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Metabolites
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Metabolomics in Plant Defence
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Metabolomics in Plant Defence

A special issue of Metabolites (ISSN 2218-1989). This special issue belongs to the section "Plant Metabolism".

Deadline for manuscript submissions: closed (1 March 2021) | Viewed by 35746

Special Issue Editors

Dr. Victoria Pastor

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Guest Editor
Departament de Ciències Agràries i del Medi Natural, Campus del Riu Sec, Metabolic Integration and Cell Signalling Group, Universitat Jaume I (UJI), E-12071-Castelló de la Plana, Spain
Interests: plant–microbe interaction; plant-induced resistance; defence priming; metabolomics
Dr. Pierre Pétriacq

E-Mail Website
Guest Editor
UMR Biologie du Fruit et Pathologie, Université de Bordeaux, INRAE, F-33140 Villenave d’Ornon, France
Interests: plant biochemistry; redox metabolism; stress responses; metabolomics; mass spectrometry
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

As sessile organisms, plants must adjust their metabolisms quickly to respond properly to the changing environment, such as pathogenic threads. Plant immunity is orchestrated by multiple events, and metabolites exert an important role in the final output of the plant-microbe interaction. The implementation of -omics in plant science has transformed the landscape in phytopathological studies. Specifically, metabolomics is a powerful systems biology tool that gathers integrative information from different biological levels. It is thus a great approach to study the functional aspects of plant–pathogen interactions.

This Special Issue will include but not be limited to research papers, reviews, technical advances, opinions that focus on the functional metabolites involved in plant–biotic interactions, including symbionts, multiway interactions, crosstalk of biotic–abiotic relationships. Dynamic aspects of metabolomics such as flux analysis and metabolic modeling and the pressing challenges of the annotation and identification of metabolites and host vs. pathogen metabolome distinction are considered of major interest.

Dr. Victoria Pastor
Dr. Pierre Pétriacq
Guest Editors

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Keywords

  • Functional metabolomics
  • Metabolites
  • Plant defenses
  • Plant–microbe/pest interaction
  • Data processing
  • Targeted metabolomics
  • Untargeted metabolomics

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Published Papers (9 papers)

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Research

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22 pages, 2654 KiB  
Article
Metabolomics and Dual RNA-Sequencing on Root Nodules Revealed New Cellular Functions Controlled by Paraburkholderia phymatum NifA
by Paula Bellés-Sancho, Martina Lardi, Yilei Liu, Leo Eberl, Nicola Zamboni, Aurélien Bailly and Gabriella Pessi
Metabolites 2021, 11(7), 455; https://doi.org/10.3390/metabo11070455 - 15 Jul 2021
Cited by 5 | Viewed by 3374
Abstract
Paraburkholderia phymatum STM815 is a nitrogen-fixing endosymbiont that nodulate the agriculturally important Phaseolus vulgaris and several other host plants. We previously showed that the nodules induced by a STM815 mutant of the gene encoding the master regulator of nitrogen fixation NifA showed no [...] Read more.
Paraburkholderia phymatum STM815 is a nitrogen-fixing endosymbiont that nodulate the agriculturally important Phaseolus vulgaris and several other host plants. We previously showed that the nodules induced by a STM815 mutant of the gene encoding the master regulator of nitrogen fixation NifA showed no nitrogenase activity (Fix−) and increased in number compared to P. vulgaris plants infected with the wild-type strain. To further investigate the role of NifA during symbiosis, nodules from P. phymatum wild-type and nifA mutants were collected and analyzed by metabolomics and dual RNA-Sequencing, allowing us to investigate both host and symbiont transcriptome. Using this approach, several metabolites’ changes could be assigned to bacterial or plant responses. While the amount of the C4-dicarboxylic acid succinate and of several amino acids was lower in Fix− nodules, the level of indole-acetamide (IAM) and brassinosteroids increased. Transcriptome analysis identified P. phymatum genes involved in transport of C4-dicarboxylic acids, carbon metabolism, auxin metabolism and stress response to be differentially expressed in absence of NifA. Furthermore, P. vulgaris genes involved in autoregulation of nodulation (AON) are repressed in nodules in absence of NifA potentially explaining the hypernodulation phenotype of the nifA mutant. These results and additional validation experiments suggest that P. phymatum STM815 NifA is not only important to control expression of nitrogenase and related enzymes but is also involved in regulating its own auxin production and stress response. Finally, our data indicate that P. vulgaris does sanction the nifA nodules by depleting the local carbon allocation rather than by mounting a strong systemic immune response to the Fix− rhizobia. Full article
(This article belongs to the Special Issue Metabolomics in Plant Defence)
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11 pages, 4251 KiB  
Article
Metabolic Mechanism of Plant Defense against Rice Blast Induced by Probenazole
by Zhaochen Wu, Guozhen Wang, Borui Zhang, Tan Dai, Anyu Gu, Xiaolin Li, Xingkai Cheng, Pengfei Liu, Jianjun Hao and Xili Liu
Metabolites 2021, 11(4), 246; https://doi.org/10.3390/metabo11040246 - 16 Apr 2021
Cited by 13 | Viewed by 3031
Abstract
The probenazole fungicide is used for controlling rice blast (Magnaporthe grisea) primarily by inducing disease resistance of the plant. To investigate the mechanism of induced plant defense, rice seedlings were treated with probenazole at 15 days post emergence, and non-treated plants [...] Read more.
The probenazole fungicide is used for controlling rice blast (Magnaporthe grisea) primarily by inducing disease resistance of the plant. To investigate the mechanism of induced plant defense, rice seedlings were treated with probenazole at 15 days post emergence, and non-treated plants were used for the control. The plants were infected with M. grisea 5 days after chemical treatment and incubated in a greenhouse. After 7 days, rice seedlings were sampled. The metabolome of rice seedlings was chemically extracted and analyzed using gas chromatography and mass spectrum (GC-MS). The GC-MS data were processed using analysis of variance (ANOVA), principal component analysis (PCA) and metabolic pathway elucidation. Results showed that probenazole application significantly affected the metabolic profile of rice seedlings, and the effect was proportionally leveraged with the increase of probenazole concentration. Probenazole resulted in a change of 54 metabolites. Salicylic acid, γ-aminobutyrate, shikimate and several other primary metabolites related to plant resistance were significantly up-regulated and some metabolites such as phenylalanine, valine and proline were down-regulated in probenazole-treated seedlings. These results revealed a metabolic pathway of rice seedlings induced by probenazole treatment regarding the resistance to M. grisea infection. Full article
(This article belongs to the Special Issue Metabolomics in Plant Defence)
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17 pages, 2055 KiB  
Article
Targeted Metabolic Profiles of the Leaves and Xylem Sap of Two Sugarcane Genotypes Infected with the Vascular Bacterial Pathogen Leifsonia xyli subsp. xyli
by Fernanda R. Castro-Moretti, Jean-Christophe Cocuron, Mariana C. Cia, Thais R. Cataldi, Carlos A. Labate, Ana Paula Alonso and Luis E. A. Camargo
Metabolites 2021, 11(4), 234; https://doi.org/10.3390/metabo11040234 - 12 Apr 2021
Cited by 7 | Viewed by 2928
Abstract
Ratoon stunt (RS) is a worldwide disease that reduces biomass up to 80% and is caused by the xylem-dwelling bacterium Leifsonia xyli subsp. xyli. This study identified discriminant metabolites between a resistant (R) and a susceptible (S) sugarcane variety at the early [...] Read more.
Ratoon stunt (RS) is a worldwide disease that reduces biomass up to 80% and is caused by the xylem-dwelling bacterium Leifsonia xyli subsp. xyli. This study identified discriminant metabolites between a resistant (R) and a susceptible (S) sugarcane variety at the early stages of pathogen colonization (30 and 120 days after inoculation—DAI) by untargeted and targeted metabolomics of leaves and xylem sap using gas chromatography-mass spectrometry (GC-MS) and liquid chromatography-tandem mass spectrometry (LC-MS/MS), respectively. Bacterial titers were quantified in sugarcane extracts at 180 DAI through real-time polymerase chain reaction. Bacterial titers were at least four times higher on the S variety than in the R one. Global profiling detected 514 features in the leaves and 68 in the sap, while 119 metabolites were quantified in the leaves and 28 in the sap by targeted metabolomics. Comparisons between mock-inoculated treatments indicated a greater abundance of amino acids in the leaves of the S variety and of phenolics, flavonoids, and salicylic acid in the R one. In the xylem sap, fewer differences were detected among phenolics and flavonoids, but also included higher abundances of the signaling molecule sorbitol and glycerol in R. Metabolic changes in the leaves following pathogen inoculation were detected earlier in R than in S and were mostly related to amino acids in R and to phosphorylated compounds in S. Differentially represented metabolites in the xylem sap included abscisic acid. The data represent a valuable resource of potential biomarkers for metabolite-assisted selection of resistant varieties to RS. Full article
(This article belongs to the Special Issue Metabolomics in Plant Defence)
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20 pages, 1973 KiB  
Article
Metabolic Profile Discriminates and Predicts Arabidopsis Susceptibility to Virus under Field Conditions
by Bernadette Rubio, Olivier Fernandez, Patrick Cosson, Thierry Berton, Mélodie Caballero, Roxane Lion, Fabrice Roux, Joy Bergelson, Yves Gibon and Valérie Schurdi-Levraud
Metabolites 2021, 11(4), 230; https://doi.org/10.3390/metabo11040230 - 9 Apr 2021
Cited by 1 | Viewed by 2694
Abstract
As obligatory parasites, plant viruses alter host cellular metabolism. There is a lack of information on the variability of virus-induced metabolic responses among genetically diverse plants in a natural context with daily changing conditions. To decipher the metabolic landscape of plant-virus interactions in [...] Read more.
As obligatory parasites, plant viruses alter host cellular metabolism. There is a lack of information on the variability of virus-induced metabolic responses among genetically diverse plants in a natural context with daily changing conditions. To decipher the metabolic landscape of plant-virus interactions in a natural setting, twenty-six and ten accessions of Arabidopsis thaliana were inoculated with Turnip mosaic virus (TuMV), in two field experiments over 2 years. The accessions were measured for viral accumulation, above-ground biomass, targeted and untargeted metabolic profiles. The phenotypes of the accessions ranged from susceptibility to resistance. Susceptible and resistant accessions were shown to have different metabolic routes after inoculation. Susceptible genotypes accumulate primary and secondary metabolites upon infection, at the cost of hindered growth. Twenty-one metabolic signatures significantly accumulated in resistant accessions whereas they maintained their growth as mock-inoculated plants without biomass penalty. Metabolic content was demonstrated to discriminate and be highly predictive of the susceptibility of inoculated Arabidopsis. This study is the first to describe the metabolic landscape of plant-virus interactions in a natural setting and its predictive link to susceptibility. It provides new insights on plant-virus interactions. In this undomesticated species and in ecologically realistic conditions, growth and resistance are in a permanent conversation. Full article
(This article belongs to the Special Issue Metabolomics in Plant Defence)
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19 pages, 839 KiB  
Article
Pinus pinaster Early Hormonal Defence Responses to Pinewood Nematode (Bursaphelenchus xylophilus) Infection
by Ana M. Rodrigues, Swen Langer, Isabel Carrasquinho, Ed Bergström, Tony Larson, Jane Thomas-Oates and Carla António
Metabolites 2021, 11(4), 227; https://doi.org/10.3390/metabo11040227 - 8 Apr 2021
Cited by 15 | Viewed by 3461
Abstract
The pinewood nematode (PWN) is the causal agent of pine wilt disease, a pathology that affects conifer forests, mainly Pinus spp. PWN infection can induce the expression of phytohormone-related genes; however, changes at the early phytohormone level have not yet been explored. Phytohormones [...] Read more.
The pinewood nematode (PWN) is the causal agent of pine wilt disease, a pathology that affects conifer forests, mainly Pinus spp. PWN infection can induce the expression of phytohormone-related genes; however, changes at the early phytohormone level have not yet been explored. Phytohormones are low-abundance metabolites, and thus, difficult to quantify. Moreover, most methodologies focus mainly on Arabidopsis or crop species. This work aimed to validate a fast (run time 6.6 min) liquid chromatography-triple quadrupole tandem mass spectrometry (LC-QqQ-MS/MS) analytical method to quantify 14 phytohormones in Pinus pinaster stem tissues. This method was further applied to evaluate, for the first time, early phytohormone changes in susceptible and resistant phenotypes of P. pinaster 24, 48 and 72 h after inoculation (HAI) with PWN. A significant increase in salicylic acid (SA, 48 and 72 HAI) and jasmonic acid methyl ester (JA-ME, 72 HAI) was observed in susceptible phenotypes. Results indicate that the higher susceptibility of P. pinaster to PWN infection might result from an inefficient trigger of hypersensitive responses, with the involvement of JA and SA pathways. This work provides an important update in forest research, and adds to the current knowledge of Pinus spp. defence responses to PWN infection. Full article
(This article belongs to the Special Issue Metabolomics in Plant Defence)
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20 pages, 2806 KiB  
Article
Concurrent Metabolic Profiling and Quantification of Aromatic Amino Acids and Phytohormones in Solanum lycopersicum Plants Responding to Phytophthora capsici
by Msizi I. Mhlongo, Lizelle A. Piater, Paul A. Steenkamp, Nico Labuschagne and Ian A. Dubery
Metabolites 2020, 10(11), 466; https://doi.org/10.3390/metabo10110466 - 16 Nov 2020
Cited by 15 | Viewed by 3193
Abstract
Pathogenic microorganisms account for large production losses in the agricultural sector. Phytophthora capsici is an oomycete that causes blight and fruit rot in important crops, especially those in the Solanaceae family. P. capsici infection is difficult to control due to genetic diversity, arising [...] Read more.
Pathogenic microorganisms account for large production losses in the agricultural sector. Phytophthora capsici is an oomycete that causes blight and fruit rot in important crops, especially those in the Solanaceae family. P. capsici infection is difficult to control due to genetic diversity, arising from sexual reproduction, and resistant spores that remain dormant in soil. In this study, the metabolomics of tomato plants responding to infection by P. capsici were investigated. Non-targeted metabolomics, based on liquid chromatography coupled to mass spectrometry (LC-MS), were used with multivariate data analyses to investigate time-dependent metabolic reprogramming in the roots, stems, and leaves of stem-infected plants, over an 8 day period. In addition, phytohormones and amino acids were determined using quantitative LC-MS. Methyl salicylate and 1-aminocyclopropane-1-carboxylate were detected as major signalling molecules in the defensive response to P. capsici. As aromatic amino acid precursors of secondary metabolic pathways, both phenylalanine and tryptophan showed a continuous increase over time in all tissues, whereas tyrosine peaked at day 4. Non-targeted metabolomic analysis revealed phenylpropanoids, benzoic acids, glycoalkaloids, flavonoids, amino acids, organic acids, and fatty acids as the major classes of reprogrammed metabolites. Correlation analysis showed that metabolites derived from the same pathway, or synthesised by different pathways, could either have a positive or negative correlation. Furthermore, roots, stems, and leaves showed contrasting time-dependent metabolic reprogramming, possibly related to the biotrophic vs. necrotrophic life-stages of the pathogen, and overlapping biotic and abiotic stress signaling. As such, the targeted and untargeted approaches complemented each other, to provide a detailed view of key time-dependent metabolic changes, occurring in both the asymptomatic and symptomatic stages of infection. Full article
(This article belongs to the Special Issue Metabolomics in Plant Defence)
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Review

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25 pages, 1546 KiB  
Review
Unravelling Plant Responses to Stress—The Importance of Targeted and Untargeted Metabolomics
by James William Allwood, Alex Williams, Henriette Uthe, Nicole M. van Dam, Luis A. J. Mur, Murray R. Grant and Pierre Pétriacq
Metabolites 2021, 11(8), 558; https://doi.org/10.3390/metabo11080558 - 22 Aug 2021
Cited by 32 | Viewed by 7288
Abstract
Climate change and an increasing population, present a massive global challenge with respect to environmentally sustainable nutritious food production. Crop yield enhancements, through breeding, are decreasing, whilst agricultural intensification is constrained by emerging, re-emerging, and endemic pests and pathogens, accounting for ~30% of [...] Read more.
Climate change and an increasing population, present a massive global challenge with respect to environmentally sustainable nutritious food production. Crop yield enhancements, through breeding, are decreasing, whilst agricultural intensification is constrained by emerging, re-emerging, and endemic pests and pathogens, accounting for ~30% of global crop losses, as well as mounting abiotic stress pressures, due to climate change. Metabolomics approaches have previously contributed to our knowledge within the fields of molecular plant pathology and plant–insect interactions. However, these remain incredibly challenging targets, due to the vast diversity in metabolite volatility and polarity, heterogeneous mixtures of pathogen and plant cells, as well as rapid rates of metabolite turn-over. Unravelling the systematic biochemical responses of plants to various individual and combined stresses, involves monitoring signaling compounds, secondary messengers, phytohormones, and defensive and protective chemicals. This demands both targeted and untargeted metabolomics approaches, as well as a range of enzymatic assays, protein assays, and proteomic and transcriptomic technologies. In this review, we focus upon the technical and biological challenges of measuring the metabolome associated with plant stress. We illustrate the challenges, with relevant examples from bacterial and fungal molecular pathologies, plant–insect interactions, and abiotic and combined stress in the environment. We also discuss future prospects from both the perspective of key innovative metabolomic technologies and their deployment in breeding for stress resistance. Full article
(This article belongs to the Special Issue Metabolomics in Plant Defence)
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26 pages, 5714 KiB  
Review
Deciphering Prunus Responses to PPV Infection: A Way toward the Use of Metabolomics Approach for the Diagnostic of Sharka Disease
by Christian Espinoza, Benoît Bascou, Christophe Calvayrac and Cédric Bertrand
Metabolites 2021, 11(7), 465; https://doi.org/10.3390/metabo11070465 - 19 Jul 2021
Cited by 9 | Viewed by 2721
Abstract
Sharka disease, caused by Plum pox virus (PPV), induces several changes in Prunus. In leaf tissues, the infection may cause oxidative stress and disrupt the photosynthetic process. Moreover, several defense responses can be activated after PPV infection and have been detected at [...] Read more.
Sharka disease, caused by Plum pox virus (PPV), induces several changes in Prunus. In leaf tissues, the infection may cause oxidative stress and disrupt the photosynthetic process. Moreover, several defense responses can be activated after PPV infection and have been detected at the phytohormonal, transcriptomic, proteomic, and even translatome levels. As proposed in this review, some responses may be systemic and earlier to the onset of symptoms. Nevertheless, these changes are highly dependent among species, variety, sensitivity, and tissue type. In the case of fruit tissues, PPV infection can modify the ripening process, induced by an alteration of the primary metabolism, including sugars and organic acids, and secondary metabolism, including phenolic compounds. Interestingly, metabolomics is an emerging tool to better understand Prunus–PPV interactions mainly in primary and secondary metabolisms. Moreover, through untargeted metabolomics analyses, specific and early candidate biomarkers of PPV infection can be detected. Nevertheless, these candidate biomarkers need to be validated before being selected for a diagnostic or prognosis by targeted analyses. The development of a new method for early detection of PPV-infected trees would be crucial for better management of the outbreak, especially since there is no curative treatment. Full article
(This article belongs to the Special Issue Metabolomics in Plant Defence)
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25 pages, 3364 KiB  
Review
Revisiting the Complex Pathosystem of Huanglongbing: Deciphering the Role of Citrus Metabolites in Symptom Development
by Yasser Nehela and Nabil Killiny
Metabolites 2020, 10(10), 409; https://doi.org/10.3390/metabo10100409 - 13 Oct 2020
Cited by 26 | Viewed by 4917
Abstract
Huanglongbing (HLB), formerly known as citrus greening disease, is one of the most devastating bacterial diseases in citrus worldwide. HLB is caused by ‘Candidatus Liberibacter asiaticus’ bacterium and transmitted by Diaphorina citri. Both ‘Ca. L. asiaticus’ and its vector manipulate the [...] Read more.
Huanglongbing (HLB), formerly known as citrus greening disease, is one of the most devastating bacterial diseases in citrus worldwide. HLB is caused by ‘Candidatus Liberibacter asiaticus’ bacterium and transmitted by Diaphorina citri. Both ‘Ca. L. asiaticus’ and its vector manipulate the host metabolism to fulfill their nutritional needs and/or to neutralize the host defense responses. Herein, we discuss the history of HLB and the complexity of its pathosystem as well as the geographical distribution of its pathogens and vectors. Recently, our recognition of physiological events associated with ‘Ca. L. asiaticus’ infection and/or D. citri-infestation has greatly improved. However, the roles of citrus metabolites in the development of HLB symptoms are still unclear. We believe that symptom development of HLB disease is a complicated process and relies on a multilayered metabolic network which is mainly regulated by phytohormones. Citrus metabolites play vital roles in the development of HLB symptoms through the modulation of carbohydrate metabolism, phytohormone homeostasis, antioxidant pathways, or via the interaction with other metabolic pathways, particularly involving amino acids, leaf pigments, and polyamines. Understanding how ‘Ca. L. asiaticus’ and its vector, D. citri, affect the metabolic pathways of their host is critical for developing novel, sustainable strategies for HLB management. Full article
(This article belongs to the Special Issue Metabolomics in Plant Defence)
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