Inoculation with Pseudomonas Pseudoalcaligenes Lead to Changes in Plant Sugar Metabolism and Defense That Enhance Tolerance Against the Pathogenic Fungus Sclerotium Rolfsii

Authors

  • Daniela Soledad Riva Universidad de Buenos Aires, Facultad de Facultad de Agronomía, Cátedra de Bioquímica, Avenida San Martín 4453, Buenos Aires C1417DSE, Argentina
  • Claudia Mónica Ribaudo Universidad de Buenos Aires, Facultad de Facultad de Agronomía, Cátedra de Bioquímica, Avenida San Martín 4453, Buenos Aires C1417DSE, Argentina

Keywords:

invertase, PGPR, Sclerotium rolfsii, sugar, tomato

Abstract

Certain Pseudomonas species promote in plants an induced systemic response (ISR), which results in pathogenic disease reduction. This is energetically expensive, implies a redistribution of sugars, and involves several enzymes such as cell-wall invertase (cwINV). The present study aimed to evaluate the role of soluble sugars and cwINV activity in the ISR of Pseudomonas pseudoalcaligenes-primed tomato plants challenged with Sclerotium rolfsii. Disease severity of infected plants was 100%, whereas that of primed plants was 43%. At 24 h after challenge, infected plants showed higher cwINV activity, increased LIN6 and SUS3 mRNA levels, upregulation of the defense marker gene PR1b1, no changes in PR2 and PR3 mRNA levels, and almost unchanged sugar content. Instead, primed plants displayed a lower induction of cwINV activity and gene expression, slightly increased PR2 and PR3 mRNA levels, and increased leaf fructose content. Cytokines also induced LIN6 expression and cwINV activity. Altogether, these results reveal that P. pseudoalcaligenes triggers changes both in sugar metabolism and plant defense, leading to enhanced tolerance against Sclerotium rolfsii.

References

. JW. Kloepper, R. Rodriguez-Ubana, GW. Zehnder, JF. Murphy, E. Sikora, C. Fernandez. “Plant Root-Bacterial Interactions in Biological Control of Soilborne Diseases and Potencial Extensión to Systemic and Foliar Diseases”. Austral. Plant. Pathol. 28, pp. 21-26. 1999.

. BR. Glick. “Plant Growth-Promoting Bacteria: Mechanisms and Applications”. Scientifica 2012, pp. 1–15. 2012.

. CMJ. Pieterse, SCM. van Wees, JA. Van Pelt, M. Knoester, R. Laan, H. Gerrits, PJ. Weisveek, LC. Van Loon. “A Novel Signaling Pathway Controlling Induced Systemic Resistance in Arabidopsis”. Plant Cell 10, pp. 1571-1580. 1998.

. MA. Pardo. “Promoción del Crecimiento y Control de Enfermedades en Plantas de Tomate Mediante Bacterias Promotoras del Crecimiento Vegetal” (Undergraduated thesis). Facultad de Agronomía, Universidad de Buenos Aires. Argentina. http://ri.agro.uba.ar/files/intranet/intensificacion/cd445.pdf. 2006.

. C. Molina. “Evaluación del Etileno en las Defensas Inducidas Contra Meloidogyne sp. en Plantas de Tomate Tratadas con Bioinoculantes” (Undergraduated thesis). Facultad de Agronomía, Universidad de Buenos Aires. Argentina. http://ri.agro.uba.ar/files/intranet/intensificacion/2018molinacatalina.pdf. 2018.

. CM. Ribaudo, DS. Riva, JI. Gori, JI. Zaballa, C. Molina. “Identification of Endophytic Bacteria and Their Characterization as Biocontrol Agents Against Tomato Southern Blight Disease”. Appli. Micro. Open Access 2 (4), pp: 1-9. 2016.

. K. Singh, RC. Foley, L. Onate-Sancuez. “Transcription Factors in Plant Defense and Stress Responses”. Curr. Opin. Plant Biol. 5, pp. 430-436. 2002.

. L. Sun, DL. Yang, Y. Kong, Y. Chen, XZ. Li, LJ. Zeng. “Sugar Homeostasis Mediated by Cell Wall Invertase GRAIN INCOMPLE TEFILLING 1 (GIF1) Plays a Role in Pre-existing and Induced Defence in Rice”. Mol. Plant. Pathol. 15, pp. 161–173.doi:10.1111/mpp.12078. 2013.

. AM. Sinha, MG. Hofmann, U. Romer, W. Koenberger, L. Elling, T. Roitsch. “Metabolizable and Non-Metabolizable Sugars Activate Different Signal Transduction Pathways in Tomato”. Plant Physiol. 128, pp. 1480–1489. 2002.

. C. Zhang, Q. Xie, RG. Anderson, G. Ng, NC. Seitz, T. Peterson. “Crosstalk Between the Circadian Clock and Innate Immunity in Arabidopsis”. PLoSPathog. 9:e1003370. doi:10.1371/journal.ppat.1003370. 2013.

. J. Essmann, P. Bones, E. Weis, J. Scharte. “Leaf Carbohydrate Metabolism During Defense”. Pl. Sign. & Behav. 3(10), pp. 885-887. 2008.

. AS. Tauzin, T. Giardina. “Sucrose and Invertases, a Part of the Plant Defense Response to the Biotic Stresses”. Front. Plant Sci. doi: 10.3389/fpls.2014.00293. 2014.

. J. Scharte, H. Schon, E Weis. “Photosynthesis and Carbohydrate Metabolism in Tobacco Leaves During an Incompatible Interaction with Phytophthora nicotianae”. Plant Cell Environ. 28, pp. 1421–1435. 2005.

. V. Fotopoulos, MJ. Gilbert, JK. Pittman, AC. Marvier, AJ. Buchanan, N. Sauer, JL. Hall, LE. Williams. “The Monosaccharide Transporter Gene, AtSTP4, and the Cell-Wall Invertase, Atbetafruct1, are Induced in Arabidopsis During Infection with the Fungal Biotroph Erysiphe cichoracearum”. Plant. Physiol. 132, pp. 821–829. 2003.

. S. Schaarschmidt, MC. González, T. Roitsch, D. Strack, U. Sonnewald, B. Hause. “Regulation of Arbuscular Mycorrhization by Carbon. The Symbiotic Interaction Cannot be Improved by Increased Carbon Availability Accomplished by Root-Specifically Enhanced Invertase Activity”. Plant Physiol. 143, pp. 1827–1840. 2007.

. S. Berger, M. Papadopoulos, U. Schreiber, W. Kaiser, T. Roitsch. “Complex Regulation of Gene Expression, Photosynthesis and Sugar Levels by Pathogen Infection in Tomato”. Physiol. Plant. 122, pp. 419–428. 2004.

. E. Fridman, D. Zamir. “Functional Divergence of a Syntenic Invertase Gene Family in Tomato, Potato, and Arabidopsis”. Plant Physiol, 131, pp. 603-609. 2003.

. T. Roitsch, R. Ehness. “Regulation of Source/Sink Relations by Cytokinins”. Plant Growth. Regul. 32, pp. 359–367. (2000)

. DE. Godt, T. Roitsch. “ Regulation and Tissue-specific Distribution of mRNAs for Three Extracellular Invertase Isoenzymes of Tomato Suggests an Important Function in Establishing and Maintaining Sink Metabolism”. Plant. Physiol. 115(1), pp. 273-282. 1997.

. DR. Hoagland, DI. Arnon. “The Water Culture for Growing Plants Without Soil”. Circ. Calif. Agric. Exp. Stn. 347, pp. 461-462. 1938.

. DK. Grobkinsky, M. Nasseem, U. Radaman, N. Plickert, T. Engelke, T. Griebel, J. Zeier, O. Nova, M. Stmad, H. Pfeifhofer, E. van der Graaf, U. Simon, T. Roitsch. “Cytokinins Mediate Resistance Against Pseudomonas syringae in Tobacco Through Increased Antimicrobial Phytoalexin Synthesis Independent of Salicylic Acid Signaling”. Plant Physiol. 157, pp. 815–830. 2011.

. JA. Di Rienzo, F. Casanoves, MG. Balzarini, L. Gonzalez, M. Tablada, CW. Robledo. Grupo Infostat, FCA, Universidad Nacional de Córdoba, Argentina. http://www.infostat.com.ar. 2018.

. A. Lehner, N. Mamadou, P. Poels, D. Come, C. Bailly, F. Corbineau. “Changes in Soluble Carbohydrates, Lipid Peroxidation and Antioxidant Enzyme Activities in the Embryo During Ageing in Wheat Grains”. Journal Cer. Sci. 47, pp. 555-565. 2008.

. NL. Hubbard, SC. Huber, DM. Pharr. “Sucrose Phosphate Synthase and Acid Invertase as Determinants of Sucrose Concentration in Developing Muskmelon (Cucumis melo L.) fruits”. Plant Physiol. 91, pp. 1527-1534. 1989.

. N. Nelson. “A Photometric Adaptation of the Somogyi Method for the Determination of Glucose”. J. Biol. Chem. 153, pp. 375-380. 1944.

. M. Somogyi. “Notes of sugar determinations”. J. Biol. Chem. 195, pp. 19-23. 1952.

. MM. Bradford. “A Rapid and Sensitive Method for the Quantitation of Microgram Quantities of Protein Utilizing the Principle of Protein-dye Binding”. Analytical. Biochem. 72, pp. 248-254. 1976

. W. Inskeep, P. Bloom. “Extinction Coefficients of Chloroplyll a and b in N,N-Dimethylformamide and 80% Acetone”. Plant Physiol 77(2), pp. 483-485. 1985.

. M. De Vos, VR. Van Oosten, RMP. Van Poecke, JA. Van Pelt, MJ. Pozo, MJ. Mueller, AJ. Buchala, JP. Métraux, LC. Van Loon, M. Dicke, CMJ. Pieterse CMJ. “ Signal Signature and Transcriptome Changes of Arabidopsis During Pathogen and Insect Attack”. Mol. Plant. Microbe Interact. 18, pp. 923–937. 2005.

. S. Ali, BA. Ganai, AN. Kamili, AA. Bhat, ZA. Mir, JA. Bhat, A. Tyagi, ST. Islam, M. Mushtaq, P. Yadav, S. Rawat, A. Grover . “Pathogenesis-Related Proteins and Peptides as Promising Tools for Engineering Plants with Multiple Stress Tolerance”. Microbiol. Res. 212-213, pp. 29-37. 2018

. N. Kocal, U. Sonnewald, S. Sonnewald. “Cell Wall-Bound Invertase Limits Sucrose Export and is Involved in Symptom Development and Inhibition of Photosynthesis During Compatible Interaction Between Tomato and Xanthomonas campestris pv vesicatoria”. Plant. Physiol. 178, pp. 1523-1536. 2008.

. PJ. Swarbrick, P. Schulze-Lefert, JD. Scholes. “Metabolic Consequences of Susceptibility and Resistance (race-specific and broad-spectrum) in Barley Leaves Challenged with Powdery Mildew”. Plant Cell Environ. 29, pp. 1061–1076. 2006.

. C. Brunkhorst, C. Andersen, E. Schneider. “Acarbose, a Pseudooligosaccharide, is Transported But Not Metabolized by the Maltose-maltodextrin System of Escherichia coli”. J. Bacteriol. 181, pp. 2612–2619.1999.

. KB. Bonfig, U. Schreiber, A. Gabler, T. Roitsch, S. Berger. “Infection with Virulent and Avirulent P. syringae Strains Differentially Affects Photosynthesis and Sink Metabolism in Arabidopsis Leaves”. Planta 225, pp. 1–12. 2006.

. RK. Proels, T. Roitsch. “ Extracellular Invertase LIN6 of Tomato: a Pivotal Enzyme for Integration of Metabolic, Hormonal, and Stress Signals is Regulated by a Diurnal Rhythm”. J. Exp. Bot. 60, pp. 1555-1567. doi: 10.1093/jxb/erp027. 2009.

. O. Stein, D. Granot. “Plant Fructokinases: Evolutionary, Developmental, and Metabolic Aspects in Sink Tissues”. Front. Plant Sci. doi: 10.3389/fpls.2018.00339. 2018.

. JE. Van de Mortel, RCH. Vos, E. De Dekkers, A. Pineda, L. Guillod, K. Bouwmeester. “Metabolic and Transcriptomic Changes Induced in Arabidopsis by the Rhizobacterium Pseudomonas”. Plant Physiol. 160, pp. 2173–2188. doi: 10.1104/pp.112.207324. 2012.

. YH. Cho, SD. Yoo. “Signaling Role of Fructose Mediated by FINS1/FBP in Arabidopsis thaliana”. PLoS Genet. 7:e1001263 10.1371/journal.pgen.1001263. 2011

. F. Lecompte, PC. Nicot, J. Ripoll, MA. Abro, AK. Raimbaul, F. Lopez-Lauri, N. Bertin. “Reduced Susceptibility of Tomato Stem to the Necrotrophic Fungus Botrytis cinerea is Associated with a Specific Adjustment of Fructose Content in the Host Sugar Pool”. Ann. Bot. 119, pp. 931-943. doi: 10.1093/aob/mcw240. 2017.

. H. Ma, F. Wang, W. Wang, G. Yin, D. Zhang, Y. Ding, MP. Timko, H. Zhang. “Alternative Splicing of Basic Chitinase Gene PR3b in the Low-Nicotine Mutants of Nicotiana tabacum L. cv Burley 21”. J. Exp. Bot. 67(19), pp. 5799–5809. doi:10.1093/jxb/erw345. 2016.

. P. Tornero, J. Gadea, V. Conejero, P. Vera. “Two PR-1 Genes From Tomato are Differentially Regulated and Reveal a Novel Mode of Expression for a Pathogenesis-Related Gene During the Hypersensitive Response and Development”. Mol. Plant Microbe Interact. 10(5), pp. 624-634. 1997.

. J. Mathys, K. De Cremer, P. Timmermans, S. Van Kerckhove, B. Lievens, M. Vanhaecke, BPA. Cammue, B. De Coninck. “Genome-Wide Characterization of ISR Induced in Arabidopsis thaliana by Trichoderma hamatum T382 Against Botrytis cinerea Infection”. Front. Plant. Sci. doi: https://doi.org/10.3389/fpls.2012.00108. 2012.

. M. Newman, T. Sundelin, JT. Nielsen, G. Erbs. “MAMP (Microbe-Associated Molecular Pattern) Triggered Immunity in Plants”. Front. Plant. Sci. doi: 10.3389/fpls.2013.00139. 2013.

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Published

2020-06-10

How to Cite

Riva, D. S. ., & Ribaudo, C. M. . (2020). Inoculation with Pseudomonas Pseudoalcaligenes Lead to Changes in Plant Sugar Metabolism and Defense That Enhance Tolerance Against the Pathogenic Fungus Sclerotium Rolfsii. American Scientific Research Journal for Engineering, Technology, and Sciences, 69(1), 89–104. Retrieved from https://www.asrjetsjournal.org/index.php/American_Scientific_Journal/article/view/5886

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Vol. 69 No. 1 (2020)

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