Plant Cell Advance Online Publication
Published on March 3, 2006; 10.1105/tpc.105.039263
Received November 15, 2005
Returned for revision January 30, 2006
Accepted February 10, 2006
Reactive Oxygen Species Play a Role in Regulating a Fungus-Perennial Ryegrass Mutualistic Interaction
Aiko Tanaka 1, Michael J. Christensen 2, Daigo Takemoto 1, Pyoyun Park 3, and Barry Scott 1*
1 Centre for Functional Genomics, Institute of Molecular BioSciences, Massey University, Private Bag 11 222, Palmerston North, New Zealand
2 AgResearch, Grasslands Research Centre, Private Bag 11 008, Palmerston North, New Zealand
3 Graduate School of Science and Technology, Kobe University, Nada, Kobe 657-8501, Japan
* To whom correspondence should be addressed. E-mail: d.b.scott{at}massey.ac.nz.
Although much is known about the signals and mechanisms that lead to pathogenic interactions between plants and fungi, comparatively little is known about fungus-plant mutualistic symbioses. We describe a novel role for reactive oxygen species (ROS) in regulating the mutualistic interaction between a clavicipitaceous fungal endophyte, Epichloë festucae, and its grass host, Lolium perenne. In wild-type associations, E. festucae grows systemically in intercellular spaces of leaves as infrequently branched hyphae parallel to the leaf axis. A screen to identify symbiotic genes isolated a fungal mutant that altered the interaction from mutualistic to antagonistic. This mutant has a single-copy plasmid insertion in the coding region of a NADPH oxidase gene, noxA. Plants infected with the noxA mutant lose apical dominance, become severely stunted, show precocious senescence, and eventually die. The fungal biomass in these associations is increased dramatically, with hyphae showing increased vacuolation. Deletion of a second NADPH oxidase gene, noxB, had no effect on the E. festucae-perennial ryegrass symbiosis. ROS accumulation was detected cytochemically in the endophyte extracellular matrix and at the interface between the extracellular matrix and host cell walls of meristematic tissue in wild-type but not in noxA mutant associations. These results demonstrate that fungal ROS production is critical in maintaining a mutualistic fungus-plant interaction.
This article has been cited by other articles:
|
|
|
|
 
N. Cano-Dominguez, K. Alvarez-Delfin, W. Hansberg, and J. Aguirre
NADPH Oxidases NOX-1 and NOX-2 Require the Regulatory Subunit NOR-1 To Control Cell Differentiation and Growth in Neurospora crassa
Eukaryot. Cell,
August 1, 2008;
7(8):
1352 - 1361.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. P. Semighini and S. D. Harris
Regulation of Apical Dominance in Aspergillus nidulans Hyphae by Reactive Oxygen Species
Genetics,
August 1, 2008;
179(4):
1919 - 1932.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Rasmussen, A. J. Parsons, K. Fraser, H. Xue, and J. A. Newman
Metabolic Profiles of Lolium perenne Are Differentially Affected by Nitrogen Supply, Carbohydrate Content, and Fungal Endophyte Infection
Plant Physiology,
March 1, 2008;
146(3):
1440 - 1453.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
F. Malagnac, B. Klapholz, and P. Silar
PaTrx1 and PaTrx3, Two Cytosolic Thioredoxins of the Filamentous Ascomycete Podospora anserina Involved in Sexual Development and Cell Degeneration
Eukaryot. Cell,
December 1, 2007;
6(12):
2323 - 2331.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Sumimoto, S. Kamakura, and T. Ito
Structure and Function of the PB1 Domain, a Protein Interaction Module Conserved in Animals, Fungi, Amoebas, and Plants
Sci. Signal.,
August 28, 2007;
2007(401):
re6 - re6.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. J. Egan, Z.-Y. Wang, M. A. Jones, N. Smirnoff, and N. J. Talbot
Generation of reactive oxygen species by fungal NADPH oxidases is required for rice blast disease
PNAS,
July 10, 2007;
104(28):
11772 - 11777.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. Molina and R. Kahmann
An Ustilago maydis Gene Involved in H2O2 Detoxification Is Required for Virulence
PLANT CELL,
July 1, 2007;
19(7):
2293 - 2309.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. P. Lee, C. Kim, F. Landgraf, and K. Apel
EXECUTER1- and EXECUTER2-dependent transfer of stress-related signals from the plastid to the nucleus of Arabidopsis thaliana
PNAS,
June 12, 2007;
104(24):
10270 - 10275.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Kobayashi, I. Ohura, K. Kawakita, N. Yokota, M. Fujiwara, K. Shimamoto, N. Doke, and H. Yoshioka
Calcium-Dependent Protein Kinases Regulate the Production of Reactive Oxygen Species by Potato NADPH Oxidase
PLANT CELL,
March 1, 2007;
19(3):
1065 - 1080.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. Takemoto, A. Tanaka, and B. Scott
A p67Phox-Like Regulator Is Recruited to Control Hyphal Branching in a Fungal-Grass Mutualistic Symbiosis
PLANT CELL,
October 1, 2006;
18(10):
2807 - 2821.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. J. SPIERING, D. H. GREER, and J. SCHMID
Effects of the Fungal Endophyte, Neotyphodium lolii, on Net Photosynthesis and Growth Rates of Perennial Ryegrass (Lolium perenne) are Independent of In Planta Endophyte Concentration
Ann. Bot.,
August 1, 2006;
98(2):
379 - 387.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
