Metabolomic Evaluation of Tissue-Specific Defense Responses in Tomato Plants Modulated by PGPR-Priming Against Infection

Overview

Journal Plants (Basel)

Date 2021 Aug 28

PMID 34451575

Citations 18

Authors

Msizi I Mhlongo

Lizelle A Piater

Paul A Steenkamp

Nico Labuschagne

Ian A Dubery

Affiliations

Soon will be listed here.

Abstract

Plant growth-promoting rhizobacteria (PGPR) can stimulate disease suppression through the induction of an enhanced state of defense readiness. Here, untargeted ultra-high performance liquid chromatography-mass spectrometry (UHPLC-MS) and targeted ultra-high performance liquid chromatography coupled to triple-quadrupole mass spectrometry (UHPLC-QqQ-MS) were used to investigate metabolic reprogramming in tomato plant tissues in response to priming by N04 and T22 against . Roots were treated with the two PGPR strains prior to stem inoculation with Metabolites were methanol-extracted from roots, stems and leaves at two-eight days post-inoculation. Targeted analysis by UHPLC-QqQ-MS allowed quantification of aromatic amino acids and phytohormones. For untargeted analysis, UHPLC-MS data were chemometrically processed to determine signatory biomarkers related to priming against . The aromatic amino acid content was differentially reprogrammed in and primed plants responding to . Furthermore, abscisic acid and methyl salicylic acid were found to be major signaling molecules in the tripartite interaction. LC-MS metabolomics analysis showed time-dependent metabolic changes in the primed-unchallenged vs. primed-challenged tissues. The annotated metabolites included phenylpropanoids, benzoic acids, glycoalkaloids, flavonoids, amino acids, organic acids, as well as oxygenated fatty acids. Tissue-specific reprogramming across diverse metabolic networks in roots, stems and leaves was also observed, which demonstrated that PGPR priming resulted in modulation of the defense response to infection.

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References

Schikora A, Schenk S, Hartmann A . Beneficial effects of bacteria-plant communication based on quorum sensing molecules of the N-acyl homoserine lactone group. Plant Mol Biol. 2016; 90(6):605-12. DOI: 10.1007/s11103-016-0457-8. View

Dempsey D, Klessig D . SOS - too many signals for systemic acquired resistance?. Trends Plant Sci. 2012; 17(9):538-45. DOI: 10.1016/j.tplants.2012.05.011. View

Farag M, Zhang H, Ryu C . Dynamic chemical communication between plants and bacteria through airborne signals: induced resistance by bacterial volatiles. J Chem Ecol. 2013; 39(7):1007-18. PMC: 3738840. DOI: 10.1007/s10886-013-0317-9. View

Tugizimana F, Steenkamp P, Piater L, Dubery I . Multi-platform metabolomic analyses of ergosterol-induced dynamic changes in Nicotiana tabacum cells. PLoS One. 2014; 9(1):e87846. PMC: 3909234. DOI: 10.1371/journal.pone.0087846. View

Granke L, Quesada-Ocampo L, Lamour K, Hausbeck M . Advances in Research on Phytophthora capsici on Vegetable Crops in The United States. Plant Dis. 2019; 96(11):1588-1600. DOI: 10.1094/PDIS-02-12-0211-FE. View

Wiklund S, Johansson E, Sjostrom L, Mellerowicz E, Edlund U, Shockcor J . Visualization of GC/TOF-MS-based metabolomics data for identification of biochemically interesting compounds using OPLS class models. Anal Chem. 2007; 80(1):115-22. DOI: 10.1021/ac0713510. View

Mhlongo M, Piater L, Madala N, Steenkamp P, Dubery I . Phenylpropanoid Defences in Nicotiana tabacum Cells: Overlapping Metabolomes Indicate Common Aspects to Priming Responses Induced by Lipopolysaccharides, Chitosan and Flagellin-22. PLoS One. 2016; 11(3):e0151350. PMC: 4792386. DOI: 10.1371/journal.pone.0151350. View

Gamir J, Pastor V, Kaever A, Cerezo M, Flors V . Targeting novel chemical and constitutive primed metabolites against Plectosphaerella cucumerina. Plant J. 2014; 78(2):227-40. DOI: 10.1111/tpj.12465. View

Pieterse C, Leon-Reyes A, van der Ent S, Van Wees S . Networking by small-molecule hormones in plant immunity. Nat Chem Biol. 2009; 5(5):308-16. DOI: 10.1038/nchembio.164. View

10.

Verhage A, Van Wees S, Pieterse C . Plant immunity: it's the hormones talking, but what do they say?. Plant Physiol. 2010; 154(2):536-40. PMC: 2949039. DOI: 10.1104/pp.110.161570. View

11.

Liu W, Liu J, Ning Y, Ding B, Wang X, Wang Z . Recent progress in understanding PAMP- and effector-triggered immunity against the rice blast fungus Magnaporthe oryzae. Mol Plant. 2013; 6(3):605-20. DOI: 10.1093/mp/sst015. View

12.

Sumner L, Amberg A, Barrett D, Beale M, Beger R, Daykin C . Proposed minimum reporting standards for chemical analysis Chemical Analysis Working Group (CAWG) Metabolomics Standards Initiative (MSI). Metabolomics. 2013; 3(3):211-221. PMC: 3772505. DOI: 10.1007/s11306-007-0082-2. View

13.

Dutta S, Podile A . Plant growth promoting rhizobacteria (PGPR): the bugs to debug the root zone. Crit Rev Microbiol. 2010; 36(3):232-44. DOI: 10.3109/10408411003766806. View

14.

Tugizimana F, Djami-Tchatchou A, Steenkamp P, Piater L, Dubery I . Metabolomic Analysis of Defense-Related Reprogramming in in Response to Infection Reveals a Functional Metabolic Web of Phenylpropanoid and Flavonoid Pathways. Front Plant Sci. 2019; 9:1840. PMC: 6328496. DOI: 10.3389/fpls.2018.01840. View

15.

Badri D, Vivanco J . Regulation and function of root exudates. Plant Cell Environ. 2009; 32(6):666-81. DOI: 10.1111/j.1365-3040.2008.01926.x. View

16.

Shah J, Chaturvedi R, Chowdhury Z, Venables B, Petros R . Signaling by small metabolites in systemic acquired resistance. Plant J. 2014; 79(4):645-58. DOI: 10.1111/tpj.12464. View

17.

Chen F, DAuria J, Tholl D, Ross J, Gershenzon J, Noel J . An Arabidopsis thaliana gene for methylsalicylate biosynthesis, identified by a biochemical genomics approach, has a role in defense. Plant J. 2003; 36(5):577-88. DOI: 10.1046/j.1365-313x.2003.01902.x. View

18.

Bari R, Jones J . Role of plant hormones in plant defence responses. Plant Mol Biol. 2008; 69(4):473-88. DOI: 10.1007/s11103-008-9435-0. View

19.

Ortiz-Castro R, Valencia-Cantero E, Lopez-Bucio J . Plant growth promotion by Bacillus megaterium involves cytokinin signaling. Plant Signal Behav. 2009; 3(4):263-5. PMC: 2634197. DOI: 10.4161/psb.3.4.5204. View

20.

Fagard M, Launay A, Clement G, Courtial J, Dellagi A, Farjad M . Nitrogen metabolism meets phytopathology. J Exp Bot. 2014; 65(19):5643-56. DOI: 10.1093/jxb/eru323. View