Research Article |
Corresponding author: Zhao-Qing Zeng ( zengzq@im.ac.cn ) Corresponding author: Wen-Ying Zhuang ( zhuangwy@im.ac.cn ) Academic editor: Danny Haelewaters
© 2019 Zhao-Qing Zeng, Wen-Ying Zhuang.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Zeng Z-Q, Zhuang W-Y (2019) The genera Rugonectria and Thelonectria (Hypocreales, Nectriaceae) in China. MycoKeys 55: 101-120. https://doi.org/10.3897/mycokeys.55.34527
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Recent collections and herbarium specimens of Rugonectria and Thelonectria from different regions of China were examined. Using combined analyses of morphological and molecular data, 17 species are recognised including three species of Rugonectria and 14 species in Thelonectria. Amongst them, R. microconidia and T. guangdongensis are new to science. Rugonectria microconidia on mossy bark is characterised by superficial, yellow to orange, pyriform to subglobose perithecia with a warted surface; ellipsoidal to broadly ellipsoidal, striate, uniseptate ascospores; and allantoid to rod-shaped, aseptate microconidia. Thelonectria guangdongensis possesses bright red perithecia with a slightly roughened surface and a prominently dark papilla; ellipsoidal, smooth, uniseptate ascospores; and subcylindrical, slightly curved, multiseptate macroconidia. Morphological distinctions and sequence divergences between the new species and their close relatives are discussed. Name changes for the previously recorded species in China are noted.
Morphology, Multigene analyses, Taxonomy
The family Nectriaceae was introduced in 1865 and circumscribed to accommodate the hypocrealean species having ascomata that are generally yellow, orange-red to purple and usually changing colour in potassium hydroxide (KOH) and lactic acid (LA) (
The genus Rugonectria P. Chaverri & Samuels, typified by R. rugulosa (Pat. & Gaillard) Samuels, P. Chaverri & C. Salgado, is characterised by perithecia solitary or in groups, seated on or partially immersed in a stroma. The perithecia are orange to red, globose to subglobose and non-papillate, with warted or rugose walls. Ascospores are ellipsoidal to oblong, striate, hyaline and 1-septate; and microconidia are ovoid to cylindrical (
The first record of Rugonectria from China dates back to 2000 when R. rugulosa (as Nectria rugulosa Pat. & Gaillard) was reported by
Specimens were collected from Beijing, Fujian, Guangdong, Hainan, Henan, Hubei, Hunan and Yunnan provinces and are deposited in Herbarium Mycologicum Academiae Sinicae (HMAS) and cultures are kept in the State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences. The methods used by
Genomic DNA was extracted from fresh mycelium following the method of
Newly obtained sequences and those retrieved from GenBank are listed in Table
List of species, herbarium/strain numbers and GenBank accession numbers of materials used in this study.
Species | Herbarium/strain numbers | GenBank Accession numbers | |||
ACT | ITS | LSU | RPB1 | ||
Cosmospora coccinea Rabenh. | CBS 114050 | GQ505967 | FJ474072 | GQ505990 | GQ506020 |
Nectria cinnabarina (Tode) Fr. | AR 4302/AR 4477 | HM484627 | HM484548 | HM484562 | HM484577 |
Rugonectria castaneicola (W. Yamam. & Oyasu) Hirooka & P. Chaverri | CBS 128360 | – | MH864901 | MH876352 | – |
R. microconidia Z.Q. Zeng & W.Y. Zhuang | HMAS 254521 | MF669044 a | MF669050 | MF669052 | MF669056 |
R. neobalansae (Samuels) P. Chaverri & Samuels | CBS 125120 | – | KM231750 | HM364322 | KM232146 |
R. rugulosa (Pat. & Gaillard) Samuels, P. Chaverri & C. Salgado | YH 1001 | JF832515 | JF832661 | JF832761 | JF832836 |
R. sinica W.Y. Zhuang, Z.Q. Zeng & W.H. Ho | HMAS 183542 | MF669046 | HM054141 | HM042430 | MF669058 |
Thelonectria asiatica C. Salgado & Hirooka | MAFF 241576 | KC121436 | KC153774 | KC121500 | KC153967 |
T. beijingensis Z.Q. Zeng, J. Luo & W.Y. Zhuang | HMAS 188498 | MF669047 | JQ836656 | MF669054 | MF669059 |
T. blattea C. Salgado & P. Chaverri | CBS 95268 | KC121387 | KC153725 | KC121451 | KC153918 |
T. brayfordii C. Salgado & Samuels | CBS 118612 | KC121381 | KC153719 | KC121445 | KC153912 |
T. conchyliata C. Salgado & P. Chaverri | GJS 8745 | KC121401 | KC153739 | KC121465 | KC153932 |
T. discophora (Mont.) P. Chaverri & C. Salgado | AR 4742 | KC121376 | KC153714 | KC121440 | KC153907 |
T. guangdongensis Z.Q. Zeng & W.Y. Zhuang | HMAS 254522 | MF669045 | MF669051 | MF669053 | MF669057 |
T. ianthina C. Salgado & Guu | GJS 10118 | KC121393 | KC153731 | KC121457 | KC153924 |
T. japonica C. Salgado & Hirooka | MAFF 241524 | KC121428 | KC153766 | KC121492 | KC153959 |
HMAS 98327 | MK556799 | HM054140 | HM042434 | – | |
T. mammoidea (W. Phillips & Plowr.) C. Salgado & R.M. Sanchez | IMI 69361 | KC121425 | KC153763 | KC121489 | KC153956 |
T. ostrina C. Salgado & P. Chaverri | GJS 9623 | KC121418 | KC153756 | KC121482 | KC153949 |
T. phoenicea C. Salgado & P. Chaverri | GJS 85179 | KC121398 | KC153736 | KC121462 | KC153929 |
HMAS 76856 | MK556800 | JQ836657 | DQ119572 | – | |
T. pinea (Dingley) C. Salgado & P. Chaverri | AR 4324 | HM352875 | HM364294 | HM364307 | HM364326 |
T. porphyria C. Salgado & Hirooka | MAFF 241515 | KC121426 | KC153764 | KC121490 | KC153957 |
HMAS 98333 | MK556798 | HM054136 | HM042433 | – | |
T. purpurea C. Salgado & P. Chaverri | GJS 10131 | KC121394 | KC153732 | KC121458 | KC153925 |
T. rubi (Osterw.) C. Salgado & P. Chaverri | CBS 11312 | KC121380 | KC153718 | KC121444 | KC153911 |
T. sinensis (J. Luo & W.Y. Zhuang) Z.Q. Zeng & W.Y. Zhuang | HMAS 183186 | MF669048 | FJ560441 | FJ560436 | MF669060 |
T. tyrus C. Salgado & P. Chaverri | GJS 9046 | KC121413 | KC153751 | KC121477 | KC153944 |
T. violaria C. Salgado & R.M. Sanchez | AR 4766 | KC121377 | KC153715 | KC121441 | KC153908 |
T. yunnanica Z.Q. Zeng & W.Y. Zhuang | HMAS 183564 | MF669049 | FJ560438 | MF669055 | MF669061 |
The sequences of ACT, ITS, LSU and RPB1 from 25 representative taxa of Rugonectria and Thelonectria were analysed. The partition homogeneity test (P = 0.03) indicated that the individual partitions were not highly incongruent (
CHINA. Hunan, Yizhang, Mangshan, (24°57'56.58"N, 112°57'34.63"E), alt. 700 m, on mossy bark, 26 October 2015, Z.Q. Zeng, X.C. Wang, K. Chen, Y.B. Zhang 10266 (HMAS 254521); ex-type culture: HMAS 247232.
The specific epithet refers to the microconidia produced in culture.
Mycelium not visible around ascomata or on natural substrata. Ascomata superficial, gregarious, with basal stroma, pyriform to subglobose, non-papillate, yellow to orange, often with a darker red ostiolar area when dry, turning dark red in KOH, becoming slightly yellow in LA, 421–549 × 333–470 μm (n = 8). Perithecial surface warted, 30–93 µm thick, of textura globulosa to textura angularis, cells 10–27 × 8–18 µm, walls 1.5–2.5 µm thick. Perithecial wall of two layers, 45–70 µm thick, outer layer 25–45 µm thick, of textura globulosa to textura angularis; inner layer 7–25 µm thick, of textura prismatica. Asci unitunicate, clavate, 8-spored, 93–130 × (11–)15–25 µm (112.6 ± 12.6 × 18.9 ± 3.2 μm). Ascospores ellipsoid to broadly ellipsoid, 1-septate, striate, uniseriate or biseriate above and uniseriate below, hyaline, 20–28 × 8–12 µm (24.0 ± 2.0 × 10.1 ± 0.9 μm). Colony on PDA 42 mm diameter after 7 d under daylight at 25 °C, surface velvety, with white aerial mycelium, producing pale pinkish pigment in medium. Colony on SNA reaches 40 mm diameter after 7 d under daylight at 25 °C, surface with sparse whitish aerial mycelium. Conidiophores simply branched, 18–50 × 2–3 μm. Microconidia allantoid to rod shaped, slightly curved, 0(1–2)-septate, 3–14(–18) × 1.2–2.5(–3) μm (6.7 ± 3.1 × 1.6 ± 0.4 μm).
Rugonectria microconidia a–d ascomata on natural substratum e colony on PDA f colony on SNA g, h median section through perithecium i–k asci with ascospores l–o ascospores p–s conidiophores and conidia t, u conidiogenous cells and conidia v, w microconidia. Scale bars: 0.5 mm (a–d); 50 μm (g, h); 10 μm (i–w).
On mossy bark.
Asia (China).
The non-papillate perithecia with warted surface, clavate asci with ellipsoidal to broadly ellipsoidal, uniseptate, striate ascospores, as well as our molecular data, suggest that this species belongs to Rugonectria (
≡ Nectria rugulosa Pat. & Gaillard, Bull. Soc. Mycol. Fr. 5(4): 115, 1890.
≡ Neonectria rugulosa (Pat. & Gaillard) Mantiri & Samuels, in Mantiri, Samuels, Rahe & Honda, Can. J. Bot. 79(3): 339, 2001.
= Cylindrocarpon rugulosum Brayford & Samuels, in Samuels & Brayford, Sydowia 46(1): 148, 1994.
CHINA. Henan, Jigongshan, alt. 400 m, on rotten twigs, 14 November 2003, W.Y. Zhuang, Y. Nong 5142 (HMAS 91774). Hainan, Changjiang, Bawangling, alt. 1100 m, on rotten twigs, 7 December 2000, W.Y. Zhuang, X.M. Zhang H25 (HMAS 83349); Ledong, Jianfengling, alt. 1100 m, on rotten twigs, 9 December 2000, W.Y. Zhuang, X.M. Zhang, Z.H. Yu H36, H41 (HMAS 83350, 83370); Qiongzhong, Limushan, alt. 700 m, on rotten twigs, 18 December 2000, W.Y. Zhuang, X.M. Zhang H124 (HMAS 76867); Tongzha, Wuzhishan, alt. 1000 m, on bark, 16 December 2000, W.Y. Zhuang, X.M. Zhang, Z.H. Yu, Y.H. Zhang H105 (HMAS 83371); on rotten twigs, W.P. Wu W7058 (HMAS 183161); Yunnan, Xichou, on rotten twigs, 11 November 1999, W.Y. Zhuang, Z.H. Yu 3407 (HMAS 183160).
On rotten twigs, wood of recently dead and dying trees.
Africa (Congo), Americas (Venezuela), Asia (China, Indonesia), possibly pantropical.
The species was formerly placed in Nectria (Fr.) Fr. and Neonectria Wollenw. until
CHINA. Hainan, Changjiang, Bawanling, alt. 1100 m, on dead twigs of Quercus sp., 7 December 2000, W.Y. Zhuang, X.M. Zhang H22, H30 (HMAS 76854, 83369); Changjiang, Bawanling, alt. 1100 m, on dead twigs, 7 December 2000, W.Y. Zhuang, X.M. Zhang H28 (HMAS 76865); Lingshui, Diaoluoshan, alt. 1100 m, on bark, 13 December 2000, W.Y. Zhuang, X.M. Zhang, Z.H. Yu H70 (HMAS 76866); Henan, Jigongshan, alt. 400 m, on dead twigs, 14 November 2003, W.Y. Zhuang, Y. Nong 5099 (HMAS 91773); Fujian, Wuyishan, on dead twigs, 21 September 2006, W.Y. Zhuang, J. Luo, W.Y. Li 6846 (HMAS 183542).
On bark and dead twigs.
Asia (China).
Morphologically Rugonectria sinica resembles R. castaneicola (W. Yamam. & Oyasu) Hirooka & P. Chaverri in having four-spored asci (
CHINA. Guangdong, Shixing, Chebaling, (24°43'17.38"N, 114°16'39.50"E), alt. 600 m, on branches, 2 November 2015, Z.Q. Zeng, X.C. Wang, K. Chen, Y.B. Zhang 10627 (HMAS 254522); ex-type culture: HMAS 247233.
The specific epithet refers to the type locality of the fungus.
Mycelium not visible around ascomata or on natural substrata. Ascomata perithecial, solitary to gregarious, up to 10 in a group, with a well–developed stroma, superficial, subglobose to globose, bright red with a prominently darkened papilla, turning dark red in KOH, becoming slightly yellow in LA, 235–382 × 245–412 μm (n = 8). Perithecial surface slightly roughened. Perithecial wall of two layers, 20–50 µm thick, outer layer 13–37 µm thick, of textura intricata; inner layer 7.5–13 µm thick, of textura prismatica. Asci not observed. Ascospores ellipsoid, 1-septate, smooth, 10–13 × 3–5 µm (11.6 ± 1.3 × 4.2 ± 0.7 μm). Colony on PDA 28 mm diameter after 7 d under daylight at 25 °C, surface velvety, with white aerial mycelium, producing purple pigment in medium. Colony on SNA 35 mm diameter after 7 d under daylight at 25 °C, surface with sparse whitish aerial mycelium. Phialides cylindrical or slightly swollen, 20–58 × 2–4 μm. Macroconidia cylindrical, slightly curved with rounded ends, 2–5-septate, 48–70 × 4.8–5.3 μm (58.9 ± 7.14 × 5.0 ± 0.2 μm). Microconidia and chlamydospores not observed in culture.
On branches.
Asia (China).
Amongst species of Thelonectria, T. guangdongensis resembles T. phoenicea in having subglobose to globose perithecia with slightly roughened surface, purple colony, lack of microconidia and number of septa in macroconidia (
Phylogenetically T. guangdongensis is closely related to T. beijingensis with strong statistical support (MLBP/MPBP/BIPP = 100%/97%/100%) (Figure
CHINA. Beijing, on bark of an unidentified tree, 1 September 2010, L. Cai 7604 (HMAS 188498), ex-type culture: HMAS 188566.
On bark.
Asia (China).
This species was introduced by
On bark of decaying shrubs and trees.
Asia (China).
≡ Nectria coronata Penz. & Sacc., Malpighia 11(11–12): 510, 1897.
CHINA. Hainan, Lingshui, Diaoluoshan, alt. 1050 m, on rotten twigs of Pinus sp., 15 December 2000, W.Y. Zhuang, X.M. Zhang H90 (HMAS 76855).
On bark of shrubs and trees, sometimes associated with small cankers.
Americas (Costa Rica), Asia (Indonesia, Taiwan), possibly pantropical.
The morphology and molecular data indicated that T. coronata is a species complex.
≡ Sphaeria discophora Mont., Annls Sci. Nat., Bot., sér. 2 3: 353, 1835.
≡ Neonectria discophora (Mont.) Mantiri & Samuels, in Mantiri, Samuels, Rahe & Honda, Can. J. Bot. 79(3): 339, 2001.
CHINA. Hainan, Changjiang, Bawangling, alt. 1100 m, 7 December 2000, on rotten twigs, W.Y. Zhuang, X.M. Zhang, Z.H. Yu H24 (HMAS 83351); Lingshui, Diaoluoshan, alt. 1050 m, 15 December 2000, on rotten twigs, W.Y. Zhuang, X.M. Zhang H83, H92-1 (HMAS 83353, 83352). Yunnan, Tengchong, 16 October 2003, W.P. Wu W7097 (HMAS 183180).
On decaying bark of shrubs and trees.
Americas (Chile), Asia (China), Europe (Scotland).
Notes. Thelonectria discophora is the type species of the genus Thelonectria. Many specimens identified as this species were determined to be species complex until
On decaying bark of trees and shrubs.
Americas (Costa Rica), Asia (China).
This species is known from Heredia Province of Costa Rica and Taiwan Province of China on decaying bark of trees and shrubs (
CHINA. Hubei, Wufeng, Houhe, alt. 800 m, 13 September 2004, on rotten twigs, W.Y. Zhuang, Y. Nong 5621 (HMAS 98327); Yunnan, Tengchong, on rotten twigs, W.P. Wu W7104a (HMAS 183155).
On decaying bark of Fagus crenata and possibly on bark of other shrubs and trees.
Asia (China, Japan).
Specimens of this fungus were treated as T. discophora sensu lato until T. japonica was introduced by
≡ Nectria lucida Höhn., Sber. Akad. Wiss. Wien, Math.-naturw. Kl., Abt. 1 118: 298, 1909.
≡ Neonectria lucida (Höhn.) Samuels & Brayford, in Brayford, Honda, Mantiri & Samuels, Mycologia 96(3): 590, 2004.
On decaying bark of shrubs and trees.
Africa (Cameroon), Americas (Costa Rica), Asia (China, Indonesia), possibly pantropical.
This is a relatively common species and recorded as Neonectria lucida by
On decaying bark of shrubs and trees.
Americas (French Guiana), Asia (China).
The specimens of this species were filed under T. lucida (
CHINA. Hainan, Lingshui, Diaoluoshan, alt. 1050 m, 15 December 2000, W.Y. Zhuang, X.M. Zhang H86 (HMAS 76856).
On decaying Acacia celsa and other plants.
Asia (China, Indonesia), Oceania (Australia).
Re-examination of HMAS 76856 indicated that T. phoenicea is the correct name for the specimen which was previously identified as T. discophora. It is distributed also in Taiwan Province (
CHINA. Hubei, Wufeng, Houhe, alt. 800 m, on rotten twigs, 12 September 2004, W.Y. Zhuang, Y. Nong 5542 (HMAS 98333).
On decaying bark of Cryptomeria japonica and other woody substrates.
Asia (China, Japan).
The collection was previously treated as T. discophora sensu lato (
≡ Neonectria sinensis J. Luo & W.Y. Zhuang, Mycologia 102(1): 147, 2010.
CHINA. Hubei, Shennongjia, alt. 1700 m, on bark of a coniferous (?) tree, 17 September 2003, X.M. Zhang, Y.Z. Wang Z108 (HMAS 183186), ex-type culture: HMAS 173255.
On bark of a coniferous (?) tree.
Asia (China).
The species was originally placed in Neonectria by
≡ Nectria veuillotiana Sacc. & Roum., Rev. Mycol. 2: 189, 1880.
≡ Neonectria veuillotiana (Sacc. & Roum.) Mantiri & Samuels, Canda. J. Bot. 79: 339, 2001.
CHINA. Anhui, Jinzhai, Tiantangzhai, alt. 1000 m, on bark, 24 August 2011, W.Y. Zhuang, H.D. Zheng, Z.Q. Zeng, S.L. Chen 7869 (HMAS 266577). Hubei, Shennongjia, alt. 1200 m, on rotten twigs associated with other fungi, 15 September 2004, W.Y. Zhuang, Y. Nong 5686 (HMAS 98332); Shennongjia, alt. 1700 m, on bark associated with other fungi, 15 September 2003, X.M. Zhang, Y. Z. Wang Z196 (HMAS 183188); Xingshan, Longmenhe, alt. 1800 m, on rotten twigs associated with other fungi, 18 September 2004, W.Y. Zhuang, Y. Nong 5832 (HMAS 99207). Jilin, Changbaishan, alt. 800 m, on rotten twigs, 27 July 2012, T. Bau, W.Y. Zhuang, H.D. Zheng, Z.Q. Zeng, Z.X. Zhu, F. Ren 8246 (HMAS 266579); Jiaohe, Qianjin forest farm, alt. 450 m, on rotten twigs, 23 July 2012, T. Bau, W.Y. Zhuang, Z.Q. Zeng, H.D. Zheng, Z.X. Zhu, F. Ren 8087b (HMAS 266578). Yunnan, Tengchong, on rotten twigs associated with other fungi, 16 September 2003, W.P. Wu W7095 (HMAS 183568).
On bark of deciduous trees, Eucalyptus sp., Fagus sp., Gleditschia triacanthos, Salix sp.
Asia (China), Europe (France and Germany), Azores Islands.
The species was first placed in Nectria, then in Neonectria (
CHINA. Yunnan, Baoshan, on bark of an unidentified tree, 15 October 2003, W.P. Wu W7122 (HMAS 183564), ex-type culture: HMAS 188567.
On bark.
Asia (China).
Thelonectria yunnanica is only known from the type locality. It is phylogenetically related to T. ostrina (Figure
≡ Nectria jungneri Henn., Bot. Jb. 22: 75, 1895.
≡ Neonectria jungneri (Henn.) Samuels & Brayford, Mycologia 96(3): 580, 2004.
≡ Macronectria jungneri (Henn.) C. Salgado & P. Chaverri, in Salgado-Salazar, Rossman & Chaverri, Fungal Diversity 80: 448, 2016.
CHINA. Guangdong, Dinghushan, on rotten twigs associated with other fungi, 9 October 1998, W.P. Wu W1871-2 (HMAS 183155).
On various woody substrates, as well as other plant organic matter.
Africa (Cameroon), Americas (Brazil, Costa Rica), Asia (China), possibly pantropical.
This fungus was originally described as Nectria jungneri and was transferred to Neonectria (
The genus Rugonectria is characterised by the non-papillate, orange to red, conspicuously warted to rugose perithecial surface (
Historically, the nectriaceous fungi with cylindrocarpon-like asexual states were assigned to Neonectria. The accumulated morphological and phylogenetic data suggest that the genus was heterogeneous (
The type species of Thelonectria, T. discophora, previously considered to be cosmopolitan, was first described based on material collected from Chile and was determined to be heterogeneous (
The authors would like to thank Dr. A.Y. Rossman for her valuable comments and corrections and Drs. X.C. Wang, K. Chen and Y.B. Zhang for collecting specimens jointly for this study. This work was supported by the National Natural Science Foundation of China (nos. 31750001, 31570018, 31870012) and Frontier Key Program of Chinese Academy of Sciences (No. QYZDY-SSW-SMC029).