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Research Article
Phylloporia lonicerae (Hymenochaetales, Basidiomycota), a new species on Lonicera japonica from Japan and an identification key to worldwide species of Phylloporia
expand article infoWen-Min Qin, Xue-Wei Wang§, Takuo Sawahata|, Li-Wei Zhou
‡ Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang, China
§ University of Chinese Academy of Sciences, Beijing, China
| Kindai University, Nara, Japan
Open Access

Abstract

Phylloporia, in the Hymenochaetaceae, is a polypore genus with a worldwide distribution. The new taxon Phylloporia lonicerae is introduced, which is the first Phylloporia species to originate from Japan. This species grows exclusively on living Lonicera japonica and is distinguished by annual, sessile basidiocarps that occur in clusters, pileal surface of narrow, concentrically sulcate zones, 6–8 pores per mm, duplex context separated by a black zone, dimitic hyphal system and broadly ellipsoid basidiospores, 3.2–4 × 2.3–3.1 µm. Phylogenetically, P. lonicerae is nested within the Phylloporia clade as a distinct terminal lineage with full statistical supports and sister to the clade of P. minutispora, P. cf. pulla and P. terrestris with weak supports. Besides Phylloporia bibulosa, P. chrysites and P. spathulata, P. lonicerae is the fourth species of Phylloporia recorded from Japan. An identification key to all accepted 48 species of Phylloporia is provided.

Keywords

Hymenochaetaceae, key, Lonicera japonica, polypore, taxonomy

Introduction

Phylloporia Murrill, in the Hymenochaetaceae Donk, was introduced for an unusual polypore species, P. parasitica Murrill growing on the underside of living leaves in Columbia (Murrill 1904). For nearly 70 years, Phylloporia was forgotten until Ryvarden (1972) transferred five taxa into the genus. Renewed interest in Phylloporia was stimulated by Wagner and Ryvarden’s (2002) phylogenetic and morphological study in which they accepted 12 species. Since then, a number of new species have been described from Africa (Ipulet and Ryvarden 2005, Decock et al. 2015, Yombiyeni et al. 2015, Yombiyeni and Decock 2017), the Americas (Valenzuela et al. 2011, Decock et al. 2013, Ferreira-Lopes et al. 2016) and Asia, especially China (Gafforov et al. 2014, Cui et al. 2010, Zhou and Dai 2012, Zhou 2013, 2015a, 2015b, 2016, Liu et al. 2015, Chen et al. 2017, Ren and Wu 2017).

Phylloporia began as a monophyletic genus based on phylogenic studies of the large subunit of the nuclear ribosomal gene (nLSU) (Wagner and Ryvarden 2002) but is now paraphyletic with the inclusion of Coltricia cf. stuckertiana (Speg.) Rajchenb. & J.E. Wright in the Phylloporia clade (Valenzuela et al. 2011, Decock et al. 2013). The genus is morphologically quite diverse and includes species with annual or perennial basidiocarps with resupinate, sessile or stipitate habits, homogenous or duplex context, monomitic or dimitic hyphal system and cylindrical to subglobose basidiospores (Wagner and Ryvarden 2002, Cui et al. 2010, Zhou 2015a). Substrate preferences of Phylloporia species are equally diverse. Some species are saprobes that colonise woody debris (Ipulet and Ryvarden 2005, Zhou 2015b, Ferreira-Lopes et al. 2016) and others are parasites usually of specific plant hosts (Zhou 2015a, Ren and Wu 2017, Yombiyeni and Decock 2017).

There are three species of Phylloporia reported from Japan – P. bibulosa (Lloyd) Ryvarden, P. chrysites (Berk.) Ryvarden and P. spathulata (Hook.) Ryvarden (Núñez and Ryvarden 2000). In this paper, a new species, Phylloporia lonicerae, is described from Nara, Japan, growing on living vines of Lonicera japonica. Morphological and molecular data support the recognition of this new species. In addition, an updated key to the known species of Phylloporia is presented.

Materials and methods

Morphological examination

The studied specimens were deposited at the herbarium of the Institute of Applied Ecology, Chinese Academy of Sciences (IFP) in China. The macroscopic characters were observed from dried specimens with the aid of a stereomicroscope. Specimen sections were mounted in Cotton Blue (CB), Melzer’s reagent (IKI) and 5 % potassium hydroxide (KOH) for observation using a Nikon Eclipse 80i microscope at magnification up to 1000×. Special colour terms follow Petersen (1996). All measurements were taken from sections mounted in CB. When presenting the size variation of basidiospores, 5% of measurements from each end of the range were put in parentheses. Line drawings of microscopic characters were made with the aid of a drawing tube. The abbreviations used in the description are as follows: L = mean basidiospore length (arithmetic average of all measured basidiospores), W = mean basidiospore width (arithmetic average of all measured basidiospores), Q = variation in the L/W ratios between the specimens studied and n = number of basidiospores measured from a given number of specimens.

Molecular sequencing

The PCR products were directly amplified from the extracts of the basidiocarps with the Phire® Plant Direct PCR Kit (Finnzymes Oy, Finland) according to the manufacturer’s protocol. The PCR protocol was as follows: initial denaturation at 98 °C for 5 min, followed by 39 cycles of denaturation at 98 °C for 5 s, annealing at 48 °C for 5 s and extension at 72 °C for 5 s and a final extension of 72 °C for 10 min. The primers LR0R and LR7 (Vilgalys and Hester 1990) were used for PCR amplification and subsequent sequencing at the Beijing Genomics Institute, China. The newly generated sequences were submitted to GenBank (http://www.ncbi.nlm.nih.gov/genbank; Fig. 1).

Figure 1. 

Phylogenetic position of Phylloporia lonicerae inferred from the nLSU dataset. The topology is inferred by maximum likelihood algorithm, while bootstrap values above 50 % and Bayesian posterior probabilities above 0.8 are given at the nodes. Newly sequenced specimens are in boldface.

Phylogenetic analysis

To explore the phylogenetic relationship of P. lonicerae, six nLSU sequences were incorporated into previous nLSU datasets of Phylloporia (Zhou 2016, Chen et al. 2017, Ren and Wu 2017, Yombiyeni and Decock 2017). Several species of Fomitiporella Murrill and Fulvifomes Murrill were included in the dataset and Inonotus hispidus (Bull.) P. Karst. was selected as the outgroup taxon.

The nLSU dataset was aligned with MAFFT 7.110 (Katoh and Standley 2013) with the g-ini-i option (Katoh et al. 2005). The best-fit evolutionary model for the resulting alignment that was deposited in TreeBASE (http://www.treebase.org; accession number S21971), was estimated as GTR + I + G using jModelTest 2.1.4 (Darriba et al. 2012). Following this model, maximum likelihood (ML) and Bayesian Inference (BI) algorithms were used to infer the phylogeny of the alignment. The ML analysis was conducted using raxmlGUI 1.2 (Silvestro and Michalak 2012, Stamatakis 2006) under the auto FC option for bootstrap (BS) replicates (Pattengale et al. 2010). MrBayes 3.2 (Ronquist et al. 2012) was carried out for BI analysis, which employed two independent runs, each including four chains of 10 million generations and starting from random trees. Trees were sampled every 1000th generation. Of the sampled trees, the first 25 % was deleted and the remaining trees were used to construct a 50 % majority consensus tree and calculate Bayesian posterior probabilities (BPPs). Chain convergence was determined using Tracer 1.5 (http://tree.bio.ed.ac.uk/software/tracer/).

Results

Six nLSU sequences of P. lonicerae were generated and included in a dataset of 105 sequences and 942 characters. ML analysis was ended after 250 BS replicates. BI analysis converged all chains as indicated by the effective sample sizes of all parameters above 2000 and the potential scale reduction factors close to 1.000. As the ML and BI analyses generated congruent topologies in main lineages, the ML tree is presented in Figure 1. Values of BS above 50 % and BPPs above 0.8 are given at the nodes. The phylogenic tree (Fig. 1) shows that the strongly supported Phylloporia clade (98 % in ML, 1 in BI) consists of 44 terminal lineages and the six P. lonicerae samples formed a new lineage with full statistical supports (100 % in ML, 1 in BI). The Phylloporia lonicerae lineage is sister to the clade that includes P. minutispora Ipulet & Ryvarden, P. cf. pulla (Mont. & Berk.) Decock & Yombiy and P. terrestris L.W. Zhou with weak supports.

Taxonomy

Phylloporia lonicerae W.M. Qin, Xue W. Wang, T. Sawahata & L.W. Zhou, sp. nov.

MycoBank No: MB823715
Figs 2, 3

Holotype

JAPAN. Nara, Research Forest of Faculty of Agriculture, Kindai University, 3 Jul 2017, on living vine of Lonicera japonica, LWZ 20170703-2 (IFP 019172).

Etymology

Lonicerae (Lat.): referring to Lonicera, the host tree genus.

Basidiocarps annual, sessile, imbricate, rarely solitary, without odour or taste, woody. Pilei semi-circular, flabelliform or fused together, applanate, single pileus projecting up to 1.5 cm long, 3 cm wide and 0.5 cm thick at base. Pileal surface greyish-brown to yellowish-brown, velutinate, concentrically sulcate with narrow zones; margin pale yellow or concolorous, sharp. Pore surface honey-yellow, slightly glancing; sterile margin distinct, curry-yellow, up to 0.5 mm wide; pores circular to angular, 6–8 per mm; dissepiments thin, entire. Context up to 2 mm thick, duplex, with a black zone, lower context olivaceous buff, hard corky, up to 1 mm thick, upper tomentum cinnamon-buff, soft, up to 1 mm thick. Tubes honey-yellow, corky, up to 3 mm long.

Figure 2. 

Basidiocarps of Phylloporia lonicerae in situ. a LWZ 20170703-2 (holotype) b LWZ 20170622-1 (paratype). Scale bars: 2 cm.

Figure 3. 

Microscopic structures of Phylloporia lonicerae (drawn from the holotype, LWZ 20170703-2). a Basidiospores b Basidia and basidioles c Hyphae from trama d Hyphae from lower context e hyphae from upper tomentum. Scale bars: a = 5 µm, b–e = 10 µm.

Hyphal system dimitic; generative hyphae simple septate; tissue darkening but otherwise unchanged in KOH. Context: in the lower context, generative hyphae hyaline to pale yellowish, slightly thick- to thick-walled with a wide lumen, frequently branched and septate, 2–4 μm in diam; skeletal hyphae golden yellow, thick-walled with a narrow lumen, unbranched, aseptate, interwoven, 2–4.5 μm in diam; in the upper tomentum, generative hyphae infrequent, pale yellowish, slightly thick- to thick-walled with a wide lumen, rarely branched, frequently septate, 2–4 μm in diam; skeletal hyphae golden yellow, thick-walled with a narrow to wide lumen, unbranched, aseptate, loosely interwoven, 2.5–5 μm in diam; in the black zone, hyphae dark brown, thick-walled with a narrow lumen, strongly agglutinated, interwoven. Tubes: generative hyphae hyaline to pale yellowish, thin- to slightly thick-walled, occasionally branched, frequently septate, 1.8–4 μm in diam; skeletal hyphae golden yellow, thick-walled with a narrow lumen, unbranched, aseptate, interwoven, 2–4 μm in diam. Setae absent. Cystidia and cystidioles absent. Basidia clavate, with four sterigmata up to 3 μm long and a simple septum at the base, 7–11 × 4–6 μm; basidioles in shape similar to basidia, but slightly smaller. Basidiospores broadly ellipsoid, pale yellowish, thick-walled, smooth, indextrinoid, inamyloid, acyanophilous, (3–)3.2–4 × (2.1–)2.3–3.1(–3.3) μm, L = 3.61 μm, W = 2.77 μm, Q = 1.28–1.33 (n = 90/3).

Additional specimens (paratypes) studied

(All on living vine of Lonicera japonica)—JAPAN. Nara, Research Forest of Faculty of Agriculture, Kindai University, 31 Oct 2016, LWZ 20161031-1 (IFP 019173); 27 Feb 2017, LWZ 20170227-1 (IFP 019174); 25 Mar 2017, LWZ 20170325-1 (IFP 019175); 22 Jun 2017, LWZ 20170622-1 (IFP 019176); 3 Jul 2017, LWZ 20170703-1 (IFP 019177).

Discussion

Phylloporia lonicerae is morphologically distinct from other species in Phylloporia by its annual, sessile basidiocarps that occur in clusters, pileal surface of narrow, concentrically sulcate zones, 6–8 pores per mm, duplex context separated by a black zone, dimitic hyphal system and broadly ellipsoid basidiospores, 3.2–4 × 2.3–3.1 µm. In the field, it is readily identified by fruiting on living vines, >1.5 cm diameter, of Lonicera japonica. Phylloporia lonicerae is most similar to P. pseudopectinata Yuan Y. Chen & B.K. Cui and P. minutipora L.W. Zhou by sharing annual, sessile basidiocarps in clusters and a dimitic hyphal system, but easily distinguished from P. pseudopectinata by larger pores (8–9 per mm) and subglobose basidiospores (Chen et al. 2017) and from P. minutipora by larger pores and basidiospores and the specific host (Zhou 2016). An updated key, based on Zhou (2016), to all accepted 48 species of Phylloporia is provided below.

Lonicera japonica is a well-known and important medicinal plant (Li 1578). Therefore, the potential medicinal applications of fungi growing on this plant are intriguing. Li et al. (2010) studied the medicinal metabolites from basidiocarps of Phylloporia ribis (Schumach.) Ryvarden that were collected on Lonicera japonica in China. Recent phylogenetic evidence, however, indicates that Chinese specimens of P. ribis collected on hosts other than Ribes are distinct from a P. ribis specimen collected on Ribes in Germany (Zhou and Dai 2012). As P. ribis was originally described from Denmark (Larsen and Cobb-Poulle 1990), P. ribis specimens used by Li et al. (2010) in their study are likely P. lonicerae or another undescribed species.

Some species of Phylloporia are parasitic and appear to be restricted by host and geographic distribution of its host. For example, Phylloporia crataegi L.W. Zhou & Y.C. Dai, which occurs exclusively on living Crataegus and P. fontanesiae L.W. Zhou & Y.C. Dai, which colonises living Fontanesia, are widely distributed in China (Zhou and Dai 2012, unpublished data). Similarly, in central African rainforests, P. flabelliformis Decock & Yombiy is found on living trunks of Dichostemma and Anthostema whereas P. gabonensis Decock & Yombiy occurs only on Dichostemma (Decock et al. 2015). In contrast, Lonicera japonica has a worldwide distribution and so far is host to a single species of Phylloporia. It will be interesting to determine if P. lonicerae is found elsewhere on Lonicera japonica or if different species of Phylloporia are found on living Lonicera japonica in other geographic regions.

Since 2010, 21 new species of Phylloporia have been described from China (Cui et al. 2010, Zhou and Dai 2012, Zhou 2013, 2015a, 2015b, 2016, Liu et al. 2015, Chen et al. 2017, Ren and Wu 2017). Yet in Japan, only four Phylloporia species, including P. lonicerae, are known. It is hoped that this paper will draw attention to this genus in Japan and lead to the discovery of additional species.

Key to worldwide species of Phylloporia

1 Basidiocarps resupinate P. parasitica
Basidiocarps sessile or stipitate 2
2 Basidiocarps stipitate and terrestrial (woody debris) 3
Basidiocarps sessile and on aerial wood 9
3 Context homogeneous P. minutispora
Context duplex 4
4 Basidiospores > 4 µm long, > 3 µm wide P. verae-crucis (Berk. ex Sacc.) Ryvarden
Basidiospores < 4 µm long, < 3 µm wide 5
5 Cystidia present 6
Cystidia absent 7
6 Hyphae in tomentum short and anticlinal P. elegans Ferreira-Lopes, Robledo & Drechsler-Santos
Hyphae in tomentum loosely interwoven P. nodostipitata Ferreira-Lopes & Drechsler-Santos
7 Pores < 10 per mm P. spathulata
Pores > 10 per mm 8
8 Basidiospores < 3.3 µm long, < 2.3 µm wide P. terrestris
Basidiospores > 3.3 µm long, > 2.3 µm wide P. afrospathulata Yombiy & Decock
9 Hyphal system dimitic 10
Hyphal system monomitic 18
10 Basidiocarps perennial 11
Basidiocarps annual 12
11 Pores 6–8 per mm P. manglietiae Yuan Y. Chen & B.K. Cui
Pores 8–11 per mm P. pectinata (Klotzsch) Ryvarden
12 Basidiocarps solitary P. nouraguensis Decock & G. Castillo
Basidiocarps in cluster 13
13 Pileal surface lighter (greyish-orange to pale cinnamon) P. fulva Yombiy & Decock
Pileal surface darker (yellowish-brown to dark brown) 14
14 Pileus attached by a small vertex and pendant 15
Pileus widely attached to the substratum 16
15 Pores 7–9 per mm; basidiospores > 3.5 µm long P. pendula Yuan Y. Chen & B.K. Cui
Pores 11–12 per mm; basidiospores < 3.5 µm long P. pulla
16 Pores 12–15 per mm; basidiospores < 3 µm long, < 2.5 µm wide P. minutipora
Pores 6–9 per mm; basidiospores > 3 µm long, > 2.5 µm wide 17
17 Pores 6–9 per mm; basidiospores broadly ellipsoid (Q = 1.28–1.33) P. lonicerae
Pores 8–9 per mm; basidiospores subglobose (Q = 1.21–1.23) P. pseudopectinata Yuan Y. Chen & B.K. Cui
18 Pores 2–4 per mm 19
Pores 4–12 per mm 22
19 Basidiospores broadly ellipsoid to subglobose P. fruticum (Berk. & M.A. Curtis) Ryvarden
Basidiospores oblong-ellipsoid, subcylindrical to cylindrical 20
20 Context duplex P. rzedowskii R. Valenz. & Decock
Context homogeneous 21
21 Context < 1 mm thick; on living branch P. oblongospora Y.C. Dai & H.S. Yuan
Context 2–4 mm thick; on living trunk P. inonotoides Yombiy & Decock
22 Basidiocarps annual to perennial, dense and hard consistency 23
Basidiocarps annual, soft corky at least at tomentum layer 29
23 Pores 10–12 per mm; on living Tilia P. tiliae L.W. Zhou
Pores 6–9 per mm; on other angiosperms 24
24 Pileal surface zonate and sulcate 25
Pileal surface azonate P. yuchengii Gafforov, Tomšovský, Langer & L.W. Zhou
25 Pores 6–7 per mm 26
Pores 7–9 per mm 27
26 Basidiospores ellipsoid; mostly on Ribes P. ribis
Basidiospores subglobose; mostly on Ephedra, Cotoneaster or Jasminum P. ephedrae (Woron.) Parmasto
27 Basidiospores > 2.7 µm wide P. dependens Y.C. Dai
Basidiospores < 2.7 µm wide 28
28 Basidiospores ellipsoid to oblong-ellipsoid with a guttule; on Abelia P. gutta L.W. Zhou & Y.C. Dai
Basidiospores broadly ellipsoid without a guttule; on living Crataegus P. crataegi
29 Basidiospores broadly ellipsoid to subglobose 30
Basidiospores ellipsoid, oblong-ellipsoid to cylindrical 40
30 Pores 5–6 per mm 31
Pores 6–11 per mm 35
31 Context duplex, separated by a black zone 32
Context not separated by a black zone 33
32 Pileal surface azonate, lower context 1–4 µm thick P. ampelina (Bondartsev & Singer) Bondartseva
Pileal surface zonate and sulcate, lower context 1 µm thick P. weberiana (Bres. & Henn. ex Sacc.) Ryvarden
33 Basidiocarps solitary covered by a thick tomentum layer, pileal surface not radially faintly wrinkled P. littoralis Decock & Yombiy
Basidiocarps in cluster without a distinct tomentum layer, pileal surface radially faintly wrinkled 34
34 Pileus < 1.5 mm thick, margin regular P. flabelliformis
Pileus > 1.5 mm thick, margin irregular P. gabonensis
35 Basidiocarps > 8 cm wide, > 15 mm thick; contextual hyphae > 5 µm in diam P. ulloai R. Valenz., Raymundo, Cifuentes & Decock
Basidiocarps < 8 cm wide, < 15 mm thick; contextual hyphae < 5 µm in diam 36
36 Contextual hyphae regularly arranged 37
Contextual hyphae interwoven 38
37 Pileus distinctly sulcate, not radially striate, margin obtuse, basal context separated by two black zones; hyphae in tomentum > 4 μm in diam; on living angiosperm trunk P. clausenae L.W. Zhou
Pileus faintly sulcate, radially striate, margin sharp, context duplex thoroughly; hyphae in tomentum < 4 μm in diam; on living liana P. radiata L.W. Zhou
38 Contextual hyphae slightly thick-walled with a wide lumen, frequently septate, large rhomboid crystals absent 39
Contextual hyphae thick-walled with a narrow lumen, occasionally septate, large rhomboid crystals present in trama and context P. chrysites
39 Pores 10–12 per mm; basidiospores < 3 µm long; on living Fontanesia P. fontanesiae
Pores 7–9 per mm; basidiospores > 3 µm long; on other angiosperms P. oreophila L.W. Zhou & Y.C. Dai
40 Basidiospores mostly > 3 µm wide 41
Basidiospores mostly < 3 µm wide 42
41 Pores 4–6 per mm P. hainaniana Y.C. Dai & B.K. Cui
Pores 8–10 per mm P. capucina (Mont.) Ryvarden
42 Basidiocarp solitary 43
Basidiocarp imbricate 46
43 Context homogeneous P. homocarnica L.W. Zhou
Context duplex 44
44 Context not separated by a black zone; on living Flacourtia P. flacourtiae L.W. Zhou
Context separated by a black zone; on other angiosperms 45
45 Pileal surface azonate, pores 6–8 per mm; basidiospores cylindrical P. cylindrispora L.W. Zhou
Pileal surface zonate and sulcate, pores 8–9 per mm; basidiospores ellipsoid P. lespedezae G.J. Ren & F. Wu
46 Basidiospores mostly < 2.5 µm wide 47
Basidiospores mostly > 2.5 µm wide P. bibulosa
47 Pores 5–6 per mm, context duplex, not separated by a black zone; basidiospores > 3.5 µm long, contextual hyphae interwoven; on living Nandina P. nandinae L.W. Zhou & Y.C. Dai
Pores 7–9 per mm, context duplex, separated by a black zone; basidiospores < 3.5 µm long, contextual hyphae regularly arranged; on living Osmanthus P. osmanthi L.W. Zhou

Acknowledgements

Dr. Karen K. Nakasone (CFMR, USA) is thanked for improving the manuscript. The research was financed by the National Natural Science Foundation of China (Project No. 31570014) and Youth Innovation Promotion Association CAS (No. 2017240).

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