The sugar sensor, trehalose-6-phosphate synthase (tps1), regulates primary and secondary metabolism during infection by the rice blast fungus: Will magnaporthe oryzae's "sweet tooth" become its "achilles' heel"?

Jessie Fernandez, Richard A. Wilson

Research output: Contribution to journalArticle

19 Citations (Scopus)

Abstract

Rice blast disease is considered one of the most serious diseases of cultivated rice and is mediated by the causal agent, Magnaporthe oryzae. During infection, dome-shaped fungal cells, called appressoria, form on the surface of the leaf and generate turgor through the accumulation of glycerol. This enormous pressure is directed down onto a thin penetration hypha emerging from the base of the cell, forcing it through the surface of the rice leaf and allowing fungal colonization of the plant interior. The non-reducing disaccharide, trehalose, is present in conidia of M. oryzae and is mobilised during appressorium formation. The first step in trehalose biosynthesis involves trehalose-6-phosphate synthase (Tps1), and deletion of the TPS1 gene in M. oryzae abolishes its ability to cause disease. This loss of pathogenicity was thought to be due to the role trehalose might play in turgor generation in the appressorium, or from the loss of the trehalose intermediate, trehalose-6-phosphate, a known signalling molecule in other organisms. However, subsequent analysis determined that, in M. oryzae, it is the Tps1 protein itself that is a central regulator of plant infection. Here, we discuss how the role of trehalose metabolism in M. oryzae development was determined to differ from other eukaryotes and show how, independent of its biosynthetic role, Tps1 functions as a sugar sensor to integrate carbon and nitrogen metabolism and regulate a subset of primary and secondary metabolic pathways, such as the oxidative pentose phosphate pathway and pigment formation, respectively, during plant colonisation. This is a critical role that allows the fungus to adapt to the nutritional and redox conditions encountered in the plant cell and establish disease.

Original languageEnglish (US)
Pages (from-to)46-53
Number of pages8
JournalMycology
Volume2
Issue number1
DOIs
StatePublished - Mar 1 2011

Fingerprint

Magnaporthe
Secondary Metabolism
Magnaporthe oryzae
blast disease
trehalose
Fungi
Trehalose
sugars
fungi
metabolism
appressoria
Infection
infection
turgor
phosphates
rice
gene deletion
pentoses
disaccharides
nitrogen metabolism

Keywords

  • Glucose-6-phosphate
  • Magnaporthe oryzae
  • Nadph-dependent genetic switch
  • Rice blast
  • Secondary metabolism
  • Trehalose-6-phosphate synthase

ASJC Scopus subject areas

  • Microbiology
  • Infectious Diseases

Cite this

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title = "The sugar sensor, trehalose-6-phosphate synthase (tps1), regulates primary and secondary metabolism during infection by the rice blast fungus: Will magnaporthe oryzae's {"}sweet tooth{"} become its {"}achilles' heel{"}?",
abstract = "Rice blast disease is considered one of the most serious diseases of cultivated rice and is mediated by the causal agent, Magnaporthe oryzae. During infection, dome-shaped fungal cells, called appressoria, form on the surface of the leaf and generate turgor through the accumulation of glycerol. This enormous pressure is directed down onto a thin penetration hypha emerging from the base of the cell, forcing it through the surface of the rice leaf and allowing fungal colonization of the plant interior. The non-reducing disaccharide, trehalose, is present in conidia of M. oryzae and is mobilised during appressorium formation. The first step in trehalose biosynthesis involves trehalose-6-phosphate synthase (Tps1), and deletion of the TPS1 gene in M. oryzae abolishes its ability to cause disease. This loss of pathogenicity was thought to be due to the role trehalose might play in turgor generation in the appressorium, or from the loss of the trehalose intermediate, trehalose-6-phosphate, a known signalling molecule in other organisms. However, subsequent analysis determined that, in M. oryzae, it is the Tps1 protein itself that is a central regulator of plant infection. Here, we discuss how the role of trehalose metabolism in M. oryzae development was determined to differ from other eukaryotes and show how, independent of its biosynthetic role, Tps1 functions as a sugar sensor to integrate carbon and nitrogen metabolism and regulate a subset of primary and secondary metabolic pathways, such as the oxidative pentose phosphate pathway and pigment formation, respectively, during plant colonisation. This is a critical role that allows the fungus to adapt to the nutritional and redox conditions encountered in the plant cell and establish disease.",
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