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-Mediated Detoxification of Reactive Oxygen
Species Is Required for Full Virulence in the Rice Blast Fungus


During plant-pathogen interactions, the plant may mount several types of defense

responses to either block the pathogen completely or ameliorate the amount of

disease. Such responses include release of reactive oxygen species (ROS) to

attack the pathogen, as well as formation of cell wall appositions (CWAs) to

physically block pathogen penetration. A successful pathogen will likely have

its own ROS detoxification mechanisms to cope with this inhospitable

environment. Here, we report one such candidate mechanism in the rice blast

fungus, Magnaporthe oryzae, governed by a gene we refer to as

MoHYR1. This gene (MGG_07460) encodes a glutathione

peroxidase (GSHPx) domain, and its homologue in yeast was reported to

specifically detoxify phospholipid peroxides. To characterize this gene in

M. oryzae, we generated a deletion

mutantΔhyr1 which showed growth inhibition with

increased amounts of hydrogen peroxide (H2O2). Moreover,

we observed that the fungal mutants had a decreased ability to tolerate ROS

generated by a susceptible plant, including ROS found associated with CWAs.

Ultimately, this resulted in significantly smaller lesion sizes on both barley

and rice. In order to determine how this gene interacts with other (ROS)

scavenging-related genes in M. oryzae, we compared expression

levels of ten genes in mutant versus wild type with and without

H2O2. Our results indicated that the

HYR1 gene was important for allowing the fungus to tolerate

H2O2

in vitro and in planta and that this ability

was directly related to fungal virulence.


Vyšlo v časopise: -Mediated Detoxification of Reactive Oxygen Species Is Required for Full Virulence in the Rice Blast Fungus. PLoS Pathog 7(4): e32767. doi:10.1371/journal.ppat.1001335
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1001335

Souhrn

During plant-pathogen interactions, the plant may mount several types of defense

responses to either block the pathogen completely or ameliorate the amount of

disease. Such responses include release of reactive oxygen species (ROS) to

attack the pathogen, as well as formation of cell wall appositions (CWAs) to

physically block pathogen penetration. A successful pathogen will likely have

its own ROS detoxification mechanisms to cope with this inhospitable

environment. Here, we report one such candidate mechanism in the rice blast

fungus, Magnaporthe oryzae, governed by a gene we refer to as

MoHYR1. This gene (MGG_07460) encodes a glutathione

peroxidase (GSHPx) domain, and its homologue in yeast was reported to

specifically detoxify phospholipid peroxides. To characterize this gene in

M. oryzae, we generated a deletion

mutantΔhyr1 which showed growth inhibition with

increased amounts of hydrogen peroxide (H2O2). Moreover,

we observed that the fungal mutants had a decreased ability to tolerate ROS

generated by a susceptible plant, including ROS found associated with CWAs.

Ultimately, this resulted in significantly smaller lesion sizes on both barley

and rice. In order to determine how this gene interacts with other (ROS)

scavenging-related genes in M. oryzae, we compared expression

levels of ten genes in mutant versus wild type with and without

H2O2. Our results indicated that the

HYR1 gene was important for allowing the fungus to tolerate

H2O2

in vitro and in planta and that this ability

was directly related to fungal virulence.


Zdroje

1. Mittler

R

Vanderauwera

S

Gollery

M

Van Breusegem

F

2004

Reactive oxygen gene network of plants.

Trends Plant Sci

9

490

498

2. Rogers

SA

2002

Detoxify or Die.

Sarasota, , FL

Sand Key Company, Inc

409

3. Thannickal

VJ

Fanburg

BL

2000

Reactive oxygen species in cell signaling.

Am J Physiol Lung Cell Mol Physiol

279

L1005

L1028

4. Jones

JDG

Dangl

JL

2006

The plant immune system.

Nature

444

323

329

5. Egan

MJ

Wang

ZY

Jones

MA

Smirnoff

N

Talbot

NJ

2007

Generation of reactive oxygen species by fungal NADPH oxidases is

required for rice blast disease.

Proc Natl Acad Sci U S A

104

11772

11777

6. Skamnioti

P

Henderson

C

Zhang

ZG

Robinson

Z

Gurr

SJ

2007

A novel role for catalase B in the maintenance of fungal

cell-wall integrity during host invasion in the rice blast fungus

Magnaporthe grisea.

Mol Plant-Microbe Interact

20

568

580

7. Neill

S

Desikan

R

Hancock

J

2002

Hydrogen peroxide signalling.

Curr Opin Plant Biol

5

388

395

8. Sagi

M

Davydov

O

Orazova

S

Yesbergenova

Z

Ophir

R

2004

Plant respiratory burst oxidase homologs impinge on wound

responsiveness and development in Lycopersicon esculentum.

Plant Cell

16

616

628

9. Parker

D

Beckmann

M

Zubair

H

Enot

DP

Caracuel-Rios

Z

2009

Metabolomic analysis reveals a common pattern of metabolic

re-programming during invasion of three host plant species by Magnaporthe

grisea.

Plant J

59

723

737

10. Shetty

NP

Mehrabi

R

Lutken

H

Haldrup

A

Kema

GHJ

2007

Role of hydrogen peroxide during the interaction between the

hemibiotrophic fungal pathogen Septoria tritici and wheat.

New Phytol

174

637

647

11. Able

AJ

2003

Role of reactive oxygen species in the response of barley to

necrotrophic pathogens.

Protoplasma

221

137

143

12. Galletti

R

Denoux

C

Gambetta

S

Dewdney

J

Ausubel

FM

2008

The AtrbohD-Mediated Oxidative Burst Elicited by

Oligogalacturonides in Arabidopsis Is Dispensable for the Activation of

Defense Responses Effective against Botrytis cinerea.

Plant Physiol

148

1695

1706

13. Kato

T

Tanabe

S

Nishimura

M

Ohtake

Y

Nishizawa

Y

2009

Differential responses of rice to inoculation with wild-type and

non-pathogenic mutants of Magnaporthe oryzae.

Plant Mol Biol

70

617

625

14. Chi

MH

Park

SY

Kim

S

Lee

YH

2009

A Novel Pathogenicity Gene Is Required in the Rice Blast Fungus

to Suppress the Basal Defenses of the Host.

PLoS Path

5

e1000401

15. Tanabe

S

Nishizawa

Y

Minami

E

2009

Effects of catalase on the accumulation of H2O2 in rice cells

inoculated with rice blast fungus, Magnaporthe oryzae.

Physiol Plant

137

148

154

16. Kim

KH

Willger

SD

Park

SW

Puttikamonkul

S

Grahl

N

2009

TmpL, a Transmembrane Protein Required for Intracellular Redox

Homeostasis and Virulence in a Plant and an Animal Fungal

Pathogen.

PLoS Path

5

e1000653

17. Inoue

Y

Matsuda

T

Sugiyama

K

Izawa

S

Kimura

A

1999

Genetic analysis of glutathione peroxidase in oxidative stress

response of Saccharomyces cerevisiae.

J Biol Chem

274

27002

27009

18. Zhang

WJ

He

YX

Yang

Z

Yu

J

Chen

Y

2008

Crystal structure of glutathione-dependent phospholipid

peroxidase Hyr1 from the yeast Saccharomyces cerevisiae.

Proteins

73

1058

1062

19. Delaunay

A

Pflieger

D

Barrault

MB

Vinh

J

Toledano

MB

2002

A thiol peroxidase is an H2O2 receptor and redox-transducer in

gene activation.

Cell

111

471

481

20. Molina

L

Kahmann

R

2007

An Ustilago maydis gene involved in H2O2 detoxification is

required for virulence.

Plant Cell

19

2293

2309

21. Delaunay

A

Isnard

AD

Toledano

MB

2000

H2O2 sensing through oxidation of the Yap1 transcription

factor.

EMBO J

19

5157

5166

22. Lee

J

Godon

C

Lagniel

G

Spector

D

Garin

J

1999

Yap1 and Skn7 control two specialized oxidative stress response

regulons in yeast.

J Biol Chem

274

16040

16046

23. Lev

S

Hadar

R

Amedeo

P

Baker

SE

Yoder

OC

2005

Activation of an AP1-like transcription factor of the maize

pathogen Cochliobolus heterostrophus in response to oxidative stress and

plant signals.

Eukaryot Cell

4

443

454

24. Levine

A

Tenhaken

R

Dixon

R

Lamb

C

1994

H2O2 from the oxidative burst orchestrates the plant

hypersensitive disease resistance response.

Cell

79

583

593

25. Lin

CH

Yang

SL

Chung

KR

2009

The YAP1 Homolog-Mediated Oxidative Stress Tolerance Is Crucial

for Pathogenicity of the Necrotrophic Fungus Alternaria alternata in

Citrus.

Mol Plant-Microbe Interact

22

942

952

26. Temme

N

Tudzynski

P

2009

Does Botrytis cinerea Ignore H2O2-Induced Oxidative Stress During

Infection? Characterization of Botrytis Activator Protein 1.

Mol Plant-Microbe Interact

22

987

998

27. McGuffin

LJ

Bryson

K

Jones

DT

2000

The PSIPRED protein structure prediction server.

Bioinformatics

16

404

28. Martin

JL

1995

Thioredoxin - a Fold for All Reasons.

Structure

3

245

250

29. Valent

B

Farrall

L

Chumley

FG

1991

Magnaporthe-grisea Genes for Pathogenicity and Virulence

Identified through a Series of Backcrosses.

Genetics

127

87

101

30. Howard

RJ

Valent

B

1996

Breaking and entering: Host penetration by the fungal rice blast

pathogen Magnaporthe grisea.

Annu Rev Microbiol

50

491

512

31. Myhre

O

Andersen

JM

Aarnes

H

Fonnum

F

2003

Evaluation of the probes 2 ′,7 ′-dichlorofluorescin

diacetate, luminol, and lucigenin as indicators of reactive species

formation.

Biochem Pharmacol

65

1575

1582

32. Kang

SH

Khang

CH

Lee

YH

1999

Regulation of cAMP-dependent protein kinase during appressorium

formation in Magnaporthe grisea.

FEMS Microbiol Lett

170

419

423

33. Smirnoff

N

2000

Ascorbic acid: metabolism and functions of a multi-facetted

molecule.

Curr Opin Plant Biol

3

229

235

34. Huckelhoven

R

2007

Cell wall - Associated mechanisms of disease resistance and

susceptibility.

Annu Rev Phytopathol

45

101

127

35. Dai

SH

Wei

XP

Alfonso

AA

Pei

LP

Duque

UG

2008

Transgenic rice plants that overexpress transcription factors

RF2a and RF2b are tolerant to rice tungro virus replication and

disease.

Proc Natl Acad Sci U S A

105

21012

21016

36. Bolwell

GP

Bindschedler

LV

Blee

KA

Butt

VS

Davies

DR

2002

The apoplastic oxidative burst in response to biotic stress in

plants: a three-component system.

J Exp Bot

53

1367

1376

37. Trujillo

M

Altschmied

L

Schweizer

P

Kogel

KH

Huckelhoven

R

2006

Respiratory Burst Oxidase Homologue A of barley contributes to

penetration by the powdery mildew fungus Blumeria graminis f. sp

hordei.

J Exp Bot

57

3781

3791

38. Davies

DR

Bindschedler

LV

Strickland

TS

Bolwell

GP

2006

Production of reactive oxygen species in Arabidopsis thaliana

cell suspension cultures in response to an elicitor from Fusarium oxysporum:

implications for basal resistance.

J Exp Bot

57

1817

1827

39. Lessing

F

Kniemeyer

O

Wozniok

W

Loeffler

J

Kurzai

O

2007

The Aspergillus fumigatus transcriptional regulator AfYap1

represents the major regulator for defense against reactive oxygen

intermediates but is dispensable for pathogenicity in an intranasal mouse

infection model.

Eukaryot Cell

6

2290

2302

40. Khang

CH

Berruyer

R

Giraldo

MC

Kankanala

P

Park

SY

2010

Translocation of Magnaporthe oryzae Effectors into Rice Cells and

Their Subsequent Cell-to-Cell Movement.

Plant Cell

22

1388

1403

41. Sweigard

JA

Chumley

FG

Valent

B

1992

Disruption of a Magnaporthe-Grisea Cutinase Gene.

Mol Gen Genet

232

183

190

42. Mosquera

G

Giraldo

MC

Khang

CH

Coughlan

S

Valent

B

2009

Interaction Transcriptome Analysis Identifies Magnaporthe oryzae

BAS1-4 as Biotrophy-Associated Secreted Proteins in Rice Blast

Disease.

Plant Cell

21

1273

1290

43. Patterson

GH

Piston

DW

Barisas

BG

2000

Forster distances between green fluorescent protein

pairs.

Anal Biochem

284

438

440

44. ThordalChristensen

H

Zhang

ZG

Wei

YD

Collinge

DB

1997

Subcellular localization of H2O2 in plants. H2O2 accumulation in

papillae and hypersensitive response during the barley-powdery mildew

interaction.

Plant J

11

1187

1194

45. Fink

JL

Hamilton

N

2007

DomainDraw: A macromolecular feature drawing

program.

In Silico Biol

7

145

150

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Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

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PLOS Pathogens


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