Where does all the carbon go? The missing sink

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  • New Phytologist

    (2002)

    153

    : 199211

    www.newphytologist.com

    199

    Forum

    Blackwell Science Ltd

    Commentary

    Pisolithus

    death of the pan-global super fungus

    1977 saw this author in his first undergraduate year it wasfairly uneventful, notable mainly as the year that ElvisPresley consumed his ultimate deep fried peanut butter andbanana sandwich, and Kilmarnock Football Club wasrelegated from the Scottish Premier League. Those interestedin the biology of

    Pisolithus

    may recall it also as the year thatD. H. Marxs oft-cited review, Tree host range and worlddistribution of the ectomycorrhizal fungus

    Pisolithus tinctorius

    ,was published. Based on literature citations, herbarium recordsand personal communications, Marx (1977) concludedthat

    P. tinctorius

    (Pers.) Coker and Couch occurred in 33countries on six continents and formed mycorrhizas withsome 51 tree species.

    P. tinctorius

    , it seemed, was somethingof a pan-global super fungus that might enhance forestproduction world-wide. Reasonable conclusions from theavailable information but, as recent work has revealed, it isnot quite that straightforward.

    P. tinctorius sensu lato

    represents a complex of species, and

    P. tinctorius sensu stricto

    is far more limited in both its host range and geographicaldistribution than was envisaged by Marx.

    The ease with which DNA sequence data can be

    compared between studies has facilitated rapid progress

    I encountered

    Pisolithus

    for the first time 10 years afterpublication of that review, and found myself an unwittingcontributor to the growing pan-global

    P. tinctorius

    myth. Asmany like me had done previously (and have done since), Iunquestioningly accepted that the

    Pisolithus

    isolate I hadreceived was

    P. tinctorius

    as described by Coker and Couch(1928). The paper published from this work indicates that

    P. tinctorius

    readily forms ECM with

    Eucalyptus pilularis

    andthat it obtains a considerable amount of recently fixed carbonfrom this host (Cairney

    et al.

    , 1989). To read between the linesof this paper is to believe that

    P. tinctorius

    occurs in Australiaand forms functionally compatible ECM with a

    Eucalyptus

    host.Not so, it turns out. The paper by Martin

    et al

    . (pp. 345357in this issue) confirms that a number of

    Pisolithus

    species existworldwide, that

    P. tinctorius

    does not occur in Australia andthat

    Eucalyptus

    spp. are not natural hosts of this taxon.

    Growing evidence for multiple

    Pisolithus

    species

    To be fair to those who have variously contributed in thearea, the writing has been on the wall for some time. Severalauthors described heterogeneity in basidiospore ornamenta-tion within

    Pisolithus

    collections (Grand, 1976; Kope &Fortin, 1990). Isolates from certain hosts were found to bepoorly compatible with other host taxa, notably

    Eucalyptus

    and

    Pinus

    (Burgess

    et al.

    , 1994), and some inter-isolate matingincompatibilities were identified (Kope & Fortin, 1990).Burgess

    et al

    . (1995) also separated a range of

    Pisolithus

    isolateson the basis of expressed polypeptide patterns and basidiosporeornamentation, emphasising the existence of considerablevariation. Together, these observations pointed to the like-lihood that not all assumed

    P. tinctorius

    were conspecific.However, the relatively limited scope of individual studies,along with the global distribution of the

    Pisolithus

    complex,served to reduce the impact of these observations.

    DNA-based analyses provided further convincing evidencefor multiple

    Pisolithus

    species, and the ease with which DNAsequence data can be compared between studies has facilitatedrapid progress. Anderson

    et al

    . (1998, 2002) separated threeputative species from Australian native sclerophyll forests byITS sequence comparison, two of which appeared to fit therecent descriptions of

    P. albus

    (M. C. Cooke & G. E. Massee)M. J. Priest

    nom. prov.

    and

    P. marmoratus

    (M. J. Berkeley)M. J. Priest

    nom. prov.

    (Bougher & Syme, 1998). Martin

    et al

    . (1998) proposed three phylogenetic

    Pisolithus

    speciesbased on combined ITS and IGS1 sequence comparisons ofbasidiome collections from Kenya. Several other groups haveused combined ITS-RFLP and isozyme (Sims

    et al.

    , 1999)or ITS sequence analyses (Gomes

    et al.

    , 2000; Dez

    et al.

    ,2001) to separate other isolates from Asia, North America,Europe and Australia into several phylogenetic groups.Furthermore, these studies alluded to possible host and/orecological specificity for certain of the putative

    Pisolithus

    species, and inferred that Australian and northern hemisphere

    Pisolithus

    have been disseminated globally via exotic eucalyptand pine plantations, respectively.

    How many species?

    The paper by Martin

    et al

    . confirms each of these observations.It further provides a singularly broad view of phylogeneticrelationships among

    Pisolithus

    collections from a range of foresttypes worldwide. ITS sequence data generated by several ofthe above investigations have been combined with animpressive array of 102 new ITS sequences to leave no doubt

    NPH_339.fm Page 199 Wednesday, January 9, 2002 11:40 AM

  • Commentary

    www.newphytologist.com

    New Phytologist

    (2002)

    153

    : 199211

    Forum200

    that

    P. tinctorius sensu lato

    comprises several species. Thequestion now is, how many? Martin

    et al

    . suggest 10 (11 if

    P. aurantioscabrosus

    is included). Delimiting species boundariesvia phylogenetic analysis is, of course, a subjective process,especially where based on data from only a single locus.According to Taylor

    et al

    . (2000), subjectivity can be reducedconsiderably by comparative analysis of data from two ormore loci. This, however, remains to be done for

    Pisolithus

    .For this reason, I believe that the species boundariesdescribed by Martin

    et al

    ., particularly in lineages AII andBI wherein isolates were from pine/oak and eucalypt/acaciahosts, respectively, must at present be regarded with a degreeof caution. Moreover, as Bruns (2001) has recently highlighted,even a lack of ITS sequence variation cannot be taken asunequivocal evidence of conspecificity. Inclusion of comparativedata from other loci, along with data from further

    Pisolithus

    populations, may thus alter these putative species boundariessignificantly.

    Using neighbour-joining analysis of ITS sequence datafor a limited number of

    Pisolithus

    isolates from central andeastern Australia, Anderson

    et al

    . (2002) observed two ter-minal groups that were equivalent to the species 7 (putative

    P. albus

    ) and 9 (putative

    P. microcarpus

    ) proposed by Martin

    et al

    . Anderson

    et al

    . (2002), however, considered that allprobably represented a single species (putative

    P. albus

    ),based largely on the absence of any clear difference in basid-iospore ornamantation/size between the two groups. Prelim-inary data from my lab (C. J. Hitchcock

    et al.

    , unpublished)indicate that isolates from these two groups can be separatedby polymorphisms in two short simple sequence repeat-richregions. It is not clear if these represent alleles that havebecome fixed within two species or simply reflect polymorph-isms within the population of a single species. Screening ofmore isolates and comparison of polymorphisms at furtheralleles will help to clarify this point. Detailed morphologicalcomparisons between the various isolates should also aid inthis respect. Indeed, mating incompatibility tests may ulti-mately be required to clarify boundaries between putativephylogenetic/morphological

    Pisolithus

    spp. With all of theabove comments in mind, there may be merit at this stage inadopting a more circumspect approach to species delimita-tion and assignment of putative names to isolates within themajor lineages than taken by either Anderson

    et al

    . (2002)or Martin

    et al

    . Perhaps simple reference to

    Pisolithus

    isolates according to their placement in the lineages (e.g.AI, BII) identified by Martin

    et al

    . may prevent unnecessaryconfusion and back-tracking at a later date.

    Final comments

    Regardless of the number of species that arise from furthermolecular and morphological analyses of

    Pisolithus

    collections,the data presented by Martin

    et al

    . represent an excellentresource that should be used by all concerned with the

    biology of

    Pisolithus

    . For the cost of obtaining an ITSsequence (these days not that much), we can place our isolateswithin the proposed lineages of the

    Pisolithus

    species complex.Not only will this allow better informed physiological andfunctional comparisons between isolates (and studies) but,by adding further ITS sequences to the databases, will increasethe available data. Placement of the sequence alignment on awebsite to allow direct downloading would be a good develop-ment and regularly updating the alignment to accommodatenew ITS sequences submitted to the databases would furtherenhance its value. With such a resource at hand, it should bepossible to start making sense of the many reports in theliterature of considerable physiological variation betweenisolates of

    P. tinctorius sensu lato

    (Chambers & Cairney, 1999).Martin

    et al

    . have clearly demonstrated that host preferenceof isolates is correlated with placement within the major

    Pisolithus

    lineages. The exciting process of investigatingecological adaptation and functional variation within andbetween the various

    Pisolithus

    lineages can now begin.

    John W. G. Cairney

    Mycorrhiza Research Group, Centre for Horticulture &Plant Sciences, Parramatta Campus, University of Western

    Sydney, Locked Bag 1797, PENRITHSOUTH DC NSW 1797, Australia

    (tel +61 29685 9903; fax +61 29685 9915;email j.cairney@uws.edu.au)

    References

    Anderson IC, Chambers SM, Cairney JWG. 1998.

    Molecular determination of genetic variation in

    Pisolithus

    isolates from a defined region in New South Wales, Australia.

    New Phytologist

    138

    : 151162.

    Anderson IC, Chambers SM, Cairney JWG. 2002.

    ITS-RFLP and ITS sequence diversity in

    Pisolithus

    from central and eastern Australia.

    Mycological Research

    (In press.)

    Bougher NL, Syme K. 1998.

    Fungi of Southeastern Australia

    . Perth, Australia: University of Western Australia Press.

    Bruns TD. 2001.

    ITS reality.

    Inoculum

    52

    : 23.

    Burgess T, Dell B, Malajczuk N. 1994.

    Variation in mycorrhizal development and growth stimulation by 20 Pisolithus isolates inoculated onto

    Eucalyptus grandis

    W.Hill ex Maiden.

    New Phytologist

    127

    : 731739.

    Burgess T, Malajczuk N, Dell B. 1995.

    Variation in

    Pisolithus

    based on basidiome and basidiospore morphology, culture characteristics and analysis of polypeptides using 1D SDS-PAGE.

    Mycological Research

    99

    : 113.

    Cairney JWG, Ashford AE, Allaway WG. 1989.

    Distribution of photosynthetically fixed carbon within root systems of

    Eucalyptus pilularis

    plants ectomycorrhizal with

    Pisolithus tinctorius

    .

    New Phytologist

    112

    : 495500.

    Chambers SM, Cairney JWG. 1999.

    Pisolithus

    . In: Cairney JWG, Chambers SM, eds.

    Ectomycorrhizal fungi: key genera in profile

    . Berlin, Germany: Springer-Verlag, 131.

    Coker WC, Couch JN. 1928.

    The Gasteromycetes of Eastern United

    NPH_339.fm Page 200 Wednesday, January 9, 2002 11:40 AM

  • Letters

    New Phytologist

    (2002)

    153

    : 199211

    www.newphytologist.com

    Forum 201

    States and Canada

    . Chapel Hill, NC, USA: University of North Carolina Press.

    Dez J, Anta B, Manjn JL, Honrubia M. 2001.

    Genetic variation of

    Pisolithus

    isolates associated with native hosts and exotic eucalyptus in the western Mediterranean region.

    New Phytologist

    149

    : 577587.

    Gomes EA, de Arbeu LM, Borges AC, Arajo EF. 2000.

    ITS sequence and mitochondrial DNA polymorphism in

    Pisolithus

    isolates.

    Mycological Research

    104

    : 911918.

    Grand LF. 1976.

    Distribution, plant associates and variation in the basidiocarps of

    Pisolithus tinctorius

    in the United States.

    Mycologia

    68

    : 672678.

    Kope HH, Fortin JA. 1990.

    Germination and comparative morphology of basidiospores of

    Pisolithus arhizus

    .

    Mycologia

    82

    : 350357.

    Martin F, Delaruelle C, Ivory M. 1998.

    Genetic variability in intergenic spacers of ribosomal DNA in

    Pisolithus

    isolates associated with pine, eucalyptus and

    Afzelia

    in lowland Kenyan forests.

    New Phytologist

    139

    : 341352.

    Martin F, Dez J, Dell B, Delaruelle C. 2002.

    Phylogeography of the ectomycorrhizal

    Pisolithus

    species as inferred from nuclear ribosomal DNA ITS sequences.

    New Phytologist

    153

    : 345357.

    Marx DH. 1977.

    Tree host range and world distribution of the ectomycorrhizal fungus

    Pisolithus tinctorius

    .

    Canadian Journal of Microbiology

    23

    : 217223.Sims KP, Sen R, Watling R, Jeffries P. 1999. Species and population

    structures of Pisolithus and Scleroderma identified by combined phenotypic and genomic marker analysis. Mycological Research 103: 449458.

    Taylor JW, Jacobson DJ, Kroken S, Kasuga T, Geiser DM, Hibbett DS, Fisher MC. 2000. Phylogenetic species recognition and species concepts in fungi. Fungal Genetics and Biology 31: 2132.

    Key words: Pisolithus, Pisolithus tinctorius, ectomycorrhizas, forest production, phylogeography, nuclear ribosomal DNA ITS sequences.

    Letters

    LettersLetters

    Does zinc move apoplastically to the xylem in roots of Thlaspi caerulescens?Thlaspi caerulescens can accumulate very large amounts of zincin its tissues, which is of significant interest in commercialstrategies for obtaining plants able to remove Zn from con-taminated land phytoremediation (Chaney, 1993; Salt et al.,1998; Schat et al., 2000). An understanding of the mechanismscontrolling Zn entry into the root and the accumulation ofZn within the shoot of such hyperaccumulators can informboth genetic modification and conventional breeding strategiesto obtain plants with improved phytoremediation potential(Lasat & Kochian, 2000). However, at present these mechan-isms are not clear. Zinc may reach the xylem (and hence theshoot) either through the symplast or apoplast. Currenthypotheses suggest that all Zn reaches the xylem through asymplastic pathway and that hyperaccumulation in T. caerulescensis the result of enhanced unidirectional influx of Zn2+ into rootcells, coupled to a greater Zn efflux to the xylem. Here, twoarguments are presented that suggest that Zn movement tothe xylem cannot be solely symplastic when roots are exposedto high Zn concentrations in the rhizosphere ([Zn]ext). First, therate of delivery of Zn to the xylem may exceed Zn influx toroot cells. Second, Zn influx to root cells cannot supply sufficientZn for hyperaccumulation with the combination of relativegrowth rates and shoot : root ratios observed in T. caerulescens.

    Zinc hyperaccumulation

    A Zn hyperaccumulator is defined as a plant with a shootZn content (tissue concentration) in excess of 10 mg Zn g- 1

    d. wt when growing in its natural habitat (Baker & Brooks,1989). They appear to have unusually active mechanismsfor Zn uptake and translocation to the shoot, as well as theability to detoxify excessive Zn2+ within the shoot. ElevenZn hyperaccumulators have been recorded, of which Thlaspicaerulescens is the most studied (Baker et al., 1994; Brooks,1998; Reeves & Baker, 2000; Broadley et al., 2001). Thi...