ARTICLE 245

et

: the “/ , Martin I. group B 4 Densospora 2017b). et al. Endogonales (Tedersoo sensu Yamamoto 3*4 Densosporaceae Endogone endophytes Jimgerdemannia multigene phylogeny Endogone Mucoromycotina et al. 2017a, Yamamoto Nothofagus

group C , James M. Trappe 3 and ·MSS!! in vitro. However, a few have been 2015b; Yamamoto Yamamoto 2015b; et al. Sphaerocreas

Endogonaceae species Eucalyptus and et al. 2015a, Orchard et al. 2016), many lineages of , Matthew E. Smith 1 Densospora, and includes the type species, F=@L<@ELBLWIBW@HB@?=ZZG?@?@HB@@HGWGLVgenus (McGee 1996) associated and with uncultured ectomycorrhizal fungi al. 2008); the “/endogone1 lineage” ( @HB@ >BJG %© B>MXE[OB@EMucoromycota. Many species in this order

HBDF<=D?EZLE[OBL@=LVG?ODEFGVVE„GD?E@WBLV using sporophores collected over the past three , Natalie Vande , Pol Natalie Vande 2 consists of the genus as the will be important for understanding fungal innovations Sclerogone Endogonales Endogonales Glomeromycotina , Alison , Jacob 2 E. pisiformis Endogonales Densosporaceae Endogonaceae participate in participate Endogone 1995) and the fossil the and 1995) et al. and is represented by the gen. nov. Members of that gen. genus nov. ( 1 and are characterized by above- and below-ground sporophores, a hollow and  V=G @< XE>E@GV O

(Wu & Lin 1997), Lin & (Wu Peridiospora 1 (Krings Densosporaceae Youngiomyce Endogonaceae is an order of early diverging fungi that belong Endogone , and Gregory Bonito Endogonaceae 2,5 , and many diverse lineages known only from environmental DNA sequences of plant-endosymbiotic Endogonales  7<=>=?@B@@DEF=@G@HGIBLLGD?MGOE[GVFW@HGB=@HFEBWL<@BX@GD  7<=>BWL<@=?G@HE?I>GDOEBXM=DM

Southern Hemispheres, sporophores of most of these fungi fungi these of most of sporophores and Hemispheres, Northern Southern the in habitats tropical and temperate across to belong plants with Endogone-related Mucoromycotina associated as the ancestral fungal mutualists of land plants (Field plants land of mutualists fungal ancestral the as of paradigm the challenge and symbionts, of Field by (Bidartondo plants environments land early terrestrial of colonization the during role Mucoromycotina Yamamoto etal.2015). and “/endogone3” were both within al. 2017b). The ectomycorrhizal fungal lineages “/endogone2" and generated from sequences putatively related to the saprotrophic DNA environmental on position. based is phylogenetic lineage” “/endogone3 their The about information no is there so taxa these for available are data sequence no but 1990) and (WarcupSclerogone eucalypti 1990). Youngiomyces(Yao aggregatus endogone2 lineage” with and the Yamamoto sensu 1882), members of and whether order,uncertainty still the within taxa the of relationships phylogenetic the of resolution poor is there above), (see genera extant four (Stürmer 2012). XELGBZG?HB„GFGGLELB?@B@G<[\=”<„GD@HGMB?@ of systematics and taxonomy the Given their range in diversity, morphology, and growth habits, Tandy1974, Trappe (Gerdemann & liverworts basidiomes, and mosses polypore amongst or decaying litter, leaf twigs, or wood heavily upon decayed or within sporophores produce may species epigeous some although hypogeous, often and enclosed or of Sporophores zygospores. of production the to by lead that gametangia reproduction apposed compatible sexual of result the are sporophores The sporophores. macroscopic produce to kingdom fungal the and ectomycorrhizal and mycorrhizal arbuscular from independent represent an early origin of a symbiotic nutrition mode by fungi, and fungi (Bonfante & Desirò 2017). Given that plants between interactions symbiotic of evolution the in role a played have might MRE understood, poorly still is bacteria spores (Desirò and mycelia their in (MRE) endobacteria Mollicutes-related to Similar 2015a). prpoe (sooap” cnann a ag nme of number zygospores. large a containing (“sporocarps”) sporophores 2013, Field early (Bidartondo fungi of group diverging this of relationships evolutionary and diversity the in t a rcnl be hpteie ta mutualistic that hypothesized been recently has It s urnl crusrbd while circumscribed, currently As h genus The Endogone ! S. eucalyptii Brly Bom 14) ope; h “/ the complex; 1846) Broome & (Berkley ! 05) Tee tde hglgt h ecology the highlight studies These 2015a). et al. . Even though they are distributed distributed are they though Even Endogonales. et al.2015b,Orchard2017b). Endogone -like et al. 2015). Even though the biology of these Endogone fungi related to related fungi were reported to grow axenically (Warcup axenically grow to reported were Glomeromycotina Densospora 05 wih nlds ebr of members includes which 2015) et al. Mucoromycotina Quercus Dikarya is 1975, Yamamoto 1975, et al. (Saccardo (Saccardo Sphaerocreas pubescens Endogone tuberculosa(Lloyd 1918), opie seis ht produce that species comprises among , there is now renewed interest renewed now is there , Tap & edmn 1972) Gerdemann & (Trappe ectomycorrhizas (Yamamoto 2011,Desirò et al. (McGee 1995) et al. Endogone Endogone Endogone h eris lnae in lineages earliest the , ug a plant-fungal as fungi . 2011,et al. Desirò Endogone Endogone Endogone tuberculosa contains contains Endogonales 1996), and numerous Glomeromycotina Glomeromycotina played a crucial a played

r sequestrate are and, potentially,and, group A (sensu n related and Endogonales can harbour can 2015). et al. E. pisiformis 2013, et al.  WGBD? et al. et al. Desiró etal. et

and and USA wereanalyzed(Table 1). of collections Endogone 45 total, In Western (PERTH). Herbarium and Australian (OSC), Herbarium University (MEL), State Victoria Oregon of University Herbarium State National (MSC), Michigan Herbarium (FLAS), Herbarium University Florida institutions: of following the or collections private Endogone these two lineages, and also synonymize introduce in morphology, sporing habit, and potentially also ecology. We delimit two deeply divergent monophyletic lineages that differ BLVVG[LG@I<[B>EXEG?IE@HEL two of Endogonales of resolution phylogenetic the enhance to marker a as time MHWXEO BLV MHWXGD? MDGD? Waltham,MA). ArRNA18S the of fragment ampli- was gene 'DGB>ŸB“ CTAB-basedmethod (Doyle 1991). a All PCR reactions were with carried out with extracted DNA genomic and sampled was sporophore each from tissue gleba of fragment Asmall $$###$* tuberculosa 1974), Trappe & (Gerdmann incrassata of specimens fungarium Dried .$$#%($ <;59= ­D@D<„?J" To address these limitations, we generated a multigene a generated we limitations, these address To a. o. Within nov. fam. Densosporaceae pce ta wr peiul unresolved previously were that species Endogone Jimgerdemannia GG <@G [D?@ @HG [MXMXE[GVIE@HB?G>E (Thaxter 1922), from Australia, Italy, Mexico, the United Kingdom, from Italy,United Australia, the Mexico, s.str )DGGL %©’B?@GD’E” 2015). Moreover, when detected, these fungi fungi Moreover,these 2015). detected, et al. when BLV=LEVGL@E[GV Endogone Endogonales rDNA,becauseITSrDNA doesnot . Our results provide a phylogenetic placement phylogenetic a provide results Our . this into sequences DNA environmental and . Endogonales (LV&' [ sporophores, and integrated available are often conspicuously conspicuously often are Endogonales ! 'G?ED gen. nov. to accommodate one of (# #© ae o rN (8; 28S) (18S; rDNA on based Endogone Endogonales E. pisiformis ! et al. 2013) and EF3 (Smit ŸHGD>< Endogonaceae, were obtained from obtained were D> ZX $ Youngiomyces Ln 1908), (Link : #E?HGDOEGL@E[O , Endogonaceae E. oregonensis IMA FUNGUS et al. with we , E. E.

$"('*$"*1Endogonales

;#)$L List of the Endogonaceae sporophores analyzed in this study and available relative information about voucher as herbarium and/or collector number (when both are available, collector numbers are in parentheses), site and date of collection. ARTICLE ( E'.$$ .$$ .$$=#

Endogone incrassata MEXU 26467 Volcano Nevado de Colima National Park, Jalisco, 25 Sep. 2009 Mexico Endogone incrassata T32417 Cofre de Perote, Veracruz, Mexico 17 Sep. 2007 Endogone incrassata T32492 San José Teacalco, Tlaxcala, Mexico 21 Sep. 2007 Endogone oregonensis OSC 130614 Polk, Oregon, USA 23 Feb. 2008

Endogone oregonensis T36235 Benton County, Oregon, USA 14 March 2013 Endogone oregonensis AD153 Monmouth, Oregon, USA 29 Dec. 2015 Endogone pisiformis AD152 Corvallis, Oregon, USA 11 March 2017 Endogone pisiformis FLAS F-59194 (MES1451) Bartlett Experimental Forest, Carroll County, New 11 Aug. 2015 Hampshire, USA Endogone pisiformis OSC 80931 (T28028) Benton, Oregon, USA 7 Feb. 2002 Endogone pisiformis OSC 112172 (T31477) Washington, USA 24 April 2006 Endogone pisiformis OSC 149839 (T37049) White Mountain National Forest, Carroll County, New 17 Aug. 2015 Hampshire, USA Endogone pisiformis T37093 Lane County, Oregon, USA 21 May 2013 Endogone sp. MEL 2024690 Loftia Recreation Park, Adelaide Hills, Australia 26 Aug. 1984 Endogone sp. FLAS F-59071 (MES866) Ordway-Swisher Reserve, Melrose, Florida, USA 23 Feb. 2015 Endogone sp. PERTH 7567251 Atherton, Queensland, Australia 7 May 1991 Endogone sp. PERTH 7591853 Cape York, Australia - Endogone sp. PERTH 7603037 Bluewater Park, Queensland, Australia 13 April 1989 Endogone sp. PERTH 7648049 Dwellingup, Australia 10 May 2002 Endogone sp. PERTH 7648847 Dwellingup, Australia 25 June 2002 Endogone sp. PERTH 7672527 Mount Windsor Tableland, Queensland, Australia 2 Feb. 1992 Endogone sp. PERTH 8092931 Leeuwin-Naturaliste National Park, Australia 17 May 2007 Endogone sp. PERTH 8127840 Karakamia Sanctuary, Australia 4 Oct. 2006 Endogone sp. PERTH 8473986 Boorabbin National Park, Australia 20 Aug. 2009 Endogone sp. T26631 Bournda National Park, Australia 22 Nov. 2000 Endogone tuberculosa OSC 146000 (T34145) Australian Capital Territory, Australia 14 May 2010 AD002 Veglio, Piemonte, Italy 7 Sep. 2013 MSC 0242545 (AD239) Lake Lansing Park North, Haslett, Michigan, USA 7 Oct. 2016 MSC 0242546 (AD244) Lake Lansing Park North, Haslett, Michigan, USA 7 Oct. 2016 AD245 Lake Lansing Park North, Haslett, Michigan, USA 7 Oct. 2016 GB716 Lake Lansing Park North, Haslett, Michigan, USA 13 Sep. 2015 MSC 0242548 (GB737) Lake Lansing Park North, Haslett, Michigan, USA 17 Sep. 2015 RH932 Ledges State Park, Iowa, USA 27 June 2009 T33849 Bosque la Primavera, Jalisco, Mexico 2 Oct. 2009 T33851 Bosque la Primavera, Jalisco, Mexico 2 Oct. 2009 AD001 Veglio, Piemonte, Italy 7 Sep. 2013 MSC 0242547 (AD251) Mason, Michigan, USA 13 Oct. 2016 AD256 Mason, Michigan, USA 13 Oct. 2016 AM2190 Cavola, Emilia Romagna, Italy 22 July 2000 CH9142 Derbyshire, United Kingdom 12 Nov. 2012 T32409 Cofre de Perote, Veracruz, Mexico 17 Sep. 2007 T32490 San José Teacalco, Tlaxcala, Mexico 21 Sep. 2007 T32544 Huamantla, Tlaxcala, Mexico 23 Sep. 2007 T32674 Miquihuana, Tamaulipas, Mexico 2 Aug. 2008 Jimgerdemannia sp. T34745-A Main Ranges National Park, Queensland, Australia 3 June 2010 Jimgerdemannia sp. T34745-B Main Ranges National Park, Queensland, Australia 3 June 2010

VOLUME 8 · NO. 2 247 248 ARTICLE

usqet nlss Ec ainet a te trimmed then was alignment Each analyses. subsequent region ITS2 BLVEL@DGL@<[@HGGXMXE[GVIE@H@HGMDE>GD? 95 °C for 5 min, 35 cycles at 95 °C for 30 s, 55 °C for 30 for °C 55 s, 30 ? for °C 95 at cycles 35 min, 5 for °C 95 AASGGTGTRGCRT-at step initial an were: conditions cycling The CACCTTC-3’). (5’- RPB2AD1r and TATGATTC-3’) (5’-ATTCATCCSAG- RPB2AD2f or CARGCKTGYGGTC-3’) IB?B>MXE[GVIE@H@HGLGIMDE>GD?© $&'[ gene (RPB2) II polymerase RNA of subunit largest second the of fragment partial A cycles. 27 with above detailed as conditions PCR and (5’-TWCACVCTYGGYGTGCGTC-3’) EndADef1f primer forward new the with PCR semi-nested a for template as used and diluted were products PCR ful, B@ HL >X[BEL EH H?@< D>D O<>FELB- MDE>GD @I< @HG?G IE@H B>MXE[OB@EEL   %[ELBLVB[LBXG”@GL?EEL HL >X[BEL BL@ ?=OOG??- L<@ IB? B>MXE[OB@EEL $ZGLG?IGDGG”OX=VGV[D<> (# BLV©  2012) or LR0R (Vilgalys1990) LR0R Hester or & 2012) et al. 02, n wr ue a qeis for queries as used were and 2012), et al.  %[< >ELBLVB[LBXG”@GL?E- ŸHG >EL , (syn. 90. Four 1990). et al.   Densospora nuda   ©  (Torres-Cruz Sphaerocreas E. aggregata   R)&&))Ÿ- (# ZGLG %[EL (#  spp., [EXXEMXE[GV[GL?OGL? [D<> IGDG [BEX=DG? B>MXE[OB@EGL?IGDGEVGL@E[GV>EXXEGD ŸHG[D?@ZD<=MO=>  © $  Œ sp. )

$"('*$"*1Endogonales

ed to the genus Endogone whereas the second represents the (Truong et al. 2017), and uncultured ectomycorrhizal ARTICLE new genus Jimgerdemannia. The Endogone clade included Mucoromycotina (Tedersoo et al. 2008). Below we the type species, E. pisiformis, together with Youngiomyces circumscribe this monophyletic sister lineage that has been aggregatus (syn. E. aggregata; see below), E. corticioides, E. referred to previously as the Sphaerocreas-Densospora incrassata, E. magnospora, E. oregonensis, E. tuberculosa, all clade (Yamamoto et al. 2015, Truong et al. 2017) as the new @HG=LEVGL@E[GVEndogone specimens investigated, and sever- family Densosporaceae. al environmental sequences. The Endogone group was divid- GVEL@<@I<OXBVG?ŸHG[D?@OXBVGGLO<>MB??GVE. pisiformis and its sister lineage E. corticioides (Figs 1–2, Supplementary TAXONOMY Figs 1–2). Interestingly, putative ectomycorrhizal Endogone sequences (Yamamoto et al. 2017a) were nested within the =(## Desirò, M.E. Sm., Bidartondo, pisiformis-corticiodes clade together with a clade constituted Trappe & Bonito, 1#%L&. by environmental DNA sequences generated from fungal sym- MycoBank MB821851 bionts of liverworts (Bidartondo et al. 2011) (Fig. 2, Supple- mentary Fig. 2). The second clade included E. aggregata, E. Type genus: DensosporaMcGee 1996. incrassata, E. magnospora, E. oregonensis, E. tuberculosa, BLV =LEVGL@E[GV Endogone specimens. The position of the Diagnosis: The family Densosporaceae is erected here taxa within this clade was not clearly resolved by single-locus @< BMMXW @< BXX VG?OGLVBL@? <[ @HG LEXW ŸB”B IE@HEL Densosporaceae have retrieved from hornworts and liverworts clustered together MDG„E<=?XWFGGLOXB??E[GVB?FGXGlomerales BLV ?<>G BDG O=DDGL@XW OXB??E[GV B? incertae closely related to it (“group E” sensu Desirò et al. 2013) (Fig. sedis (http://www.indexfungorum.org/). However, single- 2, Supplementary Figs 1–2). A third group (“groups D and locus and multigene phylogenetic reconstructions resolve H“ sensu Desirò et al. 2013) comprised Mucoromycotina Densosporaceae as a distant sister clade of Endogonaceae spp. associated with bryophytes and ferns (Bidartondo et within the order Endogonales. Densosporaceae encompasses al. 2011; Desirò et al. 2013; Rimington et al. 2015; Field et multiple divergent monophyletic clades that mostly comprise al. BLVB[LGD<<@GLVG?H[LGD<<@GLV

VOLUME 8 · NO. 2 249 250 ARTICLE

90 Endogone (L2<;5!SW!S 100 Endogone (L2<;5!W!S! Endogone 79 Endogone (L2<;5!S+SP 95 Endogone (L2<;5!WPP! Endogone (L;WWP 100 Endogone aggregata DAR 74991 Endogone magnospora DAR 69441 98 (L2<;5!WMM+ 100 Endogone Endogone (L2<;5!WMM! Endogone (L<MW+ Endogone (L2<;5++P Endogone tuberculosa 9.MW ;PMMS 91 Endogone incrassata KPM-NC 0024213 100 Endogone incrassata KPM-NC 0024214 98 100 Endogone incrassata ;PM! ;PM+ 100 Endogone incrassata Endogonaceae Endogone (L-S+!<WW 100 Endogone oregonensis =SP Endogone oregonensis ;PWPS 100 99 Endogone pisiformis =S 100 Endogone pisiformis ;P!+P Endogone pisiformis KPM-NC 0024229 100 Endogone pisiformis KPM-NC 0024232 100 Endogone pisiformis DAOM 233144 -S++M<MS 94 Endogone pisiformis 84 Endogone corticioides A-13001-3 Endogone corticioides A-13001-4 100 Endogone corticioides A-14002

Endogone corticioides A-11001 Desiró etal. Endogone corticioides A-12001 Jimgerdemannia flammicorona EF-13002 Jimgerdemannia flammicorona ,!W Jimgerdemannia 100 Jimgerdemannia flammicorona =MS 97 Jimgerdemannia flammicorona .MSMS=P+ Jimgerdemannia flammicorona = .MSM,!P! 91 Jimgerdemannia flammicorona Jimgerdemannia flammicorona 5+P Jimgerdemannia flammicorona ;PPM+ 98 Jimgerdemannia flammicorona . MSMW=MM Jimgerdemannia flammicorona ;PPS 87 Jimgerdemannia lactiflua ;PM+ 100 Jimgerdemannia lactiflua ;PM+ Jimgerdemannia lactiflua ;PW!M ;PSMM 73 Jimgerdemannia lactiflua Jimgerdemannia lactiflua .5+M 100 Jimgerdemannia lactiflua EL-14001 100 Jimgerdemannia lactiflua = Jimgerdemannia lactiflua + Jimgerdemannia lactiflua =SW 85 Jimgerdemannia lactiflua .MSM!=S 100 Jimgerdemannia (L;PM!S-A Jimgerdemannia (L;PM!S-B 100 Densospora solicarpa DAR 69421 95 Densospora solicarpa DAR 74956 100 Sphaerocreas pubescens NBRC 109377 Densosporaceae Mucoromycotina sp. MES1534 0.03 "LLPhylogenetic reconstruction of EndogonaceaeFB?GVEXWDensosporaceae, represented by Densospora solicarpa, Sphaerocreas pubescensBLVBL=LEVGL@E[GVMucoromycotina sp., was used as outgroup. The tree shows the topology obtained with the Bayesian method; branches with Bayesian posterior probabilities

IMA FUNGUS 1  BDG@HEOJGLGVBLV’žF<<@?@DBM?=MMGL?BLBXWGVEL@HE??@=VWBDGELF

Endogonales and Glomerales into modern taxonomy Synonym: Youngiomyces Y.-J. Yao, Kew Bull. S: 350 (1995). ARTICLE before the advent of DNA and phylogenetic analyses. Type species: (Trappe & Diagnosis: Differs from Jimgerdemannia by pairing two Gerd.) Trappe et al. 2017. gametangia of similar size that fuse near their tips and the zygospores mostly then budding from the junction of the two. Diagnosis: Differs from Endogone by pairing a large gametangium with a small one, the tip of the small one fusing Discussion: Spores mostly not enveloped in appressed to the side of the large one. hyphae, or, if so then the hyphae not fused with the spore wall to form a surface ornamentation at maturity. Spores Discussion: The zygospore typically buds from the tip of the either distributed randomly among the glebal hyphae or large gametangium or occasionally from the junction of the clustered in discrete aggregations separated by hyphal two gametangia. Spores typically becoming enveloped in tissue. Phylogenetic analyses reveal that Endogone s. str. tightly appressed hyphae that fuse at maturity with the spore (as circumscribed here) and Jimgerdemannia represent wall to form a surface ornamentation. Spores are distribut- separate lineages within Endogonaceae. In contrast to ed randomly among the glebal hyphae, and not clustered. the ectomycorrhizal Jimgerdemannia, most Endogone s. HWX @HB@ Jimgerdemannia and str. species are either putatively saprotrophic or perhaps Endogone s. str. represent separate lineages within Endo- fungicolous and may be either hypogeous or epigeous, gonaceae. All known Jimgerdemannia species putatively the latter sporing on various substrates. Ectomycorrhizas form ectomycorrhizas with various species of Pinaceae and M=@B@E„GXWEVGL@E[GVB?DGXB@GV@<E. pisiformis were detected the sporophores of taxa of this group are usually hypogeous in oak forest in Japan (Yamamoto et al. 2017a). Even among host rootlets. though their functional role is unknown, some taxa within the Endogone clade have been documented as symbionts Q%"%## \#%%# (Trappe & Gerd.) of liverworts. Trappe, Desirò, M.E. Sm., Bonito, Bidartondo, Endogone pisiformis, undoubtedly the most widely %)L&L distributed species of the genus, has been reported from MycoBank MB821847 Asia, Europe, and North America and proliferates on diverse Basionym: ! Trappe & Gerd., Trans. substrates, including forest litter, brown-cubical rotted Brit. Mycol. Soc. S+: 405 (1972). wood, decaying polypore basidiomes, and among mosses. It sometimes produces sporophores at the edge of melting Q%"%##$#\# (Berk. & Broome) Trappe, snowbanks or immersed in meltwater on saturated organic Desirò, M.E. Sm., Bonito & Bidartondo, %)L&L matter. It can grow in pure culture (Jabaji-Hare & Charest 1987) MycoBank MB 821853 and produce zygospores in vitro in the absence of mycorrhiza Basionym: ! Berk. & Broome, Ann. Mag. formation (Berch & Castellano 1986). Endogone tuberculosa Nat. Hist., ser. 1, : 81 (1846). and Youngiomyces aggregatus (i.e. E. aggregata) were reported to grow on agar media (Warcup 1990). However, Discussion: Jimgerdemannia and >mammal droppings in North America (Maser et al. 1978). al. 1995). However, E. pisiformis, and rarely E. incrassata, have been reported to have zygosporangia with two <" Link, Ges. Naturf. Freunde Berlin Mag. openings (Yamamoto et al. 2015). Although the type of the Neuesten Entdeckt. Gesammten Naturk. P: 33 genus Youngiomyces (Y. caroliniensis) was not included in (1809). our phylogeny, the phylogenetic position of Y. aggregatus is nested deep within the Endogone clade (Fig. 1), close to E. Type species: Endogone pisiformis Link 1809. magnospora and other Endogone species devoid of multiple openings in their zygosporangia. For those reasons, and in line

VOLUME 8 · NO. 2 251 252 ARTICLE

status as to assigned species other the species with E. stratosa. Yamamotowith MDEXW @HG VG[LG? O'P L

Densosporaceae Endogonales Endogonaceae IMA FUNGUS $B?GV We . . $"('*$"*1Endogonales ARTICLE

100 Sphaerocreas pubescens KPM-NC 22969, AB752291 Sphaerocreas pubescens NBRC 109377, AB752295 Sphaerocreas pubescens KPM-NC 22971, AB755408 Sphaerocreas pubescens KPM-NC 22973, AB752293 Mucoromycotina sp. MIB 8353 associated with Treubia lacunosa, JF414226 Mucoromycotina sp. MIB 8349 associated with Treubia tasmanica, JF414225 Mucoromycotina sp. MIB 8356 associated with Treubia pygmaea, JF414230 Mucoromycotina Haplomitrium gibbsiae 100 sp. H2-e associated with , KJ921775 Ectomycorrhizal Mucoromycotina on Eucalyptus regnans L3138, UDB002714 100 Ectomycorrhizal Mucoromycotina on Nothofagus cunninghamii L3656, UDB004033 Densospora solicarpa DAR 74956, UDB018861 100 Densospora solicarpa DAR 69421, UDB018865 Mucoromycotina sp. MIB 8365 associated with Treubia lacunosa, JF414228 Mucoromycotina sp. T3-e associated with Treubia lacunosa, KJ921773 90 Densosporaceae Mucoromycotina sp. associated with Phaeomegaceros coriaceus, KC708432 Mucoromycotina sp. MES1534, KY487058 93 Densospora nuda DAR 69416, UDB018872 89 Mucoromycotina sp. MIB 8779 associated with Megaceros leptohymenius, KC708408 96 Mucoromycotina sp. MIB 8352 associated with Haplomitrium gibbsiae, JF414222 95 Mucoromycotina sp. MIB 8438.2 associated with Phaeoceros carolinianus, KC708393 Mucoromycotina sp. associated with Phaeoceros carolinianus, KC708431 Mucoromycotina sp. MIB 8860 associated with Anthoceros sp., KC708426 96 Mucoromycotina sp. MIB 8873 associated with Phaeoceros carolinianus, KC708428 93 Mucoromycotina sp. Th6-4 associated with Lycopodiella inundata, KJ952213 81 Mucoromycotina sp. MIB 8443 associated with Anthoceros laminiferus, KC708394 Mucoromycotina sp. Th8a-4 associated with Lycopodiella inundata, KJ952214 83 Mucoromycotina sp. MIB 8445 associated with Phaeoceros carolinianus, KC708396 100 Mucoromycotina sp. MIB 8797 associated with Phaeomegaceros coriaceus, KC708413 Mucoromycotina sp. Th6-2 associated with Lycopodiella inundata, KJ952212 100 Mucoromycotina sp. MIB 8627.1 associated with Anthoceros punctatus, KC708404 Mucoromycotina sp. associated with Anthoceros laminiferus, KC708435.1 Mucoromycotina sp. MIB 8846 associated with Phaeoceros carolinianus, KC708440 71 Mucoromycotina sp. MIB 8532 associated with Anthoceros agrestis, KC708397 Mucoromycotina sp. associated with Phaeomegaceros coriaceus, KC708429 Fine root endophyte associated with Trifolium subterraneum, KX434773 Fine root endophyte associated with Trifolium subterraneum, KX434777 Mucoromycotina sp. MIB 8771 associated with Phaeomegaceros coriaceus, KC708407 86 98 Mucoromycotina sp. MIB 8387 associated with Neohodgsonia mirabilis, JF414224 Mucoromycotina sp. associated with Phaeoceros carolinianus, KC708444 98 Mucoromycotina sp. MIB 8533 associated with Phaeoceros laevis, KC708398 100 96 Mucoromycotina sp. WR865-D associated with Anogramma leptophylla, KJ952232 84 Mucoromycotina sp. MIB 8860 associated with Anthoceros sp., KC708425 Mucoromycotina sp. MIB 8783 associated with Phaeomegaceros coriaceus, KC708409 97 Mucoromycotina sp. associated with Anthoceros laminiferus, KC708434 98 Mucoromycotina sp. MIB 8553.2 associated with Anthoceros sp., KC708400 95 91 Mucoromycotina sp. MIB 8438.2 associated with Phaeoceros carolinianus, KC708392 Fine root endophyte associated with Trifolium subterraneum, KX434782 72 Mucoromycotina sp. MIB 8771 associated with Phaeomegaceros coriaceus, KC708406 D 76 Mucoromycotina sp. MIB 8846 associated with Phaeoceros carolinianus, KC708423 100 96 Mucoromycotina sp. MIB 8842 associated with Phaeoceros dendroceroides, KC708421 Mucoromycotina sp. JD78 associated with Phaeoceros laevis, KC708438 94 Mucoromycotina sp. associated with Megaceros sp., KC708436 Mucoromycotina sp. associated with Phaeoceros carolinianus, KC708441 92 Mucoromycotina sp. MIB 8797 associated with Phaeomegaceros coriaceus, KC708415 87 Mucoromycotina sp. MIB 8802 associated with Anthoceros laminiferus, KC708417 Mucoromycotina sp. WR148.B-B associated with Lycopodium fastigiatum, KJ952219 Mucoromycotina sp. MIB 8550 associated with Phaeoceros laevis, KC708399 100 Calcarisporiella thermophila CBS 279.70, AB597205 Calcarisporiella thermophila NBRC 33279, AB597204 100 Bifiguratus adelaidae AZ0501, KX372677 Bifiguratus adelaidae YP243, KU702505 Bifiguratus adelaidae TLT265, KX372676 Mortierella verticillata NRRL 6337, NG017188

0.02

"LL(Continued).

also introduced the new genus Jimgerdemannia within Furthermore, Jimgerdemannia was sister to a clade Endogonaceae and synonymized the genus Youngiomyces consisting of DNA sequences belonging to fungi associated with Endogone s. str. The new genus Jimgerdemannia with liverworts and hornworts (“group G” sensu Desirò et al. includes two species, and , and an 2013). Similarly, Endogone is nested within a monophyletic undescribed Jimgerdemannia lineage, which is sister to the group that also included two clades of fungal symbionts of - clade. Furthermore, we also provided liverworts, hornworts and ferns (“groups D and H” sensu a more detailed phylogenetic placement for E. oregonensis Desirò et al.   G“=GLOG? [D<> B @B”

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p. ncltd with inoculated spp. Warcup (1990)reportedmycorrhizaformationonEucalyptus However, non-ectomycorrhizal. considered been generally have and fungicolous perhaps or saprotrophic are species Most sporophores. epigeous may or hypogeous have They gametangia. homogeneous and mantle hyphal form otherbiotrophicinteractionswithhosts. or endophytic be and hosts some on ectomycorrhizas form We lineages. plant cannot rule out land the possibility that members of this genus can diverging early with interactions this that pce i ti genus this in species of ecology and habit sporing ld (Yamamoto clade ra the as to referred been previously name we that clade monophyletic supported well and diverse a within together environmental ous GLVB@EGV aggregatus related to an undescribed from fungal symbionts of hornworts and liverworts are closely 1985; WalkerWarcup, 1990). Interestingly, 1979, our results Grace show that sequences & Chu-Chou 1969, Palenzona rdc blw rud prpoe ad r considered are with and ectomycorrhizal sporophores ground below produce hyphal mantleandheterogeneousgametangia. They usually Densosporaceae ic monophyletic synonymize (Yamamoto in observed be morphological (i.e. key the that shown distinguish to used character been recently has It genus the Endogonaceae In contrast, taxa in A number of points can be made regarding the morphology, hlgntc eosrcin placed reconstructions Phylogenetic Densospora nuda, a zygosporangium with two to four openings) can also can openings) four to two with zygosporangium a T. pygmaea (Bidartondo within , Endogone short DNA sequences from environmental sequenc- environmental from sequences DNA short Jimgerdemannia ) Youngiomyces (i.e. Youngiomyces Mucoromycotina and 05. ae o ti rtoae we rationale, this on Based 2015). et al. Densosporaceae ZLMBG?“GO? D> [=LZBX [D<> ?G“=GLOG? MXBOGV ZGLG (#  species might associate with multiple plant multiple with associate might species et al. 2016) and present studies, there is still ee undescribed were E. aggregata E. pisiformis oto h N eune icue in included sequences DNA the of Most . E. tuberculosa n te hlgntc oiin of position phylogenetic the and Mucoromycotina Densosporaceae Endogone 05 Truong 2015, et al. Pinaceae D.

(syn. E. aggregata ae dvlpd zygosporangial developed a have species might engage in symbiotic in engage might species solicarpa Jimgerdemannia E. corticioides n u suy within study, our in with Endogones.str. (2017a) recently reported recently (2017a) et al. . However, in our analyses the analyses our in However, . Youngiomyces Jimgerdemannia . 2011) close to the ones the to close 2011) et al. , n numer- and Glomus tenue), n rrl in rarely and , h ol rpeettv of representative only the ), (Fassi s itr o h monophylet- the to sister is have a loose zygosporangial lhuh ectomycorrhizas Although . , and Sphaerocreas Mucoromycotina eune clustered sequences here. This group has group This here. 99 Fsi & Fassi 1969, et al. Sphaerocreas pube- and 07. Due 2017). etal. Treubia lacunosa sp. This indicates from Youngiomyces Youngiomyces . In particular, In . E. incrassata E. pisiformis -Densospo- Endogone Endogone Endogone Endogo- . et al. Den- Desiró etal. . .

sospora o aalbe n ulc aaae. oee, preliminary However, that indicate databases. data public in were available lineages fungal not two these for sequences and study group of fungi of requires urgent attention to: investigation (1) provide a formal comprehensive more environmental datawithcollection-based datasets. of integration the and surveys, environmental in fungi these ELOX=VELZVE[[O=X@EG?ELOEXBD@<?H

Polyporaceae. This suggests a possible Sclerogone could help in identifying and providing a pubescens and DGBV?<[[LGD<<@GLV

$"('*$"*1Endogonales

name to the clades of environmental DNA sequences related <<<.< ARTICLE to Endogone, Jimgerdemannia, and Densosporaceae; (2) provide taxonomic descriptions of the potentially novel Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, et al. (1997) species of Endogone and Jimgerdemannia used in this Gapped BLAST and PSI-BLAST: a new generation of protein study; (3) generate molecular data in order to place species database search programs. Nucleic Acids Research S: 3389– of Peridiospora and Sclerogone within a phylogenetic 3402. [DB>GISphagnum, Pinus sylvestris, Allium cepa, and various different lineages within Endogonales; and (6) Allium porrum. Canadian Journal of Botany W: 899–905. clarify taxonomic inconsistencies between Sphaerocreas Berch SM, Fortin JA (1982) Germination of zygospores of Endogone pubescens (sensu Hirose et al. 2014) and Sclerocystis in incrassata. Mycologia !M: 861–864. Glomeromycotina. Berkeley MJ, Broome CE (1874) Enumeration of the fungi of Ceylon. As we enter the “-omics” age it will be possible to use Part II. Botanical Journal of the Linnean Society M: 29-141. both fungal genomes and plant microbiomes to facilitate Berkeley MJ, Broome CE (1846) Notices of British hypogaeous fungi. future studies of Endogonales, which are rapidly emerging as Annals and Magazine of Natural History : 73–82. a key group of fungi to study. It will be critical to understand Bidartondo MI, Read DJ, Trappe JM, Merckx V, Ligrone R, et al. more about the evolution and trophic modes of this group of (2011) The dawn of symbiosis between plants and fungi. Biology fungi in order to elucidate the origin and evolutionary history Letters !: 574–577. of plant-fungal symbioses. The ecology of many species Bonfante P, Desirò A (2017) Who lives in a fungus? The diversity, of Densosporaceae and Endogonaceae is likely to be origins and functions of fungal endobacteria living in mycorrhizal (or mycorrhiza-like in rootless plants) involving Mucoromycota. The ISME Journal : 1727–1735. carbon and nutrient transfer between fungus and plant host. Chu-Chou M, Grace LJ (1984) ! and Tuber This has only been tested thus far for a few liverwort species sp. as mycorrhizal fungi of Pinus radiata in New Zealand. New (Field et al. 2015b, 2016). Genomic data have the potential Zealand Journal of Botany : 525–531. to determine the physiological abilities and differences Chu-Chou M, Grace LJ (1979) ! as a among symbiotic and free-living species, and to clarify the >WOFEGlomeromycota and Mucoromycotina fungi under a simulated (IFAS). Palaeozoic CO2 decline. The ISME Journal : 1514–1526.

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il K, rse S Dcet G Rmntn R Bdrod MI Bidartondo WR, Rimington JG, Duckett S, Pressel KJ, Field edmn J, rpe M (1974) JM Trappe JW, Gerdemann DJ, Beerling KE, Allinson MI, Bidartondo WR, Rimington KJ, Field Ihrmark K, Bödeker IT, Cruz-Martinez K, Friberg H, Kubartova A, Hirose D, Degawa Y,Degawa D, Hirose Yamamoto YamadaK, A(2014) Katoh K, Standley DM (2013) MAFFT multiple sequence alignment sequence multiple MAFFT (2013) DM Standley K, Katoh Jabaji-Hare SH, Charest PM (1987) Ultrastructural and cytochemical rns M Tyo T, oze N Prihn G 21) osl fungi Fossil (2012) G Persichini N, Dotzler TN, Taylor M, Krings, M, Cheung S, Stones-Havas A, Wilson R, Moir M, Kearse Osmundson TW, Robert VA, Schoch CL, Baker LJ, Smith A, Smith LJ, Baker CL, Schoch VA, Robert TW, Osmundson ae T, af F Shc C, ahn P, osetr V, Hofstetter PB, Matheny CL, Schoch F, Kauff TY, James ik HF Link DG, Saunders S, Ivanov Z, Zhang E, Limpens K, Lin Orchard S, Standish RJ, Dickie IA, Renton M, Walker C, Orchard S, Hilton S, Bending GD, Dickie IA, Standish RJ, mammal Fungal-small (1978) RA Nussbaum JM, Trappe C, Maser 56. 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