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      Unravelling the Roles of Nitrogen Nutrition in Plant Disease Defences

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          Abstract

          Nitrogen (N) is one of the most important elements that has a central impact on plant growth and yield. N is also widely involved in plant stress responses, but its roles in host-pathogen interactions are complex as each affects the other. In this review, we summarize the relationship between N nutrition and plant disease and stress its importance for both host and pathogen. From the perspective of the pathogen, we describe how N can affect the pathogen’s infection strategy, whether necrotrophic or biotrophic. N can influence the deployment of virulence factors such as type III secretion systems in bacterial pathogen or contribute nutrients such as gamma-aminobutyric acid to the invader. Considering the host, the association between N nutrition and plant defence is considered in terms of physical, biochemical and genetic mechanisms. Generally, N has negative effects on physical defences and the production of anti-microbial phytoalexins but positive effects on defence-related enzymes and proteins to affect local defence as well as systemic resistance. N nutrition can also influence defence via amino acid metabolism and hormone production to affect downstream defence-related gene expression via transcriptional regulation and nitric oxide (NO) production, which represents a direct link with N. Although the critical role of N nutrition in plant defences is stressed in this review, further work is urgently needed to provide a comprehensive understanding of how opposing virulence and defence mechanisms are influenced by interacting networks.

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          Most cited references147

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          Systemic acquired resistance: turning local infection into global defense.

          Systemic acquired resistance (SAR) is an induced immune mechanism in plants. Unlike vertebrate adaptive immunity, SAR is broad spectrum, with no specificity to the initial infection. An avirulent pathogen causing local programmed cell death can induce SAR through generation of mobile signals, accumulation of the defense hormone salicylic acid, and secretion of the antimicrobial PR (pathogenesis-related) proteins. Consequently, the rest of the plant is protected from secondary infection for a period of weeks to months. SAR can even be passed on to progeny through epigenetic regulation. The Arabidopsis NPR1 (nonexpresser of PR genes 1) protein is a master regulator of SAR. Recent study has shown that salicylic acid directly binds to the NPR1 adaptor proteins NPR3 and NPR4, regulates their interactions with NPR1, and controls NPR1 protein stability. However, how NPR1 interacts with TGA transcription factors to activate defense gene expression is still not well understood. In addition, redox regulators, the mediator complex, WRKY transcription factors, endoplasmic reticulum-resident proteins, and DNA repair proteins play critical roles in SAR.
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            Defense Priming: An Adaptive Part of Induced Resistance

            Priming is an adaptive strategy that improves the defensive capacity of plants. This phenomenon is marked by an enhanced activation of induced defense mechanisms. Stimuli from pathogens, beneficial microbes, or arthropods, as well as chemicals and abiotic cues, can trigger the establishment of priming by acting as warning signals. Upon stimulus perception, changes may occur in the plant at the physiological, transcriptional, metabolic, and epigenetic levels. This phase is called the priming phase. Upon subsequent challenge, the plant effectively mounts a faster and/or stronger defense response that defines the postchallenge primed state and results in increased resistance and/or stress tolerance. Priming can be durable and maintained throughout the plant's life cycle and can even be transmitted to subsequent generations, therefore representing a type of plant immunological memory.
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              Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen.

              Transcriptome analysis, using Affymetrix ATH1 arrays and a real-time reverse transcription-PCR platform for >1,400 transcription factors, was performed to identify processes affected by long-term nitrogen-deprivation or short-term nitrate nutrition in Arabidopsis. Two days of nitrogen deprivation led to coordinate repression of the majority of the genes assigned to photosynthesis, chlorophyll synthesis, plastid protein synthesis, induction of many genes for secondary metabolism, and reprogramming of mitochondrial electron transport. Nitrate readdition led to rapid, widespread, and coordinated changes. Multiple genes for the uptake and reduction of nitrate, the generation of reducing equivalents, and organic acid skeletons were induced within 30 min, before primary metabolites changed significantly. By 3 h, most genes assigned to amino acid and nucleotide biosynthesis and scavenging were induced, while most genes assigned to amino acid and nucleotide breakdown were repressed. There was coordinate induction of many genes assigned to RNA synthesis and processing and most of the genes assigned to amino acid activation and protein synthesis. Although amino acids involved in central metabolism increased, minor amino acids decreased, providing independent evidence for the activation of protein synthesis. Specific genes encoding expansin and tonoplast intrinsic proteins were induced, indicating activation of cell expansion and growth in response to nitrate nutrition. There were rapid responses in the expression of many genes potentially involved in regulation, including genes for trehalose metabolism and hormone metabolism, protein kinases and phosphatases, receptor kinases, and transcription factors.

                Author and article information

                Journal
                Int J Mol Sci
                Int J Mol Sci
                ijms
                International Journal of Molecular Sciences
                MDPI
                1422-0067
                16 January 2020
                January 2020
                : 21
                : 2
                : 572
                Affiliations
                [1 ]Jiangsu Provincial Key Lab of Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Wastes, Educational Ministry Engineering Center of Resource-saving fertilizers, Nanjing Agricultural University, Nanjing 210095, China; sunyumingagw@ 123456163.com (Y.S.); shenqirong@ 123456njau.edu.cn (Q.S.); sguo@ 123456njau.edu.cn (S.G.)
                [2 ]Jiangsu Key Laboratory for the Research and Utilization of Plant Resources, Institute of Botany, Jiangsu Province and Chinese Academy of Sciences, Nanjing 210014, China
                [3 ]Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, Aberystwyth SY23 3DA, UK; lum@ 123456aber.ac.uk
                Author notes
                [* ]Correspondence: minwang@ 123456njau.edu.cn ; Tel.: +86-25-8439-5212
                Author information
                https://orcid.org/0000-0002-0961-9817
                Article
                ijms-21-00572
                10.3390/ijms21020572
                7014335
                31963138
                938bab04-dc7d-4473-ba88-62036e8e1abd
                © 2020 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 10 December 2019
                : 13 January 2020
                Categories
                Review

                Molecular biology
                nitrogen,plant disease,physical,biochemical,molecular,disease defence
                Molecular biology
                nitrogen, plant disease, physical, biochemical, molecular, disease defence

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