3-D imaging of temporal and spatial development of Puccinia striiformis haustoria in wheat

Literature cited

• AkaikeH. 1974. A new look at the statistical model identification. IEEE T Automat Contr 19:716–723, 10.1109/TAC.1974.1100705
   Web of Science ®Google Scholar
• BaartPGJParlevlietJELimburgH. 1991. Effects of infection density on the size of barley and wheat leaf rust colonies before and on the size of uredia after the start of sporulation. J Phytopathol 131:59–64, 10.1111/j.1439-0434.1991.tb04571.x
   Google Scholar
• BakaZAM. 1992. Observations on the ultrastructure of the uredinial stage of Puccinia polypogonis on Polypogon monspeliensis. Mycopathologia 120:103–111, 10.1007/BF00578295
   Web of Science ®Google Scholar
• BerndtR. 1999. Neotropical rust fungi: new species and observations. Mycologia 91:1045–1059, 10.2307/3761636
   Web of Science ®Google Scholar
• BolteSCordelièresFP. 2006. A guided tour into subcellular colocalization analysis in light microscopy. J Microscopy 224:213–232, 10.1111/j.1365-2818.2006.01706.x
   PubMed Web of Science ®Google Scholar
• BozkurtTOMcGrannGRDMacCormackRBoydLAAkkayaMS. 2010. Cellular and transcriptional responses of wheat during compatible and incompatible race-specific interactions with Puccinia striiformis f.sp. tritici. Mol Plant Pathol 11:625–640.
   PubMed Web of Science ®Google Scholar
• BushnellWR. 1972. Physiology of fungal haustoria. Ann Rev Phytopathol 10:151–176, 10.1146/annurev.py.10.090172.001055
   Web of Science ®Google Scholar
• CartwrightDWRussellGE. 1981. Development of Puccinia striiformis in a susceptible winter-wheat variety. Tr Br Mycol Soc 76:197–204, 10.1016/S0007-1536(81)80139-8
   Google Scholar
• CatanzaritiA-MDoddsPNEllisJG. 2007. Avirulence proteins from haustoria-forming pathogens. FEMS Microbiol Lett 269:181–188, 10.1111/j.1574-6968.2007.00684.x
   PubMed Web of Science ®Google Scholar
• ChongJHarderDRohringerR. 1981. Ontogeny of mono-and dikaryotic rust haustoria: Cytochemical and ultra-structural studies. Phytopathology 71:975–983, 10.1094/Phyto-71-975
   Web of Science ®Google Scholar
• CumminsGBHiratsukaY. 2003. Illustrated genera of rust fungi. 3rd ed. St Paul, Minnesota: APS Press. 223 p.
   Google Scholar
• GodfreyDZhangZSaalbachGThordal-ChristensenH. 2009. A proteomics study of barley powdery mildew haustoria. Proteomics 9:3222–3232, 10.1002/pmic.200800645
   PubMed Web of Science ®Google Scholar
• HahnMMendgenK. 1992. Isolation by ConA binding of haustoria from different rust fungi and comparison of their surface qualities. Protoplasma 170:95–103, 10.1007/BF01378785
   Web of Science ®Google Scholar
• HarderDEChongJ. 1984. Structure and physiology of haustoria. In: BushnellWRRoelfsAP, eds. The cereal rust. Vol. 1. New York: Academic Press. p 431–476.
   Google Scholar
• HarderDEChongJ. 1991. Rust haustoria. In: MendgenKLesemannD-E, eds. Electron microscopy of plant pathogens. Berlin: Springer. p 235–250.
   Google Scholar
• HarderDERohringerRSamborskiDJRimmerSRKimWKChongJ. 1979. Electron-microscopy of susceptible and resistant near-isogenic (sr6/Sr6) lines of wheat infected by Puccinia graminis tritici II. Expression of incompatibility in mesophyll and epidermal cells and the effect of temperature on host-parasite interactions in these cells. Can J Bot 57:2617–2625, 10.1139/b79-310
   Google Scholar
• HoefleCHuesmannCSchultheissHBörnkeFHenselGKumlehnJHückelhovenR. 2011. A barley ROP GTPase activating protein associates with microtubules and regulates entry of the barley powdery mildew fungus into leaf epidermal cells. Plant Cell 23:2422–2439, 10.1105/tpc.110.082131
   Google Scholar
• HovmøllerMSWalterSJustesenAF. 2010. Escalating threat of wheat rusts. Science 329:369, 10.1126/science.1194925
   PubMed Web of Science ®Google Scholar
• HuGGRijkenbergFHJ. 1998. Ultrastructural studies of the intercellular hypha and haustorium of Puccinia recondita f.sp. tritici. J Phytopathol 146:39–50, 10.1111/j.1439-0434.1998.tb04748.x
   Google Scholar
• JaggerLJNewellCBerrySTMacCormackRBoydLA. 2011. Histopathology provides a phenotype by which to characterize stripe rust resistance genes in wheat. Plant Pathol 60:640–648, 10.1111/j.1365-3059.2011.02436.x
   Google Scholar
• JinYSzaboLJCarsonM. 2010. Century-old mystery of Puccinia striiformis life history solved with the identification of Berberis as an alternate host. Phytopathology 100:432–435, 10.1094/PHYTO-100-5-0432
   PubMed Web of Science ®Google Scholar
• JustesenAFRidoutCJHovmøllerMS. 2002. The recent history of Puccinia striiformis f.sp. tritici in Denmark as revealed by disease incidence and AFLP markers. Plant Pathol 51:13–23, 10.1046/j.0032-0862.2001.00651.x
   Web of Science ®Google Scholar
• KangZHuangLLBuchenauerH. 2002. Ultrastructural changes and localization of lignin and callose in compatible and incompatible interactions between wheat and Puccinia striiformis. J Plant Dis Protect 109: 25–37.
   Google Scholar
• KemenEKemenACRafiqiMHempelUMendgenKHahnMVoegeleRT. 2005. Identification of a protein from rust fungi transferred from haustoria into infected plant cells. Mol Plant Microb In 18:1130–1139, 10.1094/MPMI-18-1130
   PubMed Web of Science ®Google Scholar
• KohSAndréAEdwardsHEhrhardtDSomervilleS. 2005. Arabidopsis thaliana subcellular responses to compatible Erysiphe cichoracearum infections. Plant J 44:516–529, 10.1111/j.1365-313X.2005.02545.x
   PubMed Web of Science ®Google Scholar
• KramerCY. 1956. Extension of multiple range tests to group means with unequal numbers of replications. Biometrics 12:307–310, 10.2307/3001469
   Web of Science ®Google Scholar
• LittlefieldLJHeathM. 1979. Ultrastructure of rust fungi. New York: Academic Press. 277 p.
   Google Scholar
• MaQShangHS. 2004. Ultrastructural analysis of the interaction between Puccinia striiformis f.sp. tritici and wheat after thermal induction of resistance. J Plant Pathol 86:19–26.
   Google Scholar
• MaQShangHS. 2009. Ultrastructure of stripe rust (Puccinia striiformis f.sp. tritici) interacting with slow-rusting, highly resistant, and susceptible wheat cultivars. J Plant Pathol 91:597–606.
   Google Scholar
• MaresD. 1979a. Microscopic study of the development of yellow rust (Puccinia striiformis) in a wheat cultivar showing adult plant resistance. Physiol Plant Pathol 15: 289–296, 10.1016/0048-4059(79)90080-8
   Google Scholar
• MaresD. 1979b. A light and electron microscope study of the interaction of yellow rust (Puccinia striiformis) with a susceptible wheat cultivar. Ann Bot 43:183–189.
   Web of Science ®Google Scholar
• McCurdyDWPatrickJWOfflerCE. 2008. Wall ingrowth formation in transfer cells: novel examples of localized wall deposition in plant cells. Curr Opin Plant Biol 11: 653–661, 10.1016/j.pbi.2008.08.005
   PubMed Web of Science ®Google Scholar
• MicaliCONeumannUGrunewaldDPanstrugaRO’ConnellR. 2011. Biogenesis of a specialized plant-fungal interface during host cell internalization of Golovinomyces orontii haustoria. Cell Microbiol 13:210–226, 10.1111/j.1462-5822.2010.01530.x
   PubMed Web of Science ®Google Scholar
• MilusEaKristensenKHovmøllerMS. 2009. Evidence for increased aggressiveness in a recent widespread strain of Puccinia striiformis f.sp. tritici causing stripe rust of wheat. Phytopathology 99:89–94, 10.1094/PHYTO-99-1-0089
   PubMed Web of Science ®Google Scholar
• MimsCWRodriguez-LotherCRichardsonEA. 2001. Ultrastructure of the host-parasite interaction in leaves of Duchesnea indica infected by the rust fungus Frommeëla mexicana var. indicae as revealed by high pressure freezing. Can J Bot 79:49–57.
   Google Scholar
• MoldenhauerJMoerschbacherBMvan der WesthuizenAJ. 2006. Histological investigation of stripe rust (Puccinia striiformis f.sp. tritici) development in resistant and susceptible wheat cultivars. Plant Pathol 55:469–474, 10.1111/j.1365-3059.2006.01385.x
   Google Scholar
• MorenoNBougardSHaseloffJFeijóJA. 2006. Imaging plant cells. In: PawleyJB, ed. Handbook of biological confocal microscopy. 3rd ed. New York: Springer. p 769–787.
   Google Scholar
• OpalskiKSSchultheissHKogelK-HHückelhovenR. 2005. The receptor-like MLO protein and the RAC/ROP family G-protein RACB modulate actin reorganization in barley attacked by the biotrophic powdery mildew fungus Blumeria graminis f.sp. hordei. Plant J 41: 291–303, 10.1111/j.1365-313X.2004.02292.x
   PubMed Web of Science ®Google Scholar
• PerfectSEGreenJR. 2001. Infection structures of biotrophic and hemibiotrophic fungal plant pathogens. Mol Plant Pathol 2:101–108, 10.1046/j.1364-3703.2001.00055.x
   PubMed Web of Science ®Google Scholar
• PuthoffDPNeelamAEhrenfriedMLSchefflerBEBallardLSongQCampbellKBCooperBTuckerML. 2008. Analysis of expressed sequence tags from Uromyces appendiculatus hyphae and haustoria and their comparison to sequences from other rust fungi. Phytopathology 98:1126–1135, 10.1094/PHYTO-98-10-1126
   Google Scholar
• SchmidtSMPanstrugaR. 2007. Cytoskeleton functions in plant-microbe interactions. Physiol Mol Plant P 71:135–148, 10.1016/j.pmpp.2008.01.001
   Google Scholar
• SongXRampitschCSoltaniBMautheWLinningRBanksTMcCallumBBakkerenG. 2011. Proteome analysis of wheat leaf rust fungus, Puccinia triticina, infection structures enriched for haustoria. Proteomics 11:1–20, 10.1002/pmic.201000014
   Google Scholar
• TukeyJW. 1953. The problem of multiple comparisons (unpublished manuscript). In: BraunH, ed. The collected works of John W. Tukey. Volume VIII: multiple comparisons, 1948–1983. New York: Chapman & Hall.
   Google Scholar
• VoegeleRTMendgenK. 2003. Rust haustoria: nutrient uptake and beyond. New Phytol 159:93–100, 10.1046/j.1469-8137.2003.00761.x
   Web of Science ®Google Scholar
• WuytsNPalauquiJCConejeroGVerdeilJLGranierCMassonnetC. 2010. High-contrast three-dimensional imaging of the Arabidopsis leaf enables the analysis of cell dimensions in the epidermis and mesophyll. Plant Methods 6:1–14, 10.1186/1746-4811-6-17
   Google Scholar