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

References

• Bailey , A , Mueller , E and Bowyer , P. 2000 . Ornithine decarboxylase of Stagonospora (Septoria) nodorum is required for virulence toward wheat . J Biol Chem. , 275 : 14242 – 14247 .
   PubMed Web of Science ®Google Scholar
• Balhadere , PV , Foster , AJ and Talbot , NJ. 1999 . Identification of pathogenicity mutants in the rice blast fungus Magnaporthe grisea by insertional mutagenesis . Mol Plant–Microbe Interact. , 12 : 129 – 142 .
   Web of Science ®Google Scholar
• Birker , D , Heidrich , K , Takahara , H , Narusaka , M , Deslandes , L , Narusaka , Y , Reymond , M , Parker , JE and O'Connell , RJ. 2009 . A locus conferring resistance to Colletotrichum higginsianum is shared by four geographically distinct Arabidopsis accessions . Plant J. , 60 : 602 – 613 .
   PubMed Web of Science ®Google Scholar
• Boonchird , C , Messenguy , F and 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 .
   PubMedGoogle Scholar
• Both , M , Csukai , M , Stumpf , MPH and 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 .
   PubMed Web of Science ®Google Scholar
• Caldovic , L and Tuchman , M. 2003 . N-acetylglutamate and its changing role through evolution . Biochem J. , 372 : 279 – 290 .
   PubMed Web of Science ®Google Scholar
• Cunin , R , Glansdorff , N , Pierard , A and Stalon , V. 1986 . Biosynthesis and metabolism of arginine in bacteria . Microbiol Rev. , 50 : 193 – 225 .
   PubMedGoogle Scholar
• Davis , RH. 1986 . Compartmental and regulatory mechanisms in the arginine pathways of Neurospora crassa and Saccharomyces cerevisiae . Microbiol Rev. , 50 : 280 – 313 .
   PubMedGoogle Scholar
• Divon , HH and Fluhr , R. 2007 . Nutrition acquisition strategies during fungal infection of plants . FEMS Microbiol Lett. , 266 : 65 – 74 .
   PubMed Web of Science ®Google Scholar
• Divon , HH , Rothan-Denoyes , B , Davydov , O , Di Pietro , A and Fluhr , R. 2005 . Nitrogen responsive genes are differentially regulated in planta during Fusarium oxysporum f.sp. lycopersici infection . Mol Plant Pathol. , 6 : 459 – 470 .
   PubMed Web of Science ®Google Scholar
• Djulic , A , Schmid , A , Lenz , H , Sharma , P , Koch , C , Wirsel , SG and Voegele , RT. 2011 . Transient transformation of the obligate biotrophic rust fungus Uromyces fabae using biolistics . Fungal Biol. , 115 : 633 – 642 .
   PubMed Web of Science ®Google Scholar
• Duckert , P , Brunak , S and Blom , N. 2004 . Prediction of proprotein convertase cleavage site . Protein Eng Des Sel. , 17 : 107 – 112 .
   PubMed Web of Science ®Google Scholar
• Hahn , M and Mendgen , K. 1997 . Characterization of in planta induced rust genes isolated from a haustorium-specific cDNA library . Mol Plant–Microbe Interact. , 10 : 427 – 437 .
   PubMed Web of Science ®Google Scholar
• Hahn , M , Neef , U , Struck , C , Gottfert , M and 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 .
   PubMed Web of Science ®Google Scholar
• Hinebusch , AG and 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 .
   PubMed Web of Science ®Google Scholar
• Holliday , R. 1961 . Genetics of Ustilago maydis . Genet Res. , 2 : 204 – 230 .
   Google Scholar
• Horst , RJ , Doehlemann , G , Wahl , R , Hofmann , J , Schmiedl , A , Kahmann , R , Kämper , J , Sonnewald , U and 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 .
   PubMed Web of Science ®Google Scholar
• Huser , A , Takahara , H , Schmalenbach , W and 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 .
   PubMed Web of Science ®Google Scholar
• Jakupovic , M , Heintz , M , Reichmann , P , Mendgen , K and Hahn , M. 2006 . Microarray analysis of expressed sequence tags from haustoria of the rust fungus Uromyces fabae . Fungal Genet Biol. , 43 : 8 – 19 .
   PubMed Web of Science ®Google Scholar
• Kleemann , J , Takahara , H , Stuber , K and O'Connell , RJ. 2008 . Identification of soluble secreted proteins from appressoria of Colletotrichum higginsianum by analysis of expressed sequence tags . Microbiology , 154 : 1204 – 1217 .
   PubMed Web of Science ®Google Scholar
• Krebs , HA and Henseleit , K. 1932 . Untersuchungen uber die Harnstotlhildung im TierkLrper . Hoppe-Seyler's Z. Physiol. Chem. , 210 : 33 – 66 .
   Google Scholar
• Kruger , WM , Pritsch , C , Chao , S and 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 .
   PubMed Web of Science ®Google Scholar
• Mathioni , SM , Beló , A , Rizzo , CJ , Dean , RA and Donofrio , NM. 2011 . Transcriptome profiling of the rice blast fungus during invasive plant infection and in vitro stresses . BMC Genomics , 19 : 12 – 49 .
   Google Scholar
• Nakayama , K. 1997 . Furin: a mammalian subtilisin/Kex2p-like endoprotease involved in processing of a wide variety of precursor proteins . Biochem J. , : 625 – 635 .
   PubMed Web of Science ®Google Scholar
• Namiki , F , Matsunaga , M , Okuda , M , Inoue , I , Nishi , K , Fujita , Y and 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 .
   PubMed Web of Science ®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 and 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 .
   PubMed Web of Science ®Google Scholar
• O'Connell , RJ and Panstruga , R. 2006 . Tête ê tête inside a plant cell: establishing compatibility between plants and biotrophic fungi and oomycetes . New Phytol. , 171 : 699 – 718 .
   PubMed Web of Science ®Google Scholar
• O'Connell , RJ , Herbert , C , Sreenivasaprasad , S , Khatib , M , Esquerre-Tugaye , MT and Dumas , B. 2004 . A novel Arabidopsis – Colletotrichum pathosystem for the molecular dissection of plant-fungal interactions . Mol Plant–Microbe Interact. , 17 : 272 – 282 .
   PubMed Web of Science ®Google Scholar
• Parra-Gessert , L , Koo , K , Fajardo , J and Weiss , RL. 1998 . Processing and function of a polyprotein precursor of two mitochondrial proteins in Neurospora crassa . J Biol Chem. , 273 : 7972 – 7980 .
   PubMed Web of Science ®Google Scholar
• Pellier , AL , Lauge , R , Veneault-Fourrey , C and 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 .
   Web of Science ®Google Scholar
• Rockwell , NA , Kyrsan , DJ , Komiyama , T and Fuller , RS. 2002 . Precursor processing by kex2/furin proteases . Chem Rev. , 102 : 4525 – 4548 .
   PubMed Web of Science ®Google Scholar
• Price , CW , Holell , JH and Abdelal , ATH. 1978 . Purification and properties of the arginine-specific carbamoyl-phosphate synthase from Saccharomyces cerevisiae . J Gen Microbiol. , 106 : 145 – 151 .
   PubMedGoogle Scholar
• Snoeijers , SS , Perez-Garcia , A , Joosten , MHAJ and 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 .
   Web of Science ®Google Scholar
• Solomon , PS and Oliver , RP. 2001 . The nitrogen content of the tomato leaf apoplast increases during infection by Cladosporium fulvum . Planta , 213 : 241 – 249 .
   PubMed Web of Science ®Google Scholar
• Solomon , PS , Nielsen , PS , Clark , AJ and Oliver , RP. 2000 . Methionine synthase, a gene required for methionine synthesis, is expressed in planta by Cladosporium fulvum . Mol Plant Pathol , 1 : 315 – 323 .
   PubMed Web of Science ®Google Scholar
• Solomon , PS , Thomas , SW , Spanu , P and Oliver , RP . 2004 . The utilisation of di/tripeptides by Stagonospora nodorum is dispensable for wheat infection . Physiol Mol Plant Pathol , 63 : 191 – 199 .
   Web of Science ®Google Scholar
• Srb , AM and Horowitz , NH. 1944 . The ornithine cycle in Neurospora and its genetic control . J Biol Chem. , 154 : 129 – 139 .
   Google Scholar
• Stephenson , SA , Hatfield , J , Rusu , AG , Maclean , DJ and 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 .
   PubMed Web of Science ®Google Scholar
• Struck , C , Ernst , M and Hahn , M. 2002 . Characterization of a developmentally regulated amino acid transporter (AAT1p) of the rust fungus Uromyces fabae . Mol Plant Pathol. , 3 : 23 – 30 .
   PubMed Web of Science ®Google Scholar
• Struck , C , Mueller , E , Martin , H and 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 .
   PubMed Web of Science ®Google Scholar
• Sweigard , JA , Carroll , AM , Farrall , L , Chumley , FG and Valent , B. 1998 . Magnaporthe grisea pathogenicity mutants obtained through insertional mutagenesis . Mol Plant–Microbe Interact. , 11 : 404 – 412 .
   PubMed Web of Science ®Google Scholar
• Takahara , H , Tsuji , G , Kubo , Y , Yamamoto , M , Toyoda , K , Inagaki , Y , Ichinose , Y and Shiraishi , T. 2004 . Agrobacterium tumefaciens mediated transformation as a tool for random mutagenesis of Colletotrichum trifolii . J Gen Plant Pathol. , 70 : 93 – 96 .
   Google Scholar
• Takahara , H , Dolf , A , Endl , E and 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 .
   PubMed Web of Science ®Google Scholar
• Tang , W , Coughlan , S , Crane , E , Beatty , M and 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 .
   PubMed Web of Science ®Google Scholar
• Thomma , BPHJ , Bolton , MD , Clergeot , PH and De Wit , PJ. 2006 . Nitrogen controls in planta expression of Cladosporium fulvum Avr9 but no other effector genes . Mol Plant Pathol. , 7 : 125 – 130 .
   PubMed Web of Science ®Google Scholar
• Tsuji , G , Fujii , S , Fujihara , N , Hirose , C , Tsuge , S , Shiraishi , T and Kubo , Y. 2003 . Agrobacterium tumefaciens-mediated transformation for random insertional mutagenesis in Colletotrichum lagenarium . J Gen Plant Pathol. , 69 : 230 – 239 .
   Google Scholar
• Voegele , RT , Struck , C , Hahn , M and 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 .
   PubMed Web of Science ®Google Scholar
• Voegele , RT , Wirsel , S , Möll , U , Lechner , M and 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 .
   PubMed Web of Science ®Google Scholar
• Wandinger-Ness , AU and Weiss , RL. 1987 . A single precursor protein for two separable mitochondrial enzymes in Neurospora crassa . J Biol Chem. , 262 : 5823 – 5830 .
   PubMed Web of Science ®Google Scholar
• Zhang , Z , Henderson , C , Perfect , E , Carver , TLW , Skamnioti , P and Gurr , SJ. 2005 . Of genes and genomes, needles and haystacks: Blumeria graminis and functionality . Mol Plant Pathol. , 6 : 561 – 575 .
   PubMed Web of Science ®Google Scholar