Intercellular infection in the meristematic region of 'Piceirhiza gelatinosa' mycorrhizas
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1 .\nc Phylnl. (1<),S')) Intercellular infection in the meristematic region of 'Piceirhiza gelatinosa' mycorrhizas BY L HAUG Spezielle Botanik, Mykologie, Universitat Tubingen, Auf der Morgenstelle 1, 7400 Tubingen, Federal Republic of Germany {Received 20 June 1988; accepted 17 October 1988) SU M M " Piccirhiza ih'latiiioxa' m\ci)nhiz;is from Schluclisff, but not from two other sites in the Hl;ick l"\)rest, sliowed intercclluhir hyphae in the iipical region of unbranched and tinger-hke branched roots. The hyphae of the fungus were able to penetrate between tlie meristematic and immature cortical cells. In outer regions of the root, hyphae were arranged in layers one to two cells deep but towards the middle, single hyphae were most commonly encolintered. The metliod of penetration and a possihle relationship with abnormal growth are discussed. Kev words: Piccd abies (K.) Karst., ectomycorrhizas, Hartig net, intercellular h\phae in the apical region. I NTRODlirTI ON In one of the first studies of the anatomy of ectomycorrhizas, Frank (1885) observed that the apex of a mycorrhiza was free of intercellular infection and that hyphae penetrated between the cortical cells only when tbe growth in length was completed. Marks & Foster (1973) described the possible infection zone in more detail. Tbey named tbe ref^ion of tbe host where mycorrbizal symbiosis originates the 'mycorrhizal infection zone (MIZ)' and characterized tbis zone as being bebind the growing apex and in advance of the region where the primary cortex begins to deteriorate. Recently, Harley (1985) & Nylund (1987) confirmed that the zone of infection is limited, but tbey cited different reasons for tbe limitation. Harley (1985) proposed a mechanism in wbicb tbe proteins on tbe walls of tbe fungus interfere witb tbe carbobydrate-specific enzymes producing tbe cell walls of maturing bost cells. Nylund (1987) bypotbesized tbat tbe mycorrhizal infection zone is defined by a particular wall composition and a particular physiological condition. He showed that cell walls of the MIZ possess abundant pectin-like compounds, which perhaps increase wall flexibility. Nylund (1987) pointed out that the fungus can only colonize mature cortical tissue, perhaps because mature walls can be easily separated, in contrast to the more firmly attached \A'alls of the immature cortex and meristem. In tbe present paper, it is proposed that tbe fungal partner of ' Piceirhiza gelatinosa' (Gronbacb & Agerer, 1986) is able to penetrate tbe meristematic and apical regions of Picea abies. M.^TKRI.AI.S AND METHOD.S Mycorrhizas were sampled in July 1987 in the Black Forest near tbe Schlucbsee ( m above sea level) and near Villingen ( m above sea le\cl). Both stands are mixed-age forests. In Scbluchsee the age of tbe spruce trees [Picea abies (L.) Karst.] varies between 20 and 60 years and in Villingen between 80 and 120 years. In 1985 mycorrhizas were sampled in Steinwald near Freudenstadt (Black Forest, m above sea level). The spruce trees in tbis stand are between 80 and 100 years old. Root samples were taken from the bumus layer of tbe three sites. The mycorrbizas were examined under a stereo microscope ( x 20), enabling difierent mycorrbizal types to be distinguished. In tbe present work, only ' Piceirhiza gelatinosa' mycorrbizas (Cjronbacb &.Agerer, 1986) were examined. The mycorrhizas were washed, photographed and fixed in 2",, glutaraldebyde with ()-2 M arsenic buffer for 5 weeks at 4 C. I'ost-Hxation was carried out with osmium tetroxide (1 " for 2 b) and counterstained with uranyl acetate (1 " for 1 h). Spurr s FRL was used as the embedding resin. Four infiltration steps were carried out, witb ratios of
2 204 /. Haug FRL: acetone 1:2, 1:1 and 2:1 for ()-5 h each, and pure ICf<L for 3 d at 23 C. Polymerization took place at 70 C for 3 d. Semi-thin longitudinal sections (0-5-2 /im) were stained with neofuchsin-crystal violet, and ultra-thin sections ( nm) were contrasted with lead citrate. 1 RH.sti I.TS The mycorrhizas of ' Piceirhiza gelatinosa' were white to pale brown, with a smooth surface. They were mm thick, straight, very long (up to 6 mm) and normally unbranched (Fig. 1), or sometimes swollen and club-like, reaching a diameter of 0-9 mm (Fig. 2). In comparison to other mycorrhizas from Schluchsee, ' Piceirhiza gelatinosa' mycorrhizas were strikingly large (Fig. 2). Some specimens from the Schluchsee area showed abnormal, fingerlike branching (P^ig. 3). The hyphal mantle consisted of an approximately 60 //m thick layer of dark coloured hyphae embedded in a substantial extracellular matrix (Figs 4 and 5). In tangential view, the hyphae making up the mantle formed Y-shaped branches and coiled to form spiral or labyrinthine patterns (Fig. 4). Some hyphal septae were obser\ ed to have dolipores with perforated parenthesomes (Fig. 10), characteristic of basidiomycetes. There was a well developed Hartig net in all regions of the root. Of particular note were the hyphae between the meristematic and immature cortical cells (Figs 6-9 and 11-12). The unbranched as well as the branched mycorrhizas showed hyphae in the apical region. Cell divisions were noted in the lateral regions of the meristem of unbranched roots (Fig. 7). The meristematic cells were normally closely interconnected, without intercellular spaces (Fig. 8, above). Howe\ er, in regions where hyphae were present, relatively large spaces were found between the separated v.'alls of meristematic cells and between the hyphal and the meristematic cell walls (Figs 9, 11 and 12, marked with ). In the spaces, some matrix material was present. The adjacent cell walls were separated from each other by wedge-shaped hyphae without clear signs of disorganization (Fig. 12). The density of hyphae decreased from the outer region of the root apex to the middle. Near the outer cell layers, the intercellular hyphae were either one-layered or twolayered (Fig. 8, below), but in tbe middle of the root hyphae were usually solitary and small in diameter (Fig. 8, above. Figs 9, 11 and 12). No hyphae were found in the diflerentiating or mature vascular tissues. The ' Piceirhiza gelatinosa' mycorrhizas sampled from Villingen and Steinwald were similar to those described by Gronbach & Agerer (1986). DISCtlSSION Figures 1-3. Stercomicroscope photographs (scale bar, 2 mm). Figure 1. Unbranched, straight 'Piceirhiza gelatinosa' mycorrhizas. Figure 2. Club-like swollen 'Piccirhiza gelatinosa' mycorrhiza (marked with -ji^) contrasted with other mycorrhizas. Figure 3. Finger-like branched ' Pircirhiza geliitivnsa' mycorrhizas. The structure of the hyphal mantle and the multilayered Hartig net of the Schluchsee mycorrhizas were as reported by Gronbach & Agerer (1986), but the mycorrhizas were sometimes elongated, rather than swollen and clublike as previously described. Gronbach & Agerer did not describe branching of their mycorrhizas, but branching was found in
3 205 Ittteicellttlar hypltae i/i luerislents of eetomycorrhizal Picea ic " Figures Abbicviatiotts: c, c()rtic;il cells; h, hypliae; hm, Inphal in.mtk cortical cell.s; m, meristematic cells; n, nucleus; p, parenthesome.s. liii llntii; lur R lnini.inirc- Figures 4-7. Semi-thin, loiikitudinal sections of ' Piceiihiza gclatinosa' mycorrhiza. Figure 4. Tangential section in the region of the hyphal mantle (scale bar, 50 /mi). Figure 5. Basal region with hyphal mantle and Hartig net between cortical cells (scale bar, 50/mi). Figure 6,7..Epical region with hyphae (marked with arrows) between immature cortical cells and meristematic cells (scale bar, 50//m). Figure 8. Transmission electron micrograph ov Piceirhiza gelatiitosa' niycorrhizas. Section of the apex from the hyphal mantle to the meristematic cells (scale bar, 10//m).
4 206 Figures ransmission electron micrographs of ' Piceirhiza i^ctaiiuosa' mycorrhizas; intercellular spaces marked with -^. (Vm abbreviations see lekc^nd to imfjs 4 12.). Figure 9. Hyphae between the meristematic cells (scale bar, 10/;m). Figure 10. Dolipore with perforated parcnthesomes of a hypha (scale bar, 0-5 jim). Figures 11,12. Penetrating hyphae between meristematic cells (scale bars: Fig. 11, 10/(m; Fig. 12, 5/nn). ' Piceirhizagelatinosa' mycorrhizas from Schluchsee. Similarly, only these mycorrhizas from Schluchsee showed hyphae in the meristematic region. No other mycorrhizal types from Schluchsee showed finderlike branchings, or had hyphae between meristematic cells, and all of the ' Piceirhiza gelatinosa mycorrhizas from Steinwald (Haug, 1987) and Villingen were unbranched and showed no hyphae in the meristematic region. The spruces of the Schluchsee stand were younger thati those at the two other sites atid vvere growing at a higher altitude, but all sites had mixed-age forests and the humus form was mull. II there had been a meristematic disorder at Schluchsee, because of ati unktiowti environmetital variable, other mycorrhizal types would also have showti abtiormal braticbing and byphae betvveeti tbeir meristetnatic cells. Tlius, it cati be cotieluded tbat tbe ' Pieetrhiza getatitiosa' Schlucbsee strain difiered from the ' Pieeirhiza gelatinosa' strains at the other sites and, also that otily tbis strain was capable of penetrating betweeti meristematic cells. Possibly petietration between the meristetnatic cells
5 Intercellular liyphae iii meristenis of ectoinycorrhtzal Pi 207 can enhance lonjiitudinal fi;rowth and/or abnormal branching of mycorrhizas. It is difficult to interpret the spaces between h\phae and meristematie cells in the electronmicrographs. It may be that material has been lost during fixation or that the spaces are artefacts that may have arisen during Hxation. The matrix material could be of fungal, plant or mixed origin. The finding of hyphae within the meristematic region has not been reported before..according to the hypotheses of Harley (1983) and Nylund (1987), intercellular penetration is explained as being due to the special biochemical condition of the cells behind the meristem. f4ovvever, the present investigation showed that penetration can also occur between the meristematic cells of an active healthy mycorrhiza. It is difficult to know why only the fungus of the Schluchsee P. g. mycorrhizas was capable ot penetrating between the meristematic cells. The mechanism which normally prevents penetration of mycorrhizal fungi between meristematic cells must have been overcome by this fungus. Since no clear changes ill the \ery thin cell walls of the meristematic and immature cortical cells were visible, penetration probably was not enzymatic. This fact, together with the wedge shape of the h>phae, indicates that penetration was by mecbanical means, thus confirming a number of previous obser\ations (Marks & Foster, 1973; Duddridge & Read, 1984; Nylund, 1987)..w K NOW l.iux; lim I-;NTS The author is indebted to tlie Projekt Europiiisches Forschungszcntriini Karlsruhe for grunts during the investigation. I want to thank Mrs Angela Dressel for her skillful help, Dr Mary Berbee for proof reading, Dr I. Kottke and Professor Dr F. Oberwinkler for discussion ot the paper. R F Fl". R I' N C I' S DiDnrdDcn, J. A. & Ri;.\i), D. J. (1984). The development and ultrastructure ol eetomxcorrhizas. II. Ect()m\'corrhizal de\elopment on pine ;;; vilni. Nnc Phytntnijist 96, 'HANK, M. (IIS85). i'ber die auf Wurzelsymhiose beruhende I'^rnahruiiK gewisser Biiume durch unterirdische Pilze. Benchte tier Botiiiiisiilcn Gcsi't/.u/in/l 3, C;i((iNHA(ii, E. &.AGKRER, R. (1986). C'harakteri.sierung und hnentur der Fichton-.Mykorrhizen im Hoglwald und deren Keaktionen alil saure Here^'iiun^'. /''orsl^cissi'n.^fluijlltc'hrs Zi-ntralblalt 105, HAHI.I;>', J.I.. (1985). Speeility and penetration of ti.ssues hy m\corrhizai kmm. Prod'ediii^s of the liuiian.atddeniy of Sciences, Seetioii B (Ptaiit Seiences), 94, HAI'G, I. (1987). Lieht- und elektroiieiintikroskopisihe Viilersiietningeii nil Mykoirhixeii Tan FiilitenbesU'indeii iiii Sctnvinz- ^vdld. Dissertation, TLihingen. MARKS, G. C. & FO.STER, R. C. (1973). Structure, morphofjenesi.s and ultrastructure of ectoniycorrhizae. In: Eelomveoirhiztie (Rti hy C;. C. Marks & T. T. Kozlowski), pp. I 41. Aeademic Press, New ^'()rk, London. Nvi.i Ni), ].-V.. (1987). The ectomycorrhizal infection zone and its relation to acid polysaecharides of cortical cell walls. AVft' Phyldlniiist 106,
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