude extract from beneficial endophyte Paecilomyces variotii, termed ZNC (ZhiNengCong), which significantly enhanced plant resistance to pathogen even at 100 ng/ml. However, the immunoreactive components of ZNC remain unclear. Here, we further identified one of the immunoreactive components of ZNC is a nucleoside 2′-deoxyguanosine (2-dG). Objectives: This paper intends to reveal the molecular mechanism of microbial-derived 2′-deoxyguanosine (2-dG) in activating plant immunity, and the role of plant-derived 2-dG in plant immunity. Methods: The components of ZNC were separated using a high-performance liquid chromatography (HPLC), and 2-dG is identified using a HPLC–mass spectrometry system (LC-MS). Transcriptome analysis and genetic experiments were used to reveal the immune signaling pathway dependent on 2-dG activation of plant immunity. Results: This study identified 2′-deoxyguanosine (2-dG) as one of the immunoreactive components from ZNC. And 2-dG significantly enhanced plant pathogen resistance even at 10 ng/ml (37.42 nM). Furthermore, 2-dG-induced resistance depends on NPR1, pattern-recognition receptors/coreceptors, ATP receptor P2K1 (DORN1), ethylene signaling but not salicylic acid accumulation. In addition, we identified Arabidopsis VENOSA4 (VEN4) was involved in 2-dG biosynthesis and could convert dGTP to 2-dG, and vne4 mutant plants were more susceptible to pathogens. Conclusion: In summary, microbial-derived 2-dG may act as a novel immune signaling molecule involved in plant-microorganism interactions, and VEN4 is 2-dG biosynthesis gene and plays a key role in plant immunity.
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spelling doaj.art-b249b720f54d4faea8f6d51de08402382023-04-01T08:47:10ZengElsevierJournal of Advanced Research2090-12322023-04-0146115Discovery of a novel nucleoside immune signaling molecule 2′-deoxyguanosine in microbes and plantsChongchong Lu0Qingbin Wang1Yanke Jiang2Min Zhang3Xuanlin Meng4Yang Li5Baoyou Liu6Ziyi Yin7Haifeng Liu8Chune Peng9Fuchuan Li10Yingzhe Yue11Mingxia Hao12Yurong Sui13Lulu Wang14Guodong Cheng15Jianzhu Liu16Zhaohui Chu17Changxiang Zhu18Hansong Dong19Xinhua Ding20State Key Laboratory of Crop Biology, Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong Agricultural University, Taian, Shandong 271018, ChinaShandong Pengbo Biotechnology Co., LTD, Taian 271018, China; National Engineering Laboratory for Efficient Utilization of Soil and Fertilizer Resources, College of Resources and Environment, Shandong Agricultural University, Taian, Shandong 271018, ChinaState Key Laboratory of Crop Biology, Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong Agricultural University, Taian, Shandong 271018, ChinaNational Engineering Laboratory for Efficient Utilization of Soil and Fertilizer Resources, College of Resources and Environment, Shandong Agricultural University, Taian, Shandong 271018, ChinaState Key Laboratory of Crop Biology, Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong Agricultural University, Taian, Shandong 271018, ChinaState Key Laboratory of Crop Biology, Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong Agricultural University, Taian, Shandong 271018, ChinaState Key Laboratory of Crop Biology, Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong Agricultural University, Taian, Shandong 271018, ChinaState Key Laboratory of Crop Biology, Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong Agricultural University, Taian, Shandong 271018, ChinaState Key Laboratory of Crop Biology, Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong Agricultural University, Taian, Shandong 271018, ChinaState Key Laboratory of Crop Biology, Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong Agricultural University, Taian, Shandong 271018, ChinaNational Glycoengineering Research Center and Shandong Key Laboratory of Carbohydrate Chemistry and Glycobiology, Shandong University, 72 Binhai Rd, Qingdao 266200, ChinaState Key Laboratory of Crop Biology, Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong Agricultural University, Taian, Shandong 271018, ChinaState Key Laboratory of Crop Biology, Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong Agricultural University, Taian, Shandong 271018, ChinaState Key Laboratory of Crop Biology, Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong Agricultural University, Taian, Shandong 271018, ChinaState Key Laboratory of Crop Biology, Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong Agricultural University, Taian, Shandong 271018, ChinaCollege of Veterinary Medicine, Shandong Agricultural University, Taian, Shandong 271018, ChinaCollege of Veterinary Medicine, Shandong Agricultural University, Taian, Shandong 271018, ChinaState Key Laboratory of Hybrid Rice, Hubei Hongshan Laboratory, College of Life Sciences, Wuhan University, Wuhan 430072, ChinaState Key Laboratory of Crop Biology, Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong Agricultural University, Taian, Shandong 271018, ChinaState Key Laboratory of Crop Biology, Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong Agricultural University, Taian, Shandong 271018, ChinaState Key Laboratory of Crop Biology, Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong Agricultural University, Taian, Shandong 271018, China; Corresponding author.Introduction: Beneficial microorganisms play essential roles in plant growth and induced systemic resistance (ISR) by releasing signaling molecules. Our previous study obtained the crude extract from beneficial endophyte Paecilomyces variotii, termed ZNC (ZhiNengCong), which significantly enhanced plant resistance to pathogen even at 100 ng/ml. However, the immunoreactive components of ZNC remain unclear. Here, we further identified one of the immunoreactive components of ZNC is a nucleoside 2′-deoxyguanosine (2-dG). Objectives: This paper intends to reveal the molecular mechanism of microbial-derived 2′-deoxyguanosine (2-dG) in activating plant immunity, and the role of plant-derived 2-dG in plant immunity. Methods: The components of ZNC were separated using a high-performance liquid chromatography (HPLC), and 2-dG is identified using a HPLC–mass spectrometry system (LC-MS). Transcriptome analysis and genetic experiments were used to reveal the immune signaling pathway dependent on 2-dG activation of plant immunity. Results: This study identified 2′-deoxyguanosine (2-dG) as one of the immunoreactive components from ZNC. And 2-dG significantly enhanced plant pathogen resistance even at 10 ng/ml (37.42 nM). Furthermore, 2-dG-induced resistance depends on NPR1, pattern-recognition receptors/coreceptors, ATP receptor P2K1 (DORN1), ethylene signaling but not salicylic acid accumulation. In addition, we identified Arabidopsis VENOSA4 (VEN4) was involved in 2-dG biosynthesis and could convert dGTP to 2-dG, and vne4 mutant plants were more susceptible to pathogens. Conclusion: In summary, microbial-derived 2-dG may act as a novel immune signaling molecule involved in plant-microorganism interactions, and VEN4 is 2-dG biosynthesis gene and plays a key role in plant immunity.http://www.sciencedirect.com/science/article/pii/S2090123222001539Endophytic fungiPlant immune elicitorET signalingNPR1Pattern- recognition receptors/coreceptors
spellingShingle Chongchong Lu
Qingbin Wang
Yanke Jiang
Min Zhang
Xuanlin Meng
Yang Li
Baoyou Liu
Ziyi Yin
Haifeng Liu
Chune Peng
Fuchuan Li
Yingzhe Yue
Mingxia Hao
Yurong Sui
Lulu Wang
Guodong Cheng
Jianzhu Liu
Zhaohui Chu
Changxiang Zhu
Hansong Dong
Xinhua Ding
Discovery of a novel nucleoside immune signaling molecule 2′-deoxyguanosine in microbes and plants
Journal of Advanced Research
Endophytic fungi
Plant immune elicitor
ET signaling
NPR1
Pattern- recognition receptors/coreceptors
title Discovery of a novel nucleoside immune signaling molecule 2′-deoxyguanosine in microbes and plants
title_full Discovery of a novel nucleoside immune signaling molecule 2′-deoxyguanosine in microbes and plants
title_fullStr Discovery of a novel nucleoside immune signaling molecule 2′-deoxyguanosine in microbes and plants
title_full_unstemmed Discovery of a novel nucleoside immune signaling molecule 2′-deoxyguanosine in microbes and plants
title_short Discovery of a novel nucleoside immune signaling molecule 2′-deoxyguanosine in microbes and plants
title_sort discovery of a novel nucleoside immune signaling molecule 2 deoxyguanosine in microbes and plants
topic Endophytic fungi
Plant immune elicitor
ET signaling
NPR1
Pattern- recognition receptors/coreceptors
url http://www.sciencedirect.com/science/article/pii/S2090123222001539
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