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Volume 165, Issue 11

Genetic evidence for vitamin B3 acquisition from rice cells Free

Abstract

Following penetration, the devastating rice blast fungus , like some other important eukaryotic phytopathogens, grows in intimate contact with living plant cells before causing disease. Cell-to-cell growth during this biotrophic growth stage must involve nutrient acquisition, but experimental evidence for the internalization and metabolism of host-derived compounds is exceedingly sparse. This striking gap in our knowledge of the infection process undermines accurate conceptualization of the plant–fungal interaction. Here, through our general interest in metabolism and with a specific focus on the signalling and redox cofactor nicotinamide adenine dinucleotide (NAD), we deleted the gene encoding quinolinate phosphoribosyltransferase, catalyst of the last step in NAD biosynthesis from tryptophan. We show how is essential for axenic growth on minimal media lacking nicotinic acid (NA, an importable NAD precursor). However, Δ mutant strains were fully pathogenic, indicating NAD biosynthesis is dispensable for lesion expansion following invasive hyphal growth in leaf tissue. Because overcoming the loss of NAD biosynthesis can only occur if importable NAD precursors (which solely comprise the NA, nicotinamide and nicotinamide riboside forms of vitamin B3) are accessible, we unexpectedly but unequivocally demonstrate that vitamin B3 can be acquired from the host and assimilated into metabolism during growth in rice cells. Our results furnish a rare, experimentally determined example of host nutrient acquisition by a fungal plant pathogen and are significant in expanding our knowledge of events at the plant–fungus metabolic interface.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): biotrophy , leaf metabolome , Magnaporthe oryzae , metabolism , NAD , nutrient acquisition , pathogenicity , plant-microbe interactions , Pyricularia oryzae , rice , rice blast and vitamin B3
© 2019 The Authors
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2019-11-01
2024-05-17
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References

  1. Wilson RA, Talbot NJ. Under pressure: investigating the biology of plant infection by Magnaporthe oryzae . Nat Rev Microbiol 2009; 7:185–195 [View Article]
     [Google Scholar]
  2. Marroquin-Guzman M, Hartline D, Wright JD, Elowsky C, Bourret TJ et al. The Magnaporthe oryzae nitrooxidative stress response suppresses rice innate immunity during blast disease. Nat Microbiol 2017; 2:17054 [View Article]
     [Google Scholar]
  3. Sun G, Elowsky C, Li G, Wilson RA. TOR-autophagy branch signaling via Imp1 dictates plant-microbe biotrophic interface longevity. PLoS Genet 2018; 14:e1007814 [View Article]
     [Google Scholar]
  4. Kankanala P, Czymmek K, Valent B. Roles for rice membrane dynamics and plasmodesmata during biotrophic invasion by the blast fungus. Plant Cell 2007; 19:706–724 [View Article]
     [Google Scholar]
  5. Talbot NJ. Appressoria. Curr Biol 2019; 29:R144–R146 [View Article]
     [Google Scholar]
  6. Sakulkoo W, Osés-Ruiz M, Oliveira Garcia E, Soanes DM, Littlejohn GR et al. A single fungal MAP kinase controls plant cell-to-cell invasion by the rice blast fungus. Science 2018; 359:1399–1403 [View Article]
     [Google Scholar]
  7. Giraldo MC, Dagdas YF, Gupta YK, Mentlak TA, Yi M et al. Two distinct secretion systems facilitate tissue invasion by the rice blast fungus Magnaporthe oryzae . Nat Commun 1996; 2013:4
     [Google Scholar]
  8. Fernandez J, Marroquin-Guzman M, Wilson RA. Mechanisms of nutrient acquisition and utilization during fungal infections of leaves. Annu Rev Phytopathol 2014; 52:155–174 [View Article]
     [Google Scholar]
  9. Wilson RA, Fernandez J, Quispe CF, Gradnigo J, Seng A et al. Towards defining nutrient conditions encountered by the rice blast fungus during host infection. PLoS One 2012; 7:e47392 [View Article]
     [Google Scholar]
  10. Fernandez J, Yang KT, Cornwell KM, Wright JD, Wilson RA. Growth in rice cells requires de novo purine biosynthesis by the blast fungus Magnaporthe oryzae . Sci Rep 2013; 3:2398 [View Article]
     [Google Scholar]
  11. Marroquin-Guzman M, Krotz J, Appeah H, Wilson RA. Metabolic constraints on Magnaporthe biotrophy: loss of de novo asparagine biosynthesis aborts invasive hyphal growth in the first infected rice cell. Microbiology 2018; 164:1541–1546 [View Article]
     [Google Scholar]
  12. Wilson RA, Jenkinson JM, Gibson RP, Littlechild JA, Wang Z-Y et al. Tps1 regulates the pentose phosphate pathway, nitrogen metabolism and fungal virulence. EMBO J 2007; 26:3673–3685 [View Article]
     [Google Scholar]
  13. Wilson RA, Gibson RP, Quispe CF, Littlechild JA, Talbot NJ. An Nadph-Dependent Genetic Switch Regulates Plant Infection by the Rice Blast Fungus 107 USA: Proc Nat Acad Sci; 2010 pp 21902–21907
     [Google Scholar]
  14. Fernandez J, Wright JD, Hartline D, Quispe CF, Madayiputhiya N et al. Principles of carbon catabolite repression in the rice blast fungus: TPS1, Nmr1-3, and a MATE-family pump regulate glucose metabolism during infection. PLoS Genet 2012; 8:e1002673 [View Article]
     [Google Scholar]
  15. Fernandez J, Marroquin-Guzman M, Wilson RA. Evidence for a transketolase-mediated metabolic checkpoint governing biotrophic growth in rice cells by the blast fungus Magnaporthe oryzae . PLoS Pathog 2014; 10:e10004354 [View Article]
     [Google Scholar]
  16. Fernandez J, Wilson RA. Characterizing roles for the glutathione reductase, thioredoxin reductase and thioredoxin peroxidase-encoding genes of Magnaporthe oryzae during rice blast disease. PLoS One 2014; 9:e87300 [View Article]
     [Google Scholar]
  17. Segal LM, Wilson RA. Reactive oxygen species metabolism and plant-fungal interactions. Fungal Genet Biol 2018; 110:1–9 [View Article]
     [Google Scholar]
  18. Pollak N, Dölle C, Ziegler M. The power to reduce: pyridine nucleotides-small molecules with a multitude of functions. Biochem J 2007; 402:205–218 [View Article]
     [Google Scholar]
  19. Lin S-J, Guarente L. Nicotinamide adenine dinucleotide, a metabolic regulator of transcription, longevity and disease. Curr Opin Cell Biol 2003; 15:241–246 [View Article]
     [Google Scholar]
  20. Bieganowski P, Brenner C. Discoveries of nicotinamide riboside as a nutrient and conserved NRK genes establish a Preiss-Handler independent route to NAD+ in fungi and humans. Cell 2004; 117:495–502 [View Article]
     [Google Scholar]
  21. Grozio A, Mills KF, Yoshino J, Bruzzone S, Sociali G et al. Slc12a8 is a nicotinamide mononucleotide transporter. Nat Metab 2019; 1:47–57 [View Article]
     [Google Scholar]
  22. Panozzo C, Nawara M, Suski C, Kucharczyka R, Skoneczny M et al. Aerobic and anaerobic NAD + metabolism in Saccharomyces cerevisiae . FEBS Lett 2002; 517:97–102 [View Article]
     [Google Scholar]
  23. Dean RA, Talbot NJ, Ebbole DJ, Farman ML, Mitchell TK et al. The genome sequence of the rice blast fungus Magnaporthe grisea . Nature 2005; 434:980–986 [View Article]
     [Google Scholar]
  24. Li G, Marroquin-Guzman M, Wilson R. Chromatin immunoprecipitation (CHIP) assay for detecting direct and indirect protein – DNA interactions in Magnaporthe oryzae . Bio Protoc 2015; 5:e1643 [View Article]
     [Google Scholar]
  25. Marroquin-Guzman M, Sun G, Wilson RA. Glucose-ABL1-TOR signaling modulates cell cycle tuning to control terminal Appressorial cell differentiation. PLoS Genet 2017; 13:e1006557 [View Article]
     [Google Scholar]
  26. Sun G, Qi X, Wilson RA. A feed-forward subnetwork emerging from integrated TOR- and cAMP/PKA-signaling architecture reinforces Magnaporthe oryzae appressorium morphogenesis. MPMI 2019; 32:593–607 [View Article]
     [Google Scholar]
  27. Divon HH, Fluhr R. Nutrition acquisition strategies during fungal infection of plants. FEMS Microbiol Lett 2007; 266:65–74 [View Article]
     [Google Scholar]
  28. Struck C. Amino acid uptake in rust fungi. Front Plant Sci 2015; 6:40 [View Article]
     [Google Scholar]
  29. Bönnighausen J, Gebhard D, Kröger C, Hadeler B, Tumforde T et al. Disruption of the GABA shunt affects mitochondrial respiration and virulence in the cereal pathogen Fusarium graminearum . Mol Microbiol 2015; 98:1115–1132 [View Article]
     [Google Scholar]
  30. Jiang Y, Wang W, Xie Q, Liu N, Liu L et al. Plants transfer lipids to sustain colonization by mutualistic mycorrhizal and parasitic fungi. Science 2017; 356:1172–1175 [View Article]
     [Google Scholar]
  31. Mueller E, Bailey A, Corran A, Michael AJ, Bowyer P. Ornithine decarboxylase knockout in Tapesia yallundae abolishes infection plaque formation in vitro but does not reduce virulence toward wheat. Mol Plant Microbe Interact 2001; 14:1303–1311 [View Article]
     [Google Scholar]
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Genetic evidence for Magnaporthe oryzae vitamin B3 acquisition from rice cells
Microbiology 165, 1198 (2019); https://doi.org/10.1099/mic.0.000855
/content/journal/micro/10.1099/mic.0.000855
/content/journal/micro/10.1099/mic.0.000855
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