Korean Journal of Mycology (Kor. J. Mycol.)
Seung Hyo Baek1, Minjun Kyung1, Su Bin Cho2, Ji Yeon Sim2, Hyun-Do Jang2, and Ki Deok Kim1,*
1Department of Plant Biotechnology, Korea University, Seoul 02841, Korea
2Division of Gardens and Education, Korea National Arboretum, Pocheon 11186, Korea
*Correspondence to kidkim@korea.ac.kr
Korean Journal of Mycology (Kor J Mycol) 2026 June, Volume 54, Issue 2, pages 121-138.
https://doi.org/10.4489/kjm.2026.54.2.3
Received on April 16, 2026, Revised on May 04, 2026, Accepted on May 06, 2026, Published on June 30, 2026.
Copyright © The Korean Society of Mycology.
This is an Open Access article which is freely available under the Creative Commons Attribution-Non-Commercial 4.0 International License (CC BY-NC) (https://creativecommons.org/licenses/by-nc/4.0/).
Aeciospore, Gymnosporangium asiaticum, Gymnosporangium yamadae, Host diversity, Korea National Arboretum
Rusts (Pucciniales) are obligate parasites that can survive only in living organisms [1,2]; more than 8,000 species are known [1,3,4]. They are among the most severe threats to a wide range of hosts, including agricultural crops and woody plants [4]. In addition, climate change may influence the emergence and spread of new, unexpected rusts. For example, Lee et al.\[5] reported that climate changes might promote a rust spread caused by Neophysopella kraunhiae in Wisteria floribunda (primary host) and Corydalis incisa (alternative host).
Most Gymnosporangium species as causal agents of rusts are widely distributed in Asia, Europe, and North America [6]. These rust fungi generally produce four different spores (i.e., demicyclic rust), such as aeciospores, basidiospores, spermatia, and teliospores, and require two unrelated host species (i.e., heteroecious rust) to complete their life cycles [7-9]. Therefore, rusts produce spermatia and aeciospores in their aecial hosts and teliospores and basidiospores in their telial hosts. However, a few Gymnosporangium species, such as G. gaeumannii, G. nootkatense, G. paraphysatum, and G. tianschanicum, are macrocyclic rusts that can produce urediospores, including four different spores [10]. In general, aecial stages of Gymnosporangium species are characterized by distinct symptoms on infected leaves, which serve as primary indicators of rust infections [11]. However, morphological characteristics (i.e., leaf symptoms) of rust aecial stages are somewhat different between diverse host species; consequently, molecular phylogenetic analyses were needed for their precise identification [12,13].
The Korea National Arboretum (KNA) in Pocheon, Korea, originated from ‘Gwangneung Forest’, which was initially designated as the Royal Tomb Forest of King Sejo in 1468 [14]. Since then, the forest has been strictly preserved for more than 550 years. The KNA was established during 1984-1987, with various gardens; it was officially reopened as the National Arboretum on 24 May 1999. The KNA comprises 25 thematic gardens and 4,854 plant species across 102 ha [14]. The KNA has diverse plant species, including members of the family Rosaceae, which have not only economic but also aesthetic value; however, disease surveys to develop plant disease management systems have not been conducted except for a recent virus study of our co-workers [15]. Therefore, the objectives of this study were (i) to investigate rust occurrence and identification in diverse host plant species of subtribe Malinae (Rosaceae) at the KNA, and (ii) to examine host diversity (or specificity) of rusts in this study as well as in the literature and databases.
During plant disease surveys at the KNA (37°45’18.0″N, 127°09’54.0″E) in Pocheon, Korea, from June to August 2025, yellow, brownish, and/or orange to reddish symptoms were observed on upper (adaxial) and/or lower (abaxial) leaf surfaces of different host plant species. In particular, aecial structures were observed on the lower leaf surfaces of the samples from various host species (Fig. 1 and 2). Three rust samples per host species were collected from leaves of nine host species on June 20, July 7, July 21, and August 8, 2025 (Table 1). Aeciospores from aecial structures on the lower leaf surfaces of the samples were obtained by scraping the aecia with sterilized needles, followed by harvesting spores with moistened cotton swabs. The cotton swabs with aeciospores were vigorously vortexed for about 10 seconds in 2-mL microtubes (Axygen, Corning, Glendale, AZ, USA) containing 1 mL sterile distilled water. Aeciospores (pellets) were obtained by centrifuging the tubes for 5 min at 13,000 rpm at 28°C using a Mikro 200/200R centrifuge (Hettich, Tuttlingen, Germany), then discarding the supernatant. The aeciospores of rust samples from the host species were further used for morphological and molecular phylogenetic analyses. The rust-infected leaf specimens were dried and deposited at the KNA Herbarium in Pocheon, Korea (Table 1).
Fig. 1. Aecial stages of rusts caused by Gymnosporangium asiaticum in the six host plant species (A) Aria alnifolia, (B) Chaenomeles speciosa, (C) Crataegus pinnatifida, (D) Pseudocydonia sinensis, (E) Pyrus calleryana, and (F) Pyrus pyrifolia. (a) Host plant, (b) symptoms of infected leaves of the host plant, (c) necrotic lesions on the upper leaf surface, (d) aecia on the lower leaf surface, and (e) an aecium (or aecia) with (f) aeciospores on the lower leaf surface. The numbers in picture-f indicate aeciospore diameters (μm) (n = 40), expressed as width ranges from minimum to maximum (average) × length ranges from minimum to maximum (average).
Fig. 2. Aecial stages of rusts caused by Gymnosporangium yamadae in the three host plant species (A) Malus baccata, (B) Malus floribunda, and (C) Malus toringo. (a) Host plant, (b) symptoms of infected leaves of the host plant, (c) necrotic lesions on the upper leaf surface, (d) aecia on the lower leaf surface, and (e) an aecium (or aecia) with (f) aeciospores on the lower leaf surface. The numbers in picture-f indicate aeciospore diameters (μm) (n = 40), expressed as width ranges from minimum to maximum (average) × length ranges from minimum to maximum (average).
Table 1. Rust specimens collected from various host plant species at the Korea National Arboretum (KNA) in Pocheon, Korea
| Host species | Specimen no. (KNAa) | Specimen no. (GenBankb) | Collection date | GenBank accession no.c | ||
|---|---|---|---|---|---|---|
| Scientific name | English name | ITS | LSU | |||
| Aria alnifolia | Korean mountain ash | KA25 -1474 KA25 -1475 KA25 -1476 | Aa2507-1 Aa2507-2 Aa2508 | 7 July 2025 21 July 2025 8 August 2025 | PX3 52013 PX4 53359 PX4 53397 | PX3 62945 PX4 53398 PX4 53401 |
| Chaenomeles speciosa | Chinese-quince | KA25 -1477 KA25 -1478 KA25 -1479 | Cs2506 Cs2507-1 Cs2507-2 | 20 June 2025 7 July 2025 21 July 2025 | PX3 52014 PX3 52015 PX4 53645 | PX3 62946 PX3 62947 PX4 53646 |
| Crataegus pinnatifida | Mountain hawthorn | KA25 -1480 KA25 -1481 KA25 -1482 | Cp2507-1 Cp2507-2 Cp2508 | 7 July 2025 21 July 2025 8 August 2025 | PX3 52016 PX3 52017 PX4 53711 | PX3 62948 PX3 62949 PX4 53771 |
| Malus baccata | Siberian crabapple | KA25 -1492 KA25 -1493 KA25 -1494 | Mb2506 Mb2507-1 Mb2507-2 | 20 June 2025 7 July 2025 21 July 2025 | PX3 17706 PX3 62928 PX4 53872 | PX3 62931 PX3 62932 PX4 53882 |
| Malus floribunda | Japanese flowering crabapple | KA25 -1495 KA25 -1496 KA25 -1497 | Mf2507-1 Mf2507-2 Mf2508 | 7 July 2025 21 July 2025 8 August 2025 | PX3 62929 PX4 53885 PX5 69139 | PX3 62933 PX4 68897 PX4 53897 |
| Malus toringo | Three-lobe crabapple | KA25 -1498 KA25 -1499 KA25 -1500 | Mt2507-1 Mt2507-2 Mt2508 | 7 July 2025 21 July 2025 8 August 2025 | PX3 62930 PX4 68772 PX4 68778 | PX3 62934 PX4 68775 PX4 65779 |
| Pseudocydonia sinensis | Chinese flowering-quince | KA25 -1483 KA25 -1484 KA25 -1485 | Ps2506 Ps2507-1 Ps2507-2 | 20 June 2025 7 July 2025 21 July 2025 | PX3 52020 PX3 52021 PX4 53774 | PX3 52950 PX3 62951 PX4 53775 |
| Pyrus calleryana | Korean sun pear | KA25 -1486 KA25 -1487 KA25 -1488 | Pc2506 Pc2507-1 Pc2507-2 | 20 June 2025 7 July 2025 21 July 2025 | PX3 52022 PX3 52023 PX4 53777 | PX3 62952 PX3 62953 PX4 53792 |
| Pyrus pyrifolia | Sand pear | KA25 -1489 KA25 -1490 KA25 -1491 | Pp2507-1 Pp2507-2 Pp2508 | 7 July 2025 21 July 2025 8 August 2025 | PX3 52024 PX3 52025 PX4 53778 | PX3 62954 PX3 62955 PX4 53793 |
aThe specimens were deposited at the KNA Herbarium in Pocheon, Korea.
bThe specimen numbers (no.) were used in depositing their sequences in GenBank.
cGenBank accession numbers (no.) for internal transcribed spacer (ITS) and large subunit (LSU) sequences of rust specimens.
The morphological characteristics of previously prepared aeciospores from host species samples were examined under a differential interference-contrast light microscope (Zeiss AX10, Carl Zeiss, Oberkochen, Germany). Microphotographs were captured with the AxioCam MRc5 (Carl Zeiss), which was operated via AxioVision Rel. 4.8 software (Carl Zeiss). The shapes and sizes (lengths and widths) of aeciospores (n = 40) were determined as described by Kim et al. [16]. Spore sizes (μm) are expressed as width ranges from minimum to maximum (average) × length ranges from minimum to maximum (average).
For molecular phylogenetic analysis of the rust samples, genomic DNA was extracted from aeciospores prepared as described previously, using an i-genomic BYF DNA Extraction Mini Kit (iNtRON Biotechnology, Seongnam, Korea) according to the manufacturer’s instructions. Polymerase chain reaction (PCR) was performed to amplify the internal transcribed spacer (ITS) rDNA region with the primers Rust2inv (5′-GATGAAGAACACAGTGAAA-3′) [17] and ITS4rust (5′-CAGATTACAAATTTGGGCT-3′) [18]. In addition, the large subunit (LSU) region was amplified with the primers LRust1R (5′-TAAGACCTCAAATCAGGT-3′) and LRust3 (5′-GGGTCATTTAAAGCTAT-3′) [18]. The PCR amplification of the ITS and LSU regions and DNA sequencing were conducted by the Cosmogenetech sequencing service (Cosmogenetech, Seoul, Korea). Phylogenetic analyses were conducted according to the procedure described by Sang et al. [19]. Briefly, the gene sequence was edited using BioEdit 7.2 (https://bioedit.software.informer.com/7.2/) and analyzed with BLAST sequence analysis software (https://blast.ncbi.nlm.nih.gov/Blast.cgi) using the National Center for Biotechnology Information server. The ITS and LSU sequence data were then combined and aligned using ClustalW [20]. Phylogenetic trees using the maximum-likelihood (ML) and neighbor-joining (NJ) methods based on the Tamura–Nei model in MEGA 11 [21] were constructed with these concatenated gene sequences. The stability of the phylogenetic trees was assessed using the bootstrap method with 1,000 replicates. The reference sequences from GenBank used in the phylogenetic analysis are listed in Table 2 [10,12,13,22–26].
Table 2. Reference sequences [internal transcribed spacer (ITS) and large subunit (LSU) sequences] of Gymnosporangium species and an outgroup Endoraecium tropicum used for phylogenetic analyses
| Rust fungi | Host species | Specimens | GenBank accession numbers | References | |
|---|---|---|---|---|---|
| ITS | LSU | ||||
| Gymnosporangium amelanchieris | Amelanchier ovalis | 20141009 | KP261040 | KP261041 | [22] |
| Gymnosporangium annulatum | Cotoneaster sp. | BJFC-R01502 | MH178663 | MH184511 | [10] |
| Gymnosporangium asiaticum | Malus pumila | HMAS38650 | MN605764 | MN605686 | [13] |
| Gymnosporangium asiaticum | Juniperus excelsa | HMAS45640 | MN605747 | MN605669 | [13] |
| Gymnosporangium clavariiforme | Malus communis | HMAS24626 | KU288672 | KU342766 | [12] |
| Gymnosporangium confusum | Crataegus altaica | BJFC-R03203 | MH178623 | MH184471 | [10] |
| Gymnosporangium corniculans | Amelanchier canadensis | CUP-3087 | MN605771 | MN605693 | [13] |
| Gymnosporangium cornutum | Juniperus communis | 10 | OL656940 | OL656838 | [23] |
| Gymnosporangium distortum | Cotoneaster sp. | BJFC-R02544 | MH178629 | MH184477 | [10] |
| Gymnosporangium fusisporum | Cotoneaster sp. | BJFC-R02037 | MH178634 | MH184482 | [10] |
| Gymnosporangium gansuense | Sorbus sp. | BJFC-R03829 | MW901249 | MW911439 | [24] |
| Gymnosporangium globosum | Malus sp. | CUP-1553 | MN605776 | MN605698 | [13] |
| Gymnosporangium gracile | Cydonia oblonga | 20140529-1a | KM486543 | KM486545 | [22] |
| Gymnosporangium granulatosporum | Cotoneaster multiflorus | BJFC-R03827 | MW907970 | MW911441 | [24] |
| Gymnosporangium juniperi-virginianae | Malus baccata | HMAS74424 | MN642597 | MN642621 | [13] |
| Gymnosporangium lianhuaense | Crataegus sp. | BJFC-R03115 | MH178643 | MH184491 | [10] |
| Gymnosporangium miyabei | Malus sylvestris | HMAS:70746 | KU288645 | KU342747 | [12] |
| Gymnosporangium przewalskii | Sorbus koehneana | BJFC-R02084 | KX528447 | KX528445 | [25] |
| Gymnosporangium sabinae | Pyrus communis | PyC | OL657026 | OL656921 | [23] |
| Gymnosporangium sikangense | Cotoneaster sp. | BJFC-R02455 | MH178650 | MH184498 | [10] |
| Gymnosporangium turkestanicum | Sorbus tianschanica | BJFC-R02051 | MH178654 | MH184502 | [10] |
| Gymnosporangium yamadae | Malus prunifolia | HMAS30992 | MN605817 | MN605739 | [13] |
| Endoraecium tropicum | Acacia tropica | BRIP:56557 | KJ862392 | KJ862337 | [26] |
Plant species infected by aecial stages of either Gymnosporangium asiaticum or Gymnosporangium yamadae were investigated to examine their host species [i.e., host diversity (or specificity)] in the literature [13,27–30]. This investigation was further conducted using databases such as the United States Department of Agriculture (USDA) Fungal Database [6] and the European and Mediterranean Plant Protection Organization (EPPO) Global Database [31]. Additionally, the information obtained from the literature and databases was compared with aecial rusts of nine host species caused by G. asiaticum and G. yamadae examined in this study.
All collected samples of nine host plant species exhibited rust symptoms, with aecial structures on diseased leaves of the plant species (Fig. 1a–e, 2a–e), similar to typical rust symptoms in plants [9]. In the early stages of infection, the symptoms on the upper (adaxial) surfaces of infected leaves appeared as chlorotic, brownish, or orange spots, with aecial structures clearly visible on the lower (abaxial) surfaces. When infections developed, the symptoms appeared as severe chlorotic, brownish, or reddish lesions with well-developed, enlarged, and darkened aecia (Fig. 1a–e, 2a–e).
In contrast, aeciospores of aecial structures of G. asiaticum obtained from six host plant species (Aria alnifolia, Chaenomeles speciosa, Crataegus pinnatifida, Pseudocydonia sinensis, Pyrus calleryana, and Pyrus pyrifolia) were yellow to pale yellow, globose to subglobose, and verrucose with germ pores (Fig. 1f). The size of aeciospores from A. alnifolia was 17.1–23.1 (average 20.0) × 20.5–26.5 (average 23.2) μm, whereas those of aeciospores from C. speciosa and C. pinnatifida were smaller than that of A. alnifolia and were 15.6–19.3 (17.5) × 17.5–24.2 (19.6) μm and 13.6–19.4 (17.0) × 16.4–22.7 (19.7) μm, respectively (Fig. 1A–C-f). The aeciospore size of P. sinensis was 16.1–22.3 (19.3) × 19.3–24.6 (21.4) μm; those of P. calleryana and P. pyrifolia ranged in 15.4–22.6 (19.0) × 18.3–27.0 (21.2) μm and 16.4–23.8 (19.4) × 19.1–24.6 (21.7) µm, respectively (Fig. 1D–F-f).
The aeciospores of G. yamadae obtained from three host species (Malus baccata, Malus floribunda, and Malus toringo) were yellow to golden yellow, globose to subglobose or ovoid, and verrucose with or without germ pores (Fig. 2f). The sizes of aeciospores from M. baccata were 17.7–23.5 (20.2) × 19.5–24.7 (22.2) µm; those of M. floribunda were 17.6–21.3 (19.7) × 18.7–24.5 (21.7) µm (Fig. 2A-f, B-f). The aeciospore size [16.5–23.2 (19.5) × 19.2–25.3 (22.1) µm] of M. toringo was smaller than that of M. baccata but was similar to that of M. floribunda (Fig. 2C-f). These morphological characteristics of the aeciospores of rust samples from six host species and three Malus species were similar to those reported for G. asiaticum, and G. yamadae [10,13,32].
Partial ITS and LSU sequences of the rust (aeciospores) samples collected from nine host species were obtained (Table 1), and phylogenetic analyses using ML and NJ methods were conducted with the concatenated ITS and LSU gene sequences (alignment length = 778 bases).
ML analysis revealed that the aeciospores of each rust samples from A. alnifolia, C. speciosa, C. pinnatifida, P. sinensis, P. calleryana, and P. pyrifolia clustered with the reference sequences of G. asiaticum HMAS38650 (accession no. for ITS = MN605764, LSU = MN605686) or G. asiaticum HMAS45640 (accession no. for ITS = MN605747, LSU = MN605669) (Fig. 3). However, those of each rust samples from M. baccata, M. floribunda, and M. toringo clustered with G. yamadae HMAS30992 (accession no. for ITS = MN605817, LSU = MN605739). Similarly, application of the NJ method to concatenated gene sequences revealed that test aeciospores from the six and three plant species also clustered with G. asiaticum HMAS38650 and HMAS45640, as well as G. yamadae HMAS30992. Therefore, based on these results, rust samples were clearly divided into two Gymnosporangium species: those from six host species, as mentioned previously, were identified as G. asiaticum, and those from three Malus species were identified as G. yamadae (Fig. 3).
Fig. 3. Phylogenetic tree constructed with the maximum-likelihood method, showing the relationships among test rust species, other members of the genus Gymnosporangium, and Endoraecium tropicum (the outgroup) based on the concatenated alignments of the internal transcribed spacer (ITS) and large subunit (LSU) sequences. The numbers at the branching points are bootstrap values (>70%) for 1,000 replicates. Black dots indicate that the corresponding nodes were also recovered with bootstrap values (>70%) in the tree constructed using the neighbor-joining method. Scale bar = number of nucleotide (nt) substitutions per 100 nt of the sequences.
According to the literature and databases, aecial stages of all Gymnosporangium species have been recorded in eight families: Eucommiaceae, Euphorbiaceae, Grossulariaceae, Hydrangeaceae, Juglandaceae, Myricaceae, Rosaceae, and Theaceae. Among these eight families, both G. asiaticum and G. yamadae examined in this study could occur only in the family Rosaceae. Rosaceae consists of three subfamilies: Amygdaloideae, Dryadoideae, and Rosoideae. Subfamily Amygdaloideae can be divided into nine tribes, including Maleae, which contains four subtribes (Gilleniinae, Lindleyinae, Malinae, and Vauqueliniinae). Among these subtribes, Malinae contains approximately 28 genera (Amelanchier, Aria, Aronia, Chaenomeles, Chamaemeles, Cotoneaster, Crataegus, Cydonia, Dichotomanthes, Docynia, Eriobotrya, Hesperomeles, Heteromeles, Macromeles, Malacomeles, Malus, Mespilus, Osteomeles, Peraphyllum, Phippsiomeles, Photinia, Pourthiaea, Pseudocydonia, Pyracantha, Pyrus, Rhaphiolepis, Stranvaesia, and Weniomeles). Among these 28 genera, aecial host species of the rust fungi comprise nine different genera (Aria, Chaenomeles, Crataegus, Cydonia, Malus, Photinia, Pourthiaea, Pseudocydonia, and Pyrus) in the subtribe Malinae (Rosaceae). As a result, the literature and databases revealed that 37 plant species served as hosts for either G. asiaticum or G. yamadae (Table 3).
In general, G. asiaticum causes rusts in 17 species of eight different genera (Aria, Chaenomeles, Crataegus, Cydonia, Photinia, Pourthiaea, Pseudocydonia, and Pyrus), and six species of the genus Malus in the subtribe Malinae (Rosaceae). However, G. yamadae induced rusts in 20 species (except M. ioensis) of the genus Malus only, but not in other genera of the subtribe (Table 3).
Table 3. Host plant species of Gymnosporangium asiaticum and Gymnosporangium yamadae in the nine genera of the subtribe Malinaea (Rosaceae)
| Host species | Rust fungi | Host species | Rust fungi | ||
|---|---|---|---|---|---|
| G. asiaticum | G. yamadae | G. asiaticum | G. yamadae | ||
| Aria alnifoliab | +b/+c | − | Malus platycarpa | − | + |
| Chaenomeles cathayensis | + | − | Malus prunifolia | − | + |
| Chaenomeles japonica | + | − | Malus pumila | + | + |
| Chaenomeles speciosa | +/+ | − | Malus spectabilis | + | + |
| Crataegus cuneata | + | − | Malus spontanea | − | + |
| Crataegus pinnatifida | +/+ | − | Malus toringo | − | +/+ |
| Crataegus wilsonii | + | − | Malus transitoria | − | + |
| Cydonia oblonga | + | − | Malus yunnanensis | − | + |
| Malus asiatica | + | + | Malus ×scheideckeri | − | + |
| Malus baccata | − | +/+ | Photinia villosa | + | − |
| Malus domestica | + | + | Pourthiaea villosa | + | − |
| Malus floribunda | − | +/+ | Pseudocydonia sinensis | +/+ | − |
| Malus halliana | − | + | Pyrus betulifolia | + | − |
| Malus honanensis | − | + | Pyrus bretschneideri | + | − |
| Malus hupehensis | − | + | Pyrus calleryana | +/+ | − |
| Malus ioensis | + | − | Pyrus pashia | + | − |
| Malus kansuensis | + | + | Pyrus pyrifolia | +/+ | − |
| Malus manshurica | − | + | Pyrus ussuriensis | + | − |
| Malus micromalus | − | + | |||
aSubtribe Malinae contains approximately 28 genera such as Amelanchier, Aronia, Chamaemeles, Cotoneaster, Dichotomanthes, Docynia, Eriobotrya, Hesperomeles, Heteromeles, Macromeles, Malacomeles, Mespilus, Osteomeles, Peraphyllum, Phippsiomeles, Pyracantha, Rhaphiolepis, Stranvaesia, and Weniomeles, including nine genera in this table.
b+/−, rust reported/no rust reported in the literature and databases.
cRed + indicates that the plant species examined in this study also showed rust symptoms caused by G. asiaticum and G. yamadae.
This study presents the first field survey results on rusts caused by G. asiaticum and G. yamadae in diverse host plant species of the family Rosaceae at the KNA in Pocheon, Korea. Morphological and molecular phylogenetic analyses of the collected rust samples from different host plant species revealed that G. asiaticum occurred in six host species of five genera (Aria, Chaenomeles, Crataegus, Pseudocydonia, and Pyrus) in the subtribe Malinae (Rosaceae); G. yamadae occurred in three species of the genus Malus in the subtribe. Furthermore, the literature and databases indicate that G. asiaticum caused rusts in many host species across nine genera (Aria, Chaenomeles, Crataegus, Cydonia, Malus, Photinia, Pourthiaea, Pseudocydonia, and Pyrus) of the subtribe Malinae; G. yamadae was recorded only in the genus Malus.
Nine species of Gymnosporangium, such as G. asiaticum, G. clavariiforme, G. globosum, G. japonicum, G. monticola, G. nidus-avis, G. sabinae, G. unicorne, and G. yamadae, were reported in Korea [32–34]; among them, only two Gymnosporangium spp. such as G. asiaticum and G. yamadae were observed at the KNA. In the present study, G. asiaticum was found in six species across five genera in subtribe Malinae, whereas G. yamadae was found in three species within the genus Malus in the subtribe. Literature and databases [6,13,27–31] also showed similar results that G. asiaticum caused rusts in 23 species across nine genera, including Malus, in Malinae, whereas G. yamadae caused diseases in 20 species of only Malus (except M. ioensis). In this regard, these two Gymnosporangium species may exhibit different host diversity (or specificity): G. asiaticum can cause rusts in various plant species of subtribe Malinae, whereas G. yamadae can induce diseases only in the genus Malus within the subtribe. Previously, Tao et al. [9] conducted comparative transcriptome analysis with G. asiaticum and G. yamadae. Consequently, they found that G. asiaticum had a larger transcriptome than G. yamadae; they further observed that numbers and families of the candidate effectors (i.e., virulence factors) of the two species were markedly different. These results may present clues to the different host diversity (or specificity) of the two Gymnosporangium species. In another plant-microbe interaction, Wang et al. [35] recently found that host specificity (or diversity) of plant-associated bacteria was negatively (or positively) affected by host abundance and bacterial genome size; they concluded that host specialization played a crucial role in ecology and evolution of plant-microbe interactions.
In this study, aecial stages (average 120 days [36]) of the heteroecious and demicyclic rust fungi (G. asiaticum and G. yamadae) were observed in various alternative host species of the subtribe Malinae (Rosaceae) (Fig. 4) [7,9]. Because the field rust surveys at the KNA were conducted from June to August, only aecial stages (spermatia and aeciospores) were observed. However, telial stages (teliospores and basidiospores) of the rusts would be detectable in the primary hosts (Juniperus spp.) from April to May [36]. Basidiospores developed from teliospores could be released at temperatures of 10–15°C, with relative humidity >80% and dispersed over 3–5 km [36]. Therefore, further studies are needed to examine the rust telial stages in the primary hosts at the KNA area. Once the telial stages are identified in the primary hosts, cross-inoculation experiments between Juniperus and Malinae hosts could be conducted as researched by others [37–39]. Such experiments provide evidence confirming the disease cycles of G. asiaticum and G. yamadae within the KNA area and will help develop disease management strategies.
Fig. 4. Disease cycles of Gymnosporangium asiaticum and Gymnosporangium yamadae causing rusts in various host plant species of Malinae (Rosaceae), modified from Tao et al. [9]. The rust fungus G. asiaticum occurs in the six plant species Aria alnifolia, Chaenomeles speciosa, Crataegus pinnatifida, Pseudocydonia sinensis, Pyrus calleryana, and Pyrus pyrifolia; G. yamadae occurs in the three plant species Malus baccata, Malus floribunda, and Malus toringo as aecial stages (indicated by red letters). However, both rust fungi occur in Juniperus spp. as telial stages (indicated by blue letters). Both diseases are demicyclic rusts, which produce four different spores, such as teliospores, basidiospores, spermatia, and aeciospores, in disease cycles.
When managing demicyclic, heteroecious rusts in crop systems, farmers generally focus on economically important host plants, which leads to removal of alternative (or less valuable) host plants [8,40]. In contrast, management of the demicyclic rusts in arboretum systems is somewhat different because the importance of two different host plants cannot depend on the economic importance alone. The disease management may depend on not only economic value but also landscape and ecological significance. In this regard, the two different host plants such as Malinae species for aecial stages of rusts and Juniperus species for telial stages are essential components of the KNA. Thus, disease management in this arboretum system should be different from that in crop systems; consequently, it should manage rusts of both host species by applying the standard foliar disease control measures (i.e., fungicide applications). Rust management in the system using fungicide applications may also effectively limit basidiospore production and infection on both host species in the disease cycles of G. asiaticum and G. yamadae (Fig. 4). In addition, the two rust pathogens investigated in the present study are listed as quarantine pests in the EPPO A1 list of the European Union, whereas G. yamadae is listed in the USA and Canada [6,31]. Accurate identification of the two rust fungi is essential because misidentification can disrupt regular plant quarantine.
Taken together, all rust samples from nine plant species at KNA in Pocheon, Korea, were identified as G. asiaticum or G. yamadae based on morphological identification and molecular analyses of ITS and LSU gene sequences. The two species also exhibited different host diversity (or specificity): G. asiaticum caused rusts in various host plant species across many genera of subtribe Malinae (Rosaceae), whereas G. yamadae induced diseases only in the genus Malus within the subtribe. This is the first comparative study of rust occurrence caused by G. asiaticum and G. yamadae at KNA; it provides basic information on the occurrence of two different rusts and may facilitate the development of appropriate rust management strategies.
The authors declare that they have no potential conflict of interest.
This study was supported by a research grant (KNA 1-2-48-24-2) from the Korea National Arboretum, Pocheon, Korea.
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