1887

Abstract

The blast fungus Magnaporthe oryzae devastates global rice yields and is an emerging threat to wheat. Determining the metabolic strategies underlying M. oryzae growth in host cells could lead to the development of new plant protection approaches against blast. Here, we targeted asparagine synthetase (encoded by ASN1), which is required for the terminal step in asparagine production from aspartate and glutamine, the sole pathway to de novo asparagine biosynthesis in M. oryzae. Consequently, the Δasn1 mutant strains could not grow on minimal media without asparagine supplementation. Spores harvested from supplemented plates could form appressoria and penetrate rice leaf surfaces, but biotrophic growth was aborted and the Δasn1 strains were nonpathogenic. This work provides strong genetic evidence that de novo asparagine biosynthesis, and not acquisition from the host, is a critical and potentially exploitable metabolic strategy employed by M. oryzae in order to successfully colonize rice cells.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000713
2018-11-02
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/164/12/1541.html?itemId=/content/journal/micro/10.1099/mic.0.000713&mimeType=html&fmt=ahah

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][PubMed]
    [Google Scholar]
  2. Fernandez J, Wilson RA. Why no feeding frenzy? mechanisms of nutrient acquisition and utilization during infection by the rice blast fungus Magnaporthe oryzae. Mol Plant Microbe Interact 2012; 25:1286–1293 [View Article][PubMed]
    [Google Scholar]
  3. Fernandez J, Marroquin-Guzman M, Nandakumar R, Shijo S, Cornwell KM et al. Plant defence suppression is mediated by a fungal sirtuin during rice infection by Magnaporthe oryzae. Mol Microbiol 2014; 94:70–88 [View Article][PubMed]
    [Google Scholar]
  4. Fernandez J, Wilson RA. Cells in cells: morphogenetic and metabolic strategies conditioning rice infection by the blast fungus Magnaporthe oryzae. Protoplasma 2014; 251:37–47 [View Article][PubMed]
    [Google Scholar]
  5. 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][PubMed]
    [Google Scholar]
  6. 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][PubMed]
    [Google Scholar]
  7. 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][PubMed]
    [Google Scholar]
  8. Wilson RA, Gibson RP, Quispe CF, Littlechild JA, Talbot NJ. An NADPH-dependent genetic switch regulates plant infection by the rice blast fungus. Proc Natl Acad Sci USA 2010; 107:21902–21907 [View Article][PubMed]
    [Google Scholar]
  9. 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][PubMed]
    [Google Scholar]
  10. 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][PubMed]
    [Google Scholar]
  11. 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:e1004354 [View Article][PubMed]
    [Google Scholar]
  12. 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][PubMed]
    [Google Scholar]
  13. 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][PubMed]
    [Google Scholar]
  14. Segal LM, Wilson RA. Reactive oxygen species metabolism and plant-fungal interactions. Fungal Genet Biol 2018; 110:1–9 [View Article][PubMed]
    [Google Scholar]
  15. Yi M, Valent B. Communication between filamentous pathogens and plants at the biotrophic interface. Annu Rev Phytopathol 2013; 51:587–611 [View Article][PubMed]
    [Google Scholar]
  16. 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][PubMed]
    [Google Scholar]
  17. 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]
  18. Saint-Macary ME, Barbisan C, Gagey MJ, Frelin O, Beffa R et al. Methionine biosynthesis is essential for infection in the rice blast fungus Magnaporthe oryzae. PLoS One 2015; 10:e0111108 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000713
Loading
/content/journal/micro/10.1099/mic.0.000713
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error