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<I>Gymnosporangium</I> Persoonia 45, 2020: 68–100 ISSN (Online) 1878-9080 www.ingentaconnect.com/content/nhn/pimj RESEARCH ARTICLE https://doi.org/10.3767/persoonia.2020.45.03 Gymnosporangium species on Malus: species delineation, diversity and host alternation P. Zhao1, X.H. Qi 2, P.W. Crous3,4, W.J. Duan5, L. Cai1* Key words Abstract Gymnosporangium species (Pucciniaceae, Pucciniales, Basidiomycota) are the causal agents of cedar- apple rust diseases, which can lead to significant economic losses to apple cultivars. Currently, the genus contains Apple rust 17 described species that alternate between spermogonial/aecial stages on Malus species and telial stages on host alternation Juniperus or Chamaecyparis species, although these have yet to receive a modern systematic treatment. Further- new taxa more, prior studies have shown that Gymnosporangium does not belong to the Pucciniaceae sensu stricto (s.str.), species delimitation nor is it allied to any currently defined rust family. In this study we examine the phylogenetic placement of the genus Gymnosporangium. We also delineate interspecific boundaries of the Gymnosporangium species on Malus based on phylogenies inferred from concatenated data of rDNA SSU, ITS and LSU and the holomorphic morphology of the entire life cycle. Based on these results, we propose a new family, Gymnosporangiaceae, to accommodate the genus Gymnosporangium, and recognize 22 Gymnosporangium species parasitic on Malus species, of which G. lachrymiforme, G. shennongjiaense, G. spinulosum, G. tiankengense and G. kanas are new. Typification of G. asiaticum, G. fenzelianum, G. juniperi­virginianae, G. libocedri, G. nelsonii, G. nidus­avis and G. yamadae are proposed to stabilize the use of names. Morphological and molecular data from type materials of 14 Gymnospor­ angium species are provided. Finally, morphological characteristics, host alternation and geographical distribution data are provided for each Gymnosporangium species on Malus. Article info Received: 27 October 2019; Accepted: 4 December 2019; Published: 10 January 2020. INTRODUCTION of Malus species, cause premature defoliation, and eventually kill their hosts plants (Helfer 2005). Hitherto, up to 17 Gymno­ Plant parasitic rusts within the order Pucciniales represent sporangium species are known as causal agents of apple rust one of the largest groups of fungal plant pathogens, which diseases, having mostly been reported from temperate regions occur on ferns to advanced monocots and dicots (Aime 2006, in Asia, Africa, Europe and North America (Farr & Rossman Webster & Weber 2007). Approximately 7 800 rust species are 2019). Eleven Gymnosporangium species have been reported currently recognised worldwide, with many species causing on 16 Malus species and their hybrids in Asia (Azbukina 1972, significant economic losses to agricultural or forest crop plants Wang & Guo 1985, Hiratsuka et al. 1992, Zhuang et al. 2012), (Arthur 1934, Hiratsuka et al. 1992, Cummins & Hiratsuka and nine Gymnosporangium species have been reported on 17 2003). Among them, cedar rusts are one of the most important Malus species and their hybrids in North America (Arthur 1934, genera of phytopathogens (Helfer 2005). These pathogens Ziller 1974). Six Gymnosporangium spp. have been reported belong to the genus Gymnosporangium, which previously has on M. baccata, M. domestica, M. pumila and M. sylvestris in been placed in the family Pucciniaceae (Pucciniales, Basidio­ Europe, and only one Gymnosporangium species has been mycota), and are obligate biotrophic phytopathogens (Cummins reported from Africa (Hylander 1953, Jørstad 1962, Wilson & & Hiratsuka 1983, 2003). Presently over 64 species have been Henderson 1966, Farr & Rossman 2019). Among them, G. asia­ recorded, having a demicyclic (macrocyclic or microcyclic in a ticum, G. clavipes, G. globosum, G. juniper­virginianeae and few species) life cycle with a telial stage on gymnosperm trees G. yamadae are listed as quarantine pests in Asia, Europe, in Cupressaceae, and an aecial stage on trees of the apple and North America (Duan et al. 2017, EPPO 2017, 2018). tribe, Maleae, in the family Rosaceae (Kern 1973, Shen et al. Accurate and efficient species recognition, as well as a better 2018, Farr & Rossman 2019). understanding of their life cycle are thus important for plant Within the genus Gymnosporangium, cedar-apple rusts repre- quarantine and effective disease control. sent some of the most serious and devastating diseases occur- Traditional taxonomy of Gymnosporangium relies on morpho- ring in apple plantations worldwide (Sinclair & Lyon 2005, Zhao logical distinctions in spermogonia and teliospores at generic et al. 2016, Lâce 2017). They occur on leaves, fruits and stems and suprageneric level, and this genus has long been placed in Pucciniaceae (Dietel 1928, Cummins & Hiratsuka 1983, 1 State Key Laboratory of Mycology, Institute of Microbiology, Chinese 2003). However, recent molecular studies revealed a phylo- Academy of Sciences (CAS), Beijing, 100101, China; corresponding author e-mail: [email protected]. genetic distinction of Gymnosporangium from other members 2 Guangdong Institute of Microbiology, Guangdong Academy of Sciences, of the Pucciniaceae (Maier et al. 2003, Wingfield et al. 2004, Guangzhou, 510070, China. Aime 2006) but did not conclusively resolve the relationship 3 Westerdijk Fungal Biodiversity Institute, P.O. Box 85176, 3508 AD Utrecht, of Gymnosporangium within other recognized families in the The Netherlands. 4 Department of Biochemistry, Genetics and Microbiology, Forestry and order Pucciniales. Species recognition relies on the morpho- Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria logy of known spore stages, i.e., the telia or aecia occurring 0028, South Africa. on different host species (Kern 1908, 1973, Sydow & Sydow 5 Ningbo Academy of Inspection and Quarantine, Ningbo, 315012, China. 1915, Hiratsuka et al. 1992, Cummins & Hiratsuka 2003). Host © 2020 Naturalis Biodiversity Center & Westerdijk Fungal Biodiversity Institute You are free to share - to copy, distribute and transmit the work, under the following conditions: Attribution: You must attribute the work in the manner specified by the author or licensor (but not in any way that suggests that they endorse you or your use of the work). Non-commercial: You may not use this work for commercial purposes. No derivative works: You may not alter, transform, or build upon this work. For any reuse or distribution, you must make clear to others the license terms of this work, which can be found at http://creativecommons.org/licenses/by-nc-nd/3.0/legalcode. Any of the above conditions can be waived if you get permission from the copyright holder. Nothing in this license impairs or restricts the author’s moral rights. P. Zhao et al.: Gymnosporangium on Malus 69 specificity is generally also employed for species recognition To clarify the phylogenetic placement of the genus Gymnospor­ (Sydow & Sydow 1915, Kern 1964, Parmelee 1971). However, angium, sequences of rDNA SSU-ITS-LSU from 703 repre- due to their diverse life cycles, overlapping host ranges, and sentative taxa belonging to 77 genera within the order Puc­ lacking uredinial stages in most species, considerable disagree- ciniales, which cover 14 morphologically defined families, ments on species delimitation still exist (Kern 1970, Peterson were included for phylogenetic analyses. These representative 1982, Novick 2008). In addition, several morphological charac- taxa were selected based on previous phylogenetic studies as teristics in aecial or telial stages have been employed as im- listed in Table S1. Due to alignment difficulties, ITS1 regions portant criteria in distinguishing species, but their phylogenetic in all taxa were excluded from further analyses. Eight species significance has not been evaluated. Thus, previous reports of Helicobasidium, Insolibasidium, Jola, Septobasidium and of 17 Gymnosporangium species on Malus species remain Tuberculina of three orders, Helicobasidiales, Platygloeales dubious due to the lack of a consistent species concept. Our and Septobasidiales from the subphylum Pucciniomycotina previous studies have shown that the recognition of all spore were selected as outgroups. At species level in Gymnospo­ stages is essential for species recognition (Zhao et al. 2016). rangium, rDNA SSU, ITS and LSU were successfully amplified Nevertheless, the connection between aecial and telial stages from 184 fungarium specimens, and sequence data of rDNA and the characterisation of holomorphic morphology remain SSU, ITS and LSU from 212 specimens of Gymnosporangium unknown for most species. were retrieved from GenBank. All these specimens used for phylogenetic studies were listed in Table S2, together with In this study, comprehensive morphological and molecular their GenBank accession numbers and other information. studies were conducted among rusts occurring on Malus and Endoraecium tropicum was selected as outgroup based on their potential alternate hosts. The objectives of the current phylogeny of the order Pucciniales. In the final alignment, raw study were: sequence data were aligned by Bioedit v. 7.0.9 (Thompson et 1. to determine the phylogenetic placement of Gymnospor­ al. 1997), and multiple alignments were performed with MAFFT angium in the order Pucciniales (Basidiomycota); v. 7.394 (Katoh et al. 2017). SSU, ITS and LSU were combined 2. to clarify the species boundaries of Gymnosporangium to yield the best results for the phylogeny. Topologies were species
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