Structural diversity in (vesicular)–arbuscular mycorrhizal symbioses

New Phytol. (1997), 137, 373-388

Tansley Review No. 96Structural diversity in(vesicular)—arbuscular mycorrhizalsymbioses

BY F. A. SMITH'* AND S. E. S M I T H ^

^Department of Botany, The University of Adelaide., SA 5005, Australia^Department of Soil Science, University of Adelaide, SA 5005, Australia

{Received 11 February 1997)

373374375

377377379

IV.V.

VI.VII.

VIIL

Is the distinction between classes useful?The structural basisThe role of the fungal genomePhysiology revisitedConclusionsAcknowledgementsReferences

3833833843843853863S6

CONTENTSSummary

I. Introduction: Arum-types and Pom-typesII. Possible functional implications

III. Extent of the two classes in the plantkingdom1. Bryophytes and Ptendophytes2. Gymnosperms3. Angiosperms 379

SUMMARY

This review describes diversity in the structure of (vesicu!ar)-arbuscular (VA) mycorrhizas, i.e. endomycorrhizasformed by Glomalean fungi. In particular, we consider the extent in the plant kingdom of the two classes firstdescribed by Gallaud (1905). These are: (1) the Ariim-type, defined on the basis of an extensive intercellular phaseof hyphal growth in the root cortex and development of terminal arbuscules on intracellular hyphal branches; (2)the Paris-type, defined hy the absence of the intercellular phase and presence of extensive intracellular hyphalcoils. Arbuscules are intercalary structures on tbe coils. However, there have been many reports that in Paris-typesarbuscules are relatively few in numbers, small, or absent altogether.

A survey of the literature bas revealed that Fam-types occur more frequently in the plant kingdom than Arum-types and predominate in ferns, gymnosperms and many wild angiosperms. The cultivated herbs that are thesubject of much experimental work are mostly Arum-types. Although evidence is still limited, there are differencesat the family level. In 41 angiosperm families tbere are records of only Pam-type VA mycorrhizas and in 30families records of only Arum-types. Another 21 families have examples of both classes, or intermediates betweenthem. Accordingly, we consider whether the original division into two classes is still useful. We conclude that itis when considering the physiology of the symbiosis and especially the issue of whether different fungus/hostinterfaces have specialized roles in transfer of inorganic nutrients and organic carbon between the partner?. If thereis no such specialization between hyphal coils and arbuscules, then the latter might not be necessary for thefunction of Pam-types. This would account for reports of the infrequency or absence of arbuscules in this class.The control exerted on structures by the genomes of host and fungus, and possible reasons (anatomical andphysiological) for tbe existence of the VA mycorrhizal structures, are discussed. The presence or absence ofextensive intercellular spaces and differences in the wall structure of cortical cells might be particularly importantin determining which type of VA mycorrhiza is formed.

Key words: VA mycorrhizas, root anatomy, plant taxonomy, nutrient transport.

* To whom correspondence should be addressed.E-mail: asmith(a;botany. adela ide . edu. au

374 F. A. Smith and S. E. Smith

L I N T R O D U C T I O N : ARUM-HWES AND PARIS-

TYPES

Gailaud (1905) described two major structuralclasses of (vesicular)-arbuscular (VA) mycorrhizas,which he named ^rum-types and Paris-types, afterthe plants in which they were first described. In bothclasses, the initial epidermal penetration results inintracellular hyphae. often forming coils (' pelotons')in the hypodermis, where present, and outer cortex.The -4rwm-type mycorrhiza was defined by theexistence of extensive intercellular hyphae under-lying this initial phase of colonization after which,following penetration into cortical cells, arbuscutesare formed, normally as terminal structures on so-called trunk hyphae. These structures are sum-marized in Figure 1. Figure 2 shows some of themany illustrations by Gailaud (1905) and Figure 3shows ^rum-type structures in Allium as seen byconfocal laser scanning microscopy. Vesicles can beintercellular or intracellular, and are not formed byall VA mycorrhiza! fungi. Accordingly, the term'arbuscular mycorrhiza' is coming into use. Never-theless, as explained previously (Smith, 1995; Smith& Smith, 1996; Smith & Read, 1997), we will retainthis abbreviation in the present review for overallsimplicity' and for consistency with most of theliterature. Also we wish to avoid undue emphasis onarbuscules alone, since not all VA mycorrhizasappear to form arbuscules. Thus we use 'VA'generically for mycorrhizas formed by fungi of theorder Giomales sensu Morton & Benny (1990): theissue is further discussed below.

Gailaud (1905) defined the Pans-type VA mycor-rhiza by the absence of intercellular hyphae. Instead,there are extensive coils of intracellular hyphaewithin cortical cells, from which arbuscules arenormally formed as intercalary structures (Figs 1, 2).Figure 3 shows hypha! coils in the cortical cells ofPanax as seen by confocal laser scanning microscopy,One of the cells iUustrated contained no arbuscu!es,but small and indistinct arbuscules were present inadjacent cells. Vesicles, where present in Paris-types, are intracellular. On the basis of his survey,Gailaud believed this class to be the less common.Much subsequent experimental work has been donewith temperate crop plants that have .^rum-typemycorrhizas (e.g. Allium, Trifolium, Vicia etc), andthis class has-almost by default-come to be re-garded as the norm.

In an earlier and classic study (Janse, 1897), thetwo classes are also clearly distinguishab!e, althoughthe fine detail of arbuscules was not recognized. Inthat case lack of taxonomic knowledge of the fungiled to some confusion, with emphasis on similaritieswith the intracellular hyphal structures-especiallythe hyphal coils-in other endomycorrhizas that werestudied, i.e. in what are now known to be ericoid andorchid mvcorrhizas. The situation was further

confused by Peyronel (1923, 1924), who studiedboth types of structures and concluded that the fungithat produced hyphal coils in Paris-types, weresecondary colonists in roots that were alreadycolonized by the true VA mycorrhizal fungi.Peyronel believed that these secondary fungi did notproduce arbuscules or vesicles and that the hyphaewere septate to a degree that does not occur in thefungi that form VA mycorrhizas. Harley (1969) gavea summary of Peyronel's work; see also Harley(1991) for a more detailed account and biography.Peyronel's view was certain!y incorrect for Paris-types in genera! because, as shown by Ga!!aud(1905), some do produce both arbuscules andvesic!es, whereas the intraradica! hyphae in Arum-types can and do produce septa depending on thehost/fungus combination (e.g. Hildebrand & Koch(1936) and many papers subsequently). Also, bothintra- and extra-radical hyphae can become septateunder various conditions which include damage(Gerdemann, 1955), age (Kinden & Brown, 1976)and pre-penetration stages of colonization(Giovannetti et al., 1993).

The confusion over whether Pam-types are'genuine' VA mycorrhizas should have been laid torest by experimental investigations which showedconclusively that VA mycorrhizal fungi isolatedfrom Arum-type hosts produce Paris-type structuresin other hosts and vice versa. The first such reportthat we have found was a conference abstract byBarrett (1958), stating that an isolate of Rhiso-phagus—the generic name then used for Glomaleanfungi-'that developed the Arum type {sic) in Zeamays produced the Paris type in Solanum tuberomm,and a peloton type in Iris. A Paris type from Hetero-callis developed the Arum type in Zea mays.' (Wehave not identified ' Heterocallis'-it might be theliliaceous plant Hemerocallis.) Barrett continued:'These results indicate that the host, not the endo-phyte, determines the host-fungus relationships'.This immensely important point has been confirmedby others (see below). However, Barrett (1958) alsosaid that 'the tests reported here do not confirmGaUaud's findings', which seems odd, seeing thatGailaud's classification did not directly address theissue of control by the host or fungus. Also, Barrett'sdistinction between the Paris-type and peloton typedid not help, seeing that pelotons (coils) are adefinitive feature of Paris-types. Work by otherssuggests that the Solanaceae includes representativesof both classes: see below. A similar investigationwas by Gerdemann (1965), who showed that thesame Glomalean isolate produced a Pam-type VAmycorrhiza in Liriodendron (tulip-tree) and an Arum-type in Zea. Jacquelinet-Jeanmougin & Gianinazzi-Pearson (1983) likewise showed that the devel-opment of Pans-type structures in Gentiana wasproduced by Glomalean fungi that formed Arum-types in Allium. The Gentianaceae, which includes

Structural diversity in VA mycorrhiza 375

(a) Arum-type

(a) Paris-type

Figure 1. Summary of cortical structures in the twoclasses of VA mycorrhizas described by Gallaud {1905).The size of arbuscules, especially in Paris-types, can varygreatly. From Smith & Smith (1996), with permission.

achlorophyllous (mycoheterotrophic sensu Leake,1994) genera is a classic Paris-type family, as firstshown by Janse (1897); see also Gay, Grubb &Hudson (1982), McGee (1985) and other referencesgiven later. Control of many major mycorrhizalstructures by the genome of the host was alsoemphasized by Bonfante-Fasolo & Fontana (1985),Daniels-Hetrick, Bloom & Feyerherm (1985) andSmith (1995). Nevertheless, despite the impressi\'eexperimental evidence, it is still possible that thefungal genome might" also exert some control overthe structures. We discuss this point later.

There have been numerous studies of the de-velopment of Arum-type structures, including thoseby Mosse & Hepper (1975) with Trifolium, Bonfante-Fasolo & Scannerini (1977) with Ornithogalum,HoUey & Peterson (1979) with Phaseolus. Morton(1985) with Zea, Alexander et al. (1989) with Allium.Phaseolus and Zea, and Weber, Kiahr & Marron-Heimbuch (1995) with plants in the Apocynaceae.The review by Bonfante-Fasolo (1984) gives otherreferences. Detailed work on development oi Paris-types (or near-Por/s-types) includes that by Kinden& Brown (1975, 1976) with Liriodendron, Bonfante-Fasolo & Fontana (1985) with Ginkgo, Yawney &Schultz (1990) and Cooke. Widden & O'Halloran(1992, 1993) with Acer, Weber et al. (1995) withplants in the Apocynaceae, and Whitbread,McGonigle & Peterson (1996) with Panax.Bonfante-Fasolo's (1984) review covers PariS-types.although she does not use this term or distinguishthem explicitly. Surveys of the comparative anatomyof mycorrhizas by Brundrett & Kendrick (1988,1990a, 6). Brundrett, Murase & Kendrick (1990)and Cooke et al. (1992) have shown the widespreadoccurrence oi Paris-type?, in wild plants-both herbsand woody plants. Widden (1996) has describedstructures in members of the Liliaceae {sensuCronquist, 1981) that are variations w ithin the Paris-types and which were also noted by Gallaud (1905)in Colchicum (also Liliaceae sensu Cronquist), asshown in Figure 2. The elegant iUustrations in therecent papers (light and scanning electron micro-graphs) show the presence of arbuscules associatedwith intracellular hyphal coils. Brundrett &Kendrick (19906) suggested that it is not yet clearwhich class is the most common. This comment has

led to our surveying the literature in an attempt toassess the extent of P«r/5-types in relation to Arum-types. In addition, we have made some observationsof our own with tropical plants including Duriozibethinus (for which there have been conflictingcomments over its mycorrhizal status), Artocarpusand Nephelium spp. All of these turned out to havePans-type mycorrhizas with small arbuscules at-tached to very extensive intracellular hyphal coils(Smith etal, 1997).

There are many reports in the literature of absenceof arbuscules, or their presence in only limitednumbers, in Pam-type VA mycorrhizas (e.g.Boullard, 1953a. 6; Alexander, 1988; see also Smith& Smith, 1996). This obvioush- renders the defin-ition of such mycorrhizas rather hazardous in bothstructural and functional terms if it is assumed thatarbuscules are the sole basis of the mutualisticsymbiosis. Apparent absence of arbuscules might bea result of seasonal effects or environmental stress(Brundrett & Kendrick, 1990fl; Yawney & Schultz,1990; Mullen & Schmidt, 1993). The formation ofarbuscuJes in Amencan ginseng {Panax quinque-folius) has been shown to depend on the season butalso differs greatly among combinations of farms andplant age-classes, apparently reflecting the character-istics of individual seed-beds (Whitbread et al.,1996).

II. POSSIBLE FUNCTIONAL IMPLICATIONS

Our own interest in diversity in VA mycorrhizasarose from considerations of differences in 'mycor-rhizal efficiency'-i.e. the variation in nutritionalbenefits and costs to the plant that are associatedwith differences in amounts of inorganic nutrientssuch as P or Zn transferred to the plant in return fororganic carbon (e.g. sugar) transferred to the fungus.We suggested (Smith & Smith, 1996) that thephysiological basis of the symbiosis might be relatedto the structural features summarized above. Pre-viously, it has been widely assumed that bidirectionaltransfer of inorganic nutrients and organic C occurssolely across arbuscules. Indeed, in their taxonomicrevision of the Glomales, Morton & Benny (1990)took this assumedly unique role of the arbuscules asa fundamental feature of the Order. As we pointedout (Smith & Smith, 1996), there is no firm evidenceto rule out other fungus-host interfaces as sites oftransfer in VA mycorrhizas. In other mycorrhizaswhich lack arbuscules (both ecto- and endo-mycorrhizas) other such interfaces must obviouslybe the sites of transfer. The dynamics and life-spanof Arum-type arbuscules have been measured inseveral studies (e.g. Cox & Tinker, 1976; Toth &Miller, 1984; Alexander et al., 1989 and referencestherein) but estimates of the surface areas of both thearbuscules and intraradical fungal hyphae in VAmycorrhizas generally are notably lacking. This is


loop

• -ap

Figure 2. For legend see opposite.


due to the technical problems in measuring them,and especially in determining longevity and activity.In experiments with Allium porrum, the relativesurface area of the intercellular interface with respectto that of the arbuscules increased with time andbecame the larger after about 8 wk of plant growth(Smith & Dickson, 1991; Smith et al., 1994). Therehave as yet been no attempts to make comparablemeasurements in Paris-types, an omission that wehope to rectify soon using the techniques developedpreviously (Smith & Dickson, 1991; Smith et al.,1994).

It has been suggested that in Arum-types such asAllium, P and possibly other inorganic nutrients aretransferred to the host across the arbuscular inter-face-as is generally accepted-and that the inter-cellular interface is a major route for transfer of sugarfrom host to fungus (Gianinazzi-Pearson et al.,19916). Spatial separation of transport would pro-vide a structural basis for differences in mycorrhiza!efficiency. In the absence of functional arbuscules, aVA mycorrhizal fungus cou!d still survive in theinterce!lular phase, essentia!!y as a parasite or'cheater' {sensu Soberon & Martinez del Rio, 1985).'Cheating' by the fungus-i.e. gaining organic car-bon without supp!ying P to its co-symbiont-wouldeither prevent a positive growth response by theplant or produce a negative response (Janos, 1985,1987). Obviously, if transfer of solutes occurredsolely across arbuscules, extensive growth of thefungus would not be possible when arbuscules arelacking or inactive. Evidence for the occurrence ofcheating by VA mycorrhizal fungi is reviewed bySmith & Smith (1996); see also Johnson, Graham &Smith (1997).

The experimental basis of our suggestion remainsslim, though there is extensive evidence for decreasesin numbers of arbuscules in ^rum-types undervarious contro!!ed environmental conditions includ-ing low light, high external P and sometimes low-temperature (see Smith & Smith, 1996). Moreimportant, however, are the 'myc~^' mutants of theArum-type plant Pisum, in which colonization occursbut functional arbuscules are not formed (Gianinazzi-Pearson et aL, 1991a; Gianinazzi-Pearson et al.,1994). In these cases the intercellular interface mustbe involved in obtaining organic C to supportfungal growth.

Clearly, our suggestion is not valid in the sameform in Paris-type mycorrhizas, because the ex-tensive intercellular interface is absent. However,

despite the lack of quantitative measurements ofsurface areas, there is no doubt whatsoever that theintracellular hyphal coils can be extremely extensivecompared with arbuscules, as shown by illustrationsin many publications (e.g. Brundrett & Kendrick,19906; Whitbread et al., 1996; Widden, 1996), andas we have found with our own observations (Smithet al., 1997). If there is spatial separation of transfer,the coils could be the site of transfer of organic C,with transfer of P across the localized arbuscularinterface. Cheating would again be possible ifarbuscules were absent or were inactive. As yet thereis no evidence for separation of transfer of P andorganic C in Paris-type VA mycorrhizas. If there isno separation of transfer the hyphal coils mighttotally take over the role of arbuscules when thelatter are absent or not functioning. This wouldmean that there is nothing physio!ogica!!y specialabout arbuscules, i.e. that they are not essentia! for afunctional Paris-type VA mycorrhiza. There isnothing novel about this suggestion. Possible in-volvement of hyphal coils in nutrient exchange hasbeen mentioned by several workers who have studiedPan*5-t\-pe mycorrhizas in autotrophic plants (e.g.Bonfante-Fasolo & Scannerini, 1977; Reinsvold &Brent Reeves, 1986; Louis, 1990; Whitbread et al.,1996) but this role has been ignored by most VAmycorrhizologists. Demuth & Weber (1990) andImhof & Weber (1997) suggested that Par(s-t\^pestructures and absence of arbuscules in the myco-heterotrophic plant Voyria (Gentianaceae) reflects a'structural incompatibility' in which the fungusobtains no organic C from the host. In this case,transfer of organic C and inorganic nutrients to theplant must involve the intracellular hvphal coils.

Our purpose in the present review is not again torehearse the detailed arguments for spatia! separationof nutrient transfer or to assess techniques by whichthe issue might be resolved (see Smith & Smith,1996). Here we consider the relative extent of thetwo classes of VA mycorrhizas, the validity andusefulness of this division, and its structural basis interms of growth of the roots and mycorrhizal fungi.

I I I . EXTENT OF THE TWO CLASSES IN THE

PLANT KINGDOM

1. Bryophytes and Pteridophytes

The absorbing organs of a wide range of lower landplants have long been known to be mycotrophic and

Figure 2. Assemblage of illustrations photocopied from Gailaud (J905), retaining the original numbers. 27:Allium sphaerocephalum {Arum-Xypt), longitudinal section. 28: A. sphaerocephalum, longitudinal section,showing passage cell and point of penetration. 31: Anemone nemorosa (Paris-type), longitudinal section. 21:Colchicum automnale, transverse section, showing point of penetration and hyphal swellings. 41: arbuscule ofArum maculatum. 42: 'compound' arbuscule of Sequoia gigantea {Paris-type). Abbreviations: ap, epidermis;as, hypodermis; pa, root-hair; c, passage cell; end, endodermis; 1, air-space; noy, nucleus; r, hyphal swellings;V, young vesicles (according to Gailaud).

378 F.A. Smith and S. E. Smith

Figure 3. Extended focus images usin^ laser scanning confocat microscopy, (a) Pam-type structures inthe cortex of Panax quinquefolius\ Z-reconstruction of 17 slices (2/(m between slices), {b) Arum-xypestructures in the cortex oi Allium porrum; Z-reconstruction of 14 optical slices (1 /im between slices). Sampleswere embedded in LR White resin and stained with Phloxine B. S. Dickson (unpublished) with thanks to L.Peterson, M. Farquhar & Y. Uetake.


these groups were studied by Janse (1897) andGallaud (1905), among many other early workers.Rayner (1927) and Harley (1969) gave good sum-maries of the early work, and Bonfante-Fasolo (1984)has reviewed more recent developmental aspects.Bryophytes are colonized by a range of fungalendophytes and previous uncertainties about thefungal taxa are now being addressed (see, forexample, Duekett & Read, 1995). VA mycorrhizal(Glomalean) fungi occur as endophytes in manybryophytes and they are very widespread inpteridophytes. Where the cells of the absorbingorgans have ready access to the soil en\ ironment, asin some thalloid structures lacking epidermal-typelayers, there can be direct penetration of externalhyphae between cells (i.e. formation of an inter-cellular phase) but in the intracellular phase ex-tensive aseptate hyphal coils are common, andarbuscules (where present) are intercalar\- ratherthan terminal on hyphae. A good example is thegametophyte of Phaeoceros (Brj'ophyta: Antho-cerophyta). which has been studied in detail byLigrone (1988); see also Stahl (1949). The prothalli(gametophytes) of different Lycopodium spp.(pteridophytes) show variation in ' mycorrhizal'structures (the absorbing organs are not roots!), asfirst shown by Treub (1884—89, cited and discussedby Rayner. 1927). Whereas L. cernuum had in-tracellular hyphae in the peripheral region, therewere intercellular hyphae in the central tissues. Inother species described by Treub the hyphae areentirely intracellular. Interestingly, the prothalli ofL. cernuum contain photosynthetic cells while thoseof the second group studied by Treub areachlorophyllous. A more recent investigation ofLycopodium by Duekett & Ligrone (1991) confirmedTreub's findings and extended them to the ultra-structural level. These examples aside, and allowingfor the simple anatomy of the absorbing organs,bryophytes and ' lower' pteridophytes (non-Filicales) mostly have VA structures that are Paris-types. However, absence of arbuscules seems quitecommon, as found for the thalloid hepatic Crypto-thallus by Pocock & Duekett (1984), for Lycopodiumby Duekett & Ligrone (1991) and for Psilotum(pteridophyte) by Peterson, Howarth & Whittier(1981); see also Janse (1897).

Both ^rwm-type and Paris-type VA mycorrhizalstructures have been recorded in roots of the Filicales(true ferns). Extensive Arum-type intercellularhyphae and arbuscules were first described inAngiopteris (Marattiaceae: Marattiales) by Janse(1987) and Gallaud (1905). This structure was laterconfirmed by Boullard (1958), who showed that incontrast Danaea (same family) forms the Pon's-type.The position in the Ophioglossales is also not clear-cut. Janse (1897) described intercellular hyphae in'Ophioderma' (Ophioglossum) but Gallaud (1905)included the mycorrhiza in Ophioglossum as a Paris-

type, stating that coils are absent but the hyphae arealways intracellular. Descriptions and illustrationsby Boullard (1958) show Paris-type features in-cluding coils, vesicles and the remnants of arbusculesin Ophioglossum and the related genus Botrychium.As far as we are aware, representatives of all familiesin the leptosporangiate Filicales that have beenexamined appear to have Paris-type structures (e.g.Boullard. 1958; Cooper, 1976; Berch & Kendrick,1982; see also Harley. 1969).

Last, and not least, Remy et al. (1994) have nowunequivocally demonstrated the presence ofarbuscules in the early Devonian fossil Aglaophyton,which shows features of both bryophytes andvascular plants. It would be ver\' interesting to knowif this plant was a Paris-or Arum-type: it ought to bepossible to detect the occurrence of intercellularhyphae or intracellular coils in the fossils. Thestructures described by Kidston & Lang (1921) fromthe same fossil fiora (Rhynie chert) included, as wellas vesicles, coiled intracellular hyphae, suggestingthat they were Parrs-types.

2. Gymnosperms

There have been many studies of VA mycorrhizas ing\-mnosperms. and in all cases except possibly onethey can be classified as Pam-types, irrespective ofwhether or not the investigators have used this term.Examples include Podocarpaceae: (Janse, 1897;Shibata, 1902; Gallaud. 1905; Bayhs. McNabb &Morrison, 1963); Taxaceae: (Prat. 1926; Strullu etal.. 1981); Taxodiaceae (Gallaud, 1905; Konoe,1957). Bonfante-Fasolo (1984) gives a general sur-vey. The possible exception is Ginkgo (Ginkgoaceae),in which Bonfante-Fasolo & Fontana (1985) found' rare' intercellular hyphae and vesicles and abundantintracellular hyphal coils and intercalary arbusculesin the inner cortex. Accordingly. Ginkgo shouldperhaps strictly be included in a 'near-Pam' or'Intermediate' class; it is certainly not an Arum-type. We note here that the presence of rareintercellular hyphae in other examples classified asParis-types might compromise the validity of theclassification. More such examples will occur below.The methodology of the investigation might be aproblem in that the presence of rare intercellularhyphae may be obscured by the dense intracellularcoils and missed altogether when root squashes areexamined, rather than sections. Also, standardstaining methods are not uniformly successful. Earlywôrkers, such as Janse (1897) and Gallaud (1905),and others including Bonfante-Fasolo & Fontana(1985) did not fall into these traps.

3. Angiosperms

Arum-type and Pans-type VA mycorrhizas arewidely scattered through both monocotyledonousand dicotyledonous families in the angiosperms.


Table 1. Family groupings of angiosperms having distinct Arum-type and Paris-type VA mycorrhizas andthose with both types and/or intermediate types

Paris-typesBoth types (B) and/orintermediate types (I)

Monocots

Dicots

Agavaceae (1)Âraceae* (5)'^^*' Liliaceae'

Alliaceae (X)^-^^-^^-Âsphodeiaceae (1)*Anthericaceae (1)^Convallariaceae (4Hyacinthaceae (4)^Hypoxidaceae (1)'Ruscaceae (1)^

Zingiberaceae (1)^

Alangiaceae (1)*Anacardiaceae (1)"Ascepiadaceae* (4)

2.14.34

Balsaminaceae (1)^Begoniaceae (1)^Boraginaceae (2)^Campanulaceae (1)^Combretaceae (1)'Compositae (5)^-^'Cucurbitaceae (2)'Êlaeocarpaceae (2)^Guttiferae (2)"'^''Malvaceae (5)"

Proteaceae (1)'Rosaceae QY-'^-^*-'^^Staphyleaceae (1)'Symplocaceae (1)^Thymeleaceae (1)^'Turneraceae (1)"Urticaceae (2)"Vitaceae (1)'

Burmanniaceae (1)Cannaceae (1)'Dioscoraceae (2)^'Heliconiaceae (1)'' Liiiaceae'

Colchicaceae (2)^Liiiaceae s. s. (1)Trilliaceae (3)^'^'Uvulariaceae (2)

Marantaceae (1)''Thisnniaceae (l)^**Triuridaceae (1)'Aceraceae (l)''i2-i*Annonaceae (1)"Araliaceae (2)''^*AristolocbiaceaeBombacaceae (2) ' 'Caricaceae (1)'Casuarinaceae (1)'Cecropiaceae (1)'Cornaceae (1)^^Cunoniaceae (1)^'Gentianaceae (7)

1.14.22.24.27.39

Grossulariaceae (1HamamelidaceaeHippocastanaceaeLecythidaceae (1)'

Loganiaceae (1)^^Magnoliaceae (2)^Malpighiaceae (1)'Melastomaceae (1)Moraceae (2)^*»Myrsinaceae (1)^Myrtaceae (I)^Polygalaceae (1)^*Rubiaceae* (6)^'^'"Sapindaceae (1)*"Saxifragaceae (1)^Theaceae (1)Ûlmaceae (ly-^"Umbelliferae (6)^'^Violaceae (1)^ »'

Araceae* (IP)'Gramineae (> 10)(B i)^'*.'"!*

Arecaceae (3) (B)''Pandanaceae (1) (I

Apocynaceae (14) (B,I)^'Âsclepiadaceae* (I)^"Burseraceae (1) (I)^ 'Caprifoliaceae(l) (I)^'*Euphorbiaceae (6) (B,I)*'Flacourtiaceae (1) (I)'Labiatae (7) {Bf-^'-^*Leguminosae

Caesalpinoideae (1) (I)'Mimosoideae (3) (B) ' -Papilionoideae (13) (B)

2.7.19.20.23

Meliaceae(l) (I)'-^^Menyanthaceae (2) (1) "Ranunculaceae (3) (B)^"Rubiaceae* (lA)'Rutaceae (6) (B,I)"'^'Scrophulariaceae (2) (B)'Soianaceae (4) (B)^''Sterculiaceae (2) {\f-'-^^Verbenaceae (5) ( B ) ' "

The system of Cronquist (1981)-see also Mabberley (]989)-has been used except for families within ' Liliaceae' [sensuCronquist), which are as given by Dahlgren et al. (1985). Key: (1, etc), number of genera recorded; (B), both typesrecorded; (I), intermediate characters (extensive coils and intercellular hypbae). Araceae* (etc) in two columns occurswhere there is a single record that differs from the majority; (IP) or (lA) indicates the minority record in the 'Both'category.

Superscripts: - etc = references, as follows. 'Janse (1897); ^Gallaud (1905); ^Mcluckie & Burges (1932);Êndrigkeit (1937); =Asai (1944); *Laycock (1945); ^Johnston (1949); ^McLennan (1958); "Nicolson (1959);1" Gerdemann (1965); "Was t i e ( l%5) ; 2 kessler (1966);^^ Redhead (l%8);^*Stelz(l%8);>^Mosse (1973);^* Hayman(1974); ' Kinden & Brown (1975); '« Saif (1977); '«Abbott & Robson (1978); '=» Holley & Peterson (1979); ' Nadarajah(1980); " G a y et al. (1982); ^^Carling & Brown (1982); '*Jacquelinet-Jeanmougin & Gianinazzi-Pearson (1983);2^Brundrett, Picbe & Peterson (1985); ^"Frankland & Harrison (1985); " Kuhn & Weber (1986); ^^McGee (1986);2»Brundrett & Kendrick (19906); ^"Brundrett et al. (1990); ^^McGee (1990); ^^Weber & Kramer (1994); ^^Tiemann,Demuth & Weber (1994o); ^*Tiemann, Demuth & Weber (19946); ''^Weber, Klahr & Marron-Heimbuch (1995);3«Untch & Wber (1996); "Widden (1996); « Whitbread et al. (1996); ^Hmhof & Weber (1997); *"Smith et ai (1997);" H . J. Hudson (pers. comm.); ^^L. Haugen & S. E. Smith (unpublished); *^B. Thomas & S. E. Smith (unpublished);*^P. O'Connor & F. A. Smith (unpublished). Other references to genera that have been widely studied (e.g. Allium andAcer) are given in tbe text.


Table 1 !ists families in each class, giving numbers ofgenera that have been studied in each family, andusing the classification by Cronquist (1981). In somecases the names in the early literature had to be up-dated, using Mabberley (1989) for this purpose.While it is not established that all species in onegenus are all within the same class, we have foundonly one case {Ranunculus) where different specieswithin a single genus appear to form VA mycorrhizasof both classes, and another {Zea) where there maybe major differences between cultivars. These arediscussed below. Table 1 relies heavily on the surveysby Janse (1897), Gailaud (1905), Johnston (1949)and Stelz (1968), with examples from other papers aslisted. Not all authors have used Gallaud's classi-fication, and we have placed families in the Arum-type and Paris-type classes on the basis of records ofpresence or absence of intercellular hyphae in thecortex; and in the latter class, presence of hyphalcoils.

Generally, a!l examples included have beenclaimed to be VA (or arbuscular) mycorrhizas by theauthors cited, except of course where the work wasdone before these terms were introduced. For-tunately, eariy workers usually included detailedillustrations which have helped confirm the basis ofthe classification. We have not been deterred byreports of total absence of arbuscules, since all suchcases in Table 1 (though not identified there)included statements of presence of vesicles (some-times 'rare') and hyphae that are mainh' aseptate.Some potentially useful lists have been excludedbecause, although they include plants with extensiveintracellular hyphae, they do not specify whetherintercellular hyphae are absent. Examples are sur-veys by Thapar & Khan (1973) of forest trees (bothgymnosperms and angiosperms) in India, and byLouis (1990) of coastal plants in Singapore. Asalready noted, Louis was conscious of the possiblefunctional implication of absence of arbuscules.

In many cases. Table 1 gives records for only onespecies or genus per family, which is a hazardousbasis for generalizing, but where difFerent workershave made examinations of the same species orgenera they have almost always come to the sameconclusion about structures. Examples to the con-trary are discussed below. Thus, classic Arum-typefamilies include Compositae and Malvaceae, whereasParis-type families include Aceraceae andGentianaceae. This list is not exhaustive, and it doesnot include a number of early surveys published inlanguages other than English that we have not seen.Nevertheless, it shows that Pan'^-types are indeedver^' common, as suggested by Brundrett & Kendrick(1990^.).

The Liliaceae-as defined by Cronquist-seems atfirst sight a particularly ' difficult' family, withrepresentatives of both classes (Table 1). It includesvariations of Paris-types that have distinctive in-

trace!!u!ar hyphal swel!ings ('bobbits'). These weredescribed in detai! by Wîdden (1996) in Clintoniaand Medeola. Rather sitni!ar features in Colchicumwere noted by Gailaud (1905), as shown in Figure 2.The sweUings are a consistent feature of these plants.The classification of liliaceous plants is currentlyunder review and the different structural classes canbe distributed quite neatly (bearing in mind thelimited numbers of genera surveyed) between thefamilies listed by Dahlgren, Clifford & Yeo (1985).This has been done in Table 1. Table 2 gives moredetails, and shows the distinct distribution withinthe Superorder Liliiflorae sensu Dahlgren et al.(1985), which includes taxa from outside theLiliaceae sensu Cronquist (1981). Ornithogalum(Hyacinthaceae) was described as an Arum-type byGailaud. A detailed study of O. umbellatum byBonfante-Fasolo & Scannerini (1977) showed ex-tensive intracellular hyphal coils in the outer cortexwith intercellular hyphae in the inner cortex. Thisdifference appears in other plants (see below).Extensive ramifications of intercellular h>'phae be-tween epidermis and cortex in Thysanotus(Anthericaceae) are another example of a variant inthe Arum-type class (McGee, 1988). Structuralvariation within Pan'j-type dicots is illustrated bythe presence of lobed intracellular hyphae in Linumcatharticum (illustrated in Gay et al., 1982).

Families with genera of both classes are also listedin Table 1 (last column: 'B"). Examples include theApocynaceae, Euphorbiaceae and Solanaceae (thislast being a favourite for experimenta! studies).Some plants contain Pans-type features (especiallyextensive hyphal coils) but also many intercellularhyphae: see Table 1: last column ' I ' . TheApocynaceae again includes genera in this category(Weber et aL, 1995). Obviously, as with the gym-nosperm Ginkgo, discussed above, there is a com-plication where rare interceUular hyphae have beenrecorded in roots that are otherwise distinctly Paris-type. Theobroma (cacao) is one such example(Laycock, 1945; Nadarajah, 1980). Gailaud (1905)wrestled with these issues when he found that someRanunculus spp. fell into the Paris class, whereasothers had Arum-type features. This appears to bethe sole example where species of one genus were putinto both classes by a single investigator. The mostcomplicated family is the Leguminosae, where thesituation is not clarified when it is divided into thedifferent sub-families.

The Gramineae are also complicated (Table 1)and we have not attempted to sort out distribution ofthe VA mycorrhizal classes into the graminaceoussub-families. Nicolson's (1959) survey of grasses inBritain suggested that Parrs-types are very common.Greny (1973) made a detailed anatomical-morphological study of several important membersof the Gramineae and concluded that Zea, Avena,Triticum, Hordeum, Lolium and Holcus all have


Table 2, Distribution of Arum-types and Paris-types within the Superorder Liliifforae sensu Dahlgren et al.(1985) if or simplicity, only names of genera are listed)

Arum-types Paris-types References

O. AsparagalesConvallariaceae*

Ruscaceae*AgavaceaeHypoxidaceae*Asphodelaceae*Anthericaceae*Hyacinthaceae*

Aliiaceae*O. Burmanniales

Thismiaceae

O. DioscoralesDioscoraceae

Trilliaceae*

O. Liliales

Liliaceae sensu stricto*Uvulariaceae*

ConfallariaMaianthemumPolygonatumSmilacinaRuscusAgaveCurculigoAloeAnthericumHy acinthoidesMuscariOrnithogalum

ScillaAllium

Gallaud (1905)Gallaud (19()5)Gallaud (1905)Brundrett & Kendrick (1990*)Gallaud (1905)Gallaud (1905)Janse(1897)Gallaud (1905)Gallaud (1905)Gallaud (1905)Gallaud (1905)Gallaud (1905), Bonfante-Fasolo &Scannerini (1977)

Gallaud (1905)Janse (1897); et multi alii

Thismia

TamusDioscoreaParisTrilliumMedeolaiColchicum-fWurmbeaErythroniumDisporum-fCiintoniafUvularia-f

Janse (1897)McLennan (1958)

Gallaud (1905)GaDaud (1905)Gallaud (1905)Brundrett & Kendrick (1990A)Widden (1996)Gallaud (1905)McGee(1986)Brundrett & Kendrick (19906)Janse (1897)Widden (1996)Girard (1985)

* Included in the Liliaceae sensu Cronquist (1981).•f Hypha! swellings: see text.

Arum-type mycorrhizas whereas Phleum.Alopecurus, Agrostis and Agropyrum have Paris-types. By contrast, Johnston (1949) described Zea ashaving Paris-type mycorrhizas. Although he did notrefer to Gallaud's classification, his survey of plantsin the West Indies split them on the basis of (a) thepresence of an extensive intercellular phase in theouter and inner cortex, or (b) the presence ofextensive intracellular hyphal coils in the cortex.Apart from the distinction between outer and innercortex, these are essentially the same as Gallaud'sdefinitions. Since the many other workers who haveused Zea have shown it to contain extensiveintercellular hyphae, this poses a problem, and itmust be emphasized that a number of families are inthe ' B ' category- in Table 1 as a result of Johnston'ssurvey of plants from the West Indies. Geographicalfactors aside, there may be no need to have doubtsabout Johnston's powers of observation, because anumber of investigators have noted that Zea hashyphal coils in the outer cortex (e.g. Winter, 1951;Meloh, 1963; Gerdemann, 1965; Greny, 1973;Kariya & Toth, 1981; Morton, 1985). Hence in thisease there might be plasticity, which might be

exhibited in different maize cultivars. Triticum andHordeum can also have extensive hyphal coils(Greny, 1973). Hyphal coils in the outer cortex occurin other genera, including tobacco (Hildebrand &Koch, 1936) and some legumes, including A/etircaôand Trifolium spp. (Abbott, 1982). They may reflectdifferences in cortical structure and function. Inaddition to formation in the outer cortex, hyphalcoils are frequently formed during penetration offungal hyphae through cells of hypodermes of bothArum-types and Pans-types, as shown by severalearly workers, including Gallaud (1905); see alsoSmith, Long & Smith (1989)-we were then inignorance of the earlier work. Hypodermes, thoughfrequently overlooked, are present in many plants(e.g. Peterson, 1988; Perutnalla, Peterson & Enstone,1990).

Weber and his collaborators have published avaluable series of papers that survey developmentof VA mycorrhizas in the Apocynaceae,Asclepiadaceae, Gentianaceae and Loganiaceae(Table 1). These families are all members of theOrder Gentianales. As already noted, the achloro-phyllous members of the Gentianaceae are classic


Pflrz5-types. However, the other families in theOrder include Arum-types, both types or inter-nnediates-the Apocynaceae contains all of these(Table 1; Weber et al., 1995). Weber and hiscolleagues have proposed that Pam-types are phylo-genetically more advanced than .^rwm-types, reflect-ing weakened fungal vigour in some hosts and hencean evolutionary tendency towards successful myco-heterotrophy (e.g. Imhof & Weber, 1997). Given thefrequency of Paris-types, and their dominance inlower plants, we are not convinced by this argument.

Much of the information in Tables 1 and 2 hasbeen obtained wjrh field-grown plants and henceplants of uncertain age. Preliminary results bySoderstrom et al. (1996) have suggested that up to18 d Petroselinum crispum (parsley) and Daucuscarota (carrot)-both in the Umbelliferae-displaysome ^rwm-type features, with Pans-type featurespredominating afterwards. These developmentalefTects deserve further study in relation to rootanatomy and the ageing and turn-over of individualfungal colonization units.

IV. IS THE DISTINCTION BETWEEN CL.'\SSES

We believe that the answer to this question lies in thecontext in which it is asked. Systematists who areinterested in structures other than reproductive onesmight question the usefulness of the classification ifit is blurred by the occurrence of intermediates or(especially) of taxa at family or genus level withrepresentatives of both classes. However, someproblems can be cleared up by revision of plant taxa,as with the 'old' Liliaceae, and it is even possiblethat distribution of VA mycorrhizal classes might behelpful where taxonomic characters include non-reproductive features, as with liliaceous plants(Dahlgren et al., 1985). Developmental changes-assuggested by Soderstrom et al. (1996) with parsleyand carrot-are another complication in this context.

If the interest lies in the development andph}'siology oi the symbiosis and (especially) anydifferentiation in function between the differentinterfaces, then the distinction might still be im-portant. This especially relates to whether structuraldifferences can be correlated with differences inmycorrhizal responsiveness (growth increases com-pared with non-mycorrhizal controls) and the wholequestion of cheating, as summarized above. Theissue is then not whether any given interface istotally absent, but whether limitations or changes inits surface area (or molecular activity) affect rates ofsalute transfer. The presence or absence ofarbuscules, at least, is a feature in which most VAmycorrhizologists ought to be interested. Obviously,environmental considerations must to be taken intoaccount in considering structural and functional

plasticity, given evidence for changes in colonizationrates, intraradical hyphae and numbers of arbusculesunder low light, high soil P, low temperature etc (seeSmith & Smith, 1996, for discussion). However,there is no evidence that the structural basis of theclasses is under environmental control.

V. THE STRUCTURAL B.ASIS

The distinction between the two VA mycorrhizalclasses and the occurrence of intermediates iscertainly important if features of roots (morpho-logical, physiological or both) are being sought thatmight promote the formation of one class or another.The simplest possibility is that ,4rwm-types occur inroots with large intercellular spaces within thecortex. This possibility was considered over-sirnpleby Gallaud (1905). For example, he pointed out thatthose Ophioglossaceae that have mycorrhizas fallingwithin the Paris class do so despite the presence ofintercellular spaces. Other Paris-types, such asVoyria (Imhof & Weber, 1997) and Colchicum (seeFig. 2) also have obvious intercellular spaces in theirroots and there can be few roots in w-hich intercellularspaces of one sort or another are completely absent,given the need for aeration. Nevertheless, Brundrett& Kendrick (1988, 19906) have proposed that ^»-wm-types are formed in roots which have continuouslongitudinal air-spaces within their cortices (or innercortices, where most intercellular hyphal growthoften occurs), thus allowing a pathway of lowphysical resistance for hyphal growth, comparedwith the intracellular pathway. This intercellularroute then gives the opportunity for rapid sequentialpenetration of cortical cells and grow-th of arbuscules,and intracellular vesicles, where present. The oc-currence of limited or discontinuous intercellularspaces in roots, or differences between outer andinner cortices, might account for the intermediateVA mycorrhizal structures.

Brundrett & Kendrick (1990^) demonstrated thatthe intracellular spread of colonization in Paris-typesw-as relatively slow when compared with spread inArum-type%. However, it is still not clear why, inParis-types, hyphae do not grow extensively betweenappressed root cell walls and along tortuous in-tercellular pathways. Perhaps these pathways arephysically and biochemically less favourable thansequential penetrations of cell walls, ln other words,differences in cell wall structure and modificationsproduced during fungal colonization might be im-portant (Bonfante-FasoJo & Fontana, 1985;Bonfante-Fasolo, 1988).

The structural basis of the classes proposed byBrundrett & Kendrick is based on few examples andneeds to be tested more rigorously with a widerrange of plants. Justin & Armstrong (1987) surveyedthe root structure and porosity of 91 plant species,


grown in non-mycorrhizal conditions, with the aimof assessing anatomical responses to flooding. Theirresults certainly showed quantitatively that even indrained soil there are large air-spaces in roots ofsome plants that form Arum-type mycorrhizas (e.g.Zea-particularly in the inner cortex) or that are fromArum-type families (e.g. Compositae: Table 1).However, the porosity of roots of Allium and otherputative Arum-types (e.g. Vicia and Lotus spp.) is nogreater than that of Pans-types such as Viola andmembers of the Umbelliferae (Justin & Armstrong,1987). What is required to put Brundrett andKendrick's proposal on a firmer foundation iscomparison of the (three-dimensional) intraradicaispread of the fungal hyphae with the developmentand distribution of intercellular spaces, as deter-mined by appropriate infiltration techniques, in awider range of Arum-type, Paris-type and inter-mediate plants. Intercellular spaces in roots havereceived little direct attention from most VA mycor-rhizologists and their distribution and extent canbecome obscured where root squashes or cross-sections are used to identify the presence of VAmycorrhizas.

If the formation of the individual classes of VAmycorrhiza depends primarily on the presence orabsence of cortical intercellular spaces, or indeed onany other anatomical property of the plant root, thenthe taxonomic issue is transferred immediately tothat of the value of root anatomy as a taxonomiccharacter. Certainly, it is not surprising that there ismuch consistency of root anatomy in individualgenera or families, especially where plants have notbeen bred for cultivation; i.e. for rapid growth. Itthen seems a truism that the formation of the twoclasses or intermediates between them is primarilyunder the genetic control of the host. We note againhere the seminal demonstrations of the formation of^rum-types or Paru-types when different hosts werecolonized by the one species or isolate of VAmycorrhizal fungi (Barrett, 1958; Gerdemann, 1965;Jacquelinet-Jeanmougin & Gianinazzi-Pearson,1983). Inevitably, however, there are complicationsand more questions to address.

VI. THE ROLE OF THE FUNGAL GENOME

Abbott (1982) compared the anatomy of tenGlomalean endophytes in the ^rwm-type Trifoliumsubterraneum. She showed that isolates diflfered withrespect to production of vesicles, hyphal branchingand diameter, etc, as found by others. Moreimportant in the present context, she found thatisolates of Gigaspora and Glomus formed extensive'loops' of intracellular hyphae in the outer cortexwith intercellular hyphae plus (intracellular)arbuscules in the inner cortex. Acaulospora wasdifferent in that it produced 'predominantly' in-

tracellular hyphae (including coils) throughout thecortex of T. subterraneum. Differences betweenfungal species or strains in (primarily) Arum-typesmight result from differences in their ability topenetrate the various cell types within the root.However, it is still not clear why some fungi prefer amore tortuous intracellular pathway when extensiveintercellular spaces are common. Demuth, Fors-treuter & Weber (1991) found differences in the sizeof hyphal coils and in the size and shapes ofarbuscules when species of Gentiana {Paris-type)were colonized by different isolates of Glomus andAcaulospora. We conclude that it is possible for thefungal genome to exert significant control on VAmycorrhizal structure at the Arum/Paris-type level.It seems unlikely that an individual fungal species orstrains can greatly affect the extent of intercellularspaces within the root. The amount of plasticity inhyphal structures that can be superimposed bygenomic variation in fungi as well as in hosts clearlyrequires more study with other host/fungus com-binations, and especially the quantification of therelative sizes of intracellular and intercellular inter-faces that can be produced by different fungi on theone plant species.

More subtle variation has been found by B.Soderstrom & S. Dickson (unpublished) in Petro-selinum (parsley), in which Glomus sp. (WUM 16)formed extensive coils and few arbuscules. Thereverse w as the case with G. mosseae. The distinctionwas not apparent in Daucus (carrot), again pointingto interactions betw een genomes of fungus and hostin determining structural features.

VII. PHYSIOLOGY REVISITED

The issue of whether the intercellular and intra-cellular environments are the more favourable forgrowth of the fungal endophyte is itnportant to theplant physiologist interested in VA mycorrhizas.Intuitively, an intracellular interface (whether a coilor arbuscule) seems a more favourable environmentfor nutrient transfer than an intercellular one. Eventhough the intracellular interface is topologically stillapoplastic, with modified cell walls between thefungal and plant plasma membranes, the latter aremuch more closely appressed than they are in anintercellular interface-especially one of compara-tively large volume. Intuition aside, however, thereis no reason to suspect that cortical intercellularspaces in roots are nutritionally unfavourable forgrowth of VA mycorrhizal fungi. Concentrations of40-50 mM hexose equivalents (20-25 mM sucrose)have been measured in cortical apoplasts of non-mycorrhizal roots of barley (Farrar, 1985) andRicinus (Chapleo & Hall, 1989). These concentra-tions were quite similar to the cytoplasmic concentra-tions. The condition that is necessary for sustainedfungal uptake of organic C in the cortical apoplast is

Structural diversity in VA mvcorrhiza 385

that the rate of release from cortical cel!s must keeppace with (or be increased by) funga! demand. Thereare at present too many unknowns to approach thisissue mathematica!!y. In addition, the intercellularphase might be more favourable for maintenance ofOg levels for fungal respiration. As already noted, thepresence or absence of hypodermes-which increasethe isolation of the cortical apoplast from the externa!(soil) environment-does not appear to be associatedwith the occurrence of the two classes.

Possible interrelationships between mycorrhiza!structures and function are well worth furtherinvestigation in mycoheterotrophic plants. Thosethat are VA mycorrhizal appear aH to have Paris-type mycorrhizas. Besides the Gentianaceae, ex-amples include Thismia spp. (Thismiaceae: some-times included in Burmanniaceae): see Table 1.Since VA mycoheterotrophic plants receive organicC via their fungal endophyte from an adjacent donorplant (rather than directly from soil) there must besignificant physiologica! differences from 'normal'VA mycorrhizal plants, at least at the leve! ofmembrane transport proteins and their operationalcontrol. There seem to be strong parallels instructure between the Pans-type VA mycorrhizas inheterotrophic gametophytes of Lycopodium, plantsof the Burmanniaceae and Gentianaceae and the(non-VA) mycorrhizas in orchids. The cells of thelast contain hyphal coils, as shown by Janse (1897)and many workers subsequently: representativeillustrations are in Smith & Read (1997). Althoughheterotrophic growth of orchids mostly depends ona supply of organic C from soil via the fungalhyphae, there can be transfer from an autotrophic'donor' plant via the hyphae. Control of mycorrhiza]structures by the plant is nicely shown by theformation of hyphal coils in orchids by fungi from anectomycorrhizal host (Zelmer & Currah, 1995).Since protocorms or roots of orchids seem to lacklarge intercellular spaces (as shown by illustrationsin Smith & Read, 1997), absence of an intercellularphase is not surprising if the reasoning applied aboveto VA mycorrhizas is again applied.

There can also be transfer of organic C betweenlinked autotrophic VA mycorrhizal plants of thesame or a different species: see Smith & Smith(1996). Despite previous uncertainties about thesignificance of amounts of organic C transferred andits form (Smith & Smith, 1996), the use of stableisotopes is now giving good evidence of significantnet transfer of organic C between ectomycorrhiza]plants at least (Simard et al., 1997). There is nothingyet to implicate the structural considerations in thisreview in transfer of solutes between linked VAmycorrhizal p!ants. Nevertheless, following thereasoning of Imhof & Weber (1997), it wou!d be niceto know if Par;s-type interfaces are better adaptedthan ^rum-type interfaces as sites for transfer oforganic C in autotrophic receiver p!ants

V I I I . C O N C L U S I O N S

This survey of the relative extent of Arum- andParis-type VA mycorrhizas has shown that the !atterare not rare and anomalous cases, as has beensometimes thought. They occur in a vast number ofwild plants, including woody ones in which it is noteasy to distinguish details of structures-as we foundwhen examining Duria, Nephelium and Artocarpus(Smith et al., 1997). In examples such as these,arbuscules can often be obscured by the densehyphal coils and vesicles can be rare or lacking,depending on the funga! endophyte and environ-mental conditions. Accordingly, some Pam-t\pesmay we!! have not have been recognized as VAmycorrhizas. There is now considerab!e scope forDNA 'finger-printing', to identify unknown funga!endophytes, especially in lower plants and in otherexamples where normal features used for identifica-tion-whether vesicles, arbuscules or both-are ab-sent. Increasing use of this technique to identifymycorrhizal fungi from plants collected from thefield can be anticipated.

Whether there are significant functional differ-ences between the various interfaces in the twoclasses remains to be seen. It is particularly im-portant to establish if the presence of extensiveintracellular hyphal coils in Pan'5-types can renderarbuscules unnecessary as sites for nutrient transfer.This would help explain the numerous reports ofabsence of arbuscuJes in this class. However, it ispossible that in at least some cases absence ofarbuscules only occurs in some phases of rootgrowth, as shown with an Alpine Ranunculus sp. byMullen & Schmidt (1993). This will be a problemwith surveys of field-grown material where the age ofthe roots is uncertain. Control of formation ofarbuscules by the host vis-a-vis the fungus is highlyrelevant to the vexed question of nomenclature (cf.Smith, 1995; Walker, 1995). If a so-called'arbuscular' mycorrhizal fungus can form a func-tional mycorrhiza without arbuscules, owing tocontrol solely exerted by the host (the emphasis isimportant) what is the best nomenclature to use-forfungus and symbiosis ? Perhaps we should startreferring to 'Glomalean mycorrhizas' to avoid allstructural and functional issues. In that case, it willcertainly be unwise to define the GJomales by thepresence of arbuscules, with an explicitly statedfunctional role for these structures in nutrientinterchange, as was done by Morton & Benny (1990).It is for this reason that we have not adopted' Glomalean mycorrhizas' throughout the presentreview. Another possibility-though difficult to pro-nounce at first sight-is "zygomycetous'or-simpler-'Z-mycorrhiza' (Trappe, 1987). Thisavoids all structural issues.

Less provocatively, we hope that this review willprompt renewed interest in the distribution of the


two classes between and within families and willawaken interest in comparative studies of structureand function. It would be useful if check-lists couldinclude structural details of the VA mycorrhizas. W esuggest that classifications of Arum-types and Paris-types, based on the presence or total absence ofintercellular hyphae in the cortex, and intermediatet\'pes (e.g. 'near-Pan',?'), based on limited or rareintercellular hyphae but extensive intracellular coilsin the inner cortex and (where present) intercalaryarbuscules are useful in this regard. Presence orabsence of arbuscules sbould certainly be recorded,along with presence or absence of vesicles. Werecognize that this may increase the work-load infuture studies of VA mycorrhizal diversity!

ACKNOWLEDGEMENTS

This review was commenced while F.A.S. was on StudyLeave in the Department of Soil Science, University ofAdelaide, and use of facilities there is gratefully ack-nowledged. It was inspired in large measure by amemorable visit by F. A. S. and S. E. S. to the laboratory ofLarry Peterson, University of Guelph, Canada. We thankLarry and his research group for their hospitality and help,including the assistance that they gave Sandy Dickson inproducing Figure 3. Carol Peterson deserves our thanksfor very valuable discussions about the occurrence,structure and function of hypodermes, and Paul Widdenkindly discussed with us his then unpublished findings.Peter Barlow helped point us towards publications aboutintercellular spaces, and Stephan Imhof alerted to us hisrecent work and to other papers by Professor H. C. Weberand associates that we nearly overlooked. We also thankValentin Furlan for providing us with a copy of Janse(1897), David Read for a very prolonged 'loan' of his copyof Gallaud (1905), John Conran for helping to sort out theLiliaceae for us, and Bengt Soderstrom for stimulatingdiscussions during his sabbatical visit to S.E.S.'s lab-oratory. Last, and certainly not least, a referee made somemost helpful suggestions that greatly improved themanuscript. Our experimental work is supported by theAustralian Research Council.

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Structural diversity in (vesicular)–arbuscular mycorrhizal symbioses