Systematics, taxonomy, and distribution of species of Myriogenospora G.F. Atk. (Clavicipitaceae, Hypocreales, Ascomycota) Armando J. Cruz-Laufer1, 2, Melissa Mardones3, 2, Meike Piepenbring2 1 UHasselt – Hasselt University, Faculty of Sciences, Centre for Environmental Sciences, Research Group Zoology: Biodiversity and Toxicology, Agoralaan Gebouw D, 3590 Diepenbeek, Belgium. 2 Department of Mycology, Goethe University Frankfurt am Main, Biologicum, Max-von- Laue-Str. 13, 60438 Frankfurt am Main, Germany. 3 Escuela de Biología, Universidad de Costa Rica, San Pedro, 11501 San José, Costa Rica. Corresponding author: Meike Piepenbring, piepenbring@bio.uni-frankfurt.de Abstract Based on new specimens of Myriogenospora spp. from Costa Rica and Panama, we present morphological analyses, systematic conclusions, additions to host ranges, and geographical distribution data for the two species currently clas- sified in this genus. Myriogenospora atramentosa (Berk. & M.A. Curtis) Diehl differs from Myriogenospora linearis (Rehm) J.F. White & Glenn in the ascus and part-spore morphology, a different position in the molecular phylogeny, and the host range. We conclude that the two species are not congeneric and propose that M. linearis should be called Balansia linearis (Rehm) Diehl. Keywords Balansia, Clavicipitaceae, Costa Rica, grass epibionts, Panama, phylogeny, Poaceae. Academic editor: Panu Kunttu | Received 9 May 2019 | Accepted 15 August 2019 | Published 6 September 2019 Citation: Cruz-Laufer AJ, Mardones M, Piepenbring M (2019) Systematics, taxonomy, and distribution of species of Myriogenospora G.F. Atk. (Clavicipitaceae, Hypocreales, Ascomycota). Check List 15 (5): 735–746. https://doi.org/10.15560/15.5.735 Introduction The wide host range and diverse host interactions of clavicipitaceous fungi have led to a series of studies on the ecology (Saikkonen et al. 2006), evolution (Kepler et al. 2012b), toxicology (Bacon et al. 1975; Kallen- bach 2015), and biotechnological application (Kusari et al. 2014) of species of Clavicipitaceae (Hypocreales, Ascomycota). To address these topics, knowledge on the morphology, systematics, taxonomy, host range, and geo- graphical distribution is important. Several studies have paid special attention to plant-infecting species of Clavi- cipitaceae including those classified in the tribe Balan- sieae or the Ephelis clade (Kuldau et al. 1997). These species can increase plant resistance against herbivory (Clay et al. 1985, 1989) and drought (Ren and Clay 2009), and some of their metabolites could have medicinal and agricultural applications (Tan and Zou 2001). However, few studies have contributed to our knowledge on the distribution and systematics of balansioid fungi in recent years. Therefore, many species concepts rely only on morphological observations with DNA sequence data being incomplete or entirely missing. The genus Myriogenospora G.F. Atk. was established by Atkinson (1894) and includes M. atramentosa (Berk. & M.A. Curtis) Diehl (type species, syn. M. paspali G.F. Atk.) and M. linearis (Rehm) J.F. White & Glenn accord- ing to the most recent taxonomic revision by White and Glenn (1994). Myriogenospora spp. are characterized by perithecia arranged in lines embedded in linear stromata parallel to and mostly surrounded by grass leaf blades Check List 15 (5): 735–746 https://doi.org/10.15560/15.5.735 5 15 Copyright Cruz-Laufer et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unre- stricted use, distribution, and reproduction in any medium, provided the original author and source are credited. NOTES ON GEOGRAPHIC DISTRIBUTION 736 Check List 15 (5) (Poaceae). The asci are fusiform and, as the genus name indicates, they include numerous part-spores. These part-spores are small, fusoid, and result from ascospore fragmentation and bipolar growth with secondary spore production (White and Glenn 1994). Using recently collected samples from both species of Myriogenospora, we reassess the geographical distri- bution, host range, morphological descriptions, and sys- tematic relationships of M. atramentosa and M. linearis. Methods During field sampling of plant-parasitic microfungi in southern Central America, we collected several speci- mens of Myriogenospora spp. in Costa Rica and Panama between 1992 and 2015. Collection sites with ecological details are mentioned together with the records below. Dried specimens were deposited in the following her- baria: specimens collected in Costa Rica were deposited in the Herbario de la Universidad de Costa Rica (USJ), and specimens from Panama in the Herbario de la Uni- versidad de Panama (PMA) and the Herbario de la Uni- versidad de Chiriqui (UCH). All the specimens were also deposited in the Botanische Staatssammlung, München (M), Germany. We examined the morphology of Myriogenospora spp. using dry material in 10% KOH with or without aniline blue aqueous solution. Using a freezing micro- tome Leica (CM 1510-1), we obtained microscopic, about 30 µm thick sections to image the stroma morphology. Imaging and measurements were done using a camera Nikon DS-Fi2 adapted to the microscope and operated by the imaging software NIS-Elements D 2.2. The measure- ments indicate the mean value ± the standard deviation of n measurements (n ≥ 20) and extreme values in parenthe- ses. Line drawings were traced using a drawing tube and edited with Photoshop CS5 (Adobe, San Jose, California). DNA extraction and PCR protocols followed the pro- cedure described by Mardones et al. (2017). Three par- tial nuclear gene regions (two ribosomal loci and one protein-coding gene) were amplified and sequenced: a fragment of the large subunit nuclear ribosomal DNA (nrLSU) with primers NL1 and NL4 (O’Donnell 1993), the complete internal transcribed spacer region of ribo- somal DNA (ITS1-5.8S-ITS2) with primers ITS5 and ITS4 (White et al. 1990), and a fragment of the transla- tion elongation factor 1 (TEF1) with primers EF1-983f (Carbone and Kohn 1999) and EF1-2218r (Rehner and Buckley 2005). For phylogenetic analyses of Myriogenospora spp. and other Clavicipitaceae, we compiled a three-locus concatenated alignment (nrLSU, ITS, TEF1) including 33 species. These analyses were rooted using Tolypo- cladium capitatum (Holmsk.) C.A. Quandt, Kepler & Spatafora and T. japonicum (Lloyd) CA Quandt, Kepler & Spatafora (Ophiocordycipitaceae) as outgroups. The taxa of Clavicipitaceae used in the analyses as well as the newly generated sequences deposited in GenBank are listed in Table 1 together with their locality, host plant, voucher numbers, and GenBank accession numbers. The alignments were deposited in TreeBASE (http://www. treebase.org/) under accession number 24171. Phylogenetic analyses were conducted applying max- imum likelihood (ML) and Bayesian methods and fol- lowed the procedures outlined by Mardones et al. (2017). Data were partitioned by gene and by codon position in the case of the protein-coding sequences. The HKY + G model was applied to ITS, GTR + I + G model to nrLSU, and TIM + I + G model to TEF1. Bayesian posterior probabilities (BPP) ≥0.95 and Bootstrap values (BS) ≥70 were considered to be significant. Results Balansia linearis (Rehm) Diehl, Agric. Monogr. No. 4: 47 (1950) Figures 1, 2, 3A Material examined. Costa Rica • Cartago Province, Cerro de la Muerte, Cerro de la Asunción, Pan-Ameri- can Highway km 89, near the entrance of the Tapantí National Park; alt. about 3100 m a.s.l.; 10 Jan. 2015; M. Piepenbring, O. Cáceres, M. Eichenlaub, M. Mardones leg.; on leaves of Chusquea subtessellata Hitchc. (det. M. Piepenbring) (MP 5242; M 141351; USJ109414). Identification. Infected shoots of the host plant without flowers and with all leaves presenting stromata. Stromata wrapped in host leaf blades except for a linear exposed part containing perithecia, epibiotic, one to several cen- timeters long, hyaline except for a black outer surface. Leaf blades held in rolled position (supervolute ptyxis) by a plectenchyma consisting of fungal cells. Perithe- cia immersed, arranged in 1–2 rows, pyriform or bottle- shaped, (475–)505–590(–625) × (225–)265–375(–405) µm. Ostioles appear as warts on the black outer stroma surface. Asci cylindrical, unitunicate, containing numer- ous part-spores, (150–)170–250(–280) × (5.5–)6.5–9.5(– 11) µm (difficult to measure because the asci intermingle and easily break), with a truncate, light refractive body perforated by a central pore at the tip of each ascus. Part- spores cylindrical, containing guttules, (17–)21–27(–28) × 1.0–1.5 µm, hyaline, smooth. No part-spore initials resulting from ascospores fragmentation followed by reinitiated bipolar growth were observed. Synonyms. Ophiodothis linearis Rehm. Linearistroma lineare (Rehm) Höhn. Myriogenospora linearis (Rehm) J.F. White & Glenn. Type. Brazil, Campo Bello, on Chusquea sp., 1894, E. Ule 2105 (type, n.v., not in BPI). For heterotypic synonyms see White and Glenn (1994). Known distribution. Until now, Balansia linearis (M. linearis) is only known from Brazil (Pazschke 1896). Here, we report this species for the first time for Costa Rica and for the first time outside of Brazil (Fig. 3A). http://www.treebase.org/ http://www.treebase.org/ Cruz-Laufer et al. | Systematics and distribution Myriogenospora spp. 737 Ta b le 1 . S pe ci m en d at a of p la nt -in fe ct in g sp ec ie s of th e fa m ily C la vi ci pi ta ce ae in cl ud ed in th e ph yl og en et ic a na ly se s. A cc es si on n um be rs w rit te n in b ol d re fe r t o se qu en ce s ge ne ra te d du rin g th e pr es en t s tu dy . 1 M or e ex ac t l oc at io n da ta a re n ot a va ila bl e. Sp ec ie s Lo ca lit y H os t P la nt Vo uc he r G en B an k ac ce ss io n nu m be rs Re fe re nc e( s) IT S 28 S rD N A TE F1 Ba la ns ia b ru nn an s E .A . L ew is & J. F. W hi te M ex ic o Pa ni cu m la xi flo ru m L am . AT CC M YA -2 10 5 AY 32 70 46 Le w is e t a l. (2 00 2) Ba la ns ia c la vi ce ps S pe g. In di a Cy rt oc oc cu m o xy ph yl lu m (S te ud .) St ap f CB S 50 1. 70 M H 85 98 16 M H 87 15 88 Vu e t a l. (2 01 9) Ba la ns ia c yp er i E dg er to n U SA Cy pe ru s v ire ns M ic hx . B1 07 5 U 68 11 8 Ku ld au e t a l. (1 99 7) Ba la ns ia d is co id ea H en n. Co st a Ri ca Pa ni cu m p ilo su m S w . M P 52 39 b M K6 60 20 5 M N 10 46 84 Ba la ns ia e pi ch lo ë (W ee se ) D ie hl A m er ic as ¹ Po ac ea e A EG 9 6- 15 a JN 04 98 48 EF 46 87 43 Su ng e t a l. (2 00 7) ; K ep le r e t a l. (2 01 2a ) Ba la ns ia e pi ch lo ë (W ee se ) D ie hl A m er ic as ¹ Sp or ob ol us in di cu s ( L. ) R .B r. B1 13 U 68 12 1 Ku ld au e t a l. (1 99 7) Ba la ns ia h en ni ng si an a (M öl le r) D ie hl U SA Pa ni cu m s p. A EG 96 -2 7a JN 04 98 15 AY 48 97 15 AY 48 96 10 Ca st le bu ry e t a l. (2 00 4) ; K ep le r e t a l. (2 01 2a ) Ba la ns ia h yp ox yl on (P ec k) G .F . A tk . U SA D an th on ia sp ic at a (L .) Ro em . & Sc hu lt. B1 12 U 68 11 4 Ku ld au e t a l. (1 99 7) Ba la ns ia li ne ar is (R eh m ) D ie hl (M yr io - ge no sp or a lin ea ris (R eh m ) J .F . W hi te & G le nn ) Co st a Ri ca Ch us qu ea su bt es se lla ta H itc hc . M P 52 42  M K6 60 19 9 M K6 60 21 2 Ba la ns ia n ig ric an s ( Sp eg .) J. F. W hi te , T .E . D ra ke & T .I. M ar tin U SA A xo no pu s f ur ca tu s ( Fl üg gé ) H itc hc . B2 52 U 68 11 9 Ku ld au e t a l. (1 99 7) Ba la ns ia o bt ec ta D ie hl A m er ic as ¹ Ce nc hr us e ch in at us L . B2 49 JF ZS 01 00 06 44 JF ZS 01 00 06 44 KP 68 95 49 Sc ha rd l e t a l. (2 01 4) Ba la ns ia p ilu la ef or m is (B er k. & M .A . Cu rt is ) D ie hl U SA Ch as m an th iu m la xu m (L .) H .O .Y at es AT CC 9 07 22 U 68 12 2 Ku ld au e t a l. (1 99 7) Ba la ns ia sp . M ex ic o Bo th rio ch lo a pe rt us a (L .) A . C am us M P 19 34 M K6 60 20 4 Ba la ns ia st ra ng ul an s ( M on t.) D ie hl A m er ic as ¹ Pa ni cu m a ci cu la re D es v. B4 93 U 68 12 4 Ku ld au e t a l. (1 99 7) Ba la ns ia te xe ns is (D ie hl ) P .V . R ed dy , C la y & J. F. W hi te A m er ic as ¹ N as se lla le uc ot ric ha (T rin . & R up r.) R. W .P oh l B6 15 5 KP 68 95 47 Sc ha rd l e t a l. (2 01 4) Cl av ic ep s a fr ic an a Fr ed er ., M an tle & D e M ill ia no U SA So rg hu m s p. U SD A B PI 8 06 25 6 A F2 45 29 4 Su lli va n et a l. (2 00 1) Cl av ic ep s f us ifo rm is Lo ve le ss U nk no w n U nk no w n AT CC 2 60 19 U 17 40 2 D Q 52 23 20 Re hn er a nd S am ue ls (1 99 5) ; S pa ta - fo ra e t a l. (2 00 7) Cl av ic ep s p as pa li F. S te ve ns & J. G . H al l Ita ly Pa sp al um d is tic hu m L . AT CC 1 38 92 U 68 12 7 D Q 52 23 21 Ku ld au e t a l. (1 99 7) ; S pa ta fo ra e t a l. (2 00 7) Cl av ic ep s r an un cu lo id es M öl le r Co st a Ri ca Se ta ria s p. U nk no w n A F2 45 29 5 Su lli va n et a l. (2 00 1) Ep he lis ja po ni ca H en n. Ja pa n U nk no w n N IA ES 6 58 4 A B1 14 63 1 Yo ko ya m a et a l. (2 00 6) Ep ic hl oë a m ar ill an s J .F . W hi te U SA Ag ro st is hy em al is (W al te r) B rit to n, St er n & P og ge nb . E 57 L0 71 42 KP 68 95 62 Ts ai e t a l. (1 99 4) Ep ic hl oë a m ar ill an s J .F . W hi te U SA Sp he no ph ol is ob tu sa ta (M ic hx .) Sc rib n. U 57 68 0 Su h et a l. (1 99 8) Ep ic hl oë b ac on ii J. F. W hi te Eu ro pe ¹ Ca la m ag ro st is vi llo sa (C ha ix ) J .F . G m el . AT CC 2 00 74 5 JF G Y0 10 00 97 5 JF G Y0 10 00 97 5 KP 68 95 61 Sc ha rd l e t a l. (2 01 4) 738 Check List 15 (5) Sp ec ie s Lo ca lit y H os t P la nt Vo uc he r G en B an k ac ce ss io n nu m be rs Re fe re nc e( s) IT S 28 S rD N A TE F1 Ep ic hl oë b ra ch ye ly tr i S ch ar dl & Le uc ht m . N or th A m er ic a¹ Br ac hy el yt ru m e re ct um (S ch re b. ) P. Be au v. E4 80 4 KP 68 95 64 Sc ha rd l e t a l. (2 01 4) Ep ic hl oë b ro m ic ol a Le uc ht m . & S ch ar dl Eu ra si a¹ Br om us to m en te llu s B oi ss . A L0 43 4 KP 68 95 58 Sc ha rd l e t a l. (2 01 4) Ep ic hl oë co en op hi al a (M or ga n- Jo ne s & W . G am s) C .W . B ac on & S ch ar dl Eu ro pe ¹ Fe st uc a ar un di na ce a Sc hr eb . AT CC 9 06 64 (E 19 ) U 68 11 5 KP 68 95 56 Ku ld au e t a l. (1 99 7) ; S ch ar dl e t a l. (2 01 3) Ep ic hl oë e ly m i S ch ar dl & L eu ch tm . U SA El ym us v ill os us M uh l. ex W ill d. AT CC 2 01 55 5 AY 98 69 24 Ch av er ri et a l. (2 00 5) Ep ic hl oë fe st uc ae L eu ch tm ., Sc ha rd l & M .R . S ie ge l U nk no w n Fe st uc a ru br a L. E3 2 U 68 11 6 Ku ld au e t a l. (1 99 7) Ep ic hl oë g ly ce ria e Sc ha rd l & L eu ch tm . U SA G ly ce ria st ria ta (L am .) H itc hc . AT CC 2 00 74 7 L0 71 36 A FR G 01 00 13 28 KP 68 95 60 Ku ld au e t a l. (1 99 7) ; S ch ar dl e t a l. (2 01 3) Ep ic hl oë sy lv at ic a Le uc ht m . & S ch ar dl G er m an y Br ac hy po di um sy lv at ic um (H ud s. ) P . Be au v. H LW 2 03 8 M K6 60 19 8 M K6 60 20 6 M N 10 46 80 pr es en t s tu dy Ep ic hl oë ty ph in a (P er s. ) B ro ck m . N ew Z ea la nd Fe st uc a ru br a L. AT CC 5 64 29 JN 04 98 32 U 17 39 6 A F5 43 77 7 Re hn er a nd S am ue ls (1 99 5) ; C ur rie e t al . ( 20 03 ); Ke pl er e t a l. (2 01 2a ) M yr io ge no sp or a at ra m en to sa (B er k. & M .A . C ur tis ) D ie hl Co st a Ri ca H om ol ep is at ur en sis (K un th ) C ha se M P 52 8 M K6 60 20 3 M K6 60 21 1 Pr es en t s tu dy M yr io ge no sp or a at ra m en to sa (B er k. & M .A . C ur tis ) D ie hl Pa na m a A xo no pu s c om pr es su s ( Sw .) P. B ea uv . M P 49 55 M K6 60 20 0 M K6 60 20 8 Pr es en t s tu dy M yr io ge no sp or a at ra m en to sa (B er k. & M .A . C ur tis ) D ie hl Pa na m a A xo no pu s c om pr es su s ( Sw .) P. B ea uv . M P 51 14 M K6 60 20 2 M K6 60 21 0  M N 10 46 85 Pr es en t s tu dy M yr io ge no sp or a at ra m en to sa (B er k. & M .A . C ur tis ) D ie hl Pa na m a H om ol ep is at ur en sis (K un th ) C ha se M P 51 13 M K6 60 20 1 M K6 60 20 9 Pr es en t s tu dy M yr io ge no sp or a at ra m en to sa (B er k. & M .A . C ur tis ) D ie hl Pa na m a Pa sp al um co nj ug at um P .J . B er gi us M P 49 53 M K6 60 20 7 Pr es en t s tu dy M yr io ge no sp or a at ra m en to sa (B er k. & M .A . C ur tis ) D ie hl U SA An dr op og on v irg in ic us L . A EG 9 6- 32 JN 04 98 35 AY 48 97 33 Ca st le bu ry e t a l. (2 00 4) ; K ep le r e t a l. (2 01 2a ) N ig ro co rn us sc le ro tic us (P at .) Ry le y Be ni n An dr op og on g ay an us K un th LB 20 15 _0 9- 24 /1 M K6 60 21 3 M N 10 46 83 pr es en t s tu dy N ig ro co rn us sc le ro tic us (P at .) Ry le y Be ni n An dr op og on g ay an us K un th LB 20 15 _0 9- 17 /2 M K6 60 21 4 M N 10 46 81 pr es en t s tu dy N ig ro co rn us sc le ro tic us (P at .) Ry le y Be ni n An dr op og on sc hi re ns is H oc hs t. LB 20 15 _0 9- 18 /3 M K6 60 21 5 M N 10 46 82 pr es en t s tu dy N ig ro co rn us sc le ro tic us (P at .) Ry le y In di a Cy m bo po go n ci tr at us (D C .) St ap f AT CC 1 81 54 U 68 12 3 Ku ld au e t a l. (1 99 7) N ig ro co rn us sc le ro tic us (P at .) Ry le y In di a Cy m bo po go n ci tr at us (D C .) St ap f CB S 36 5. 67 M H 87 06 95 Vu e t a l. (2 01 9) N ig ro co rn us sc le ro tic us (P at .) Ry le y In di a U nk no w n AT CC 1 65 82 U 47 82 1 Sp at af or a an d Bl ac kw el l ( 19 93 ) Pa re pi ch lo ë ci ne re a (B er k. & B ro om e) J. F. W hi te & P .V . R ed dy N ep al Sp or ob ol us s p. N e- 01 A B0 65 42 5 Ta na ka e t a l. (2 00 2) To ly po cl ad iu m c ap ita tu m (H ol m sk .) C .A . Q ua nd t, Ke pl er & S pa ta fo ra Ja pa n El ap ho m yc es sp . N BR C 10 09 97 JN 94 33 13 JN 94 14 01 A B9 68 59 7 Sc ho ch e t a l. (2 01 2) ; B an e t a l. (2 01 5) To ly po cl ad iu m ja po ni cu m (L lo yd ) C .A . Q ua nd t, Ke pl er & S pa ta fo ra U nk no w n El ap ho m yc es sp . O SC 1 10 99 1 JN 04 98 24 D Q 51 87 61 D Q 52 23 30 Sp at af or a et a l. (2 00 7) ; K ep le r e t a l. (2 01 2a ) Ta b le 1 . C on tin ue d. Cruz-Laufer et al. | Systematics and distribution Myriogenospora spp. 739 Figure 1. Balansia linearis (Myriogenospora linearis) on leaves of Chusquea subtessellata (MP 5242). A–C. Fresh specimen in the field. A. Infected shoot (arrow) and healthy shoot (right). B. Infected shoots. C. One linear stroma with ostioles of perithecia evident as warts. D. Transverse section of a leaf blade held in a rolled position by the fungal stroma including two perithecia below the black surface of the stroma as seen by light microscopy. Scale bar = 500 μm. Host plants. Until now, Balansia linearis (M. linearis) is known from Chusquea sp., Olyra micrantha Kunth, Pariana sp. (Möller 1901; White and Glenn 1994), and Merostachys speciosa Spreng. (Möller 1901, cited as “Microstachys speciosa Spr.”, see explanation below) all classified in Bambusoideae (Poaceae). Here, we report B. linearis (M. linearis) on Chusquea subtessellata as a new host plant species. Möller (1901) reported Ophiodothis raphidospora Rehm (syn. of Myriogenospora linearis according to White and Glenn, 1994) on Microstachys speciosa Spr. for Brazil. The name of the host species is questionable as the genus Microstachys A. Juss. belongs to Euphorbi- aceae and the name Microstachys speciosa is not validly published (see http://www.ipni.org). Due to the similar spelling of the name, the identical author, and the classifi- cation in Bambusoideae (Poaceae), we assume that Möller (1901) wanted to cite Merostachys speciosa Spreng. Taxonomy. According to the most recent study on spe- cies of Myriogenospora presented by White and Glenn (1994), the fungus collected on Chusquea subtessellata in Costa Rica should be cited as M. linearis (Rehm) J.F. White & Glenn. We consider an older name, Balansia linearis (Rehm) Diehl, to be more convenient based on molecular sequence data, microscopical characteristics, and the host relationship (for details see below). Myriogenospora atramentosa (Berk. & M.A. Curtis) Diehl, Agric. Monogr. No. 4: 59 (1950) Figures 3B, 4, 5 Material examined. Costa Rica • Limón Province, Valle de Talamanca, 26 Oct. 1992; M. Piepenbring leg., MP 528 (M 141354; USJ109407). Panama • Chiriquí Province, Dolega, Los Algarro- bos, path close to house of S. Cáceres; 08°29′36″ N, 082° 25′31″ W; alt. about 150 m a.s.l.; 8 Mar. 2010; M. Piepen- bring, T. Hofmann leg.; MP 4953 (M 141355; PMA; UCH). • Chiriquí Province, border of road to Chiriquí Grande, before arriving at Fortuna, close to entrance of La Suiza; 08°39′24″ N, 082°12′37″ W; alt. about 1,150 m a.s.l.; 08 Mar. 2010; M. Piepenbring, O. Cáceres leg.; MP 4955 (M 141356; PMA; UCH). • Chiriquí Province, road to Chorogo; alt. about 400 m a.s.l.; 13 Jul. 2012; M. Piepenbring, D. Cáceres, A. Krohn, M. Rosas leg.; on leaves of Homolepis aturensis (Kunth) Chase (det. M. Piepenbring); MP 5113 (M 141357). • Chiriquí Province, road to Chorogo; alt. about 400 m a.s.l.; 13 July 2012; M. Piepenbring, D. Cáceres, A. Krohn, M. Rosas leg.; on http://www.ipni.org 740 Check List 15 (5) Figure 3. Maps showing known distribution and localities of new records and specimens. A. Balansia linearis (Myriogenospora linearis). B. Myriogenospora atramentosa. Localities of new records and specimens are indicated by red dots. The occurrence of these species in different countries according to literature is indicated by bright colors. Figure 2. Balansia linearis (Myriogenospora linearis) on leaves of Chusquea subtessellata (MP 5242), as seen by light microscopy. A. Trans- verse section of a leaf blade with a fungal stroma (dots) including two perithecia. B. Part of a transverse section of an infected leaf with one perithecium. C. Ascus with ascospores. D. Ascus tip with a light refractive body. E. Ascospore fragments resulting from incomplete ascospore fragmentation (left) and cylindrical part-spores resulting from completed ascospore fragmentation. Scale bars: A = 1000 μm; B = 500 μm; C = 100 μm; D = 20 μm; E = 100 μm. Cruz-Laufer et al. | Systematics and distribution Myriogenospora spp. 741 leaves of Axonopus compressus (Sw.) P. Beauv. (det. M. Piepenbring); MP 5114 (M 141358). Identification. Infected shoots of the host plants with- out flowers and with all leaves presenting stromata. Stro- mata wrapped in leaf blades except for a linear exposed part containing perithecia, epibiotic, one to several cen- timeters long, hyaline except for black outer surface. Leaf blades held together by a hyaline plectenchyma consisting of fungal mycelium in rolled or folded posi- tion (supervolute or conduplicate ptyxis). Perithecia immersed, arranged in one row, globose or subglobose, (225–)290–400(–465) × (235–)275–360(–440) µm. Osti- oles appear as warts on the black outer stroma surface. Asci fusiform (cylindrical when young), unitunicate, containing numerous part-spores, (120–)135–255(–330) × (5–)8–16(–21) µm with dome-shaped ascus tips with- out light refractive bodies. Part-spore initials resulting from ascospore fragmentation ovoid to slightly fusiform, immediately growing at both tips and becoming mature part-spores, elongated fusoid, without septa, containing guttules, (20–)29–39(–45) × (0.5–)1.0–2.0 µm, hyaline, smooth. Synonyms. Hypocrea atramentosa Berk. & M.A. Cur- tis. Epichloë atramentosa (Berk. & M.A. Curtis) Cooke. Hypocrella atramentosa (Berk. & M.A. Curtis) Sacc. Type. Cuba, no date, on Andropogon sp., C. Wright 419 (holotype, K(M) 198287). For heterotypic synonyms see White and Glenn (1994). Figure 5. Myriogenospora atramentosa. A. Transverse section of a leaf blade of Homolepis aturensis with one perithecium (MP 528). B. Asci at different stages of development (MP 5114). C. Dome-shaped ascus tip (MP 4953). D. Two part-spore initials (on the left side) and four more or less mature part-spores after bipolar growth (MP 5114). Scale bars: A = 500 μm; B = 100 μm; C = 50 μm, D = 20 μm. Figure 4. Myriogenospora atramentosa on leaves of Paspalum con- jugatum in the field (MP 4953). A. Infected plants. B. An infected plant with black stromata wrapped in leaf blades. 742 Check List 15 (5) Known distribution. Until now, Myriogenospora atra- mentosa is known from Brazil, Colombia, Cuba, the Dominican Republic, Grenada, Nicaragua, Panama, Peru, Puerto Rico, Trinidad and Tobago, the United States, and Venezuela (Seaver and Chardon 1926; Viégas 1944; Hanlin and Tortolero 1990; Kirschner et al. 2010; Lenné 1990). The species has also been cited for Ghana, Nigeria, and Sierra Leone (Deighton 1936a; Lenné and Calderón 1989; Lenné 1990). Here, we report M. atra- mentosa for Costa Rica for the first time (Fig. 3B). Known host plants. Until now, Myriogenospora atra- mentosa is known from Andropogon bicornis L., A. gayanus Kunth, A. leucostachyus Kunth, A. virginicus L., Axonopus compressus (Sw.) P. Beauv., Brachiaria mutica (Forssk.) Stapf, Chloris gayana Kunth, Cymbo- pogon sp., Eragrostis hirsuta (Michx.) Nees, Eremo- chloa ophiuroides (Munro) Hack., Ichnanthus pallens (Sw.) Munro ex Bent., Imperata brasiliensis Trin., Pani- cum anceps Michx., P. hemitomon Schult., P. scopa rium Lam., Paspalum ciliatifolium Michx., P. conjugatum P.J. Bergius, P. dilatatum Poir., P. laeve Michx., P. notatum Flügge, P. pilosum Lam., P. scrobiculatum L., P. urvillei Steud., Saccharum brevibarbe (Michx.) Pers., S. contor- tum (Elliott) Nutt., S. giganteum (Walter) Pers., S. offi- cinarum L., Schizachryrium scoparium (Michx.) Nash, Sorghastrum nutans (L.) Nash, Sporobolus indicus (L.) R.Br., and Tridens flavus (L.) Hitchc. (Seaver and Char- don 1926; Deighton 1936b; Viégas 1944; USDA Crops Research Division Agriculture Research Service 1960; Luttrell and Bacon 1977; Hanlin and Tortolero 1990; Lenné 1990). Here, we report M. atramentosa on Homo- lepis aturensis (Kunth) Chase for the first time. Viégas (1944) cited Microstachys speciosa as host species of M. atramentosa. We assume that Viégas (1944) copied this information from Möller (1901) (see above) and erroneously considered M. linearis a syn- onym of M. atramentosa. Phylogenetic analysis We extracted DNA from Myriogenospora spp. (see spec- imen data above) and from specimens of additional spe- cies of Clavicipitaceae: Balansia discoidea Henn. Costa Rica • Limón Prov- ince, Puerto Viejo de Talamanca, between Coclé and Punta Uva, Finca One World; 09°37′31″ N, 082°42′56″ W; alt. approx. 46 m a.s.l.; 3 Jan. 2015; M. Piepenbring, C. Tiemann, O. Cáceres, M. Eichenlaub, M. Mardones leg.; on leaves of Panicum pilosum Sw. (det. M. Piepen- bring); MP 5239b (M 141350). Balansia sp. Mexico • Yucatán Province, between Mérida and Chichen Izá, Libre Unión; alt. approx. 10 m a.s.l.; 21 Oct 1995; M. Piepenbring leg.; on leaves of Bothriochloa pertusa (L.) A. Camus (det. M. Piepen- bring); MP 1934 (M 141352). Epichloë sylvatica Leuchtm. & Schardl. Germany • Hesse State, Kreis Groß-Gerau, Mörfelden-Walldorf, close to parking ground “Schützenhaus”; 49°58′16″ N, 008°32′33″ E; alt. approx. 150 m a.s.l.; 15 Jun. 2013; H. Lotz-Winter leg.; on leaves of Brachypodium sylvaticum (Huds.) P. Beauv. (det. H. Lotz-Winter); HLW 2038 (M 141353). Nigrocornus scleroticus (Pat.) Ryley. Benin • Atakora Department, Kossokouangou; 10°10′37″ N, 001°12′13″ E; alt. approx. 570 m a.s.l.; 17 Sep. 2015; L. Beenken, N. S. Yorou, M. Piatek, R. Mangelsdorff et al. leg.; on leaves of Andropogon gayanus Kunth (det. pre- lim. M. Piatek); LB 2015.09.17/1 (M 141359; UNIPAR). • Atakora Department, at road RN11 South of Kouandé; 10°15′37″ N, 001°39′15″ E; alt. approx. 490 m a.s.l.; 18 Sep. 2015; L. Beenken, N. S. Yorou, M. Piatek, R. Man- gelsdorff et al. leg.; on leaves of Andropogon schiren- sis Hochst. (det. M. Piepenbring); LB 2015.09.18/1 (M 141360; UNIPAR). • Borgou Department, Wari Maro, South of Mont Soubakperou; 09°08′20″ N, 002°09′42″ E; alt. approx. 410 m a.s.l., 24 Jul. 2015; L. Beenken, N. S. Yorou, M. Piatek, R. Mangelsdorff et al. leg.; on leaves of Andropogon gayanus Kunth (det. prelim. M. Piatek); LB 2015.09.24/1 (M 141362; UNIPAR). In total, we generated 24 sequences for six species of Clavicipitaceae including 21 sequences for five species of Balansieae. These sequences correspond to six ITS sequences, 12 nrLSU sequences, and six TEF1 sequences. Sequence alignments included 19 sequences/560 base pairs for ITS, 39/589 for LSU, and 23/999 for TEF1. The combined sequence data set includes 46 specimens of 33 species and had an aligned length of 2148 base pairs. The Bayesian inference analysis and the ML analy- ses resulted in similar topologies; therefore, we present here only the ML tree for this dataset (Fig. 6). According to our results, the family Clavicipitaceae (100/1.00) as well as the tribes Balansieae (84/0.97) and Clavicipiteae (79/0.98) including the genera Claviceps (four species) and Epichloë (10 species) are monophyletic with signifi- cant statistical support. The genera Claviceps (94/1.00) and Epichloë (99/1.00) are also monophyletic. Within Balansieae, we found four monophyletic clades (A–D), three of them with significant statistical support. The Myriogenospora clade (A) (100/1.00) includes the spe- cies M. atramentosa (6 specimens). The Nigrocornus clade (B) (70/0.95) includes the species B. nigricans (1 specimen) and N. scleroticus (6 specimens). The first Balansia clade (C) (14/0.50) shows no significant support and includes the species B. claviceps (type species of Balansia), B. cyperi, B. hypoxylon, B. texensis, Ephelis japonica, M. linearis, and Parepichloë cinerea. The sec- ond Balansia clade (D) (75/0.97) includes the species B. brunnans, B. sp., B. discoidea, B. epichloë, B. henning- siana, B. pilulaeformis, and B. strangulans. We found no clustering of M. linearis and the type species of Myrio- genospora, i.e., M. atramentosa. Instead, M. linearis is embedded in a clade comprising of mostly Balansia spp. Therefore, we refer to the specimen MP5242 from Costa Rica by the name Balansia linearis (M. linearis). Cruz-Laufer et al. | Systematics and distribution Myriogenospora spp. 743 Figure 6. Phylogenetic relationships within the tribe Balansieae (Clavicipitaceae, Hypocreales, Ascomycota) focusing on Myriogenospora spp. This maximum likelihood (ML) phylogeny is based on three nuclear markers (nrLSU, ITS, TEF1). Support values are ML bootstrap values based on 1000 replicates and posterior probabilities from a Bayesian analysis. Values of ML BS >70% and Bayesian PP > 0.95 are given at nodes at the first and second positions, respectively. Internal branches considered strongly supported by both analyses are indicated by thickened branches. 744 Check List 15 (5) Discussion We propose to place Myriogenospora linearis in the genus Balansia as B. linearis (Rehm) Diehl due to (i) the contradictions of key morphological characteristics pre- sented by White and Glenn (1994) with observations by us, Pazschke (1896), Möller (1901), and von Höhnel (1910), (ii) no support for a close relationship of B. linearis (M. linearis) with M. atramentosa (type species) in our phylo- genetic analysis, and (iii) different host relationships. (i) White and Glenn (1994) described B. linearis (M. linearis) part-spores as fusoid with a resemblance to M. atramentosa part-spores. However, our morpho- logical analysis showed the presence of cylindrical part- spores with blunt tips for B. linearis (M. linearis). Earlier studies describe these part-spores as filiform (Pazschke 1896; von Höhnel 1910) or rod-shaped (Möller 1901). The distinct ascus morphologies further highlight the dispar- ity of the two species as the ascus tips of B. linearis (M. linearis) are truncate and present light refractive bodies as in most clavicipitaceous and balansioid fungi (Jones and Clay 1987) whereas the dome-shaped tips of M. atramentosa are a unique, possibly derived feature of this species (Luttrell and Bacon 1977). We believe that these inaccuracies in the part-spore description might have been caused by a deteriorated state of the B. linearis (M. linearis) specimens examined by White and Glenn (1994) caused by the age of the material, as their most recent specimen was collected in 1934. Furthermore, the language barrier could be a source of errors as the rel- evant studies (Möller 1901; von Höhnel 1910) were pub- lished in German. (ii) We found no evidence for a monophyletic clade that includes Balansia linearis (M. linearis) and M. atra- mentosa. Therefore, B. linearis is unlikely a member of Myriogenospora despite the similar linear stromata wrapped in leaf blades. (iii) Host plants of Balansia linearis (M. linearis) are classified as members of the BOP clade whereas M. atramentosa hosts are classified in the PACMAD clade of Poaceae (Grass Phylogeny Working Group II 2012; Soreng et al. 2015). All fungi reported as B. linearis (M. linearis) infect species of the subfamily Bambusoideae, whereas M. atramentosa infects species of Chloroideae and Panicoideae. This difference in host range empha- sizes the disparity between the B. linearis (M. linearis) and M. atramentosa. By placing B. linearis (M. linearis) and M. atramen- tosa in distinct genera, we conclude that the presence of linear epibiotic stromata with regular files of perithecia surrounded by leaf blades and numerous part-spores in the asci are less indicative of systematic relationships than ascus tip structure and part-spore shape. Our study on Myriogenospora spp. demonstrates that we require more information on Balansieae systematics to optimize our knowledge on the systematic position of balansioid fungi such as B. linearis (M. linearis). This study confirms that the tribe Balansieae, which includes the genera Balansia, Ephelis, Myriogenospora, Nigro- cornus, and Parepichloë, is monophyletic but also high- lights the need of a systematic revision of this taxon; we found at least three clades in Balansieae with significant support. All clades included Balansia species grouped with species from Nigrocornus and Parepichloë. These relationships confirm the paraphyly of the genus Balan- sia mentioned in previous studies (Kuldau et al. 1997; White et al. 2000). Some studies have created new mono- typic balansioid genera based on morphological observa- tions such as Nigrocornus and Parepichloë (White and Reddy 1998; Ryley 2003). Hence, an updated systematic revision could also lead to a classification of B. linearis (M. linearis) in its own separate genus as Linearistroma lineare (Rehm) Höhn. However, we recommend treating L. lineare as a member of Balansia until detailed mor- phological and complete molecular data of more species of Balansieae are available, especially those infecting BOP clade hosts such as Balansia nigricans, B. texensis, and Heteroepichloë spp. (Leuchtmann and Clay 1989; White et al. 1996; Tanaka et al. 2002). Some of the species included in the phylogenetic analysis have broad geographical distributions spanning continents such as B. claviceps and M. atramentosa, which are reported from Old and New World habitats, or N. scleroticus, which is reported from Africa (i.e., Benin), Asia (i.e., India), and Australia. Misidentified specimens and the usage of species names for species complexes could cause these inaccuracies such as for B. claviceps, whose Asian specimens resemble descriptions of B. andropogonis Syd. (Leuchtmann 1993; Reddy et al. 1998). As M. atramentosa is reported from the Ameri- cas and Africa, specimens from these continents might belong to different species. Hence, sampling and gener- ating sequence data from a range of populations could elucidate species identity, phylogenetic relationship, and geographical distribution of M. atramentosa specimens. Future research should focus on fieldwork to obtain more fresh specimens of the generally rare and there- fore poorly collected plant pathogenic species of Hypo- creales (see Judith et al. 2015). These specimens will allow detailed morphological analyses and the genera- tion of larger and more complete sequence data sets that will increase the statistical power of phylogenetic analy- ses for Balansieae. This approach combined with a host range analysis could resolve the systematics of this tribe and provide a systematically correct classification of B. linearis (M. linearis) amongst other balansioid fungi. Acknowledgements We are thankful to L. Beenken and H. Lotz-Winter for contributing specimens as well as to numerous friend ly collaborators in the field, namely D. Cáceres, O. Cáceres, M. Eichenlaub, T.A. Hofmann, A. Krohn, R. Mangels dorff, M. Piatek, N.S. Yorou, M. Rosas, and C. Tiemann. O. Cáceres, T.A. Hofmann, and N.S. Yorou col- laborated for collection permits. Cruz-Laufer et al. | Systematics and distribution Myriogenospora spp. 745 We acknowledge institutional support by the Univer- sidad Autónoma de Chiriquí (Panama), Universidad de Costa Rica (Costa Rica), and the Université de Parakou (Benin). The field activities in Central America were made possible with the financial support of the Ger- man Research Foundation (DFG) and the German Aca- demic Exchange Service (DAAD), those in Africa with the financial support of the Volkswagen Foundation. We thank the Autoridad Nacional del Ambiente (ANAM) in Panama and MINAE (SINAC and CONAGEBIO) in Costa Rica for collecting and export permits. We thank anonymous reviewers for improving the manuscript. Authors’ Contributions AC conducted detailed morphological and molecular anal yses, contributed scientific drawings. AC and MM conducted phylogenetic analyses. MM compiled figures and tables and submitted sequences to GenBank. MP contributed most specimens, photos of fungi in the field, identified host plants, did preliminary identifications of the fungi, organized the infrastructure and permits. AC and MP wrote this article with input from MM. 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