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Species Delimitation for Neonectria Coccinea Group Including the Causal Agents of Beech Bark Disease in Asia, Europe, and North America

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Species Delimitation for Neonectria Coccinea Group Including the Causal Agents of Beech Bark Disease in Asia, Europe, and North America 菌物学报 [email protected] 15 May 2013, 32(3): 485-517 Http://journals.im.ac.cn Mycosystema ISSN1672-6472 CN11-5180/Q © 2013 IMCAS, all rights reserved. Species delimitation for Neonectria coccinea group including the causal agents of beech bark disease in Asia, Europe, and North America Yuuri HIROOKA1* Amy Y. ROSSMAN2 Wen-Ying ZHUANG3 Catalina SALGADO-SALAZAR4 Priscila CHAVERRI4 1Forestry & Forest Products Research Institute, Department of Forest Microbiology, 1 Matsunosato, Tukuba, Ibaraki, 305-8687, JAPAN 2Systematic Mycology and Microbiology Laboratory, United States Department of Agriculture, Agricultural Research Service, 10300 Beltsville Ave., Beltsville, Maryland 20705, USA 3State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, P.R. China 4University of Maryland, Department of Plant Science and Landscape Architecture, 2112 Plant Sciences Building, College Park, Maryland 20742, USA Abstract: Neonectria coccinea has historically been known as a serious pathogen of beech trees in North America and Europe. Phylogenetic relationships of this species and its relatives have been determined. Neonectria faginata, previously referred to as Neo. coccinea var. faginata has been delimited from Neo. coccinea sensu stricto and Neo. punicea. Five additional lineages supported by relatively high phylogenetic values are allied with Neo. coccinea and its relatives. Until now, these lineages have not been recognized as species because no significant morphological differences among them were found. Although each phylogenetic species appeared to be unique in host specificity and geography, relatively few specimens of these species existed. We re-evaluated these species using newly obtained specimens and isolates from Asia, Europe, and North America. Based on sequences of multiple loci, specifically act, ITS, LSU, rpb1, tef1 and tub, our results indicate that these isolates represent four phylogenetic species, Neo. coccinea, Neo. faginata, Neo. microconidia, and Neo. punicea. In our phylogeny, each species is well supported by high BI PP, MP BP, and ML BP values. The single-locus analyses of ITS and LSU did not correlate with our species recognition criteria. Based on morphology, phylogeny, host specificity and geographical traits, these four species are conclusively delimited. Each of them is re-described and illustrated. Epitype specimens for Sphaeria coccinea and Neonectria coccinea var. faginata are designated. Because no type specimen of Neo. punicea was found, this name is neotypified. Within Neo. coccinea, Neo. microconidia, and Neo. punicea, some sublineages were supported by high phylogenetic values. In the future these may warrant recognition as distinct species. Key words: invasive pathogens, molecular systematics, Neonectria coccinea, Neonectria faginata, Neonectria microconidia, Neonectria punicea, species concept, typification *Corresponding author. E-mail: [email protected] Received: 18-12-2012, accepted: 13-03-2013 486 ISSN1672-6472 CN11-5180/Q Mycosystema May 15, 2013 Vol.32 No.3 含亚洲、欧洲、北美洲山毛榉病害病原菌的 Neonectria coccinea 复合群的物种概念 Yuuri HIROOKA1* Amy Y. ROSSMAN2 Wen-Ying ZHUANG3 Catalina SALGADO-SALAZAR4 Priscila CHAVERRI4 1Forestry & Forest Products Research Institute, Department of Forest Microbiology, 1 Matsunosato, Tukuba, Ibaraki, 305-8687, JAPAN [日本] 2Systematic Mycology and Microbiology Laboratory, United States Department of Agriculture, Agricultural Research Service, 10300 Beltsville Ave., Beltsville, Maryland 20705, USA [美国] 3State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, P.R. China [中国] 4University of Maryland, Department of Plant Science and Landscape Architecture, 2112 Plant Sciences Building, College Park, Maryland 20742, USA [美国] 摘 要：对包含亚洲、欧洲、北美洲山毛榉病害病原菌在内的 Neonectria coccinea 复合群中物种之间的系统演化关系 以及物种概念进行了探讨。Neonectria faginata（曾处理为 Neo. coccinea var. faginata）与狭义的 Neo. coccinea 和 Neo. punicea 有明显区别。系统树显示 5 个分支与 Neo. coccinea 群的关系较为接近，由于缺乏显著的形态差异，它们始终 没有在物种的等级上区分。根据形态学、系统发育、寄主专化性和地理因素，采用多基因 act、ITS、LSU、rpb1、tef1 和 tub 序列分析的方法，对亚洲、欧洲、北美洲的相关材料进行了研究，结果表明，它们代表 4 个独立的物种，即 Neo. coccinea，Neo. faginata，Neo. microconidia 和 Neo. punicea，对每个种进行了详尽的描述和图示。并为 Sphaeria coccinea 和 Neonectria coccinea var. faginata 指定了附加模式。 关键词：入侵性病原菌，分子系统学，猩红新丛赤壳，Neonectria faginata，小孢新丛赤壳，Neonectria punicea，物种 概念，选模式 INTRODUCTION The beech scale insect was introduced into Nova The beech bark disease (BBD) constitutes one Scotia through seedling beech trees brought from of the greatest global threats to beech forests. This Europe in 1890 (Ehrlich 1934; Hewitt 1914). Recent disease occurs following the interaction between the molecular studies indicate that the causal agents of beech scale insect, Cryptococcus fagisuga Lind. and BBD were introduced from Europe, yet it is unclear one of the three ascomycetous fungi, Neonectria if the beech scale insect and BBD fungal pathogens coccinea (Pers.) Rossman & Samuels, Neo. faginata were introduced into North America at the same (M.L. Lohman, A.M.J. Watson & Ayers) Castl. & time (Mahoney et al. 1999; Gwiazdowski et al. Rossman, and Neo. ditissima (Tul. & C. Tul.) 2006). The disease has now rapidly spread across Samuels & Rossman. The disease was first the northeastern United States and southeastern documented in Germany in 1849 (McIntosh 1849). Canada (Houston 1994; Griffin et al. 2003) with http://journals.im.ac.cn/jwxtcn Yuuri HIROOKA et al. / Species delimitation for Neonectria coccinea group including the causal agents of beech bark disease in Asia, … 487 80%–90% mortality rates of mature beech (Houston tubercularia-like anamorph (Hirooka et al. 2011, 1994). 2012). Previously considered to be a synonym of The BBD pathogenic fungi are Neonectria Nectria, Rossman et al. (1999) resurrected the genus coccinea on Fagus in Europe, Neo. faginata on Neonectria Wollenw. (Wollenweber 1916), typified Fagus in North America, and Neo. ditissima on by Neo. ramulariae Wollenw., for nectria-like hardwoods in North America and Europe, rarely species having a cylindrocarpon-like anamorph. Asia. These fungi have red, globose, slightly Many nectrioid species having cylindrocarpon-like roughened perithecia, 1-septate ascospores, and anamorphs were included in the genus Neonectria. cylindrocarpon-like anamorphs (Rossman et al. Chaverri et al. (2011) divided Neonectria into five 1999). They are morphologically similar and often genera: Campylocarpon Halleen, Schroers & Crous, misidentified because they are distinguished by only Ilyonectria P. Chaverri & C. Salgado, Neonectria small differences in ascospore size. Castlebury et al. Wollenw., Rugonectria P. Chaverri & Samuels, and (2006) conducted taxonomic studies of these fungi Thelonectria P. Chaverri & C. Salgado. These genera based on morphological observation and combined were defined based on a multiple locus phylogeny phylogenetic analyses of rpb2, tef1, and tub gene and morphological observations. regions. They clarified the differences between Neonectria coccinea with its anamorph Neonectria coccinea, Neo. ditissima, and Neo. Cylindrocarpon candidum (Link: Fr.) Wollenw. has faginata (=Neo. coccinea var. faginata), newly been considered a common species distributed recognized at the species rank. The phylogenetic tree widely in the northern hemisphere, frequently of Castlebury et al. (2006) also showed that reported on twigs and wood of beech trees as well as potentially five distinct species exist that are sister to on other deciduous trees, dung, and soil (Domsch et Neo. coccinea. Although each phylogenetic species al. 2007). The basionym of the anamorphic fungus, seemed to be segregated by host specificity and Fusidium candidum Link, was described by Link geography, no significant morphological differences (1809) and sanctioned by Fries (1832). Wollenweber among them were found due to the limited number (1928) transferred Fusidium candidum to of samples. Cylindrocarpon. Booth (1966) first introduced the Neonectria coccinea was originally described teleomorph-anamorph connection as states of one as Sphaeria coccinea Pers.: Fr. by Persoon (1800). species, and recent studies have confirmed the After Fries (1823) sanctioned Sphaeria coccinea, he connection. The recent study by Castlebury et al. transferred this species to Nectria (Fries 1849). (2006) restricted this species to Fagus in Europe. Because Persoon (1800) and Fries (1823, 1849) did Using combined sequences of several loci, a not typify any specimens, Booth (1959) found number of new species within Neonectria sensu lato several Persoon specimens of S. coccinea and were recently described from China (Luo & Zhuang designated one of them as the lectotype. Since the 2010; Zhao et al. 2011). Neonectria confusa J. Luo 19th century, the broadly conceived genus Nectria & W.Y. Zhuang was placed in the Neo. coccinea has been narrowed. Most recently the genus Nectria group while Neo. microconidia J. Luo, P. Zhao & was determined to include fungi having red W.Y. Zhuang was sister to the Neo. coccinea clade. perithecia without bright yellow scurf and Although Luo & Zhuang (2010) and Zhao et al. Mycosystema 488 ISSN1672-6472 CN11-5180/Q Mycosystema May 15, 2013 Vol.32 No.3 (2011) recognized Neo. confusa and Neo. low nutrient agar (SNA; Nirenberg 1976). Cultures microconidia as distinct species, the variation on SNA were incubated at 25℃ with alternating between them was relatively low with subtle 12h/12h fluorescent light/darkness for 2–3 wks. morphological differences from other species in the Images were captured
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