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Root Hair Infection in Actinomycete-Induced Root Nodule Initiation in Casuarina, Myrica, and Comptonia Author(S): Dale Callaham, William Newcomb, John G

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Root Hair Infection in Actinomycete-Induced Root Nodule Initiation in Casuarina, Myrica, and Comptonia Author(S): Dale Callaham, William Newcomb, John G Root Hair Infection in Actinomycete-Induced Root Nodule Initiation in Casuarina, Myrica, and Comptonia Author(s): Dale Callaham, William Newcomb, John G. Torrey, R. L. Peterson Source: Botanical Gazette, Vol. 140, Supplement: Symbiotic Nitrogen Fixation in Actinomycete-Nodulated Plants (Mar., 1979), pp. S1-S9 Published by: The University of Chicago Press Stable URL: http://www.jstor.org/stable/2474196 . Accessed: 30/08/2011 15:59 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. The University of Chicago Press is collaborating with JSTOR to digitize, preserve and extend access to Botanical Gazette. http://www.jstor.org BOT.GAZ. 14O(SUPP1.): S1-S9. 1979. (¢ 1979by The Universityof Chicago.0006-8071/79/40OS-0001$00.88 ROOT HAIR INFECTION IN ACTINOMYCETE-INDUCED ROOT NODULE INITIATION IN CASUARINA, MYRICA, AND COMPTONIA DALE CALLAHAM,1* WILLIAM NEWCOMB,2t JOHN G. TORREY,* AND R. L. PETERSONt *CabotFoundation, Harvard University, Petersham, Massachusetts 01366, and tDepartmentof Botany and Genetics Universityof Guelph,Guelph, Ontario, Canada N1G 2W1 The infection process leading to the developmentof root nodules of Comptonia peregrina, Casuarina cunninghamiana, Myrica gale, and M. cerifera was studied by light and electronmicroscopy. Deformed growth of root hairs was observedas early as 24 h after seedlingsgrown aeroponically or hydroponically wereinoculated with suspensionsof crushednodules or culturesof the actinomycetousendophyte of Comp- tonia. The extent of root hair deforIrJationshowed a positive correlationwith the numberof noduleswhich subsequentlydeveloped. The essentialfeatures of infectionin each of these specieswere very similar.The actinomyceteentered a deformedroot hair of the host in a regionof foldingof the cell wall. A convoluted elaborationof the root hair wall which occurredat this presumptivepenetration site was continuouswith the moreevenly depositedcapsule of the endophyticactinomycete. An associatedfeature of this wall deposi- tion was thickeningof the cell wall of the infectedroot hair and the adjacentprenodular cells. The actino- mycete encapsulationwas thickestat the presumedsite of penetrationand thinnerin later stages of endo- phytic growthaway from this site. These observationssuggest a periodof initial disequilibriumcaused by the infection,followed by more harmonioussymbiotic growth. The observationof a morphologicallyand cytologicallysimilar root hair infection process in these three genera indicates that root hair infection involves a specificand orderlyinteraction which representsthe commonmode of invasionin the initiation of actinomycete-inducedroot nodules. Introduction The ultrastructuralstudies of LALONDE(1977) The developmentof actinomycete-inducednod- showed the endophyte within a root hair to be ules on the roots of certainwoody dicots represents encapsulatedby host-derivedwall materialas the a complexseries of events. Three major stages in actinomycetegrows tonard the root hair base. The developmentcan be distinguished:the infectionof infectionof C. peregrina roots observedin the light the root hair, the induction and invasion of a microscope(CALLAHAM and TORREY1977) occurred prenodularproliferation of the cortex, and the by penetrationof a roothair at a site of invagination inductionand invasionof primaryand higher-order or foldingof the cell wall. nodule lobe primordia.The anatomicaldetails of Despite these observationsof the actinomycete root nodule morphogenesishave become better enteringthe host throughroot hairs,there has been understoodwith studies of this process in A Inus little understandingof how this processoccurs. The glutinosa (POMMER1956; TAUBERT1956; ANGULO direct involvementof root hair deformationin the CARMONA1974), Casuarina cunninghamiana (TOR- infectionprocess was questionedby QUISPEL(1955, REY1976), Comptoniaperegrina (BOWES, CALLAHAM, 1974), w ho claimed his experimentsshowed an and TORREY1977; CALLAHAMand TORREY1977; inabilits7of the actinomaceteto proliferateoutside NEWCOMBet al. 1978), and Myrica gale (FLETCHER of host cells;thus, he eliminatedthe possibilitythat 1955; TORREYand CALLAHAM1978, 1979). the actinomyceteeas responsiblefor root hair de- The processof root infectionby the actinom)cete formation. Conclusionsdrawn from these results which initiates this developmentalsequence is not shouldbe reconsideredin light of new evidencethat clearlyunderstood. Compelling evidence by TAUBERT at least one of these nodule endophytescan grow (1956) and ANGULOCARMONTA (1974) established outside of host tissues (CALLAHAM,DEL TREDICI, that the actinomyceteinitially enters the rootsof A. and TORREY1978). glutinosa by penetrationof a deformedroot hair. The observationsof LALONDE(1977) of a specific LALONDE(1977) observed root hair deformation "exoencapsulation"process preliminary to the root within 24 h after inoculationof the plants. A11 hair infection in A. glutinosa were based on the elongatingroot hairs appearedto be affected,and assumptionthat the noduleendophyte exhibits rod- filamentpleomorphism (LALONDE, KNOWLES, and eachexhibited deformed growth with furtherelonga- FORTIN1975; LALONDE 1977) when growing outside tion occurringin branchesof the originalroot hair as opposedto eithin the host cells. However,the axis. The result of this responsewas a "slope"of rhizospherebacterium discussed by LALONDE(1977) deformedroot hairswith newly initiatedroot hairs was not identifiedby availableimmunological meth- distal to this regionremaining short and branched. ods (LALONDEet al. 1975)or by directobservations l Present address: Department of Botany, University of of root hair penetration.In his exoencapsulation Massachusetts,Amherst, Massachusetts 01003. theory, LALONDEdid not interpret the root hair 2 Present address: Department of Biology, Queen's Uni- deformationas directlyinvolved in the mechanism versity, Kingston, Ontario,Canada K7L 3N6. of penetrationof the root hairwall, althoughhe did S1 :_^^ \'X.IS.,,1 ts / /F > f f t.Xit _ v>:- ::vx;fJk -- . - _Z 1u - _ S2 BOTANICALGAZETTE view the deformationas a plant responseto the Materialand methods actinomycete. PLANTCULTURE. Locally collected fruit of Comp- There are consistent observationsof root hair tonia peregrina were scarified,soaked for 24 h in deformationassociated with nodulationin Alnus, 500 ppm gibberellicacid (GA3),and germinatedin Comptonia,Cas?sarina, and M. gale. Convincing flats of washed sand in the greenhouseat the evidence for root hair infection associated with HarvardForest (DEL TREDICIand TORREY1976). deformationwas providedfor A. glutinosa(POM1HER Locallycollected fruit of MyricagaZe and M. cerifers 1956; TAUBERT1956; ANGULOCARMONA 1974), A. were treated similarlybut without scarificationof crispa (LALONDE1977), and Comptonia(CALLAHAM the fruit of M. gale. Seeds of Casuarinacunning- and TORREY1977). The researchreported here is an hamianawere germinated in flats of washedsand in investigationof the infectionprocess in the initiation the greenhousewithout scarification.All seedlings of the root nodulesof M. gale, M. cerifera, and C. weretransferred to aeroponicculture tanks (ZOBEL, cunninghamtanafor whichobservations of the initial DEL TREDICI,and TORREY1976) when the shoots infectionhave not been recorded.Further evidence wereabout 3 cm high and weregrown under condi- of root hair infection of C. peregrina, extending tions specifiedby CALLAHAMand TORREY(1977). earlierobservations (CALLAHAM and TORREY1977), Two weeks after germination,seedlings of M. gale is also reported. weretransferred to smalltest tubewater cultures for 1 w} ,= t . | v.e t>.>*t.6 K # #e g ^_ .<. 8 l#^.Z*. F.F_ t t fi{ x # r : 1 r -*> r j . | # drP | _ -* i ; tl " ; _ " n 'i ,,' *j- lf,ljifs X f - FIGS.1-4. Root hairs of Myricagale from seedlingsgrown in water cultures.Fig. 1, Uninoculatedroot hairs which developed long and straight;scale = 200 ,um.Fig. 2, FU11Yelongated root hair 24 h after applicationof CI inoculum;fragments of the inocu- lum are entwinedabout the root hair which still exhibitedactive streamingbut failed to branch;phase contrast; scale = 50 ,am. Fig. 3, Elongatingroot hair 24 h after applicationof CI inoculum,showing branching and continuedgrowth from several points; phase contrast;scale = 50 ,um.Fig. 4, Deformedroot hair 24 h after inoculationwith the CI; branchingcan be quite ex- tensive; CI filamentsare not associatedwith each branchpoint; anoptralphase contrast;scale = 20 ,um. FIGS. 5-10. Fig. 5, Sectionof infectedroot hair (IRH) of Casuarinacunninghamiana cut longitudinally;the endophytewithin the root hair (arrows)was traceableto the infectednodule cortex in other sections;scale = 10 ,am. Fig. 6, Section throughthe highlybranched distal part of the infectedroot hair of Casuarinain fig. S; the filamentousendophyte (arrows) is presentthroughout this lobed root hair tip; scale = 10 ,um.Fig. 7, Transmissionelectron micrograph (TEM) of a section of the Casxarinaroot hair cut adjacent to the section in fig. 6; the endophyte (E) within the root hair is encapsulatedby a layer (c) which joins several filamentsat the lowerright into a largestrand; scale = 1 ,am.Fig. 8, TEM
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