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Calcium/calmodulin-dependent signaling for prepenetration development in Cochliobolus miyabeanus infecting rice

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Abstract

Cochliobolus miyabeanus forms a specialized infection structure, an appressorium, to infect rice. Contacting a hard surface induces appressorium formation in C. miyabeanus, while the hydrophobicity of the substratum does not affect this morphogenic infection event. To determine whether the calcium/calmodulin-dependent signaling system is involved in prepenetration morphogenesis in C. miyabeanus, the effects of a calcium chelator (ethylene glycol tetraacetic acid; EGTA), phospholipase C inhibitor (neomycin), intracellular calcium channel blocker (TMB-8), calmodulin antagonists (chlorpromazine, phenoxybenzamine, and W-7), and calcineurin inhibitor (cyclosporin A) on morphogenesis and infection were examined. Addition of Ca2+ and the calcium ionophore A23187 did not affect conidial germination, while the number of appressoria decreased with higher concentrations. EGTA inhibited conidial germination and appressorium formation. The calcium channel blocker did not affect appressorium formation at any concentration; however, calmodulin antagonists and the calcineurin inhibitor specifically reduced appressorium formation at the micromolar level. One of the calmodulin antagonists, W-7, also inhibited accumulation of mRNA of the calmodulin gene within germinating conidia and/or appressorium-forming germ tubes. Thus, biochemical processes controlled by the calcium/calmodulin signaling system seem to be involved in the induction of prepenetration morphogenesis on rice.

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References

  • N Agell R Aligue V Alemany A Castro M Jaime MJ Pujol E Rius J Serratosa M Taules O Bachs (1998) ArticleTitleNew nuclear functions for calmodulin Cell Calcium 23 115–121 Occurrence Handle9601606 Occurrence Handle10.1016/S0143-4160(98)90109-9 Occurrence Handle1:CAS:528:DyaK1cXisFymt7k%3D

    Article  PubMed  CAS  Google Scholar 

  • I-P Ahn S Kim W-B Choi Y-H Lee (2003a) ArticleTitleCalcium restores prepenetration morphogenesis abolished by polyamines in Colletotrichum gloeosporioides infecting red pepper FEMS Microbiol Lett 227 237–241 Occurrence Handle10.1016/S0378-1097(03)00686-4 Occurrence Handle1:CAS:528:DC%2BD3sXosFSltbc%3D

    Article  CAS  Google Scholar 

  • I-P Ahn K-H Uhm S Kim Y-H Lee (2003b) ArticleTitleSignaling pathways involved in preinfection development of Colletotrichum gloeosporioides, C. coccoides, and C. dematium pathogenic on red pepper Physiol Mol Plant Pathol 63 281–289 Occurrence Handle10.1016/j.pmpp.2004.01.001 Occurrence Handle1:CAS:528:DC%2BD2cXlt1agtbk%3D

    Article  CAS  Google Scholar 

  • PJ Belde JH Vossen GW Borst-Pauwels AP Theuvenet (1993) ArticleTitleInositol 1,4,5-trisphosphate releases Ca2+ from vacuolar membrane vesicles of Saccharomyces cerevisiae FEBS Lett 323 113–118 Occurrence Handle8495722 Occurrence Handle10.1016/0014-5793(93)81460-H Occurrence Handle1:CAS:528:DyaK3sXksVCqt7k%3D

    Article  PubMed  CAS  Google Scholar 

  • MJ Berridge (1993) ArticleTitleInositol triphosphate and calcium signalling Nature 361 315–325 Occurrence Handle8381210 Occurrence Handle10.1038/361315a0 Occurrence Handle1:CAS:528:DyaK3sXhvVGrt7o%3D

    Article  PubMed  CAS  Google Scholar 

  • EJ Braun RJ Howard (1994) ArticleTitleAdhesion of Cochliobolus heterostrophus conidia and germlings to leaves and artificial surfaces Exp Mycol 18 211–220 Occurrence Handle10.1006/emyc.1994.1021

    Article  Google Scholar 

  • T Breuder CS Hemenway NR Mowa ME Cardenas J Heitman (1994) ArticleTitleCalcineurin is essential in cyclosporin A- and FK506-sensitive yeast strains Proc Natl Acad Sci USA 91 5372–5376 Occurrence Handle7515500 Occurrence Handle10.1073/pnas.91.12.5372 Occurrence Handle1:CAS:528:DyaK2cXktlSqurc%3D

    Article  PubMed  CAS  Google Scholar 

  • J Chaky K Anderson M Moss LJ Vaillancourt (2001) ArticleTitleSurface hydrophobicity and surface rigidity induce spore germination in Colletotrichum graminicola Phytopathology 91 558–564 Occurrence Handle1:CAS:528:DC%2BD3MXkvVKqtr8%3D

    CAS  Google Scholar 

  • RP Clay CW Bergmann MS Fuller (1997) ArticleTitleIsolation and characterization of an endopolygalacturonase from Cochliobolus sativus and a cytological study of fungal penetration of barley Phytopathology 87 1148–1159 Occurrence Handle1:CAS:528:DyaK2sXntl2js7k%3D

    CAS  Google Scholar 

  • JM Comeron (1995) ArticleTitleA method for estimating the numbers of synonymous and nonsynonymous substitutions per site J Mol Evol 41 1152–1159 Occurrence Handle8587111 Occurrence Handle10.1007/BF00173196 Occurrence Handle1:CAS:528:DyaK28XivFOnsQ%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • G Cornelius G Gebauer D Techel (1989) ArticleTitleInositol triphosphate induces calcium release from Neurospora crassa vacuoles Biochem Biophys Res Commun 162 852–856 Occurrence Handle2527035 Occurrence Handle10.1016/0006-291X(89)92388-7 Occurrence Handle1:CAS:528:DyaL1MXltFaitrY%3D

    Article  PubMed  CAS  Google Scholar 

  • J Cui JA Kaandorp (2006) ArticleTitleMathematical modeling of calcium homeostasis in yeast cells Cell Calcium 39 337–348 Occurrence Handle16445978 Occurrence Handle10.1016/j.ceca.2005.12.001 Occurrence Handle1:CAS:528:DC%2BD28XitVejsL0%3D

    Article  PubMed  CAS  Google Scholar 

  • EC David (1995) ArticleTitleCalcium signaling Cell 47 423–431

    Google Scholar 

  • KR Davis FM Ausubel (1989) ArticleTitleCharacterization of elicitor-induced defense responses in suspension-cultured cells of Arabidopsis Mol Plant Microbe Interact 2 363–368

    Google Scholar 

  • TN Davis (1992) ArticleTitleMutational analysis of calmodulin in Saccharomyces cerevisiae Cell Calcium 13 435–444 Occurrence Handle1505005 Occurrence Handle10.1016/0143-4160(92)90056-X Occurrence Handle1:CAS:528:DyaK38Xlt1Ort7o%3D

    Article  PubMed  CAS  Google Scholar 

  • RA Dean (1997) ArticleTitleSignal pathways and appressorium morphogenesis Annu Rev Phytopathol 35 211–234 Occurrence Handle15012522 Occurrence Handle10.1146/annurev.phyto.35.1.211 Occurrence Handle1:CAS:528:DyaK2sXmtVGhsrs%3D

    Article  PubMed  CAS  Google Scholar 

  • O Degani R Maor R Hadar A Sharon BA Horwitz (2004) ArticleTitleHost physiology and pathogenic variation of Cochliobolus heterostrophus strains with mutations in the G protein alpha subunit, CGA1 Appl Environ Microbiol 70 5005–5009 Occurrence Handle15294841 Occurrence Handle10.1128/AEM.70.8.5005-5009.2004 Occurrence Handle1:CAS:528:DC%2BD2cXms1eksL4%3D

    Article  PubMed  CAS  Google Scholar 

  • N Devecha RF Irvine (1995) ArticleTitlePhospholipid signaling Cell 80 269–278 Occurrence Handle10.1016/0092-8674(95)90409-3

    Article  Google Scholar 

  • OD Dhingra JB Sinclair (1985) Basic plant pathology methods CRC Boca Raton

    Google Scholar 

  • S Ganem S-W Lu B-N Lee DY-T Chou R Hadar BG Turgeon BA Horwitz (2004) ArticleTitleG-protein β-subunit of Cochliobolus heterostrophus involved in virulence, asexual and sexual reproductive ability, and morphogenesis Eukary Cell 3 1653–1663 Occurrence Handle10.1128/EC.3.6.1653-1663.2004 Occurrence Handle1:CAS:528:DC%2BD2cXhtFartr7N

    Article  CAS  Google Scholar 

  • I Goto (1958) ArticleTitleStudies on the Helminthosporium leaf blight of rice plants Bull Yamagata Univ Agric Sci 2 237–388

    Google Scholar 

  • EJM Helmreich (2001) The biochemistry of cell signaling Oxford University Press New York

    Google Scholar 

  • BA Horwitz A Sharon SW Lu V Ritter TM Sandrock OC Yoder BG Turgeon (1999) ArticleTitleA G protein alpha subunit from Cochliobolus heterostrophus involved in mating and appressorium formation Fungal Genet Biol 26 19–32 Occurrence Handle10072317 Occurrence Handle10.1006/fgbi.1998.1094 Occurrence Handle1:CAS:528:DyaK1MXhs1Smu7c%3D

    Article  PubMed  CAS  Google Scholar 

  • SL Jackson IB Heath (1993) ArticleTitleRoles of calcium ions in hyphal tip growth Microbiol Rev 57 367–382 Occurrence Handle8336672 Occurrence Handle1:CAS:528:DyaK3sXlslOitbw%3D

    PubMed  CAS  Google Scholar 

  • MJ Jaffe AC Leopold RC Staples (2002) ArticleTitleThigmo responses in plants and fungi Am J Bot 89 375–382

    Google Scholar 

  • S Kim I-P Ahn Y-H Lee (2001) ArticleTitleAnalysis of genes expressed during rice–Magnaporthe grisea interactions Mol Plant Microbe Interact 14 1340–1346 Occurrence Handle11763134 Occurrence Handle1:CAS:528:DC%2BD3MXotFGjtLk%3D

    PubMed  CAS  Google Scholar 

  • YK Kim D Li PE Kolattukudy (1998) ArticleTitleInduction of Ca2+-calmodulin signaling by hard-surface contact primes Colletotrichum gloeosporioides conidia to germinate and form appressoria J Bacteriol 180 5144–5150 Occurrence Handle9748448 Occurrence Handle1:CAS:528:DyaK1cXms1ehs7k%3D

    PubMed  CAS  Google Scholar 

  • S-C Lee Y-H Lee (1998) ArticleTitleCalcium/calmodulin-dependent signaling for appressorium formation in the plant pathogenic fungus Magnaporthe grisea Mol Cell 6 698–704

    Google Scholar 

  • Y-H Lee RA Dean (1993) ArticleTitlecAMP regulates infection structure formation in the plant pathogenic fungus Magnaporthe grisea Plant Cell 5 693–700 Occurrence Handle12271080 Occurrence Handle10.1105/tpc.5.6.693 Occurrence Handle1:CAS:528:DyaK2cXht12nsrk%3D

    Article  PubMed  CAS  Google Scholar 

  • Y-H Lee RA Dean (1994) ArticleTitleHydrophobicity of contact surface induces appressorium formation in Magnaporthe grisea FEMS Microbiol Lett 115 71–75 Occurrence Handle10.1111/j.1574-6968.1994.tb06616.x

    Article  Google Scholar 

  • S Lev A Sharon R Hadar H Ma BA Horwitz (1999) ArticleTitleA mitogen-activated protein kinase of the corn leaf pathogen Cochliobolus heterostrophus is involved in conidiation, appressorium formation, and pathogenicity: diverse roles for mitogen-activated protein kinase homologs in foliar pathogens Proc Natl Acad Sci USA 96 13542–13547 Occurrence Handle10557357 Occurrence Handle10.1073/pnas.96.23.13542 Occurrence Handle1:CAS:528:DyaK1MXns1Gmu7g%3D

    Article  PubMed  CAS  Google Scholar 

  • S Liu RA Dean (1997) ArticleTitleG protein a subunit genes control growth, development, and pathogenicity of Magnaporthe grisea Mol Plant Microbe Interact 10 1075–1086 Occurrence Handle9390422 Occurrence Handle1:CAS:528:DyaK2sXnslait7s%3D

    PubMed  CAS  Google Scholar 

  • T Liu JG Williams M Clarke (1992) ArticleTitleInducible expression of calmodulin antisense RNA in Dictyostelium cells inhibits the completion of cytokinesis Mol Biol Cell 3 1403–1413 Occurrence Handle1493336 Occurrence Handle1:CAS:528:DyaK3sXktVCkt7c%3D

    PubMed  CAS  Google Scholar 

  • Z-M Liu PE Kolattukudy (1999) ArticleTitleEarly expression of the calmodulin gene, which precedes appressorium formation in Magnaporthe grisea, is inhibited by self-inhibitors and requires surface attachment J Bacteriol 181 3571–3577 Occurrence Handle10348871 Occurrence Handle1:CAS:528:DyaK1MXjs1yqsr0%3D

    PubMed  CAS  Google Scholar 

  • MA Lydan DH O'Day (1988) ArticleTitleDifferent developmental functions for calmodulin in Dictyostelium: trifluoperazine and R24571 both inhibit cell and pronuclear fusion but enhance gamete formation Exp Cell Res 178 51–63 Occurrence Handle3409979 Occurrence Handle10.1016/0014-4827(88)90377-1 Occurrence Handle1:CAS:528:DyaL1cXlvVOjtrY%3D

    Article  PubMed  CAS  Google Scholar 

  • RL Mach S Zeilinger D Kristufek CP Kubicek (1998) ArticleTitleCa2+-calmodulin antagonists interfere with xylanase formation and secretion in Trichoderma reesei Biochim Biophys Acta 1403 281–289 Occurrence Handle9685681 Occurrence Handle10.1016/S0167-4889(98)00068-8 Occurrence Handle1:CAS:528:DyaK1cXkslyhtrY%3D

    Article  PubMed  CAS  Google Scholar 

  • BP Magalhaes R Wayne RA Haumber EJ Shields DW Roberts (1991) ArticleTitleCalcium-regulated appressorium formation of the entomopathogenic fungus Zoophthora radicans Protoplasma 160 77–88 Occurrence Handle10.1007/BF01539959 Occurrence Handle1:CAS:528:DyaK38XjslOnug%3D%3D

    Article  CAS  Google Scholar 

  • K Mendgen M Hahn H Deising (1996) ArticleTitleMorphogenesis and mechanisms of penetration by plant pathogenic fungi Annu Rev Phytopathol 34 367–386 Occurrence Handle15012548 Occurrence Handle10.1146/annurev.phyto.34.1.367 Occurrence Handle1:CAS:528:DyaK28XlsFOhsLg%3D

    Article  PubMed  CAS  Google Scholar 

  • JD Molkentin J-R Lu CL Antos B Markham J Richardson J Robbins SR Grant EN Olson (1998) ArticleTitleA calcineurin-dependent transcriptional pathway for cardiac hypertrophy Cell 93 215–228 Occurrence Handle9568714 Occurrence Handle10.1016/S0092-8674(00)81573-1 Occurrence Handle1:CAS:528:DyaK1cXivVygtrs%3D

    Article  PubMed  CAS  Google Scholar 

  • H-S Oh Y-H Lee (2000) ArticleTitleA target-site-specific screening system for antifungal compounds on appressorium formation in Magnaporthe grisea Phytopathology 90 1162–1168 Occurrence Handle1:CAS:528:DC%2BD3cXnt1Knsbc%3D

    CAS  Google Scholar 

  • SH Ou (1985) Rice diseases EditionNumber2nd edn Commonwealth Mycological Institute Kew, UK

    Google Scholar 

  • BD Shaw HC Hoch (2000) ArticleTitleCa2+ regulation of Phyllosticta ampelicida pycnidiospore germination and appressorium formation Fungal Genet Biol 31 43–53 Occurrence Handle11118134 Occurrence Handle10.1006/fgbi.2000.1223 Occurrence Handle1:CAS:528:DC%2BD3cXoslKlsr4%3D

    Article  PubMed  CAS  Google Scholar 

  • AWM Simpson TJ Hallman TJ Rink (1984) ArticleTitleTMB-8 inhibits secretion evoked by phorbol ester at basal cytoplasmic free calcium in quin-2-loaded platelets much more effectively than it inhibits thrombin-induced mobilization FEBS Lett 176 139–143 Occurrence Handle6237932 Occurrence Handle10.1016/0014-5793(84)80928-X Occurrence Handle1:CAS:528:DyaL2MXjslyh

    Article  PubMed  CAS  Google Scholar 

  • RJ St. Leger DW Roberts RC Staples (1991) ArticleTitleA model to explain differentiation of appressoria by germlings of Metarhizium anisopliae J Invert Pathol 57 299–310 Occurrence Handle10.1016/0022-2011(91)90134-C

    Article  Google Scholar 

  • DD Stuthman (2002) ArticleTitleContribution of durable disease resistance to sustainable agriculture Euphytica 124 253–258 Occurrence Handle10.1023/A:1015694803221 Occurrence Handle1:CAS:528:DC%2BD38XkslKntrY%3D

    Article  CAS  Google Scholar 

  • Z Su P Csutora D Hunton RL Shoemaker RB Marchase JE Blalock (2001) ArticleTitleA store-operated nonselective cation channel in lymphocytes is activated directly by Ca2+ influx factor and diacylglycerol Am J Physiol Cell Physiol 280 C1284–C1292 Occurrence Handle11287342 Occurrence Handle1:CAS:528:DC%2BD3MXjsVahsr4%3D

    PubMed  CAS  Google Scholar 

  • Y Takano K Komeda K Kojima T Okuno (2001) ArticleTitleProper regulation of cyclic AMP-dependent protein kinase is required for growth, conidiation, and appressorium function in the anthracnose fungus Colletotrichum lagenarium Mol Plant Microbe Interact 14 1149–1157 Occurrence Handle11605954 Occurrence Handle1:CAS:528:DC%2BD3MXnsVeltL0%3D

    PubMed  CAS  Google Scholar 

  • K-H Uhm I-P Ahn S Kim Y-H Lee (2003) ArticleTitleCalcium/calmodulin-dependent signaling for prepenetration development in Colletotrichum gloeosporioides Phytopathology 93 82–87 Occurrence Handle1:CAS:528:DC%2BD3sXksV2isg%3D%3D

    CAS  Google Scholar 

  • CG Van Edick DM Waterson (1995) Calmodulin structure and function D Marme (Eds) Calcium and cell physiology Springer Berlin Heidelberg New York 105–126

    Google Scholar 

  • M Viaud A Brunet-Simon Y Brygoo J-M Pradier C Levis (2003) ArticleTitleCyclophilin A and calcineurin functions investigated by gene inactivation, cyclosporin A inhibition and cDNA arrays approaches in the phytopathogenic fungus Botrytis cinerea Mol Microbiol 50 1451–1465 Occurrence Handle14651630 Occurrence Handle10.1046/j.1365-2958.2003.03798.x Occurrence Handle1:CAS:528:DC%2BD3sXhtVShtbzJ

    Article  PubMed  CAS  Google Scholar 

  • MC Viaud PV Balhadere NJ Talbot (2002) ArticleTitleA Magnaporthe grisea cyclophilin acts as a virulence determinant during plant infection Plant Cell 14 917–930 Occurrence Handle11971145 Occurrence Handle10.1105/tpc.010389 Occurrence Handle1:CAS:528:DC%2BD38XjsFWktrg%3D

    Article  PubMed  CAS  Google Scholar 

  • V Warwar MB Dickman (1996) ArticleTitleEffects of calcium and calmodulin on spore germination and appressorium development in Colletotrichum trifolii Appl Environ Microbiol 62 74–79 Occurrence Handle16535223 Occurrence Handle1:CAS:528:DyaK28XitFegtw%3D%3D

    PubMed  CAS  Google Scholar 

  • V Warwar S Oved MB Dickman (2000) ArticleTitleAntisense expression of the calmodulin gene from Colletotrichum trifolii impairs prepenetration development FEMS Microbiol Lett 191 213–219 Occurrence Handle11024266 Occurrence Handle1:CAS:528:DC%2BD3cXmvFyru7Y%3D

    PubMed  CAS  Google Scholar 

  • I Weiergang LD Dunkle KV Wood RL Nicholson (1996) ArticleTitleMorphogenic regulation of pathotoxin synthesis in Cochliobolus carbonum Fungal Genet Biol 20 74–78 Occurrence Handle8812288 Occurrence Handle10.1006/fgbi.1996.0012 Occurrence Handle1:CAS:528:DyaK28Xlt1Gnu7w%3D

    Article  PubMed  CAS  Google Scholar 

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  1. Rural Development Administration, National Institute of Agricultural Biotechnology, Suwon, 441-100, Republic of Korea

    Il-Pyung Ahn & Seok-Cheol Suh

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Ahn, IP., Suh, SC. Calcium/calmodulin-dependent signaling for prepenetration development in Cochliobolus miyabeanus infecting rice. J Gen Plant Pathol 73, 113–120 (2007). https://doi.org/10.1007/s10327-006-0326-4

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