Cytoplasmic Streaming in Neurospora Disperse the Plug To Increase the Flow

Cytoplasmic Streaming in Neurospora Disperse the Plug To Increase the Flow CytoplasmicStreaminginNeurospora:DispersethePlug ToIncreasetheFlow? MichaelPlamann* SchoolofBiologicalSciences,UniversityofMissouri–KansasCity,KansasCity,Missouri,UnitedStatesofAmerica Filamentous fungi grow as extending large organelles such as nuclei through cortex in N. crassa keeps the septal pores and branching tubular cells (hyphae) that septa. However, in this issue of PLoS clear and allows unrestricted cytoplasmic generate radially symmetric colonies. As Genetics, Seng Kah Ng et al. describe a streaming. As a test of their model, the colonies expand, hyphal tips at the pe- curious modification of the tethering authorsfusedthelah-1andlah-2genesto mechanism for the Woronin body in N. riphery avoid each other to allow maxi- mimicthelahgeneorganizationseenwith mum coverage of the medium, while crassa [10].Ng et al.describe the identifi- other filamentous ascomycetes. Interest- hyphal tips at the colony center actively cationofleashin(lah),afungal-specificgene ingly,thestraincontainingthelah-1/lah-2 fuse to generate an interconnected net- that encodes an organellar tether for gene fusion showed localization of Wor- work of hyphae that allows the bulk Woroninbodyinheritanceandcellcortex oninbodiestobothsidesofseptalporesas movementofcytoplasmtowardthecolony association. In most of the filamentous inotherfilamentousascomycetes,andthe ascomycetes,thelahgeneencodesasingle edge [1]. Hyphal growth is a wonderful fusion protein appeared functional as protein; however, in N. crassa and the adaptation for efficient penetration and protoplasmic ‘‘bleeding’’ of damaged hy- acquisition of nutrients from live or dead closely related fungus Sordaria fimicola, lah phaewassignificantlyreduced.Consistent organisms,especiallyplants.Unlikemulti- hasbeensplitintotwogenes,lah-1andlah- with the authors’ prediction that such an cellulareukaryotesthatexistascollections 2. The authors show that in N. crassa, arrangement would restrict cytoplasmic of distinct cells, the syncytial mode of LAH-1linksWoroninbodieswiththecell streaming, the lah-1/lah-2 strain grew at growthplacesfilamentousfungiatserious cortexandnottheseptalpore.Mutations one-thirdtherateofwildtype. The Woronin body protein HEX, the risk of ‘‘bleeding’’ to death if there is a eliminating LAH-1 function result in loss break in the cell wall. To avoid this fate, of Woronin body inheritance and greatly Woronin sorting complex protein WSC, fungal hyphae have cross-walls or septa increased ‘‘bleeding’’ of hyphae. LAH-2 andtheLeashinprotein(s)arefoundonly that are perforated to allow the flow of was shown to localize to the hyphal apex within the filamentous ascomycetes [2]. cytoplasm,butcanbepluggedinresponse and the septal pore rim and to play an Thefilamentousbasidiomycete fungirep- to cellular wounding [2–4]. The septal important role in colony development. resent an immense group that have a ‘‘plug’’ used by filamentous ascomycete These findings have led the authors to completely different septum architecture fungiisknownastheWoroninbody,and propose a model (Figure 1) where the [2,3]. Insomeofthefilamentousbasidio- it is typically tethered to the rim of the rapid growth rate of N. crassa hyphae mycetes, there are reports of cytoplasmic septalpore[4–8]. (.1mm/sec)isdependentontheextreme- flowratesofupto70mm/sec[11].Itwill In the filamentous fungus Neurospora ly high rates of cytoplasmic streaming be of great interest to see if future work crassa,cytoplasmicstreamingcanoccurat through septal pores. In fungi with Wor- finds that the filamentous basidiomycetes incrediblerates,upto60mm/sec[9].The onin bodies tethered directly to septal with fast cytoplasmic streaming have also typical ‘‘trap-door’’ arrangement of the pores,thefreeflowofcytoplasmandlarge dispersedthe‘‘plug’’toensurefreeflowof Woronin body seen in most ascomycetes organelleswouldbereduced;however,the materials through septal pores, allowing mightbeexpectedtoimpederapidflowof tethering of Woronin bodies to the cell rapidhyphalandcolonygrowth. Citation: Plamann M (2009) Cytoplasmic Streaming in Neurospora: Disperse the Plug To Increase the Flow?PLoSGenet5(6):e1000526.doi:10.1371/journal.pgen.1000526 Editor:SusanK.Dutcher,WashingtonUniversitySchoolofMedicine,UnitedStatesofAmerica PublishedJune19,2009 Copyright: ß 2009 Michael Plamann. This is an open-access article distributed under the terms of the CreativeCommonsAttributionLicense,whichpermitsunrestricteduse,distribution,andreproductioninany medium,providedtheoriginalauthorandsourcearecredited. Funding:Theauthorreceivednospecificfundingforthisarticle. CompetingInterests:Theauthorhasdeclaredthatnocompetinginterestsexist. *E-mail:plamannm@umkc.edu PLoSGenetics | www.plosgenetics.org 1 June2009 | Volume 5 | Issue 6 | e1000526 Figure1.Adispersedseptalplug(Woroninbody[WB])mayfacilitaterapidcytoplasmicstreamingandhyphalgrowthinN.crassa. (A)LegendillustratestheancestralformofLeashinfoundinmostfilamentousascomycetesandthesplitversions(LAH-1andLAH-2)foundinN. crassa.(B)ModelforlocalizationofWoroninbodiesinthemajorityoffilamentousascomycetes.NotethatLAHconnectsWoroninbodiestotheseptal porerim.Intheseascomycetes,cytoplasmicstreamingoccursatslowrates,andhyphaldiametersandgrowthratesarereducedrelativetoN.crassa. (C)ModelforlocalizationofWoroninbodiesinthefilamentousascomycetesN.crassa.NotethatLAH-1localizestheWoroninbodytothecellcortex andnottheseptalporerim;however,LAH-2,lackingthelargeWoroninbodycomplex,doeslocalizetotheseptalporerim.Thedouble-headedarrow indicatestheabilityofcytoplasmtoflowthroughseptalporesinanunimpededmanner.Ngetal.suggestthatthismodificationofLAHtethering proteinstructureandfunctionmayhavebeenadeterminingeventinallowingN.crassatoevolveextremeratesofcytoplasmicstreamingandhyphal growth.ThisfigurewasadaptedfromFigure7of[10]. doi:10.1371/journal.pgen.1000526.g001 References 1. Alexopolous CJ, Mims CW, Blackwell M (1996) of the plasma membrane. Nat Cell Biol 2: 8. Momany M, Richardson EA, Van Sickle C, IntroductorymycologyJohnWiley&Sons.652p. 226–231. JeddG(2002)MappingWoroninbodypositionin X, 2. Soundararajan 6. S, Jedd G, Li Ramos- Aspergillusnidulans.Mycologia94:260–266. Dhavale T, Jedd G (2007) The fungal Woronin Pamplona M, Chua NH, et al. 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