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Invited Article | Open Access

Two arginine biosynthesis genes are essential for pathogenicity of Colletotrichum higginsianum on Arabidopsis

Hiroyuki Takaharaa,b( ), Aurelie Huserb, Richard O'Connellb
Faculty of Bioresources and Environmental Sciences, Ishikawa Prefectural University, Nonoichi, Ishikawa, Japan
Max Planck Institute for Plant Breeding Research, Department of Plant–Microbe Interactions, Cologne, Germany
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Abstract

Random insertional mutagenesis of Colletotrichum higginsianum using Agrobacterium tumefaciens-mediated transformation was utilised to tag genes required for fungal pathogenicity. Two of the mutants, path-19 and path-35, were arginine auxotrophs and produced no symptoms on susceptible Arabidopsis thaliana plants. The T-DNA tagged genes showed high homology to the polyprotein arg-6 precursor and carbamoyl-phosphate synthetase, respectively, both of which are involved in arginine biosynthesis. In both mutants, conidial germination and appressorium formation were similar to the wild-type strain, but appressorial penetration and subsequent invasive growth in planta were severely reduced. Complementation of the T-DNA tagged mutants with cosmid genomic clones containing wild-type copies of the respective genes fully restored pathogenicity and the ability to grow on minimal media. These results suggest that arginine biosynthesis is critical for the early stages of plant infection by C. higginsianum.

Keywords

pathogenicityanthracnoseColletotrichum higginsianumauxotrophamino acid biosynthesishemibiotrophy

References

 

Bailey A, Mueller E, Bowyer P. 2000. Ornithine decarboxylase of Stagonospora (Septoria) nodorum is required for virulence toward wheat. J Biol Chem. 275:14242–14247.
Crossref Google Scholar
 

Balhadere PV, Foster AJ, Talbot NJ. 1999. Identification of pathogenicity mutants in the rice blast fungus Magnaporthe grisea by insertional mutagenesis. Mol Plant–Microbe Interact. 12:129–142.
Crossref Google Scholar
 

Birker D, Heidrich K, Takahara H, Narusaka M, Deslandes L, Narusaka Y, Reymond M, Parker JE, O'Connell RJ. 2009. A locus conferring resistance to Colletotrichum higginsianum is shared by four geographically distinct Arabidopsis accessions. Plant J. 60:602–613.
Crossref Google Scholar
 

Boonchird C, Messenguy F, Dubois E. 1991. Determination of amino acid sequences involved in the processing of the ARG5/ARG6 precursor in Saccharomyces cerevisiae. Eur J Biochem. 199:325–335.
Crossref Google Scholar
 

Both M, Csukai M, Stumpf MPH, Spanu PD. 2005. Gene expression profiles of Blumeria graminis indicate dynamic changes to primary metabolism during development of an obligate biotrophic pathogen. Plant Cell 17:2107–2122.
Crossref Google Scholar
 

Caldovic L, Tuchman M. 2003. N-acetylglutamate and its changing role through evolution. Biochem J. 372:279–290.
Crossref Google Scholar
 

Cunin R, Glansdorff N, Pierard A, Stalon V. 1986. Biosynthesis and metabolism of arginine in bacteria. Microbiol Rev. 50:193–225.
Crossref Google Scholar
 

Davis RH. 1986. Compartmental and regulatory mechanisms in the arginine pathways of Neurospora crassa and Saccharomyces cerevisiae. Microbiol Rev. 50:280–313.
Crossref Google Scholar
 

Divon HH, Fluhr R. 2007. Nutrition acquisition strategies during fungal infection of plants. FEMS Microbiol Lett. 266:65–74.
Crossref Google Scholar
 

Divon HH, Rothan-Denoyes B, Davydov O, Di Pietro A, Fluhr R. 2005. Nitrogen responsive genes are differentially regulated in planta during Fusarium oxysporum f.sp. lycopersici infection. Mol Plant Pathol. 6:459–470.
Crossref Google Scholar
 

Djulic A, Schmid A, Lenz H, Sharma P, Koch C, Wirsel SG, Voegele RT. 2011. Transient transformation of the obligate biotrophic rust fungus Uromyces fabae using biolistics. Fungal Biol. 115:633–642.
Crossref Google Scholar
 

Duckert P, Brunak S, Blom N. 2004. Prediction of proprotein convertase cleavage site. Protein Eng Des Sel. 17:107–112.
Crossref Google Scholar
 

Hahn M, Mendgen K. 1997. Characterization of in planta induced rust genes isolated from a haustorium-specific cDNA library. Mol Plant–Microbe Interact. 10:427–437.
Crossref Google Scholar
 

Hahn M, Neef U, Struck C, Gottfert M, Mendgen K. 1997. A putative amino acid transporter is specifically expressed in haustoria of the rust fungus Uromyces fabae. Mol Plant–Microbe Interact. 10:438–445.
Crossref Google Scholar
 

Hinebusch AG, Natarajan K. 2002. Gcn4p, a master regulator of gene expression, is controlled at multiple levels by diverse signals of starvation and stress. Eukaryot Cell. 1:22–32.
Crossref Google Scholar
 

Holliday R. 1961. Genetics of Ustilago maydis. Genet Res. 2:204–230.
Crossref Google Scholar
 

Horst RJ, Doehlemann G, Wahl R, Hofmann J, Schmiedl A, Kahmann R, Kämper J, Sonnewald U, Voll LM. 2010. Ustilago maydis infection strongly alters organic nitrogen allocation in maize and stimulates productivity of systemic source leaves. Plant Physiol. 152:293–308.
Crossref Google Scholar
 

Huser A, Takahara H, Schmalenbach W, O'Connell RJ. 2009. Discovery of pathogenicity genes in the crucifer anthracnose fungus Colletotrichum higginsianum, using random insertional mutagenesis. Mol Plant–Microbe Interact. 22:143–156.
Crossref Google Scholar
 

Jakupovic M, Heintz M, Reichmann P, Mendgen K, Hahn M. 2006. Microarray analysis of expressed sequence tags from haustoria of the rust fungus Uromyces fabae. Fungal Genet Biol. 43:8–19.
Crossref Google Scholar
 

Kleemann J, Takahara H, Stuber K, O'Connell RJ. 2008. Identification of soluble secreted proteins from appressoria of Colletotrichum higginsianum by analysis of expressed sequence tags. Microbiology 154:1204–1217.
Crossref Google Scholar
 

Krebs HA, Henseleit K. 1932. Untersuchungen uber die Harnstotlhildung im TierkLrper. Hoppe-Seyler's Z. Physiol. Chem. 210:33–66.
Crossref Google Scholar
 

Kruger WM, Pritsch C, Chao S, Muehlbauer GJ. 2002. Functional and comparative bioinformatic analysis of expressed genes from wheat spikes infected with Fusarium graminearum. Mol Plant–Microbe Interact. 15:445–455.
Crossref Google Scholar
 

Mathioni SM, Beló A, Rizzo CJ, Dean RA, Donofrio NM. 2011. Transcriptome profiling of the rice blast fungus during invasive plant infection and in vitro stresses. BMC Genomics 19:12–49.
Crossref Google Scholar
 
Nakayama K. 1997. Furin: a mammalian subtilisin/Kex2p-like endoprotease involved in processing of a wide variety of precursor proteins. Biochem J. 327:625–635.
Crossref
 

Namiki F, Matsunaga M, Okuda M, Inoue I, Nishi K, Fujita Y, Tsuge T. 2001. Mutation of an arginine biosynthesis gene causes reduced pathogenicity in Fusarium oxysporum f.sp. melonis. Mol Plant–Microbe Interact. 14:580–584.
Crossref Google Scholar
 

Narusaka Y, Narusaka M, Park P, Kubo Y, Hirayama T, Seki M, Shiraishi T, Ishida J, Nakashima M, Enju A, Sakurai T, Satou M, Kobayashi M, Shinozaki K. 2004. RCH1, a locus in Arabidopsis that confers resistance to the hemibiotrophic fungal pathogen Colletotrichum higginsianum. Mol Plant–Microbe Interact. 17:749–762.
Crossref Google Scholar
 

O'Connell RJ, Panstruga R. 2006. Tête ê tête inside a plant cell:establishing compatibility between plants and biotrophic fungi and oomycetes. New Phytol. 171:699–718.
Crossref Google Scholar
 

O'Connell RJ, Herbert C, Sreenivasaprasad S, Khatib M, Esquerre-Tugaye MT, Dumas B. 2004. A novel Arabidopsis–Colletotrichum pathosystem for the molecular dissection of plant-fungal interactions. Mol Plant–Microbe Interact. 17:272–282.
Crossref Google Scholar
 

Parra-Gessert L, Koo K, Fajardo J, Weiss RL. 1998. Processing and function of a polyprotein precursor of two mitochondrial proteins in Neurospora crassa. J Biol Chem. 273:7972–7980.
Crossref Google Scholar
 

Pellier AL, Lauge R, Veneault-Fourrey C, Langin T. 2003. CLNR1, the AREA/NIT2-like global nitrogen regulator of the plant fungal pathogen Colletotrichum lindemuthianum is required for the infection cycle. Mol Microbiol. 48:635–655.
Crossref Google Scholar
 

Rockwell NA, Kyrsan DJ, Komiyama T, Fuller RS. 2002. Precursor processing by kex2/furin proteases. Chem Rev. 102:4525–4548.
Crossref Google Scholar
 

Price CW, Holell JH, Abdelal ATH. 1978. Purification and properties of the arginine-specific carbamoyl-phosphate synthase from Saccharomyces cerevisiae. J Gen Microbiol. 106:145–151.
Crossref Google Scholar
 

Snoeijers SS, Perez-Garcia A, Joosten MHAJ, De Wit PJGM. 2000. The effect of nitrogen on disease development and gene expression in bacterial and fungal plant pathogens. Eur J Plant Pathol. 106:493–506.
Crossref Google Scholar
 

Solomon PS, Oliver RP. 2001. The nitrogen content of the tomato leaf apoplast increases during infection by Cladosporium fulvum. Planta 213:241–249.
Crossref Google Scholar
 

Solomon PS, Nielsen PS, Clark AJ, Oliver RP. 2000. Methionine synthase, a gene required for methionine synthesis, is expressed in planta by Cladosporium fulvum. Mol Plant Pathol 1:315–323.
Crossref Google Scholar
 

Solomon PS, Thomas SW, Spanu P, Oliver RP. 2004. The utilisation of di/tripeptides by Stagonospora nodorum is dispensable for wheat infection. Physiol Mol Plant Pathol 63:191–199.
Crossref Google Scholar
 

Srb AM, Horowitz NH. 1944. The ornithine cycle in Neurospora and its genetic control. J Biol Chem. 154:129–139.
Crossref Google Scholar
 

Stephenson SA, Hatfield J, Rusu AG, Maclean DJ, Manners JM. 2000. CgDN3:An essential pathogenicity gene of Colletotrichum gloeosporioides necessary to avert a hypersensitive-like response in the host Stylosanthes guianensis. Mol Plant–Microbe Interact. 13:929–941.
Crossref Google Scholar
 

Struck C, Ernst M, Hahn M. 2002. Characterization of a developmentally regulated amino acid transporter (AAT1p) of the rust fungus Uromyces fabae. Mol Plant Pathol. 3:23–30.
Crossref Google Scholar
 

Struck C, Mueller E, Martin H, Lohaus G. 2004. The Uromyces fabae UfAAT3 gene encodes a general amino acid permease that prefers uptake of in planta scarce amino acids. Mol Plant Pathol. 5:183–190.
Crossref Google Scholar
 

Sweigard JA, Carroll AM, Farrall L, Chumley FG, Valent B. 1998. Magnaporthe grisea pathogenicity mutants obtained through insertional mutagenesis. Mol Plant–Microbe Interact. 11:404–412.
Crossref Google Scholar
 

Takahara H, Tsuji G, Kubo Y, Yamamoto M, Toyoda K, Inagaki Y, Ichinose Y, Shiraishi T. 2004. Agrobacterium tumefaciens mediated transformation as a tool for random mutagenesis of Colletotrichum trifolii. J Gen Plant Pathol. 70:93–96.
Crossref Google Scholar
 

Takahara H, Dolf A, Endl E, O'Connell R. 2009. Flow cytometric purification of Colletotrichum higginsianum biotrophic hyphae from Arabidopsis leaves for stage-specific transcriptome analysis. Plant J. 59:672–683.
Crossref Google Scholar
 

Tang W, Coughlan S, Crane E, Beatty M, Duvick J. 2006. The application of laser microdissection to in planta gene expression profiling of the maize anthracnose stalk rot fungus Colletotrichum graminicola. Mol Plant–Microbe Interact. 19:1240–1250.
Crossref Google Scholar
 

Thomma BPHJ, Bolton MD, Clergeot PH, De Wit PJ. 2006. Nitrogen controls in planta expression of Cladosporium fulvum Avr9 but no other effector genes. Mol Plant Pathol. 7:125–130.
Crossref Google Scholar
 

Tsuji G, Fujii S, Fujihara N, Hirose C, Tsuge S, Shiraishi T, Kubo Y. 2003. Agrobacterium tumefaciens-mediated transformation for random insertional mutagenesis in Colletotrichum lagenarium. J Gen Plant Pathol. 69:230–239.
Crossref Google Scholar
 

Voegele RT, Struck C, Hahn M, Mendgen K. 2001. The role of haustoria in sugar supply during infection of broad bean by the rust fungus Uromyces fabae. Proc Natl Acad Sci USA 98:8133–8138.
Crossref Google Scholar
 

Voegele RT, Wirsel S, Möll U, Lechner M, Mendgen K. 2006. Cloning and characterization of a novel invertase from the obligate biotroph Uromyces fabae and analysis of expression patterns of host and pathogen invertases in the course of infection. Mol Plant–Microbe Interact. 19:625–634.
Crossref Google Scholar
 

Wandinger-Ness AU, Weiss RL. 1987. A single precursor protein for two separable mitochondrial enzymes in Neurospora crassa. J Biol Chem. 262:5823–5830.
Crossref Google Scholar
 

Zhang Z, Henderson C, Perfect E, Carver TLW, Skamnioti P, Gurr SJ. 2005. Of genes and genomes, needles and haystacks: Blumeria graminis and functionality. Mol Plant Pathol. 6:561–575.
Crossref Google Scholar
Mycology
Volume 3 Issue 1,
March 2012
Pages 54-64
DOI: 10.1080/21501203.2011.654353
Cite this article:
Takahara H, Huser A, O'Connell R. Two arginine biosynthesis genes are essential for pathogenicity of Colletotrichum higginsianum on Arabidopsis. Mycology, 2012, 3(1): 54-64. https://doi.org/10.1080/21501203.2011.654353

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Received: 15 November 2011
Revised: 18 December 2011
Published: 24 January 2012
© 2012 Mycological Society of China
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