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DOI 10.1007/s00572-005-0033-6
REVIEW
Received: 22 June 2005 / Accepted: 15 December 2005 / Published online: 6 May 2006
# Springer-Verlag 2006
Abstract A survey of 659 papers mostly published since plants (Pirozynski and Malloch 1975; Malloch et al. 1980;
1987 was conducted to compile a checklist of mycorrhizal Harley and Harley 1987; Trappe 1987; Selosse and Le Tacon
occurrence among 3,617 species (263 families) of land 1998; Read et al. 2000; Brundrett 2002). Since Nägeli first
plants. A plant phylogeny was then used to map the my- described them in 1842 (see Koide and Mosse 2004), only a
corrhizal information to examine evolutionary patterns. Sev- few major surveys have been conducted on their phyloge-
eral findings from this survey enhance our understanding of netic distribution in various groups of land plants either by
the roles of mycorrhizas in the origin and subsequent diver- retrieving information from literature or through direct ob-
sification of land plants. First, 80 and 92% of surveyed land servation (Trappe 1987; Harley and Harley 1987; Newman
plant species and families are mycorrhizal. Second, arbus- and Reddell 1987). Trappe (1987) gathered information on
cular mycorrhiza (AM) is the predominant and ancestral type the presence and absence of mycorrhizas in 6,507 species of
of mycorrhiza in land plants. Its occurrence in a vast majority angiosperms investigated in previous studies and mapped the
of land plants and early-diverging lineages of liverworts phylogenetic distribution of mycorrhizas using the classifi-
suggests that the origin of AM probably coincided with the cation system by Cronquist (1981). He found that 82% of the
origin of land plants. Third, ectomycorrhiza (ECM) and its species were mycorrhizal. From the occurrence of various
derived types independently evolved from AM many times types of mycorrhizas in different subclasses and orders of
through parallel evolution. Coevolution between plant and angiosperms, he further inferred that the ancestral type was
fungal partners in ECM and its derived types has probably glomeromycetous (the original word “zygomycotous” is not
contributed to diversification of both plant hosts and fungal used because fungi forming this type of mycorrhiza are now
symbionts. Fourth, mycoheterotrophy and loss of the mycor- placed in the new phylum Glomeromycota, see Schussler et
rhizal condition also evolved many times independently in al. 2001) mycorrhiza, and ascomycetous and basidiomyce-
land plants through parallel evolution. tous mycorrhizas belong to the derived types, and that evo-
lution of mycorrhizas in plants had progressed from obligate
Keywords Mycorrhizas . Land plants . Fungi . to facultative mycorrhizas and ultimately to nonmycorrhizas.
Parallel evolution In the same year, Harley and Harley (1987) published a
checklist of the mycorrhizal status of 144 families of vascular
plants in the British flora, documenting various types of
Introduction mycorrhizas in an entire flora for the first time. More re-
cently, Gemma et al. (1992) and Zhao (2000) investigated the
Mycorrhizas, dual organs of absorption formed when sym- mycorrhizal status of 89 and 256 species of pteridophytes in
biotic fungi inhabit healthy tissues of most terrestrial plants Hawaii and Yunnan, China, respectively. They found that the
(Trappe 1996), have widespread occurrence among land percentages of mycorrhizal species in pteridophytes (74 and
plants and are increasingly believed to have played an im- 33%, respectively) were lower than in angiosperms as
portant role in the successful colonization of the land by reported by Trappe (1987). Whether bryophytes have mycor-
rhizas or not is still a debatable issue, but many liverworts
and hornworts have fungal associations (Read et al. 2000). In
B. Wang . Y.-L. Qiu (*) two surveys of British liverworts, Pocock and Duckett
Department of Ecology and Evolutionary Biology, (1985) and Duckett et al. (1991) reported that among the 206
The University Herbarium, University of Michigan, and 284 examined species, respectively, 16% contained
830 N. University Avenue, Ann Arbor, MI 48109-1048, USA
e-mail: ylqiu@umich.edu fungal endophytes in their rhizoids or thalli.
Tel.: +1-734-7648279 Mycorrhizal research has advanced at an astonishing pace
Fax: +1-734-7630544 over the last two decades due to a recent surge of interest in
300
the subject by botanists, mycologists, and ecologists. A large The information in Table 1 was then mapped onto a land
number of new reports on mycorrhizal occurrence in land plant phylogeny drawn according to a multigene analysis of
plants, especially in pteridophytes and liverworts, have been nonflowering land plants (Qiu et al. unpublished) and the
published since the surveys by Trappe (1987) and Harley and angiosperm classification system proposed by Stevens
Harley (1987). During the same period, our understanding of (2004). Family was used as the unit of reconstruction (i.e.,
the land plant phylogeny was greatly improved through terminal node) in this phylogeny. For each family, the
major efforts by molecular systematists. An explicit phylo- percentages of obligate, facultative, and nonmycorrhizal
genetic classification system of angiosperms is now available species, and the percentage of each type of mycorrhizas
(Stevens 2004), and a nonflowering land plant phylogeny among all mycorrhizal species were calculated and plotted
will be published soon (Qiu et al. unpublished data). Hence, onto the land plant phylogeny.
reviewing mycorrhizal occurrence in land plants and map- One major improvement of this review over those by
ping this information onto the newly available plant Trappe (1987) and Harley and Harley (1987) is the use of a
phylogeny will update our knowledge on mycorrhizal abun- rigorously reconstructed land plant phylogeny to map the
dance in plants, facilitate examination of the origin and mycorrhizal information down to the family level for a
evolutionary pattern of mycorrhizal symbiosis in land plants, worldwide coverage. Trappe (1987) covered only angio-
and enhance our understanding of this important biological sperms, whereas Harley and Harley (1987) surveyed only the
interaction and its impact on evolution of both plants and British vascular flora. Cronquist’s (1981) classification sys-
fungi. Areas that require further study, especially the taxa that tem of angiosperms used by Trappe (1987) has been signif-
occupy critical positions in the land plant phylogeny and for icantly revised by molecular systematists (Soltis et al. 2000;
which mycorrhizal information is still lacking, can also be Stevens 2004). Another major improvement is that informa-
identified through these efforts. tion on mycorrhizal occurrence, more precisely fungal asso-
ciation in bryophytes, is included for the first time. Hence,
this review should allow a thorough examination of origin
Materials and methods and evolution of mycorrhizal symbiosis in land plants.
Vulpia ciliata ssp. ambigua AM 110 Persea americana AM 41, 250, 326,
Zea mays AM 123 609
Zoysia japonica AM 326 Phoebe lanceolata AM 422
Commelinaceae Aristolochiaceae
Amischotolype hispida AM 655 Asarum europaeum AM + NM 260, 261
Commelina communis AM 294 Piperaceae
NM 643 Peperomia hesperomannii AM 326
Commelina aff. erecta AM 143 Peperomia membranacea AM 326
Musaceae Piper longum AM 422, 655
Musa acuminata AM 163 Piper nigrum AM 578
Heliconiaceae Piper sarmentosum AM 422
Heliconia psittacorum AM 510 Piper sp. NM 422
Cannaceae Papaveraceae
Canna coccinea NM 510 Chelidonium majus NM 260, 261
Zingiberaceae Macleaya cordata AM 343
Alpinia conchigera AM 655 Papaver rhoeas AM + NM 260, 261
Amomum villosum AM 422 Papaver somniferum NM 260, 261
Costus speciosus AM 422 Menispermaceae
Paramomum petaloideum AM 655 Cocculus trilobus AM 326
Renealmia guianensis AM 510 Berberidaceae
Costaceae Berberis buxifolia AM 207
Costus scaber AM 510 Berberis darwinii NM 207
Costus spiralis var. spiralis AM 510 Berberis vulgaris AM 260, 261
Myristicaceae Mahonia aquifolium AM 260, 261
Horsfieldia pandurifolia AM 655 Podophyllum peltatum AM 410, 621
Horsfieldia tetratepala AM 422 Ranunculaceae
Myristica yunnanensis AM 655 Aconitum delphinifolium AM 594
Pycnanthus angolensis AM 445 Aconitum napellus AM + NM 260, 261
Staudtia kamerunensis AM 445 Actea spicata AM + NM 260, 261
Magnoliaceae Anemone nemorosa AM + NM 260, 261
Liriodendron tulipifera AM 362, 470 Anemone ranunculoides AM 260, 261
Magnolia henryi AM 422, 655 Anemone vulgaris AM 260, 261
Talauma ovata NM 548 Batrachium circinatum NM 62
Annonaceae Batrachium peltatum NM 62
Annona cherimola AM 42 Caltha palustris NM 62
Enantia chlorantha AM 445 AM + NM 260, 261
Goniothalamus griffithii AM 422, 655 Clematis stans AM 636
Hexalobus crispiflorus AM 445 Clematis vitalba AM 368
Mitrephora calcarea AM 655 AM + ECM 260, 261
Pseuduvaria indochinensis NM 655 Consolida ambigua AM 260, 261
Lauraceae Corydalis lutea NM 260, 261
Beilschmiedia pendula AM 356, 357 Corydalis solida NM 260, 261
Cryptocarya angulata AM 222 Fumaria officinalis AM + NM 260, 261
Cryptocarya mackinnoniana AM 222 Helleborus foetidus AM 260, 261
Cryptocarya yunnanensis AM 422 Myosurus minimus AM 260, 261
Laurus nobilis AM 368, 603 Pulsatilla patens AM 408
Lindera benzoin AM 140 Pulsatilla pratensis AM 408
Litsea dileniifolia AM 655 Pulsatilla vulgaris AM + NM 260, 261
Litsea liyuyingi AM 655 Ranunculus acris AM 194, 456, 586,
Nectandra rigida AM 31 260, 261
Ocotea indecora AM 651 Ranunculus acris AM 503
Ocotea puberula AM 651 ssp. pumilus
Ranunculus adoneus AM 416, 519
319
Table 1 (continued) Table 1 (continued)
Examined speciesa Mycorrhizal References Examined speciesa Mycorrhizal References
statusb,c statusb,c
Anagallis tenella AM 260, 261 Arbutus unedo ABM 200, 238, 421,
Asterolinum stellatum AM 472 368, 472, 260,
Cyclamen hederifolium AM 260, 261 261
Glaux maritima AM 260, 261 Arctostaphylos alpinus ABM 594
Hottonia palustris AM + NM 260, 261 ERM 260, 261
Lysimachia japonica AM 643 Arctostaphylos uva-ursi ABM 259, 507
Lysimachia nemorum AM + NM 260, 261 M(endo) + ERM + 260, 261
Lysimachia nummularia AM + NM 260, 261 ABM + ECM +
Lysimachia terrestris AM 140 EEM
AM + NM 260, 261 Calluna vulgaris ERM 72, 238, 299,
Lysimachia thyrsiflora NM 62 260, 261
AM + NM 260, 261 Cassiope tetragona ERM 594
Lysimachia vulgaris AM 368 Cavendishia capitulata ERM 474
AM + NM 260, 261 Cavendishia melastomoides ERM 474
Primula elatior AM 260, 261 Daboecia cantabrica ERM 260, 261
Primula farinosa AM 260, 261 Disterigma humboldtii ERM 474
Primula veris AM + NM 260, 261 Empetrum nigrum ERM 594, 260, 261
Primula vulgaris AM 260, 261 Erica arborea ERM 368
Samolus valerandi AM 368, 260, 261 Erica cinerea ERM 99, 260, 261
Trientalis europaea AM 501 Erica erigena ERM 260, 261
AM + NM 260, 261 Erica mackaiana ERM 260, 261
Myrsinaceae Erica multiflora ERM 472
Ardisia crenata AM 87 Erica tetralix ERM 260, 261
Ardisia tenera AM 422, 655 Erica vagans ERM 260, 261
Measa indica AM 422 Gaultheria erecta ERM 474
Myrsine alyxifolia AM 326 Gaultheria procumbens ERM 238
Rapanea ferruginea AM 31 Gaultheria shallon ERM 22, 639
Styracaceae Gonocalyx costaricense ERM 474
Strichinus brasiliensis AM 651 Kalmia latifolia ERM 238
Diapensiaceae Ledum palustre ERM 260, 261
Diapensia lapponica ERM 260, 261 Ledum palustre ERM 594
Lecythidaceae ssp. decumbens
Barringtonia macrostachya AM 655 Ledum palustre ERM 594
Barringtonia racemosa AM 655 ssp. groenlandicum
Cariniana estrellensis AM 651 Leucopogon parviflorus ERM 401
Sapotaceae Leucothoe fontanesiana ERM 238
Aningeria adolfi-friedericii AM 637, 638 Loiseleuria procumbens ERM 594, 260, 261
Aningeria robusta AM 445 Oxydendrum arboreum ERM 238
Argania spinosa AM 434 Pernettya mucronata ERM 207
Autranella congolensis AM 445 Phyllodoce caerulea ERM 260, 261
Baillonella toxisperma AM 445 Pieris floribunda ERM 238, 555
Gambeya africana AM 445 Rhododendron ERM 154
Omphalocarpum procerum AM 445 brachycarpum
Palaquium gutta AM 568 Rhododendron ERM 238
Actinidiaceae calendulaceum
Actinidia deliciosa AM 523 Rhododendron ERM 238
Clethraceae carolinianum
Clethra barbinervis AM 335 Rhododendron catawbiense ERM 238
Ericaceae Rhododendron maximum ERM 238
Andromeda polifolia ERM 260, 261 Rhododendron ERM 238
Arbutus menziesii ABM 374 mucronulatum
ECM 375 Rhododendron obtusum ERM 601
323
Table 1 (continued) Table 1 (continued)
Examined speciesa Mycorrhizal References Examined speciesa Mycorrhizal References
statusb,c statusb,c
264. Hartnett DC, Samenus RJ, Fischer LE, Hetrick BAD (1994) 298. Jin L, Gu YJ, Xiao M, Chen JK, Li B (2004) Funct Plant Biol
Oecologia 99:21–26 31:979–986
265. Haskins KE, Gehring CA (2004) Ecology 85:2687–2692 299. Johansson M (2000) Oecologia 123:418–424
266. Haug I, Lempe J, Homeier J, Weiss M, Setaro S, Oberwinkler 300. Johnson NC (1998) J Appl Ecol 35:86–94
F, Kottke I (2004) Can J Bot 82:340–356 301. Johnson-Green PC, Kenkel NC, Booth T (2001) Mycol Res
267. Haug I, Weber R, Oberwinkler F, Tschen J (1991) New Phytol 105:1094–1100
117:25–35 302. Johnson-Green PC, Kenkel NC, Booth T (1995) Can J Bot
268. He XL, Mouratov S, Steinberger Y (2002) J Arid Environ 73:1318–1327
52:379–387 303. Jones MD, Durall DM, Harniman SMK, Classen DC,
269. Heijne B, Dueck TA, van der Eerden LJ, Heil GW (1994) Simard SW (1997) Can J For Res 27:1872–1889
New Phytol 127:685–696 304. Jurkiewiez A, Turnau K, Mesjasz-Przybylowicz J, Przybylowicz
270. Heijne B, vanDam D, Heil GW, Bobbink R (1996) Plant Soil W, Godzik B (2001) Protoplasma 218:117–124
179:197–206 305. Kapoor R, Giri B, Mukerji KG (2004) Bioresource Technol
271. Helm DJ, Allen EB, Trappe JM (1996) Can J Bot 74:1496–1506 93:307–311
272. Hepper CM, Azcón-Aguilar C, Rosendahl S, Sen R (1988) 306. Karagiannidis N, Nikolaou N (2000) Am J Enol Viticult
New Phytol 110:207–215 51:269–275
273. Hernández G, Cuenca G, García A (2000) Biol Fert Soils 307. Kasowska D (2002) Acta Soc Bot Pol 71:155–161
31:232–236 308. Kasuya MCM, Igarashi T (1996) Mycorrhiza 6:451–454
274. Hetrick BAD, Hartnett DC, Wilson GWT, Gibson DJ (1994) 309. Kawai M (1997) Mycologia 89:228–232
Can J Bot 72:168–176 310. Kaya C, Higgs D, Kirnak H, Tas I (2003) Plant Soil
275. Hetrick BAD, Wilson GWT, Figge DAH (1994) Environ Pollut 253:287–292
86:171–179 311. Kemery RD, Dana MN (1995) Hortscience 30:1015–1016
276. Hetrick BAD, Wilson GWT, Schwab AP (1994) Can J Bot 312. Kemp E, Adam P, Ashford AE (2003) Plant Soil 250:241–248
72:1002–1008 313. Kernaghan G, Berch S, Carter R (1995) Can J For Res
277. Hildebrandt U, Janetta K, Ouziad F, Renne B, Nawrath K, 25:891–901
Bothe H (2001) Mycorrhiza 10:175–183 314. Kernaghan G, Currah RS, Bayer RJ (1997) Can J Bot
278. Hoefnagels MH, Broome SW, Shafer SR (1993) Estuaries 75:1843–1850
16:851–858 315. Khade SW, Rodrigues BF (2003) J Trop Forest Sci 15:320–331
279. Hood LA, Swaine MD, Mason PA (2004) J Ecol 92:816–823 316. Khan AG (1993) Mycorrhiza 3:31–38
280. Horton TR, Bruns TD (1998) New Phytol 139:331–339 317. Khan AG (2001) Environ Int 26:417–423
281. Horton TR, Cázares E, Bruns TD (1998) Mycorrhiza 8:11–18 318. Khan AG, Chaudhry TM, Hayes WJ, Khoo CS, Hill L,
282. Huat OK, Awang K, Hashim A, Majid NM (2002) Forest Ecol Fernandez R, Gallardo P (1998) Water Air Soil Poll 104:389–402
Manag 158:51–58 319. Khan AH, Islam A, Islam R, Begum S, Huq SMI (1988) J Plant
283. Hume LJ, August JA (1988) New Zeal J Agr Res 31:331–338 Physiol 133:84–88
284. Hurd TM, Schwintzer CR (1997) Physiol Plantarum 99:680–689 320. Kieliszewska-Rokicka B, Rudawska M, Leski T (1997)
285. Husted L, Lavender DP (1989) Ann Sci Forest 46:S750–S753 Environ Pollut 98:315–324
286. Huynh TT, McLean CB, Coates F, Lawrie AC (2004) 321. Kiers ET, Lovelock CE, Krueger EL, Herre EA (2000)
Aust J Bot 52:231–241 Ecol Lett 3:106–113
287. Ikombo BM, Edwards DG, Asher CJ (1991) Aust J Agr Res 322. Koide RT, Landherr LL, Besmer YL, Detweiler JM,
42:129–138 Holcomb EJ (1999) Hortscience 34:1217–1220
288. Ikram A, Jensen ES, Jakobsen I (1994). Soil Biol Biochem 323. Kong FX, Zhou CL, Liu Y (1998) Chemosphere 37:179–187
26:1541–1547 324. Koske RE, Gemma JN (1997) Am J Bot 84:118–130
289. Ikram A, Mahmud AW, Chong K, Faizah AW (1993) 325. Koske RE, Gemma JN, Englander L (1990) Am J Bot 77:64–68
Field Crop Res 31:131–144 326. Koske RE, Gemma JN, Flynn T (1992) Am J Bot 79:853–862
290. Imhof S (1999) Can J Bot 77:637–643 327. Kothari SK, Singh UB (1996) Plant Soil 178:231–237
291. Imhof S (2003) Mycorrhiza 13:327–332 328. Kottke I, Beiter A, Weiss M, Haug I, Oberwinkler F, Nebel M
292. Imhof S, Weber HC (2000) Symbiosis 29:201–211 (2003) Mycol Res 107:957–968
293. Ingham ER, Wilson MV (1999) Mycorrhiza 9:233–235 329. Kovács GM, Kottke I, Oberwinkler F (2003) Plant Biol 5:574–580
294. Ishii T, Matsumoto I, Shrestha YH, Wamocho LS, Kadoya K 330. Kovács GM, Vagvolgyi C, Oberwinkler F (2003)
(1998) J Jpn Soc Hortic Sci 67:556–558 Folia Microbiol 48:369–378
295. Ishii T, Narutaki A, Sawada K, Aikawa J, Matsumoto I, 331. Kowalchuk GA, de Souza FA, van Veen JA (2002) Mol Ecol
Kadoya K (1997) Plant Soil 196:301–304 11:571–581
296. Jacobson KM, Jacobson PJ, Miller OK (1993) Mycorrhiza 332. Kretzer AM, Bidartondo MI, Grubisha LC, Spatafora JW,
3:13–17 Szaro TM, Bruns TD (2000) Am J Bot 87:1778–1782
297. Jayachandran K, Shetty KG (2003) Aquat Bot 76:281–290 333. Kristiansen KA, Freudenstein JV, Rasmussen FN, Rasmussen
HN (2004) Mol Phylogenet Evol 33:251–258
348
Table 1 (continued) Table 1 (continued)
334. Kristiansen KA, Taylor DL, Kjøller R, Rasmussen HN, 372. Marques MS, Pagano M, Scotti M (2001) Agroforestry Syst
Rosendahl S (2001) Mol Ecol 10:2089–2093 52:107–117
335. Kubota M, McGonigle TP, Hyakumachi M (2001) Can J Bot 373. Martin J, Bereau M, Louisanna E, Ocampo JA (2001)
79:300–306 Symbiosis 31:283–291
336. Kulkarni SS, Raviraja NS, Sridhar KR (1997) J Coastal Res 374. Massicotte HB, Melville LH, Molina R, Peterson RL (1993)
13:931–936 Mycorrhiza 3:1–11
337. Kumaran S, Azizah HC (1995) Trop Agr 72:39–43 375. Massicotte HB, Molina R, Tackaberry LE, Smith JE,
338. Landhäusser SM, Muhsin TM, Zwiazek JJ (2002) Can J Bot Amaranthus MP (1999) Can J Bot 77:1053–1076
80:684–689 376. Masuhara G, Katsuya K (1992) Bot Mag Tokyo 105:453–460
339. Lansac AR, Marín A, Roldán A (1995) Arid Soil Res Rehab 377. Mathew J, Johari BN (1988) Curr Sci India 57:156–158
9:167–175 378. Mathur N, Vyas A (1995) J Plant Physiol 147:328–330
340. Lau TC, Lu X, Koide RT, Stephenson AG (1995) Plant Cell 379. Mathur N, Vyas A (1996) Natl Acad Sci Lett 19:1–3
Environ 18:169–177 380. Mathur N, Vyas A (1996) Bot Bull Acad Sinica 37:209–212
341. Launonen TM, Ashton DH, Keane PJ (1999) Plant Soil 381. Mathur N, Vyas A (2000) J Arid Environ 45:191–195
210:273–283 382. Matosevic I, Costa G, Giovannetti M (1997) Mycorrhiza 7:51–53
342. Laursen GA, Treu R, Seppelt RD, Stephenson SL (1997) 383. Matsubara Y, Harada T (1996) J Jpn Soc Hortic Sci 65:565–570
Arctic Alpine Res 29:483–491 384. Matsuda Y, Yamada A (2003) Mycologia 95:993–997
343. Li T, Li JP, Zhao ZW (2004) Mycorrhiza 14:323–327 385. Matthessears U, Neeser C, Larson DW (1992)
344. Ligrone R (1988) Bot Gaz 149:92–100 Ecography 15:262–266
345. Ligrone R, Duckett JG (1994) Ann Bot 73:577–586 386. McArthur DAJ, Knowles NR (1993) Plant Physiol 102:771–782
346. Ligrone R, Lopes C (1989) New Phytol 111:423–433 387. McGee PA (1990) Aust J Bot 38:583–592
347. Ligrone R, Pocock K, Duckett JG (1993) Can J Bot 71:666–679 388. McGee PA, Bullock S, Summerell BA (1999) Aust J Bot
348. Linderman RG, Davis EA (2003) Horttechnology 13:482–487 47:85–95
349. Linderman RG, Davis EA (2004) Horttechnology 14:196–202 389. McGee PA, Furby JH (1992) Aust J Bot 40:291–304
350. Linderman RG, Davis EA (2004) Sci Hortic 99:67–78 390. McGonigle TP, Hovius JP, Peterson RL (1999) Can J Bot
351. Lioi L, Giovannetti M (1987) Biol Fert Soils 4:193–197 77:1028–1034
352. Little LR, Maun MA (1996) J Ecol 84:1–7 391. McHugh JM, Dighton J (2004) Restor Ecol 12:533–545
353. López-Gutiérrez JC, Toro M, López-Hernández D (2004) 392. McKendrick SL, Leake JR, Taylor DL, Read DJ (2000)
Agr Ecosyst Environ 103:405–411 New Phytol 145:523–537
354. Loree MAJ, Williams SE (1987) New Phytol 106:735–744 393. McLean C, Lawrie AC (1996) Ann Bot 77:405–411
355. Louis I (1990) Mycologia 82:772–778 394. McLean CB, Anthony J, Collins RA, Steinke E, Lawrie AC
356. Lovelock CE, Kyllo D, Popp M, Isopp H, Virgo A, Winter K (1998) New Phytol 139:589–593
(1997) Aust J Plant Physiol 24:185–194 395. Meharg AA, Bailey J, Breadmore K, Nacnair MR (1994)
357. Lovelock CE, Kyllo D, Winter K (1996) Funct Ecol 10:662–667 Plant Soil 160:11–20
358. Lovera M, Cuenca G (1996) Mycorrhiza 6:111–118 396. Mendoza RE, Pagani EA (1997) J Plant Nutr 20:625–639
359. Lu XH, Malajczuk N, Dell B (1998) Mycorrhiza 8:81–86 397. Meney KA, Dixon KW, Scheltema M, Pate JS (1993)
360. Ludwig-Müller J, Bennett RN, García-Garrido JM, Piché Y, Aust J Bot 41:733–737
Vierheilig H (2002) J Plant Physiol 159:517–523 398. Merryweather J, Fitter A (1995) New Phytol 129:629–636
361. Lumini E, Bosco M, Puppi G, Isopi R, Frattegiani M, 399. Merryweather JW, Fitter AH (1998) Mycorrhiza 8:87–91
Buresti E, Favilli F (1994) Soil Biol Biochem 26:659–661 400. Michel-Rosales A, Valdés M (1996) Mycorrhiza 6:105–109
362. Lux HB, Cumming JR (2001) Can J For Res 31:694–702 401. Midgley DJ, Chambers SM, Cairney JWG (2004) Aust J Bot
363. MacFall JS, Iyer J, Slack S, Berbee J (1990) Agr Ecosyst 52:63–71
Environ 28:321–324 402. Miller RM, Smith CI, Jastrow JD, Bever JD (1999) Am J Bot
364. Maehara N, Kikuchi J, Futai K (1993) Can J Bot 71:1562–1567 86:547–553
365. Malajczuk N (1988) T Brit Mycol Soc 90:375–382 403. Miller SL, McClean TM, Stanton NL, Williams SE (1998)
366. Malcová R, Vosátka M, Albrechtová J (1998) Plant Soil Can J For Res 28:115–122
207:45–57 404. Miller SP (2000) New Phytol 145:145–155
367. Mamoun M, Olivier JM (1992) Plant Soil 139:265–273 405. Ming T, Hui C (1999) Trees-Struct Funct 14:113–115
368. Maremmani A, Bedini S, Matosevic I, Tomei PE, 406. Miyasaka SC, Habte M, Matsuyama DT (1993) J Plant Nutr
Giovannetti M (2003) Mycorrhiza 13:33–40 16:1339–1356
369. Marin M, Ybarra M, Fe A, Garcia-Ferriz L (2002) Agr Food 407. Mohandas S (1987) Plant Soil 98:295–297
Sci Finland 11:245–251 408. Moora M, Öpik M, Sen R (2004) Funct Ecol 18:554–562
370. Markkola A, Kuikka K, Rautio P, Härmä E, Roitto M, Tuomi J 409. Moora M, Zobel M (1998) Can J Bot 76:613–619
(2004) Oecologia 140:234–240 410. Moraes RM, De Andrade Z, Bedir E, Dayan FE, Lata H,
371. Marler MJ, Zabinski CA, Wojtowicz T, Callaway RM (1999) Khan I, Pereira AMS (2004) Plant Sci 166:23–29
Northwest Sci 73:217–224
349
Table 1 (continued) Table 1 (continued)
411. Morte A, Díaz G, Rodriguez P, Alarcón JJ, Sánchez-Blanco MJ 444. O’Neill EG, Luxmoore RJ, Norby RJ (1987) Can J For Res
(2001) Biologia Plantarum 44:263–267 17:878–883
412. Morte MA, Díaz G, Honrubia M (1996) Agronomie 16:633–637 445. Onguene NA, Kuyper TW (2001) Forest Ecol Manag
413. Moyersoen B, Fitter AH (1999) Mycorrhiza 8:247–253 140:277–287
414. Muhsin TM, Zwiazek JJ (2002) Plant Soil 238:217–225 446. Orlowska E, Zubek S, Jurkiewicz A, Szarek-Lukaszewska G,
415. Mullahey JJ, Speed CS (1991) Soil Crop Sci Soc Fl Turnau K (2002) Mycorrhiza 12:153–160
50:44–47 447. Osundina MA (1998) Biol Fert Soils 26:95–99
416. Mullen RB, Schmidt SK (1993) Oecologia 94:229–234 448. Otero JT, Ackerman JD, Bayman P (2004) Mol Ecol
417. Muller F, Dexheimer J, Gerard J (1994) Acta Bot Gallica 13:2393–2404
141:565–569 449. Palmieri M, Swatzell LJ (2004) Northeast Nat 11:57–66
418. Munyanziza E, Kuyper TW (1995) Mycorrhiza 5:283–287 450. Panwar J, Vyas A (2002) Curr Sci India 82:576–578
419. Munyanziza E, Oldeman RAA (1995) Fert Res 40:235–242 451. Parlade J, Luque J, Pera J, Rincon AM (2004) Ann For Sci
420. Münzenberger B, Golldack J, Ullrich A, Schmincke B, 61:507–514
Hüttl RF (2004) Mycorrhiza 14:193–202 452. Patreze CM, Cordeiro L (2004) Forest Ecol Manag 196:275–285
421. Münzenberger B, Kottke I, Oberwinkler F (1992) Trees-Struct 453. Pattanaik R, Sahu S, Padhi GS, Mishra AK (1995) Indian J Agr
Funct 7:40–47 Sci 65:186–190
422. Muthukumar T, Sha LQ, Yang XD, Cao M, Tang JW, Zheng Z 454. Pattinson GS, McGee PA (2004) Mycorrhiza 14:119–125
(2003) Mycorrhiza 13:289–297 455. Paula MA, Urquiaga S, Siqueira JO, Döbereiner J (1992)
423. Muthukumar T, Udaiyan K (2002) Mycorrhiza 12:213–217 Biol Fert Soils 14:61–66
424. Muthukumar T, Udaiyan K (2002) Acta Oecol 23:337–347 456. Pawlowska TE, Blaszkowski J, Rühling A (1996) Mycorrhiza
425. Muthukumar T, Udaiyan K, Karthikeyan A, Manian S (1997) 6:499–505
Agr Ecosyst Environ 61:51–58 457. Pendleton RL (2000) Int J Plant Sci 161:683–689
426. Muthukumar T, Udaiyan K, Shanmughavel P (2004) 458. Pera J, Alvarez IF (1995) Mycorrhiza 5:193–200
Mycorrhiza 14:65–77 459. Perkins AJ, Masuhara G, McGee PA (1995) Aust J Bot 43:85–91
427. Muthukumar T, Udayan K, Rajeshkannan V (2001) 460. Perkins AJ, McGee PA (1995) Aust J Bot 43:565–575
Biol Fert Soils 34:417–426 461. Pfeiffer CM, Bloss HE. 1988. New Phytol 108:315–321
428. Naik BH, Nalawadi UG, Sreenivasa MN, Patil AA (1995) 462. Philip LJ, Posluszny U, Klironomos JN (2001) Can J Bot
Sci Hortic 62:129–133 79:381–388
429. Nemec S, Vu JCV (1990) Plant Soil 128:257–263 463. Pimienta-Barrios E, Pimienta-Barrios E, Nobel PS (2004)
430. Neville J, Tessier JL, Morrison I, Scarratt J, Canning B, J Arid Environ 59:1–17
Klironomos JN (2002) Appl Soil Ecol 19:209–216 464. Pimienta-Barrios E, Salas-Galvan ME, Zanudo-Hernandez J,
431. Nezzar-Hocine H, Perrin R, Halli-Hargas R, Chevalier G Nobel PS (2002) Tree Physiol 22:667–674
(1998) Mycorrhiza 8:47–51 465. Pirazzi R, Rea E, Bragaloni M (1999) Geomicrobiol J 16:79–84
432. Nielsen KB, Kjøller R, Olsson PA, Schweiger PF, 466. Pocock K, Duckett JG (1985) New Phytol 99:281–304
Andersen FØ, Rosendahl S (2004) Mycol Res 108:616–625 467. Podeszfinski C, Dalpe Y, Charest C (2002) J Sustain Agr
433. Noldt G, Bauch J (2001) J Appl Bot-Angew Bot 75:168–172 20:57–74
434. Nouaim R, Lineres M, Esvan JM, Chaussod R (1994) 468. Poole BC, Sylvia DM (1990) Can J Bot 68:2703–2707
Agroforestry Syst 27:67–77 469. Potty VP (1990) Plant Soil 125:146–148
435. Nowak J (2004) Symbiosis 37:259–266 470. Pregitzer KS, DeForest JL, Burton AJ, Allen MF, Ruess RW,
436. Núñez-Castillo O, Álvarez-Sánchez FJ (2003) Mycorrhiza Hendrick RL (2002) Ecol Monogr 72:293–309
13:271–276 471. Pritsch K, Munch JC, Buscot F (1997) Mycorrhiza 7:201–216
437. Nuortila C, Kytöviita MM, Tuomi J (2004) New Phytol 472. Puppi G, Tartaglini N (1991) Acta Ecol 12:295–304
164:543–553 473. Raghuwanshi R, Upadhyay RS (2004) World Microb Biot
438. O'Connor PJ, Smith SE, Smith FA (2001) Aust J Bot 20:1–5
49:493–499 474. Rains KC, Nadkarni NM, Bledsoe CS (2003) Mycorrhiza
439. Oba H, Shinozaki N, Oyaizu H, Tawaraya K, Wagatsuma T, 13:257–264
Barraquio WL, Saito M (2004) Soil Sci Plant Nutr 50:1195–1203 475. Rajagopal D, Madhavendra SS, Jamil K (1989) Curr Sci India
440. Odonnell JJ, Sylvia DM, Pitman WD, Rechcigl JE (1992) 58:687–689
Trop Grasslands 26:120–129 476. Rajan SK, Reddy BJD, Bagyaraj DJ (2000) Forest Ecol Manag
441. Okon IE, Osonubi O, Sanginga N (1996) Agroforest Syst 126:91–95
33:165–175 477. Rao AV, Tak R (2001) Appl Soil Ecol 17:279–284
442. Oliveira VL, Schmidt VDB, Bellei MM (1997) Ann Sci Forest 478. Rao VU, Rao AS (1996) Indian J Agr Sci 66:613–616
54:473–481 479. Rashid A, Ahmed T, Ayub N, Khan AG (1997) Mycorrhiza
443. Olsson PA, Eriksen BE, Dahlberg A (2004) Can J Bot 7:217–220
82:1547–1556 480. Rasmussen HN (1990) New Phytol 116:137–147
481. Rasmussen HN (1992) Physiol Plantarum 86:161–167
350
Table 1 (continued) Table 1 (continued)
482. Ravikumar R, Ananthakrishnan G, Appasamy T, Ganapathi A 516. Scales PF, Peterson RL (1991) Can J Bot 69:2149–2157
(1997) Forest Ecol Manag 98:205–208 517. Schellenbaum L, Berta G, Ravolanirina F, Tisserant B,
483. Read DJ, Duckett JG, Francis R, Ligrone R, Russell A (2000) Gianinazzi S, Fitter AH (1991) Ann Bot 68:135–141
Philos T Roy Soc B 355:815–830 518. Scheloske S, Maetz M, Schneider T, Hildebrandt U, Bothe H,
484. Reddell P, Hopkins MS, Graham AW (1996) J Trop Ecol Povh B (2004) Protoplasma 223:183–189
12:763–777 519. Scherff EJ, Galen C, Stanton ML (1994) Oikos 69:405–413
485. Reddell P, Yun Y, Shipton WA (1997) Aust J Bot 45:41–51 520. Schiavo JA, Martins MA (2003) Pesqui Agropecu Bras
486. Reddy B, Bagyaraj DJ (1994) Sci Hortic 59:69–73 38:173–178
487. Reddy MS, Natarajan K (1994) Mycorrhiza 5:115–117 521. Schmid E, Oberwinkler F (1993) New Phytol 124:69–81
488. Regvar M, Vogel K, Irgel N, Wraber T, Hildebrandt U, Wilde P, 522. Schmid E, Oberwinkler F (1996) Mycol Res 100:843–849
Bothe H (2003) J Plant Physiol 160:615–626 523. Schubert A, Bodrino C, Gribaudo I (1992) Agronomie
489. Reis VM, de Paula MA, Döbereiner J (1999) Pesqui Agropecu 12:847–850
Bras 34:1933–1941 524. Schultz PA, Miller RM, Jastrow JD, Rivetta CV, Bever JD
490. Rice RW, Datnoff LE, Raid RN, Sanchez CA (2002) J Plant (2001) Am J Bot 88:1650–1656
Nutr 25:1839–1853 525. Schüßler A (2000) Mycorrhiza 10:15–21
491. Richter BS, Stutz JC (2002) Restor Ecol 10:607–616 526. Schwob I, Ducher M, Coudret A (1999) Plant Pathol 48:19–25
492. Rillig MC, Allen MF (1998) Soil Biol Biochem 30:2001–2008 527. Schwob I, Ducher M, Coudret A (2000) J Plant Physiol
493. Rillig MC, Allen MF, Klironomos JN, Field CB (1998) 156:284–287
Mycologia 90:199–205 528. Scotti MR, Correa EJA (2004) Ann Forest Sci 61:87–95
494. Rincon E, Huante P, Ramirez Y (1993) Mycorrhiza 3:79–81 529. Selosse MA, Bauer R, Moyersoen B (2002) New Phytol
495. Rojas-Andrade R, Cerda-García-Rojas CM, Frías-Hernández 155:183–195
JT, Dendooven L, Olalde-Portugal V, Ramos-Valdivia AC (2003) 530. Selosse MA, Faccio A, Scappaticci G, Bonfante P (2004)
Mycorrhiza 13:49–52 Microbial Ecol 47:416–426
496. Roldán A, Díaz G, Albaladejo J (1992) Arid Soil Res Rehab 531. Selvaraj T, Subramanian G (1987) Curr Sci India 56:1112–1114
6:33–39 532. Semones SW, Young DR (1995) Mycorrhiza 5:423–429
497. Roldan-Fajardo BE (1994) New Phytol 127:115–121 533. Sengupta A, Chaudhuri S (1989) Curr Sci India 58:1372–1372
498. Ronikier M, Miskiewicz A, Mleczko P (2002) Acta Soc Bot 534. Senthilkumar S, Krishnamurthy KV (1998) Biol Plant
Pol 71:235–242 41:111–119
499. Rosendahl CN, Rosendahl S (1991) Environ Exp Bot 535. Setua GC, Kar R, Ghosh JK, Das KK, Sen SK (1999) Bio Fert
31:313–318 Soils 29:98–103
500. Ruiz-Lozano JM, Azcón R (1995) Physiol Plantarum 536. Sharma AK, Singh R, Singh US (1988) Curr Sci India
95:472–478 57:901–902
501. Ruotsalainen AL, Aikio S (2004) Can J Bot 82:443–449 537. Sharma MP, Adholeya A (2004) Can J Bot 82:322–328
502. Ruotsalainen AL, Kytöviita MM (2004) Oecologia 140:226–233 538. Sharma MP, Bhatia NP, Adholeya A (2001) New Forest
503. Ruotsalainen AL, Väre H, Vestberg M (2002) Mycorrhiza 21:89–104
12:29–36 539. Sharrock RA, Sinclair FL, Gliddon C, Rao IM, Barrios E,
504. Russell AJ, Bidartondo MI, Butterfield BG (2002) New Phytol Mustonen PJ, Smithson P, Jones DL, Godbold DL (2004)
156:283–295 Mycorrhiza 14:103–109
505. Russell J, Bulman S (2005) New Phytol 165:567–579 540. Shefferson RP, Weiss M, Kull T, Taylors DL (2005) Mol Ecol
506. Rygiewicz PT, Johnson MG, Ganio LM, Tingey DT, Storm MJ 14:613–626
(1997) Plant Soil 189:275–287 541. Shockley FW, McGraw RL, Garrett HE (2004) Agroforest Syst
507. Salemaa M, Monni S (2003) Environ Pollut 126:435–443 60:137–142
508. Sannazzaro AI, Ruiz OA, Albertó E, Menéndez AB (2004) 542. Sidhu OP, Behl HM, Gupta ML, Janardhanan KK (1990) Curr
Mycorrhiza 14:139–142 Sci India 59:422–423
509. Santiago-Martinez G, Estrada-Torres A, Varela L, Herrera T 543. Sigüenza C, Espejel I, Allen EB (1996) Mycorrhiza 6:151–157
(2003) Agrociencia 37:575–584 544. Singh CS (1992) Zbl Mikrobiol 147:503–508
510. Santos BA, Silva GA, Maia LC, Alves MV (2000) Mycorrhiza 545. Singh CS (1992) Zbl Mikrobiol 147:447–453
10:151–153 546. Singh CS, Tyagi SP (1989) Zbl Mikrobiol 144:241–248
511. Sasaki A, Fujiyoshi M, Shidara S, Nakatsubo T (2001) 547. Singh S, Kapoor KK (1998) Mycorrhiza 7:249–253
Ecol Res 16:165–172 548. Siqueira JO, Carneiro MAC, Curi N, Rosado SCS, Davide AC
512. Sattelmacher B, Reinhard S, Pomikalko A (1991) J Agron Crop (1998) Forest Ecol Manag 107:241–252
Sci 167:350–355 549. Sisti D, Giomaro G, Cecchini M, Faccio A, Novero M,
513. Scagel CF (2004) Hortscience 39:1432–1437 Bonfante P (2003) Mycorrhiza 13:107–115
514. Scagel CF (2004) Horttechnology 14:39–48 550. Smith JE, Johnson KA, Cázares E (1998) Mycorrhiza 7:279–285
515. Scagel CF, Reddy K, Armstrong JM (2003) Horttechnology 551. Sohn BK, Kim KY, Chung SJ, Kim WS, Park SM, Kang JG,
13:62–66 Rim YS, Cho JS, Kim TH, Lee JH (2003) Sci Hortic 98:173–183
351
Table 1 (continued) Table 1 (continued)
552. Stahl PD, Schuman GE, Frost SM, Williams SE (1998) Soil Sci 587. Titus JH, Tsuyuzaki S (2002) Mycorrhiza 12:271–275
Soc Am J 62:1309–1313 588. Tonin C, Vandenkoornhuyse P, Joner EJ, Straczek J, Leyval C
553. Stanley MR, Koide RT, Shumway DL (1993) Oecologia (2001) Mycorrhiza 10:161–168
94:30–35 589. Torpy FR, Morrison DA, Bloomfield BJ (1999) Mycorrhiza
554. St-Arnaud M, Hamel C, Vimard B, Caron M, Fortin JA (1997) 8:289–296
Can J Bot 75:998–1005 590. Torres P, Honrubia M, Morte MA (1991) Mycotaxon 41:437–443
555. Starrett MC, Blazich FA, Shafer SR, Grand LF (2001) 591. Torti SD, Coley PD (1999) Biotropica 31:220–228
Hortscience 36:353–356 592. Torti SD, Coley PD, Janos DP (1997) J Trop Ecol 13:623–629
556. Steinke E, Williams PG, Ashford AE (1996) Ann Bot 77:413–419 593. Tótola MR, Borges AC (2000) Braz J Microbiol 31:257–265
557. Stenlund DL, Charvat ID (1994) Mycorrhiza 4:131–137 594. Treu R, Laursen GA, Stephenson SL, Landolt JC, Densmore R
558. Stevens KJ, Peterson RL (1996) Mycorrhiza 6:99–104 (1996) Mycorrhiza 6:21–29
559. Stockey RA, Rothwell GW, Addy HD, Currah RS (2001) 595. Trindade AV, Faria NG, de Almeida FP (2000) Pesqui
Mycol Res 105:202–205 Agropecu Bras 35:1389–1394
560. Strullu DG, Frenot Y, Maurice D, Gloaguen JC, Plenchette C 596. Tsang A, Maun MA (1999) Plant Ecol 144:159–166
(1999) CR Acad Sci III-Vie 322:771–777 597. Turnau K, Mesjasz-Przybylowicz J (2003) Mycorrhiza 13:185–190
561. Sykorova Z, Rydlova J, Vosatka M (2003) Folia Geobot 598. Turnau K, Ronikier M, Unrug J (1999) Acta Soc Bot Pol
38:177–189 68:63–68
562. Sylvia DM, Alagely AK, Chellemi DO, Demchenko LW 599. Turner SD, Amon JP, Schneble RM, Friese CF (2000)
(2001) Biol Fert Soils 34:448–452 Wetlands 20:200–204
563. Sylvia DM, Burks JN (1988) Mycologia 80:565–568 600. Udaiyan K, Karthikeyan A, Muthukumar T (1996)
564. Tam PCF (1994) Mycorrhiza 4:255–263 Trees-Struct Funct 11:65–71
565. Tan TK, Loon WS, Khor E, Loh CS (1998) Plant Cell Rep 601. Usuki F, Narisawa K (2005) Mycorrhiza 15:61–64
18:14–19 602. Vaast P, Zasoski RJ (1991) Cafe Cacao The 35:121–128
566. Tang F, White JA, Charvat I (2001) Mycologia 93:1042–1047 603. Vallini G, Pera A, Avio L, Valdrighi M, Giovannetti M (1993)
567. Tarafdar JC, Rao AV (1997) Agr Ecosyst Environ 61:13–18 Biol Fert Soils 16:1–4
568. Tawaraya K, Takaya Y, Turjaman M, Tuah SJ, Limin SH, 604. van Auken OW, Brown SC (1998) Tex J Sci 50:291–304
Tamai Y, Cha JY, Wagatsuma T, Osaki M (2003) Forest Ecol 605. van der Heijden EW, de Vries FW, Kuyper TW (1999)
Manag 182:381–386 Can J Bot 77:1821–1832
569. Taylor DL, Bruns TD (1997) Proc Natl Acad Sci USA 606. Vasanthakrishna M, Bagyaraj DJ, Muthanna MB (1994)
94:4510–4515 Microbiol Res 149:23–25
570. Taylor DL, Bruns TD (1999) Mol Ecol 8:1719–1732 607. Verkade SD (1991) Sci Hortic 48:125–129
571. Taylor DL, Bruns TD, Hodges SA (2004) 608. Verma RK, Arya ID (1998) Mycorrhiza 8:113–116
P Roy Soc Lond B Bio 271:35–43 609. Vidal MT, Azcón-Aguilar C, Barea JM, Pliegoalfaro F (1992)
572. Taylor DL, Bruns TD, Szaro TM, Hodges SA (2003) Am J Bot Hortscience 27:785–787
90:1168–1179 610. Vierheilig H, Bennett R, Kiddle G, Kaldorf M,
573. Taylor J, Harrier L (2000) Plant Soil 225:53–61 Ludwig-Müller J (2000) New Phytol 146:343–352
574. Taylor JH, Peterson CA (2000) Trees-Struct Funct 14:239–247 611. Vierheilig H, Iseli B, Alt M, Raikhel N, Wiemken A, Boller T
575. Taylor K (1989) Ann Bot Fenn 26:421–425 (1996) Plant Soil 183:131–136
576. Tewari L, Johri BN, Tandon SM (1993) World J Microbiol 612. Vijayalakshmi M, Rao AS (1993) Zbl Mikrobiol 148:483–486
Biotechnol 9:191–195 613. Visser S, Danielson RM, Parkinson D (1991) Can J Bot
577. Thangaswamy S, Padmanabhan C, Jeong YJ, Kim H (2004) 69:1321–1328
J Microbiol Biotechnol 14:885–890 614. Vogel-Mikus K, Drobne D, Regvar M (2005) Environ Pollut
578. Thanuja TV, Hegde RV, Sreenivasa MN (2002) Sci Hortic 133:233–242
92:339–346 615. Vosatka M, Dodd JC (1998) Plant Soil 200:251–263
579. Theodorou C, Reddell P (1991) New Phytol 118:279–288 616. Vovides AP (1990) Am J Bot 77:1532–1543
580. Thomas GV (1988) Indian J Agr Sci 58:145–147 617. Walker RF (2001) Forest Ecol Manag 149:163–179
581. Tian CJ, He XY, Zhong Y, Chen JK (2002) Forest Ecol Manag 618. Walker RF, Johnson DW, Geisinger DR, Ball JT (1998)
170:307–312 Forest Ecol Manag 109:9–20
582. Tian CJ, He XY, Zhong Y, Chen JK (2003) New Forest 619. Walker RF, McLaughlin SB, West DC (2004) Restor Ecol
25:125–131 12:8–19
583. Tisserant B, Brenac V, Requena N, Jeffries P, Dodd JC (1998) 620. Wang FY, Liu RJ, Lin XG, Zhou JM (2004) Mycorrhiza
New Phytol 138:225–239 14:133–137
584. Titus JH, del Moral R (1998) Oikos 81:495–510 621. Watson MA, Scott K, Griffith J, Dieter S, Jones CS, Nanda S
585. Titus JH, del Moral R (1998) Am J Bot 85:370–375 (2001) Evol Ecol 15:425–442
586. Titus JH, Leps J (2000) Am J Bot 87:392–401 622. Weber G, Claus M (2000) J Plant Nutr Soil Sci 163:609–616
352
Table 1 (continued) Table 1 (continued)
623. Weber HC, Klahr A, Marron-Heimbuch M (1995) Bot Acta 656. Brundrett MC (2002) New Phytol 154:275–304 (Also see the
108:525–534 author’s website: Introduction to mycorrhizas. [WWW document]
624. Wellings NP, Wearing AH, Thompson JP (1991) URL: http://www.ffp.csiro.au/research/mycorrhiza/)
Aust J Agr Res 42:835–845 657. Cameron KM, Chase MW, Rudall PJ (2003) Brittonia
625. West HM (1995) New Phytol 129:107–116 55:214–225
626. Wetzel PR, van der Valk AG (1996) Can J Bot 74:883–890 658. Leake JR (1994) New Phytol 127:171–216
627. Whitbeck JL (2001) Biotropica 33:303–311 659. Woltz P, Stockey RA, Gondran M, Cherrier JF, Bernard J
628. Whitbread F, McGonigle TP, Peterson RL (1996) Can J Bot (1994) Acta Bot Gallica 141:731–746
74:1104–1112
629. White JA, Charvat I (1999) Mycorrhiza 9:191–197 Furthermore, liverworts are clearly favored as the earliest
630. Whitfield L, Richards AJ, Rimmer DL (2004) Mycorrhiza divergent lineage of extant land plants according to emerging
14:47–54 molecular evidence (Qiu et al. 1998; Dombrovska and Qiu
631. Wigand C, Stevenson JC (1994) Estuaries 17:206–215 2004; Groth-Malonek et al. 2005; Qiu et al. unpublished),
632. Wigand C, Stevenson JC (1997) Hydrobiologia 342:35–41 despite some lingering controversy on relationships among
633. Wilson GWT, Hartnett DC, Smith MD, Kobbeman K (2001)
three bryophyte lineages: liverworts, mosses, and hornworts
Am J Bot 88:1452–1457
(see Qiu and Lee 2000; Renzaglia et al. 2000). Hence, the
widespread occurrence of fungal association in liverworts
634. Wu B, Nara K, Hogetsu T (1999) Mycorrhiza 9:151–159
deserves some attention here.
635. Wu B, Watanabe I, Hayatsu M, Nioh I (1999) Biol Fert Soils
Mycorrhizas, or more precisely mycorrhizoids and
28:136–138
mycothalli, are found in many of the liverworts that have
636. Wu BY, Isobe K, Ishii R (2004) Mycorrhiza 14:391–395
been investigated (Pocock and Duckett 1985; Boullard
637. Wubet T, Kottke I, Teketay D, Oberwinkler F (2003)
1988; Duckett et al. 1991). Several aspects of these
Forest Ecol Manag 179:387–399 symbioses revealed by recent studies may help clarify their
638. Wubet T, Weiss M, Kottke I, Oberwinkler F (2003) Can J Bot evolutionary relationship to mycorrhizas in vascular plants.
81:255–266 First, in cases where detailed ultrastructural analysis has
639. Xiao G, Berch SM (1995) Mycologia 87:467–470 been done, structures similar to those in the endomycor-
640. Xie ZP, Müller J, Wiemken A, Broughton WJ, Boller T (1998) rhizas of vascular plants, i.e. arbuscules, have been
New Phytol 139:361–366 observed in some liverworts (Read et al. 2000; Carafa et
641. Yamanaka T, Li CY, Bormann BT, Okabe H (2003) Plant Soil al. 2003; Russell and Bulman 2005). Second, cross-
254:179–186 inoculation experiments have convincingly demonstrated
642. Yamato M (2001) Mycorrhiza 11:83–88 that the same fungi can infect both liverworts and
643. Yamato M (2004) Mycorrhiza 14:127–131 angiosperms and produce similar structures for either
644. Yang GT, Cha JY, Shibuya M, Yajima T, Takahashi K (1998) glomeromycetous or ascomycetous mycorrhizas (Read et
Mycol Res 102:1503–1508 al. 2000). Third, although isotopic tracing of nutrient,
645. Yang WQ, Goulart BL (1997) J Am Soc Hortic Sci 122:24–30 water, and carbon exchange has not been done for most
646. Yoshida LC, Allen EB (2001) Am J Bot 88:1430–1436 liverwort–fungus symbioses, the carbon flow from Betula
647. Young BW, Massicotte HB, Tackaberry LE, Baldwin QF, through the ectomycorrhizal fungus Tulasnella to the
Egger KN (2002) Mycorrhiza 12:75–82 mycoheterotrophic liverwort Cryptothallus has been con-
648. Youpensuk S, Lumyong S, Dell B, Rerkasem B (2004) firmed by a 14C feeding experiment (Bidartondo et al.
Agroforestry Syst 60:239–246 2003). Finally, the evolutionary pattern of plant–fungus
649. Zak JC, McMichael B, Dhillion S, Friese C (1998) symbiosis observed in angiosperms by Trappe (1987) and
Agr Ecosyst Environ 68:245–254 in vascular plants (this study), i.e., glomeromycetous
650. Zandavalli RB, Dillenburg LR, de Souza PVD (2004) mycorrhizas being the common type and occurring in
Appl Soil Ecol 25:245–255 early-diverging plant lineages and ascomycetous and
651. Zangaro W, Nisizaki SMA, Domingos JCB, Nakano EM basidiomycetous mycorrhizas being the rare type and
(2003) J Trop Ecol 19:315–324 found in late-evolving plant lineages, is also seen in
652. Zettler LW, Stewart SL, Bowles ML, Jacobs KA (2001) liverworts (Fig. 1). These four lines of evidence indicate
Am Midl Nat 145:168–175 that even though the plant structures involved in symbiosis
653. Zhang Y, Guo LD, Liu RJ (2004) Mycorrhiza 14:25–30 are probably structurally and functionally analogous
654. Zhao ZW (2000) Mycorrhiza 10:145–149 between liverworts and vascular plants, the nature of the
655. Zhao ZW, Xia YM, Qin XZ, Li XW, Cheng LZ, Sha T,
biological interaction is almost certain to be evolutionarily
Wang GH (2001) Mycorrhiza 11:159–162
homologous. Besides further investigations of the func-
tional aspects of mycorrhizas in liverworts and other
mosses (Fig. 1; but see Boullard 1988 for mycorrhizoids in bryophytes as suggested by Read et al. (2000), one line of
Takakia), tends to suggest that these plant–fungus interac- evidence that will provide conclusive support for evolu-
tions began when land plants originated. At present, there is tionary homology between the mycorrhizal symbioses in
no doubt that bryophytes preceded vascular plants during bryophytes and vascular plants could come from studies of
early evolution of land plants (Kenrick and Crane 1997). plant genes that are involved in the processes, some of
353
Table 2 Mycorrhizal investigation of four major groups of land plants at both family and species levels
Group Total number of No. (%) of mycorrhizal No. (%) of No. (%) of No. (%) of No. (%) of
families/species families (obligate and obligately facultatively nonmycorrhizal nonmycorrhizal
surveyed facultative) mycorrhizal mycorrhizal species families species
species
which have been identified in recent studies (Stracke et al. bryophytes where the plant structures involved in symbi-
2002; Liu et al. 2003; Ane et al. 2004; Demchenko et al. osis are rhizoids and thalli of the gametophyte, glomer-
2004; Levy et al. 2004). If the same genes are found to omycetous fungi-mediated symbiosis results in formation
control development of mycorrhizas in all groups regard- of AM-like structures and is found in most early-diverging
less of their expression in the gametophytes of bryophytes lineages of liverworts and in hornworts (Ligrone and Lopes
or the sporophytes of vascular plants, and if the gene 1989; Read et al. 2000; Russell and Bulman 2005). These
phylogenies are congruent to the plant phylogeny, the final two aspects of AM symbiosis suggest that the genetic
doubt about homology of the two types of symbioses will mechanism underlying interaction between the plants and
be dispelled. glomeromycetous fungi might have been established in the
If the mycorrhizal symbiosis in liverworts, other bryo- common ancestor of all land plants. Future molecular
phytes, such as the moss Takakia (see Boullard 1988), and studies should be able to test this hypothesis to determine if
hornworts proves to be homologous to that in vascular the same genes are involved in plants–glomeromycetous
plants, it becomes obvious that mycorrhiza was indeed an fungi symbioses throughout land plants.
important means of water and nutrient uptake adopted by the Trappe (1987) reported that AM is the ancestral type of
earliest land plants (Pirozynski and Malloch 1975). Fossil mycorrhiza in angiosperms. Our survey, which broadens
evidence is in agreement with such a scenario. Both the scope to include all land plants, extends this conclusion
glomeromycetous fungi (Redecker et al. 2000) and liver- to all land plants. This result is not likely to change even if
worts (Wellman et al. 2003) evolved by the Ordovician, relationships among three bryophyte lineages and vascular
when plants colonized the land (Kenrick and Crane 1997). plants are altered (see Qiu and Lee 2000) because all of
Fossil mycorrhizas formed between nonseptate fungi and the their early-diverging lineages possess AM when they are
protracheophyte Aglaophyton major have been uncovered mycorrhizal. Furthermore, fossil evidence clearly indicates
from the Rhynie chert, confirming that this type of plant– that AM is the most ancient type of mycorrhiza. The
fungus interaction existed at least 400 million years ago Devonian protracheophyte Aglaophyton major provides
(Remy et al. 1994; Kerp et al. 2004; Taylor et al. 2005). It is the best fossil record for existence of AM-like symbiosis as
possible that evolution of mycorrhiza might even have early as 400 million years ago; the arbuscules are visible in
predated the origin of land plants, if fungal association in the the protosteles of this early Devonian plant (Remy et al.
extinct charophyte Palaeonitella (Taylor et al. 1992) is 1994; Taylor et al. 2005). Fossil roots of younger age from
mycorrhizal. We conclude that although more work is the Triassic show that this type of symbiosis has been
needed to solidify the relationship between mycorrhizal present continuously in early land plant evolution
symbioses in bryophytes and vascular plants, including (Stubblefield et al. 1987). On the other hand, the oldest
morphological, physiological, and molecular characteriza- ectomycorrhizal fossils have so far been found only in the
tion of the plant–fungus interactions in both bryophytes and middle Eocene (50 million years ago) (LePage et al.
early vascular plants (see Read et al. 2000), all available 1997). The fossil record of glomeromycetous fungi, found
evidence seems to point to an origin of mycorrhizas at the in the Ordovician (Redecker et al. 2000), also clearly
beginning of land plant evolution. predates that of ascomycetous fungi unearthed from the
Lower Devonian (Taylor et al. 1999). Given all these lines
of evidence, it seems safe to conclude that AM represents
Arbuscular mycorrhiza is the ancestral type the ancestral type of mycorrhiza in land plants.
of mycorrhiza
When the different types of mycorrhizas are mapped onto Many independent conversions of arbuscular
the land plant phylogeny, it becomes clear that arbuscular mycorrhiza to other types of mycorrhizas
mycorrhiza (AM), the endomycorrhiza formed by glom-
eromycetous fungi and plants, is the ancestral type, as it If the ancestral state of AM in land plants is accepted, and
occurs in a vast majority of plants and in all early-diverging further, if it can be agreed upon that the glomeromycetous
lineages of major clades of land plants (Fig. 1). Even in fungi–plant interaction is underpinned by a genetic mech-
354
anism that has been stably inherited since its establishment in conclusion. Our study revealed many more events of
the common ancestor of all land plants, the phylogenetic evolution of this type of mycorrhiza in land plants (Fig. 1).
distribution of AM and other types of mycorrhiza shown in Examination of the evolutionary histories of both plants
Fig. 1 leads to the conclusion that there have been many and fungi may provide some ideas to understand how this
independent conversions of AM to these other types of type of mycorrhiza evolved repeatedly. The plants that
mycorrhizas. Brundrett (2002) previously proposed these form ECM typically grow in nutrient-poor environments,
evolutionary changes. In this review, we find overwhelming e.g., temperate and timberline forests of both Southern and
evidence in support of this hypothesis. Many plant lineages, Northern Hemispheres (Malloch et al. 1980), the spruce–
ranging from pteridophytes through gymnosperms to an- hemlock–redwood forest of the coastal fog belt in the
giosperms, contain some species that can form both AM and Pacific Northwestern USA, the wet eucalyptus forest in
other types of mycorrhizas, e.g., Dryopteridaceae, Pinaceae, Australia, and the wet dipterocarp forest of Australasia (J.
Gnetaceae, Araucariaceae, Cupressaceae, Orchidaceae, Cy- Trappe, personal communication). Phylogenetically, these
peraceae, Poaceae, Ranunculaceae, Polygonaceae, Caryo- plants represent derived lineages of some major land plant
phyllaceae, Ericaceae, Rubiaceae, Oleaceae, Aquifoliaceae, clades that once lived in a less nutrient-deficient environ-
Campanulaceae, Goodeniaceae, Asteraceae, Caprifoliaceae, ment, e.g., Pinaceae and Cupressaceae, as opposed to other
Grossulariaceae, Myrtaceae, Melastomataceae, Euphorbia- conifers such as Cephalotaxaceae, Taxaceae, and Taxo-
ceae, Salicaceae, Polygalaceae, Fabaceae, Rosaceae, diaceae, and Fagales and some Malvales vs other rosids.
Rhamnaceae, Juglandaceae, Betulaceae, Casuarinaceae, Meanwhile, the fungal species that participate in ECM
Cistaceae, Malvaceae, and Sapindaceae (Table 1; Fig. 1). symbiosis evolved repeatedly from saprotrophic homo-
These species might be in a transitional state from AM to basidiomycetes and also reverted to free-living condition
other types of mycorrhizas. These other types of mycor- many times independently (Hibbett et al. 2000), and they
rhizas have probably evolved as a consequence of also represent derived lineages of fungi as a whole (Lutzoni
emergence of new lineages in fungi on one side (e.g., et al. 2004). Thus, evolution of ECM could be viewed as an
certain groups of Ascomycetes and Basidiomycetes) and in adaptation by those major plant clades to the change of
plants on the other side (e.g., Pinaceae, Orchidaceae, environment when the climate on earth became more
Ericaceae, Fagales, and Malvales), and the associations seasonal and arid (Hickey and Doyle 1977; Malloch et al.
formed by these new lineages that were able to colonize 1980), which immobilized nutrients, or simply as an
habitats that were previously not very successfully adaptation to the environments that were limited in nutrient
occupied by AM plants (Malloch et al. 1980). Because availability. From these considerations, it may be argued
these other types of mycorrhizas have been classified using that the plasticity exhibited by ECM evolution reflects the
both morphological and plant partner criteria (Smith and opportunistic nature of a collective response by both plant
Read 1997), we follow this classification in our discussion and fungal partners to environmental challenges. This
below. seems to be a short-term evolutionary strategy in compar-
ison to AM, which clearly represents a major evolutionary
innovation to solve a permanent water-and-nutrients defi-
Ectomycorrhiza ciency problem faced by plants when they first made the
virtually irreversible invasion onto the land in the
Ectomycorrhiza (ECM) is a partnership between mostly Ordovician.
basidiomycetous fungi and various groups of land plants. It
primarily occurs in Pinaceae, Araucariaceae, Cupressaceae,
Gnetaceae, Polygonaceae, Nyctaginaceae, Myrtaceae, Fig. 1 A phylogenetic tree of 263 land plant families mapped with "
Salicaceae, Fabaceae, Fagales, and Malvales. In addition, mycorrhizal information. a Non-angiosperms (including bryophytes,
many other families of vascular plants contain a small pteridophytes, and gymnosperms), b angiosperms except core
eudicots, c core eudicots except rosids, and d rosids. For each
percentage of species that form this type of mycorrhiza. family, the number in the column Total shows the total number of
Most leafy liverworts also have ascomycetous and basid- examined species; the M% column shows the percentage of
iomycetous fungal associations (Table 1; Fig. 1). Although obligately mycorrhizal species. The FM% column shows the
ECM is much rarer than AM in land plants, among all types percentage of facultatively mycorrhizal species, and the NM%
of mycorrhizas formed by ascomycetous and basidiomy- column shows the percentage of nonmycorrhizal species. Thicker
terminal branches were used to indicate 21 nonmycorrhizal
cetous fungi, it is the most common one. When viewed in a families. For each of the 242 mycorrhizal families, the percentages
plant phylogenetic perspective, the distribution of ECM of different types of mycorrhizae among all mycorrhizal species are
clearly suggests many independent origins of this type of shown in the M type column. The mycorrhizal types are consistent to
mycorrhiza because its occurrence is sporadic throughout the current widely used system of Smith and Read (1997): AM
arbuscular mycorrhiza, ECM ectomycorrhiza, EEM ectendomycor-
land plants and it is mostly found in derived lineages in rhiza, ORM orchid mycorrhiza, ERM ericoid mycorrhiza, MTM
major plant clades. Previously, Bruns and Shefferson monotropoid mycorrhiza, ABM arbutoid mycorrhiza, as well as
(2004) estimated at least 12 independent origins of ECM mycoheterotrophy. For the bryophytes, fungal associations were
within angiosperms by mapping ectomycorrhizal informa- used instead of mycorrhiza: A, B, and G indicate ascomycetous,
basidiomycetous, and glomeromycetous fungal associations, respec-
tion provided in Smith and Read (1997) onto an angio- tively. ①Families in which ectomycorrhizal species have been
sperm phylogeny (Soltis et al. 2000). Fitter and Moyersoen reported. ②Families in which mycoheterotrophic species have been
(1996) conducted a similar survey and reached a similar reported
355
a
Total M% FM% NM% M type
angiosperms
Taxaceae 2 100 0 0 AM only
Cupressaceae 1 11 100 0 0 82% AM,18% AM+ECM
Taxodiaceae 3 100 0 0 AM only
gymnosperms
Podocarpaceae 2 6 100 0 0 83% AM, 17% mycoheterotrophy?
Araucariaceae 1 5 100 0 0 60% AM, 20% ECM, 20% AM+EEM
Gnetaceae 1 3 100 0 0 67% ECM, 33% AM+ECM
Welwitschiaceae 1 100 0 0 AM only
Ephedraceae 2 100 0 0 AM only
Pinaceae 1 43 98 2 0 86% ECM, 7% AM+ECM, 5% ECM+EEM, 2% AM+ECM+EEM
Ginkgoaceae 1 100 0 0 AM only
Zamiaceae 5 100 0 0 AM only
Cycadaceae 2 100 0 0 AM only
Davalliaceae 4 75 0 25 AM only
Grammitidaceae 8 38 0 63 AM only
Polypodiaceae 37 8 3 89 AM only
Nephrolepidaceae 3 33 0 67 AM only
Dryopteridaceae 1 40 53 8 40 96 %AM, 4% AM+ECM
Blechnaceae 11 64 9 27 AM only
Thelypteridaceae 33 36 6 58 AM only
Aspleniaceae 99 32 12 56 AM only
Dennstaedtiaceae 20 60 5 35 AM only
Adiantaceae 25 48 12 40 AM only
Vittariaceae 3 33 0 67 AM only
pteridophytes
Pteridaceae 22 45 9 45 AM only
Dicksoniaceae 4 75 0 25 AM only
Cyatheaceae 6 33 0 67 AM only
Plagiogyriaceae 1 100 0 0 AM only
Azollaceae 1 0 0 100
Marsileaceae 1 0 100 0 AM only
Schizaeaceae 4 75 25 0 AM only
Gleicheniaceae 10 40 0 60 AM only
Hymenophyllaceae 11 36 0 64 50% AM, 50% endo-M (also AM?)
Osmundaceae 3 67 33 0 AM only
Ophioglossaceae 11 91 9 0 AM only
Psilotaceae 3 67 0 33 AM only
Marattiaceae 17 88 0 12 AM only
Equisetaceae 12 25 42 33 AM only
Selaginellaceae 17 76 6 18 AM only
Isoetaceae 3 0 0 100
Lycopodiaceae 17 35 24 41 AM only
Anthocerotaceae 2 100 0 0 fungal association (G), AM-like
Gymnomitriaceae 7 0 14 86 fungal association
Jungermanniaceae 21 48 0 52 fungal association (A, B)
Calypogeiaceae 8 100 0 0 fungal association (A, B)
Cephaloziaceae 14 71 14 14 fungal association (A)
Cephaloziellaceae 6 67 0 33 fungal association (A)
Scapaniaceae 8 13 13 75 fungal association
Lepidoziaceae 9 67 0 33 fungal association (A)
Geocalycaceae 10 30 10 60 fungal association
Arnelliaceae 1 100 0 0 fungal association (B)
Plagiochilaceae 5 20 0 80 fungal association
bryophytes
Herbertaceae 1 0 0 100
Pseudolepicoleaceae 1 0 100 0 fungal association
Lejeuneaceae 11 0 0 100
Jubulaceae 6 0 0 100
Porellaceae 5 0 0 100
Radulaceae 3 0 0 100
Codoniaceae 2 100 0 0 fungal association (G)
Pelliaceae 3 100 0 0 fungal association (G), AM-like
Aneuraceae 2 5 40 0 60 ORM-like (mycoheterotrophy via ECM)
Metzgeriaceae 6 0 0 100
Ricciaceae 1 0 0 100
Conocephalaceae 1 100 0 0 fungal association (G), AM-like
Aytoniaceae 1 100 0 0 fungal association (G), AM-like
Marchantiaceae 2 100 0 0 fungal association (G), AM-like
Lunulariaceae 1 100 0 0 fungal association (G)
Blasiaceae 1 0 0 100
Haplomitriaceae 2 100 0 0 fungal association (G), AM-like
Characeae
356
Fig. 1 (continued)
b
Total M% FM% NM% M type
core eudicots
Gunneraceae 1 100 0 0 AM only
basal eudicots
Buxaceae 1 100 0 0 AM only
Proteaceae 6 67 0 33 AM only
Ranunculaceae 1 39 54 33 13 97% AM, 3% AM+ECM
Berberidaceae 5 80 0 20 AM only
Menispermaceae 1 100 0 0 AM only
Papaveraceae 4 25 25 50 AM only
Piperaceae 6 83 0 17 AM only
magnoliids
Aristolochiaceae 1 0 100 0 AM only
Lauraceae 13 100 0 0 AM only
Annonaceae 6 83 0 17 AM only
Magnoliaceae 3 67 0 33 AM only
Myristicaceae 5 100 0 0 AM only
Costaceae 2 100 0 0 AM only
Zingiberaceae 5 100 0 0 AM only
Cannaceae 1 0 0 100
Heliconiaceae 1 100 0 0 AM only
Musaceae 1 100 0 0 AM only
Commelinaceae 3 67 33 0 AM only
Poaceae 1 267 71 20 9 99.6% AM, 0.4% AM+ECM
Restionaceae 2 100 0 0 AM only
Cyperaceae 1 253 35 19 46 99.3% AM, 0.7% AM+ECM
Juncaceae 27 37 37 26 AM only
Bromeliaceae 4 75 0 25 AM only
Typhaceae 3 33 67 0 AM only
Sparganiaceae 5 40 20 40 AM only
Arecaceae 9 89 0 11 AM only
Ruscaceae 6 17 83 0 AM only
Asparagaceae 2 100 0 0 AM only
Agavaceae 9 100 0 0 AM only
Hyacintheaceae 5 100 0 0 AM only
Themidaceae 1 100 0 0 AM only
Amaryllidaceae 5 80 20 0 AM only
monocots
Alliaceae 12 92 8 0 AM only
Asphodelaceae 3 100 0 0 AM only
Hemerocallidaceae 1 100 0 0 AM only
Iridaceae 8 75 13 13 AM only
Hypoxidaceae 1 100 0 0 AM only
Asteliaceae 1 100 0 0 AM only
Orchidaceae 1 2 83 98 2 0 82% ORM, 4% AM, 8% ORM+ECM, 6% mycoheterotrophy via ECM
Liliaceae 5 80 20 0 AM only
Smilacaceae 4 100 0 0 AM only
Melanthiaceae 3 67 33 0 AM only
Colchicaceae 1 100 0 0 AM only
Alstroemeriaceae 1 100 0 0 AM only
Corsiaceae 2 1 100 0 0 mycoheterotrophy via AM
Cyclanthaceae 1 0 0 100
Pandanaceae 3 33 0 67 AM only
Triuridaceae 2 2 100 0 0 mycoheterotrophy via AM
Dioscoreaceae 2 50 0 50 AM only
Burmanniaceae 2 2 100 0 0 mycoheterotrophy via AM
Nartheciaceae 1 0 100 0 AM only
Petrosaviaceae 2 2 100 0 0 mycoheterotrophy
Potamogetonaceae 7 0 14 86 AM only
Juncaginaceae 2 0 50 50 AM only
Limnocharitaceae 1 0 0 100
Alismataceae 7 57 29 14 AM only
Butomaceae 1 0 0 100
Hydrocharitaceae 4 25 0 75 AM only
Araceae 18 78 0 22 AM only
Tofieldiaceae 1 100 0 0 AM only
Acoraceae 1 100 0 0 AM only
Nymphaeaceae 5 20 0 80 AM only
non-angiosperm land plants
357
Fig. 1 (continued)
c
Total M% FM% NM% M type
rosids
Valerianaceae 4 25 25 50 AM only
Dipsacaceae 6 83 17 0 AM only
Caprifoliaceae 1 13 69 31 33 92% AM, 8% AM+ECM
Adoxaceae 1 0 0 100
Asteraceae 1 233 84 13 3 97% AM, 3% AM+ECM
Goodeniaceae 1 10 100 0 0 70% AM, 30% AM+ECM
Menyanthaceae 2 0 0 100
Campanulaceae 1 21 81 14 5 95% AM, 5% AM+ECM
Apiaceae 1 46 65 24 11 98% AM, 2% ECM
Pittosporaceae 1 100 0 0 AM only
Araliaceae 9 67 0 33 AM only
Aquifoliaceae 1 3 100 0 0 67% AM, 33% AM+ECM
Solanaceae 20 85 10 5 AM only
Convolvulaceae 12 92 0 8 AM only
Lentibulariaceae 2 0 0 100
Scrophulariaceae 58 40 26 34 AM only
Acanthaceae 6 100 0 0 AM only
Lamiaceae 69 78 16 6 AM only
Verbenaceae 15 100 0 0 AM only
Bignoniaceae 9 89 0 11 AM only
Plantaginaceae 10 100 0 0 AM only
Pedaliaceae 1 100 0 0 AM only
Gesneriaceae 2 100 0 0 AM only
asterids
Amaranthaceae 42 36 19 45 AM only
Caryophyllaceae 1 54 15 26 59 95% AM, 5% AM+ECM
Polygonaceae 1 38 29 24 47 80% AM, 10% ECM, 10% AM+ECM
Plumbaginaceae 3 33 67 0 AM only
Tamaricaceae 2 100 0 0 AM only
Frankeniaceae 2 50 0 50 AM only
Droseraceae 3 0 67 33 AM only
Dilleniaceae 1 100 0 0 AM only
* Ericaceae: MTM is mycoheterotrophic. 9% others include 1.3% AM, 1.3% endoM, 1.3% ABM, 1.3% ABM+ECM,
1.3% ABM+ERM, 1.3% Mono M+ERM, 1.3% ERM+ABM+ECM+EEM
358
Fig. 1 (continued)
d
Total M% FM% NM% M type
The very different evolutionary pattern of ECM from ericaceous mycorrhizas share many characteristics with
that of AM might suggest a different underlying genetic ECM, but exhibit a high degree of intracellular penetration
mechanism. Also, the structure is quite different between (Smith and Read 1997). Brundrett (2002) suggested that
the two types of mycorrhizas. In ECM, the fungal hyphae ABM, MTM, and ERM were derived from ECM. Our
do not penetrate the cell wall, and instead form a Hartig net mapping of ECM and these other types of mycorrhizas
(an intercellular meshwork in the root epidermis and onto the land plant phylogeny and examination of their
cortex) and a sheath around the root derived from this net. distribution within Ericaceae supports this interpretation.
On the other hand, the fungal hyphae in AM penetrate the Further, we add that EEM probably represents a transitional
cell wall and often form arbuscules. At present, little is stage between ECM and the three types of ericaceous
known about the molecular genetic basis of ECM devel- mycorrhizas, ABM, MTM, and ERM, as ECM and EEM
opment. All plant genes involved in mycorrhizal symbiosis are found only in the basal lineages of Ericaceae,
identified so far control AM development (Stracke et al. Monotropoideae, and Arbutoideae (Kron et al. 2002).
2002; Liu et al. 2003; Ane et al. 2004; Demchenko et al. Previous studies have identified the fungal symbionts of
2004; Levy et al. 2004). One of these genes has a homolog the ericaceous mycorrhizas. One interesting phenomenon
in the moss Physcomitrella patens and several other early is that the fungal strains isolated from these three types of
land plants (Wang and Qiu, unpublished data). Hence, it mycorrhizas can also form ECM with other plant species
can be inferred that there might be a general genetic (reviewed by Smith and Read 1997). This observation
program in plants that mediates plant–fungus interaction, a strongly suggests a close relationship between ECM and
small portion of which might even be involved in plant– the ericaceous mycorrhizas. An interesting question that
fungal pathogen interaction as well (Harrison 1999). This arises is why the same fungi cannot penetrate into root cells
program was most likely established at the beginning of of ectomycorrhizal hosts yet are able to do so with
land plant evolution, if not earlier, and mostly targets ericaceous plants. One answer could be that host plants
glomeromycetous fungi. It has been inherited in land plants play an important role in controlling development of
since its inception and is responsible for the prevalence of different types of mycorrhizas.
AM seen today. When ECM evolved in a particular plant
lineage, the homobasidiomycetous fungi might have
adopted much of this general genetic program, but also Orchid mycorrhiza
modified some aspects of it to suit a slightly different
plant–fungus partnership. One intriguing question is how Orchid mycorrhiza (ORM) is generally thought to be
different plant lineages, particularly those as diverse as restricted to the Orchidaceae, which involve mostly
ferns, gymnosperms, and angiosperms, adapted the general basidiomycetous fungi (Leake 1994). Occurrence of this
genetic program for ECM development, as the structures of type of mycorrhiza in other plants such as the subterranean
mycorrhizas are apparently very similar between these nonphotosynthetic liverwort Cryptothallus mirabilis
diverse lineages. Perhaps different genes are involved in (Ligrone et al. 1993; Bidartondo et al. 2003) and the
each case, thus, the host specificity developed with monocot Thismia sp. (Brundrett 2002 see http://www.
different fungal symbionts in each case of ECM (as ffp.csiro.au/research/mycorrhiza/) probably represents
opposed to AM). Indeed, difference in gene expression was functional and structural convergence, as the fungal
observed to be related to host specificity (Le Quere et al. partners are of different types than those of the true ORM
2004). Future work will likely reveal more details to help in Orchidaceae (Leake 1994). In this perspective, ORM,
us understand how many independent conversions of ECM like the ericaceous mycorrhizas discussed above, can be
from AM had occurred. considered to occur exclusively in one plant family,
Orchidaceae, and probably represents a highly specia-
lized type of ectomycorrhiza. One fact supporting this
The ericaceous mycorrhizas and their close idea is that some species of lower Epidendroideae, an
relationship to ectomycorrhiza early-diverging lineage within Orchidaceae (Cameron et
al. 1999), still have ECM (Bidartondo et al. 2004;
There are six types of mycorrhizas in Ericaceae. With the Selosse et al. 2004).
exception of AM, five of them are partnerships between
ascomycetous or basidiomycetous fungi and plants: ECM,
ectendomycorrhiza (EEM), arbutoid mycorrhiza (ABM), Did evolution of ectomycorrhiza and its derived types
monotropoid mycorrhiza (MTM), and ericoid mycorrhiza of mycorrhizas spur diversification of plant lineages
(ERM). Among these five types, ECM occurs in many that harbor these symbiotic systems?
plant lineages outside of Ericaceae (see above), and EEM is
found in Pinaceae, Araucariaceae, Ericaceae, Salicaceae, If AM was instrumental in the origin and subsequent
Fabaceae, Betulaceae, and Cistaceae (Fig. 1). ABM, MTM, diversification of land plants in a newly exploited niche,
and ERM can be deemed to be genuinely ericaceous did evolution of ECM and its derived types of mycorrhizas,
mycorrhizas, as they occur almost exclusively in this which involve Ascomycetes and Basidiomycetes, contri-
family. The only exception is ERM, which has also been bute to diversification of plant lineages that forged these
found in Diapensiaceae, a close relative of Ericaceae. The new partnerships? Our review provides a rather positive
360
answer to this question. In plant families where ECM and Hence, evolution of mycoheterotrophy reinforces the
its derivatives are the main types of mycorrhizas or account evolutionary parallelism commonly seen in mycorrhizal
for a significant percentage (>20%), e.g., Pinaceae, Orchi- evolution, which has dominated evolution of ECM as
daceae, Nyctaginaceae, Polygonaceae, Ericaceae, Aqui- discussed above and loss of mycorrhiza to be discussed
foliaceae, Salicaceae, Fagaceae, Betulaceae, Cistaceae, below. Although one may think that an exploitative
Dipterocarpaceae, Myrtaceae, and Melastomataceae relationship such as mycoheterotrophy can be evolutiona-
(Mabberley 1987), the species number is often high to rily unstable, which seems to be supported by the general
very high in comparison to their close relatives that have paucity of species in most clades of mycoheterotrophic
AM (Fig. 1). In the case of woody plants, the members of plants (Leake 1994), this unique type of interaction among
these families are often dominant species in their more than two species of very different modes of nutrition
communities (Malloch et al. 1980). Although there are uptake (autotrophy and heterotrophy) might have played a
many factors that may affect speciation rate, we believe special role to facilitate some major transitions during land
that the correlation between high occurrence rate of ECM plant evolution. In the case of lycophytes and ferns,
and its derived types of mycorrhizas and the species mycoheterotrophy probably helped to ease the transition
richness of plant clades that harbor these symbiotic from a gametophyte generation-dominant life cycle in
systems are not coincidental. This observation becomes bryophytes to a sporophyte generation-dominant life cycle
particularly striking when compared to mycoheterotro- in vascular plants. For most Orchidaceae, mycoheterotro-
phy, another type of plant–fungus symbiosis, which will phy has perhaps alleviated the problem of extremely small
be discussed below. Because ascomycetous and basidio- size of the seeds, which can be advantageous for dispersal
mycetous mycorrhizal fungi have a much higher host but at the same time, limits nutrition packaging for the next
specificity than glomeromycetous fungi (Horton and generation, and thus has probably contributed significantly
Bruns 1998; Newton and Haigh 1998; Bidartondo and to the success of the family. These two examples once
Bruns 2002), diversification of the plant hosts had likely again highlight the important roles played by fungi not only
in turn driven the speciation rate of the fungal symbionts. in the origin, but also in many subsequent radiations of land
This coevolutionary arms race probably explains the large plant evolution.
number of Basidiomycetes that are ectomycorrhizal today
(Molina et al. 1992). In comparison, AM has obviously
contributed very little to the diversification of glomer- Many independent losses of mycorrhiza in land plants
omycetous fungi, and the relatively low host specificity of
these fungi may be to blame. Many families of land plants have not been found to form
mycorrhizas with fungi in their natural habitats. In
liverworts, no fungal association has been observed in
Mycoheterotrophy Blasiaceae, Ricciaceae, Metzgeriaceae, Radulaceae, Por-
ellaceae, Jubuliaceae, Lejeuneaceae, or Herbertaceae. In
Mycoheterotrophy represents a shift of balanced mutualis- pteridophytes, species in Isoetaceae and Azollaceae are
tic symbiosis between plants and fungi toward an nonmycorrhizal. Similarly in angiosperms, species in
exploitative use of mycorrhizal fungi by plants that are Nymphaeaceae, Butomaceae, Limnocharitaceae, Cyclan-
no longer fully photosynthetic (Leake 1994). It is clearly a thaceae, Cannaceae, Loranthaceae, Loasaceae, Lentibular-
derived condition in mycorrhizal evolution. In our survey, iaceae, Menyanthaceae, Adoxaceae, Eryothroxylaceae, and
we found that mycoheterotrophy had evolved many times Bataceae are nonmycorrhizal. In addition, nonmycorrhizal
independently in land plants, in the following families: species occur together with mycorrhizal species in many
Aneuraceae, Podocarpaceae, Petrosaviaceae, Burmannia- families, and approximately half of the ten or more species
ceae, Triuridiaceae, Corsiaceae, Orchidaceae, Ericaceae examined in the following families are nonmycorrhizal:
(Monotropoideae), Gentianaceae, and Polygalaceae (Fig. 1). Geocalycaceae, Jungermanniaceae, Lycopodiaceae, Hyme-
The mycoheterotrophy in the moss genus Buxbaumia needs nophyllaceae, Gleicheniaceae, Pteridaceae, Adiantaceae,
more thorough investigation (Leake 1994). In addition, Aspleniaceae, Thelypteridaceae, Dryopteridaceae, Polypo-
gametophytes of Lycopodium, Psilotum, and Botrychium are diaceae, Cyperaceae, Polygonaceae, Amaranthaceae, Cary-
also mycoheterotrophic (reviewed by Brundrett 2002). How- ophyllaceae, Crassulaceae, and Brassicaceae (Table 1,
ever, it has been suggested that mycoheterotrophy in these Fig. 1). The fact that these families are deeply embedded
latter cases and most species of Orchidaceae may be different among mycorrhizal families and are not closely related to
from that in other plant groups mentioned above (Bidartondo each other provides convincing evidence that these plants
2005) because these plants only engage in mycoheterotrophy lost their ability to form mycorrhiza independently.
for a part of their life cycles during establishment, and they are There are two interesting features for phylogenetic
photosynthetic for the rest of their life cycles and enter distribution of nonmycorrhizal plants. One is that leafy
mutualistic symbiosis with mycorrhizal fungi. liverworts and pteridophytes in general tend to have a high
The independent evolution of mycoheterotrophy in concentration of nonmycorrhizal species. Of course,
many unrelated lineages of land plants is further under- mosses, as an entire clade, lack mycorrhiza as well (Read
scored by the fact that it evolved repeatedly from AM and et al. 2000) except Takakia (Boullard 1988). Gymno-
ECM and ECM-derived types of mycorrhizas (Fig. 1). sperms, on the other hand, are all mycorrhizal and almost
361
all obligately mycorrhizal. Angiosperms generally are also Areas of further study
mycorrhizal, and have only a few groups that have a high
percentage of nonmycorrhizal species, alismatids (includ- This study and those by Trappe (1987) and Harley and
ing Araceae according to Stevens’ (2004) new classifica- Harley (1987) represent the three most extensive surveys of
tion system, see Fig. 1b), Cyperaceae, caryophyllids, and mycorrhizal occurrence in land plants, but the total number
Brassicaceae. This feature may be related to the fact that of species included in the three studies is only slightly over
early land plants had not fully adapted to the symbiotic 10,000 (assuming that there is little overlap among the
system with the fungi. Indeed, these plants generally have three surveys), which is about 3% of all listed land plant
the Paris-type AM, which lacks well-developed systems of species that live on our planet. As can be seen from Table 1
intercellular hyphae and do not always form arbuscules and Fig. 1, for most plant families we have knowledge of
(Read et al. 2000). It will be interesting to see if future the mycorrhizal status for only one or a few species. Hence,
studies can demonstrate that a simpler genetic system is the first area that deserves more attention in the future is the
behind this rather unstable symbiotic relationship in basal investigation of mycorrhizal status of more species. From
land plants. The other feature is that almost all nonmycor- this study and those by Trappe (1987) and Harley and
rhizal plants are derived from ancestors that engaged in Harley (1987), as well as several reviews published earlier
AM symbiosis. In the several families where ECM and on this topic (Pirozynski and Malloch 1975; Malloch et al.
ECM-derived mycorrhizas dominate or account for a large 1980; Selosse and Le Tacon 1998; Read et al. 2000;
percentage, e.g., Pinaceae, Orchidaceae, Ericaceae, Brundrett 2002), it is clear that mycorrhizas were instru-
Myrtaceae, Salicaceae, Fagales, and Cistaceae, very few mental in the origin and subsequent diversification of land
species are nonmycorrhizal. This feature is perhaps related plants and are continuing to play a vital role in maintaining
to the highly specialized nature of the ECM symbiosis. floristic diversity and ecosystem function on earth. Thus,
As to the mechanisms responsible for mycorrhizal loss, mycorrhizal symbiosis should be viewed as an integral part
Trappe (1987) noticed several characters that tend to be of any floristic, ecological, or evolutionary studies in the
shared by nonmycorrhizal species, and his observations future.
still hold true here. First, many nonmycorrhizal vascular Besides the general increase of mycorrhizal research, a
plants grow in aquatic or wetland habitat. In these few specific areas should be pursued. First, more basal land
environments, both nutrients and water supplies are not plants should be investigated, as they occupy an especially
as limited as in the typical terrestrial environment. Hence, important position in our understanding of the origin of
the plants can develop independence from the fungal mycorrhizal symbiosis in land plants. Despite several
symbionts and reduce the carbon cost that would normally studies on basal land plants (Pocock and Duckett 1985;
be provided to the fungal partners in exchange for nutrients Duckett et al. 1991; Read et al. 2000), our knowledge on
and water. The loss of mycorrhiza in alismatids and other phylogenetically critically positioned taxa such as Treubi-
aquatic plants likely occurred through this mechanism. aceae, many simple thalloid liverworts, mosses, and some
Second, species that grow in nutrient-rich environments hornworts, remains fragmentary. In this regard, mosses
tend to be nonmycorrhizal. The ruderals in caryophyllids, deserve special attention, as they represent the only major
Brassicaceae, and Crassulaceae, and the spring ephemerals clade of land plants that is nonmycorrhizal (Read et al.
in Ranunculaceae, Papaveraceae, and Saxifragaceae be- 2000), a situation which by itself is very puzzling. Several
long to this category. Third, the plants that have a long, basal moss lineages such as Andreaeaceae, Tetraphidaceae,
fine, and highly branched root system with well-developed Polytrichaceae, Buxbaumiaceae, and Diphysciaceae all
root hairs also have a high tendency to become grow on nutrient-poor, sandy soil or rocks. It will be
nonmycorrhizal. Cyperaceae and the ruderals perhaps interesting to know how they manage to grow on these
developed independence from fungal symbionts through poor substrates if they are truly nonmycorrhizal. Takakia, a
this route. It has been suggested that root hairs and sister group to all other mosses, is reported to be
mycorrhizal fungi were two alternative mechanisms for mycorrhizal (Boullard 1988) and grows on thin soil and
plant nutrient uptake (Baylis 1970; Koide 1991). If a plant rocks (Gao 2000). Second, several early-diverging lineages
can absorb sufficient nutrients through its own root hairs, of angiosperms, Amborella, Austrobaileyales, Chloranth-
any genetic changes preventing the formation of mycor- aceae, and magnoliids should be investigated; the informa-
rhiza with fungi would be favorably selected. Besides these tion on their mycorrhizal status is currently lacking. Even
three observations made by Trappe (1987), we also noticed when Trappe’s (1987) survey is included, our knowledge
that many liverworts that lack fungal association are leaf of these plants is still quite poor. A focused study on these
and bark epiphytes, e.g., Radulaceae, Jubulaceae, Porella- plants will fill an important gap in our understanding of
ceae, and Lejeuneaceae. A possible explanation could be mycorrhizal evolution in early angiosperms. Finally, as we
that fungal development is thwarted by defense mecha- learn more from studies of model organisms such as
nisms of the plant on which these epiphytes live. legumes (Stracke et al. 2002; Liu et al. 2003; Ane et al.
2004; Demchenko et al. 2004; Levy et al. 2004), char-
acterization of molecular aspects of mycorrhizas in
nonmodel organisms will significantly expand the dimen-
sion and depth of our knowledge of this important
symbiotic system. In summary, the mycorrhizal research
362
conducted over the last several decades has brought this Fitter AH, Moyersoen B (1996) Evolutionary trends in root–microbe
long neglected field into mainstream biology, and future symbioses. Philos Trans R Soc Lond B 351:1367–1375
Gao C (2000) Takakiaceae. In: Yunnanica F (ed) Kunming Institute
research will undoubtedly further enhance our under- of Botany, Chinese Academy of Sciences , vol. 17, Bryophyta:
standing of this important biological interaction and its Hepaticae, Anthocerotae. Science, Beijing, pp 1–2
impact on the evolution of both plants and fungi, as Gemma JN, Koske RE, Flynn T (1992) Mycorrhizae in Hawaiian
well as the establishment and functioning of the terrestrial pteridophytes: occurrence and evolutionary significance. Am J
Bot 79:843–852
ecosystem. Grolle R (1983) Nomina generica Hepaticarum; references, types
and synonymies. Acta Bot Fenn 121:1–62
Acknowledgements We would like to thank Rong-rong Xu for Groth-Malonek M, Pruchner D, Grewe F, Knoop V (2005)
helping with figure preparation, Malini Jane Sridharan for critically Ancestors of trans-spliced mitochondrial introns support serial
reading the manuscript, and Jim Trappe and two reviewers for their sister group relationships of hornworts and mosses with
insightful comments. This work was supported by an Early Career vascular plants. Mol Biol Evol 22:117–125
Award (DEB 0332298) and ATOL grants (DEB 0431239, DEB Harley JL, Harley EL (1987) A check-list of mycorrhiza in the
0531689) from NSF to Y-L Qiu. British flora. New Phytol 105:1–102
Harrison MJ (1999) Molecular and cellular aspects of the arbuscular
mycorrhizal symbiosis. Annu Rev Plant Physiol Plant Mol Biol
50:361–389
References Hibbett DS, Gilbert L-B, Donoghue MJ (2000) Evolutionary
instability of ectomycorrhizal symbiosis in basidiomycetes.
Ane JM, Kiss GB, Riely BK, Penmetsa RV, Oldroyd GED, Ayax C, Nature 407:506–508
Levy J, Debelle F, Baek JM, Kalo P, Rosenberg C, Roe BA, Hickey LJ, Doyle JA (1977) Early Cretaceous fossil evidence for
Long SR, Denarie J, Cook DR (2004) Medicago truncatula- angiosperm evolution. Bot Rev 43:3–104
DMI1 required for bacterial and fungal symbioses in legumes. Horton TR, Bruns TD (1998) Multiple-host fungi are the most
Science 303:1364–1367 frequent and abundant ectomycorrhizal types in a mixed stand
Baylis GTS (1970) Root hairs and phycomycetous mycorrhizas in of Douglas fir (Pseudotsuga menziesii) and bishop pine (Pinus
phosphorus-deficient soil. Plant Soil 33:713–716 muricata). New Phytol 139:331–339
Bidartondo MI (2005) The evolutionary ecology of myco-hetero- Kenrick P, Crane PR (1997) The origin and early diversification
trophy. New Phytol 167:335–352 of land plants: a cladistic study. Smithsonian Institution,
Bidartondo MI, Bruns TD (2002) Fine-level mycorrhizal specificity Washington DC
in the Monotropoideae (Ericaceae): specificity for fungal Koide RT (1991) Nutrient supply, nutrient demand and plant
species groups. Mol Ecol 11:557–569 response to mycorrhizal infection. New Phytol 117:365–386
Bidartondo MI, Bruns TD, Weiß M, Sergio C, Read DJ (2003) Koide RT, Mosse B (2004) A history of research on arbuscular
Specialized cheating of the ectomycorrhizal symbiosis by an mycorrhiza. Mycorrhiza 14:145–163
epiparasitic liverwort. Proc R Soc Lond B 270:835–842 Kerp H, Trewin NH, Hass H (2004) New gametophytes from the
Bidartondo MI, Burghardt B, Gebauer G, Bruns TD, Read DJ Early Devonian Rhynie chert. Trans R Soc Edinb Earth Sci
(2004) Changing partners in the dark: isotopic and molecular 94:411–428
evidence of ectomycorrhizal liaisons between forest orchids Kron KA, Judd WS, Stevens PF, Crayn DM, Anderberg AA, Gadek
and trees. Proc R Soc Lond B 271:1799–1806 PA, Quinn CJ, Luteyn JL (2002) Phylogenetic classification of
Boullard B (1988) Observations on the coevolution of fungi and Ericaceae: molecular and morphological evidence. Bot Rev
hepatics. In: Pirozynski KA, Hawksworth DL (eds) Coevolu- 68:335–423
tion of fungi with plants and animals. Academic, London, Leake JR (1994) The biology of mycoheterotrophic (‘saprophytic’)
pp 107–124 plants. New Phytol 127:171–216
Brundrett MC (2002) Coevolution of roots and mycorrhizas of land LePage BA, Currah RS, Stockey RA, Rothwell GW (1997) Fossil
plants. New Phytol 154:275–304 ectomycorrhizae from the Middle Eocene. Am J Bo t
Bruns TD, Shefferson RP (2004) Evolutionary studies of ectomy- 84:410 – 4 1 2
corrhizal fungi: recent advances and future directions. Can J Le Quere A, Schutzendubel A, Rajashekar B, Canback B, Hedh J,
Bot 82:1122–1132 Erland S, Johansson T, Tunlid A (2004) Divergence in gene
Cameron KM, Chase MW, Whitten WM, Kores PJ, Jarrell DC, expression related to variation in host specificity of an
Albert VA, Yukawa T, Hills HG, Goldman DH (1999) A ectomycorrhizal fungus. Mol Ecol 13:3809–3819
phylogenetic analysis of the Orchidaceae: evidence from rbcL Levy J, Bres C, Geurts R, Chalhoub B, Kulikova O, Duc G, Journet
nucleotide sequences. Am J Bot 86:208–224 EP, Ane JM, Lauber E, Bisseling T, Denarie J, Rosenberg C,
Carafa A, Duckett JG, Ligrone R (2003) Subterranean gametophytic Debelle F (2004) A putative Ca2+ and calmodulin-dependent
axes in the primitive liverwort Haplomitrium harbour a unique protein kinase required for bacterial and fungal symbioses.
type of endophytic association with aseptate fungi. New Phytol Science 303:1361–1364
160:185–197 Ligrone R, Lopes C (1989) Cytology and development of a
Cronquist A (ed) (1981) An integrated system of classification of mycorrhiza-like infection in the gametophyte of Conocephalum
flowing plants. Columbia Univ Press, New York conium (L.) Dum. (Marchantiales, Hepatophyta). New Phytol
Demchenko K, Winzer T, Stougaard J, Parniske M, Pawlowski K 111:423–433
(2004) Distinct roles of Lotus japonicus SYMRK and SYM15 in Ligrone R, Pocock K, Duckett JG (1993) A comparative ultrastruc-
root colonization and arbuscule formation. New Phytol tural study of endophytic basidiomycetes in the parasitic
163:381–392 achlorophyllous hepatic Cryptothallus mirabilis and the closely
Dombrovska O, Qiu Y-L (2004) Distribution of introns in the allied photosynthetic species Aneura pinguis (Metzgeriales).
mitochondrial gene nad1 in land plants: phylogenetic and Can J Bot 71:666–679
molecular evolutionary implications. Mol Phylogenet Evol Liu JY, Blaylock LA, Endre G, Cho J, Town CD, VandenBosch KA,
32:246–263 Harrison MJ (2003) Transcript profiling coupled with spatial
Duckett JG, Renzaglia KS, Pell K (1991) A light and electron expression analyses reveals genes involved in distinct devel-
microscope study of rhizoid–ascomycete associations and opmental stages of an arbuscular mycorrhizal symbiosis. Plant
flagelliform axes in British hepatics with observations on the Cell 15:2106–2123
effects of the fungi on host morphology. New Phytol
118:233–257
363
Lutzoni F, Kauff F, Cox CJ, McLaughlin D, Celio G, Dentinger B, Russell J, Bulman S (2005) The liverwort Marchantia foliacea
Padamsee M, Hibbett D, James TY, Baloch E, Grube M, Reeb forms a specialized symbiosis with arbuscular mycorrhizal
V, Hofstetter V, Schoch C, Arnold AE, Miadlikowska J, fungi in the genus Glomus. New Phytol 165:567–579
Spatafora J, Johnson D, Hambleton S, Crockett M, Shoemaker Schussler A, Schwarzott D, Walker C (2001) A new fungal phylum,
R, Hambleton S, Crockett M, Shoemaker R, Sung GH, Lucking the Glomeromycota: phylogeny and evolution. Mycol Res
R, Lumbsch T, O’Donnell K, Binder M, Diederich P, Ertz D, 105:1413–1421
Gueidan C, Hansen K, Harris RC, Hosaka K, Lim YW, Selosse MA, Faccio A, Scappaticci G, Bonfante P (2004)
Matheny B, Nishida H, Pfister D, Rogers J, Rossman A, Chlorophyllous and achlorophyllous specimens of Epipactis
Schmitt I, Sipman H, Stone J, Sugiyama J, Yahr R, Vilgalys R microphylla (Neottieae, Orchidaceae) are associated with
(2004) Assembling the fungal tree of life: progress, classifica- ectomycorrhizal septomycetes, including truffles. Microb Ecol
tion and evolution of subcellular traits. Am J Bot 91:1446–1480 47:416–426
Mabberley DJ (1987) The plant-book—a portable dictionary of the Selosse MA, Le Tacon F (1998) The land flora: a phototroph–
higher plants. Cambridge Univ Press, Cambridge fungus partnership? Trends Ecol Evol 13:15–20
Malloch DW, Pirozynski KA, Raven PH (1980) Ecological and Smith SE, Read DJ (1997) Mycorrhizal symbiosis, 2nd edn.
evolutionary significance of mycorrhizal symbioses in vascular Academic, San Diego
plants (A review). Proc Natl Acad Sci U S A 77:2113–2118 Soltis DE, Soltis PS, Chase MW, Mort ME, Albach DC, Zanis M,
Molina R, Massicotte H, Trappe JM (1992) Specificity phenomena Savolainen V, Hahn WH, Hoot SB, Fay MF, Axtell M,
in mycorrhizal symbiosis: community–ecological consequences Swensen SM, Prince LM, Kress WJ, Nixon KC, Farris JS
and practical implications. In: Allen MF (ed) Mycorrhizal (2000) Angiosperm phylogeny inferred from 18S rDNA, rbcL,
functioning. Chapman & Hall, London, pp 357–423 and atpB sequences. Bot J Linn Soc 133:381–461
Newman EI, Reddell P (1987) The distribution of mycorrhizas Stevens PF (2004) Angiosperm phylogeny website. Version 5. http://
among families of vascular plants. New Phytol 106:745–751 www.mobot.org/MOBOT/research/APweb/. Cited May 2004
Newton AC, Haigh JM (1998) Diversity of ectomycorrhizal fungi in Stracke S, Kistner C, Yoshida S, Mulder L, Sato S, Kaneko T,
Britain: a test of the species–area relationship, and the role of Tabata S, Sandal N, Stougaard J, Szczyglowski K, Parniske M
host specificity. New Phytol 138:619–627 (2002) A plant receptor-like kinase required for both bacterial
Pirozynski KA, Malloch DW (1975) The origin of land plants: and fungal symbiosis. Nature 417:959–962
a matter of mycotrophism. Biosystems 6:153–164 Stubblefield SP, Taylor TN, Trappe JM (1987) Vesicular–arbuscular
Pocock K, Duckett JG (1985) On the occurrence of branched and mycorrhizae from the Triassic of Antarctica. Am J Bot
swollen rhizoids in British hepatics: their relationships with 74:1904–1911
the substratum and associations with fungi. New Phytol Taylor TN, Hass H, Remy W (1992) Devonian fungi: interactions
99:281–304 with the green alga Paleonitella. Mycologia 84:901–910
Qiu Y-L, Cho Y, Cox JC, Palmer JD (1998) The gain of three Taylor TN, Hass H, Kerp H (1999) The oldest fossil ascomycetes.
mitochondrial introns identifies liverworts as the earliest land Nature 399:648
plants. Nature 394:671–674 Taylor TN, Kerp H, Hass H (2005) Life history biology of early land
Qiu Y-L, Lee J (2000) Transition to a land flora: a molecular plants: deciphering the gametophyte phase. Proc Natl Acad Sci
phylogenetic perspective. J Phycol 36:799–802 U S A 102:5892–5897
Read DJ, Duckett JG, Francis R, Ligrone R, Russell A (2000) Trappe JM (1987) Phylogenetic and ecologic aspects of mycotrophy
Symbiotic fungal associations in ‘lower’ land plants. Philos in the angiosperms from an evolutionary standpoint. In: Safir
Trans R Soc Lond B 355:815–831 GR (ed) Ecophysiology of VA mycorrhizal plants. CRC, Boca
Redecker D, Kodner R, Graham LE (2000) Glomalean fungi from Raton, pp 5–25
the Ordovician. Science 289:1920–1921 Trappe JM (1996) What is a mycorrhiza? In: Azcon-Aguilar C,
Remy W, Taylor TN, Hass H, Kerp H (1994) Four hundred-million- Barrea J-M (eds) Mycorrhiza in integrated systems–from genes
year-old vesicular arbuscular mycorrhizae. Proc Natl Acad Sci to plant development. Proceedings of the 4th European
U S A 91:11841–11843 Symposium on Mycorrhizae, EC Report EUR 16728, Luxem-
Renzaglia KS, Duff RJ, Nickrent DL, Garbary DJ (2000) Vegetative bourg, pp 3–6
and reproductive innovations of early land plants: implications Wellman CH, Osterloff PL, Mohiuddin U (2003) Nature 425:
for a unified phylogeny. Philos Trans R Soc Lond B 355: 282–285
769–793 Zhao Z-W (2000) The arbuscular mycorrhizas of pteridophytes in
Yunnan, southwest China: evolutionary interpretations.
Mycorrhiza 10:145–149