An NADPH-dependent genetic switch regulates plant infection by the rice blast fungus

Richard A Wilson, Robert P. Gibson, Cristian F. Quispe, Jennifer A. Littlechild, Nicholas J. Talbot

Research output: Contribution to journalArticle

75 Citations (Scopus)

Abstract

To cause rice blast disease, the fungus Magnaporthe oryzae breaches the tough outer cuticle of the rice leaf by using specialized infection structures called appressoria. These cells allow the fungus to invade the host plant and proliferate rapidly within leaf tissue. Here, we show that a unique NADPH-dependent genetic switch regulates plant infection in response to the changing nutritional and redox conditions encountered by the pathogen. The biosynthetic enzyme trehalose-6-phosphate synthase (Tps1) integrates control of glucose-6-phosphate metabolism and nitrogen source utilization by regulating the oxidative pentose phosphate pathway, the generation of NADPH, and the activity of nitrate reductase. We report that Tps1 directly binds to NADPH and, thereby, regulates a set of related transcriptional corepressors, comprising three proteins, Nmr1, Nmr2, and Nmr3, which can each bind NADP. Targeted deletion of any of the Nmr-encoding genes partially suppresses the nonpathogenic phenotype of a Δtps1 mutant. Tps1-dependentNmr corepressors control the expression of a set of virulence-associated genes that are derepressed during appressorium-mediated plant infection. When considered together, these results suggest that initiation of rice blast disease by M. oryzae requires a regulatory mechanism involving an NADPH sensor protein, Tps1, a set of NADP-dependent transcriptional corepressors, and the nonconsuming interconversion ofNADPHandNADPacting as signal transducer.

Original languageEnglish (US)
Pages (from-to)21902-21907
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume107
Issue number50
DOIs
StatePublished - Dec 14 2010

Fingerprint

NADP
Fungi
Co-Repressor Proteins
Infection
Nitrate Reductase (NADPH)
Magnaporthe
Pentose Phosphate Pathway
Glucose-6-Phosphate
Mycoses
Transducers
Genes
Oxidation-Reduction
Virulence
Proteins
Nitrogen
Oryza
Phenotype
Enzymes

Keywords

  • Ascomycete
  • Cofactor
  • Fungal pathogenicity

ASJC Scopus subject areas

  • General

Cite this

An NADPH-dependent genetic switch regulates plant infection by the rice blast fungus. / Wilson, Richard A; Gibson, Robert P.; Quispe, Cristian F.; Littlechild, Jennifer A.; Talbot, Nicholas J.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 107, No. 50, 14.12.2010, p. 21902-21907.

Research output: Contribution to journalArticle

Wilson, Richard A ; Gibson, Robert P. ; Quispe, Cristian F. ; Littlechild, Jennifer A. ; Talbot, Nicholas J. / An NADPH-dependent genetic switch regulates plant infection by the rice blast fungus. In: Proceedings of the National Academy of Sciences of the United States of America. 2010 ; Vol. 107, No. 50. pp. 21902-21907.
@article{e958196bdfc84574bf24a8695004e105,
title = "An NADPH-dependent genetic switch regulates plant infection by the rice blast fungus",
abstract = "To cause rice blast disease, the fungus Magnaporthe oryzae breaches the tough outer cuticle of the rice leaf by using specialized infection structures called appressoria. These cells allow the fungus to invade the host plant and proliferate rapidly within leaf tissue. Here, we show that a unique NADPH-dependent genetic switch regulates plant infection in response to the changing nutritional and redox conditions encountered by the pathogen. The biosynthetic enzyme trehalose-6-phosphate synthase (Tps1) integrates control of glucose-6-phosphate metabolism and nitrogen source utilization by regulating the oxidative pentose phosphate pathway, the generation of NADPH, and the activity of nitrate reductase. We report that Tps1 directly binds to NADPH and, thereby, regulates a set of related transcriptional corepressors, comprising three proteins, Nmr1, Nmr2, and Nmr3, which can each bind NADP. Targeted deletion of any of the Nmr-encoding genes partially suppresses the nonpathogenic phenotype of a Δtps1 mutant. Tps1-dependentNmr corepressors control the expression of a set of virulence-associated genes that are derepressed during appressorium-mediated plant infection. When considered together, these results suggest that initiation of rice blast disease by M. oryzae requires a regulatory mechanism involving an NADPH sensor protein, Tps1, a set of NADP-dependent transcriptional corepressors, and the nonconsuming interconversion ofNADPHandNADPacting as signal transducer.",
keywords = "Ascomycete, Cofactor, Fungal pathogenicity",
author = "Wilson, {Richard A} and Gibson, {Robert P.} and Quispe, {Cristian F.} and Littlechild, {Jennifer A.} and Talbot, {Nicholas J.}",
year = "2010",
month = "12",
day = "14",
doi = "10.1073/pnas.1006839107",
language = "English (US)",
volume = "107",
pages = "21902--21907",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
number = "50",

}

TY - JOUR

T1 - An NADPH-dependent genetic switch regulates plant infection by the rice blast fungus

AU - Wilson, Richard A

AU - Gibson, Robert P.

AU - Quispe, Cristian F.

AU - Littlechild, Jennifer A.

AU - Talbot, Nicholas J.

PY - 2010/12/14

Y1 - 2010/12/14

N2 - To cause rice blast disease, the fungus Magnaporthe oryzae breaches the tough outer cuticle of the rice leaf by using specialized infection structures called appressoria. These cells allow the fungus to invade the host plant and proliferate rapidly within leaf tissue. Here, we show that a unique NADPH-dependent genetic switch regulates plant infection in response to the changing nutritional and redox conditions encountered by the pathogen. The biosynthetic enzyme trehalose-6-phosphate synthase (Tps1) integrates control of glucose-6-phosphate metabolism and nitrogen source utilization by regulating the oxidative pentose phosphate pathway, the generation of NADPH, and the activity of nitrate reductase. We report that Tps1 directly binds to NADPH and, thereby, regulates a set of related transcriptional corepressors, comprising three proteins, Nmr1, Nmr2, and Nmr3, which can each bind NADP. Targeted deletion of any of the Nmr-encoding genes partially suppresses the nonpathogenic phenotype of a Δtps1 mutant. Tps1-dependentNmr corepressors control the expression of a set of virulence-associated genes that are derepressed during appressorium-mediated plant infection. When considered together, these results suggest that initiation of rice blast disease by M. oryzae requires a regulatory mechanism involving an NADPH sensor protein, Tps1, a set of NADP-dependent transcriptional corepressors, and the nonconsuming interconversion ofNADPHandNADPacting as signal transducer.

AB - To cause rice blast disease, the fungus Magnaporthe oryzae breaches the tough outer cuticle of the rice leaf by using specialized infection structures called appressoria. These cells allow the fungus to invade the host plant and proliferate rapidly within leaf tissue. Here, we show that a unique NADPH-dependent genetic switch regulates plant infection in response to the changing nutritional and redox conditions encountered by the pathogen. The biosynthetic enzyme trehalose-6-phosphate synthase (Tps1) integrates control of glucose-6-phosphate metabolism and nitrogen source utilization by regulating the oxidative pentose phosphate pathway, the generation of NADPH, and the activity of nitrate reductase. We report that Tps1 directly binds to NADPH and, thereby, regulates a set of related transcriptional corepressors, comprising three proteins, Nmr1, Nmr2, and Nmr3, which can each bind NADP. Targeted deletion of any of the Nmr-encoding genes partially suppresses the nonpathogenic phenotype of a Δtps1 mutant. Tps1-dependentNmr corepressors control the expression of a set of virulence-associated genes that are derepressed during appressorium-mediated plant infection. When considered together, these results suggest that initiation of rice blast disease by M. oryzae requires a regulatory mechanism involving an NADPH sensor protein, Tps1, a set of NADP-dependent transcriptional corepressors, and the nonconsuming interconversion ofNADPHandNADPacting as signal transducer.

KW - Ascomycete

KW - Cofactor

KW - Fungal pathogenicity

UR - http://www.scopus.com/inward/record.url?scp=78650745996&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=78650745996&partnerID=8YFLogxK

U2 - 10.1073/pnas.1006839107

DO - 10.1073/pnas.1006839107

M3 - Article

VL - 107

SP - 21902

EP - 21907

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 50

ER -