Taxonomy, Phylogeny, and Life Cycle of Four Neophysopella Species on Meliosma myriantha and M. oldhamii in Korea
1
Department of Biological Science, Kunsan National University, Gunsan 54150, Republic of Korea
2
Division of Environmental Science and Ecological Engineering, College of Life Sciences and Biotechnology, Korea University, Seoul 02841, Republic of Korea
3
Center for Convergent Agrobioengineering, Kunsan National University, Gunsan 54150, Republic of Korea
*
Author to whom correspondence should be addressed.
Forests 2023, 14(10), 1934; https://doi.org/10.3390/f14101934
Submission received: 23 August 2023
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Revised: 2 September 2023
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Accepted: 13 September 2023
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Published: 22 September 2023
(This article belongs to the Special Issue DNA Barcoding for Species Identification of Forest Organisms)
Abstract
:The present study performed an in-depth investigation of rust diseases affecting Meliosma myriantha and Meliosma oldhamii trees (Sabiaceae) in Korea. The analysis identified four distinct species of the genus Neophysopella (Pucciniales) as the causal agents. Among these, N. hornotina was found to infect only M. oldhamii, whereas three Neophysopella species (N. meliosmae, N. meliosmae-myrianthae, and N. vitis) were parasitic on M. myriantha. To our knowledge, this is the first report of the former two species (N. hornotina and N. meliosmae) in Korea. In addition, we specified their alternate host plants for two heteroecious species (N. meliosmae-myrianthae and N. vitis) in Korea, completing the life cycles of the four rust species, and provided detailed morphological descriptions at each stage of their life cycles. Phylogenetic relationships of these rust species were uncovered using a comprehensive sample size, and we have constructed a phylogenetic tree for Neophysopella using the cytochrome c oxidase subunit III (cox3) gene sequences, demonstrating an effective approach for species delineation within this genus. The findings contribute to identifying and managing rust diseases affecting Meliosma species.
1. Introduction
Rust diseases, caused by numerous members of Pucciniales, are significant threats to a wide range of host plants worldwide [1,2,3]. Their impact on agriculture and forests makes understanding their pathogens a subject of great importance. Among these rust pathogens, the genus Neophysopella has been reported to parasitize several plant species, including Meliosma myriantha Siebold & Zucc. and Meliosma oldhamii Maxim. (Sabiaceae) [4,5,6,7]. Native to East Asia, these trees have ornamental value with white flowers, red fruits, and captivating autumn foliage, remaining largely overlooked for landscaping purposes despite their suitability as mid-canopy trees [8].
In East Asia, three species of rust fungi affect M. myriantha, namely, Neophysopella meliosmae (Kusano) Jing X. Ji & Kakish., N. meliosmae-myrianthae (Henn. & Shirai) Jing X. Ji & Kakish., and N. vitis (P. Syd.) Jing X. Ji & Kakish. [9,10]. However, only a rust species, N. hornotina (Cummins) Jing X. Ji & Kakish., was known to infect M. oldhamii. Neophysopella meliosmae-myrianthae and N. vitis are heteroecious species that develop spermogonial and aecial stages on M. myriantha, but the former species forms uredinial and telial stages on grapevines (Vitis spp.), while the latter species on ivies (Parthenocissus tricuspidata (Siebold & Zucc.) Planch., P. quinquefolia (L.) Planch., P. heterophylla (Blume) Merr., and P. semicordata (Wall) Planch.) [3,7,11]. Neophysopella meliosmae and N. hornotina were autoecious species, completing their life cycles on M. myriantha and M. oldhamii, respectively. The distinctiveness of the four rust species of Neophysopella parasitic to Meliosma and allied plants has been confirmed by phylogenetic studies of ITS and LSU rDNA sequences [11,12].
In Korea, the rust-causing agent on Meliosma myriantha and M. oldhamii had been previously listed as Aecidium meliosmae-myrianthae Henn. & Shirai (now classified as Neophysopella meliosmae-myrianthae) [10,13,14]. However, the studies lacked essential information, such as geographic origin, date, and mycological and pathological features. Moreover, after these records, there have been no official reports of rust diseases on M. myriantha and M. oldhamii. Recent studies have identified N. vitis as a pathogen affecting M. myriantha [15] and Parthenocissus spp. [11]. Despite these findings, a comprehensive exploration of the rust pathogens impacting M. myriantha and M. oldhamii remains absent. In this context, we initiated an extensive investigation into the rust diseases on these plants in Korea.
Our objective was to identify the specific rust pathogens involved and thoroughly describe their morphological characteristics, molecular phylogenetic relationships, and life cycles by specifying their alternate host plants in Korea. Furthermore, this study makes the first instance of constructing a phylogenetic tree for Neophysopella using the cytochrome c oxidase subunit III (cox3) gene, providing a new tool for species delineation in this genus.
2. Materials and Methods
2.1. Sample Collection
Rust-infected leaves of Meliosma myriantha and Meliosma oldhamii were collected across various locations in Korea. We sourced the occurrence data for the two plants in Korea from the Global Biodiversity Information Facility (GBIF.org, GBIF Occurrence Download https://doi.org/10.15468/dl.43h4bn (accessed on 31 August 2023) for M. myriantha; GBIF.org, GBIF Occurrence Download https://doi.org/10.15468/dl.uygkfb (accessed on 31 August 2023) for M. oldhamii). A total of 73 samples were examined and deposited at Korea University (KUS-F) in Seoul and Kunsan National University (KSNUH) in Gunsan, Korea (Table 1). Photographs were taken in the field to detail the unique symptoms of each developmental stage (spermogonia, aecidia, uredinia, and telia) of Neophysopella species on both primary and alternate host plants.
2.2. Histopathological and Morphological Analyses
Histopathological and morphological characteristics of four rust species were examined at each stage of their lifecycle. Macro-histopathological characters of each stage were observed from the rust-infected leaves under a dissecting microscope (Leica, Wetzlar, Germany), for which photographs were taken using a Dhyana 400DC camera (Tucsen, Fuzhou, China) attached to the microscope. For micro-histopathological characters, the scaffold samples of the diseased leaves were frozen in Surgipath FSC 22 Frozen Section Embedding Medium (Leica Biosystems, Richmond, VA, USA) and then sectioned to give 40–70 μm thick sections using a Leica CM1860 (Leica Biosystems). They were mounted on slides and observed using a Zeiss Imager M2 AX10 microscope (Carl Zeiss, Jena, Germany). A morphological characterization was conducted using a Zeiss Imager M2 AX10 microscope (Carl Zeiss) and captured using an attached AxioCam 512 camera (Carl Zeiss). A scanning electron microscope (S-4800+EDS; Hitachi, Tokyo, Japan) was utilized to conduct a detailed morphological analysis of each species.
2.3. Molecular Phylogenetic Analysis
Genomic DNA was extracted from rust pustules on dried herbarium specimens using a MagListo 5M plant Genomic DNA Extraction Kit (Bioneer, Daejeon, Republic of Korea). The internal transcribed spacer (ITS), large subunit (LSU) rDNA regions, and the cytochrome oxidase 3 (cox3) gene were amplified using primer pairs ITS5-u/ITS4rust [16,17], LRust1R/LRust3 [16] and CO3_F1/CO3_R1 [18], respectively. The PCR products were purified using an AccuPrep® PCR/Gel Purification Kit (Bioneer, Daejeon, Republic of Korea) and were sequenced in both directions by a DNA sequencing service (Macrogen, Seoul, Republic of Korea) with the same primers used for the amplification. The obtained sequences were edited and assembled using the DNASTAR software package, version 11 (Lasergen, Madison, WI, USA). The sequences were aligned with the reference sequences of Neophysopella species that were obtained from the NCBI GenBank database using BLASTn. Phylogenetic trees were constructed using the maximum likelihood (ML) and minimum evolution (ME) methods based on the Tamura-Nei model in the MEGA X software [19]. The confidence level of each branch was tested with 1000 bootstrap (BS) replications.
2.4. Field Observation
In order to understand the complete life cycle of four Neophysopella species in Korea, nearby potential alternate host plants to the infected Meliosma plants were identified and monitored for any signs of rust disease at different development stages. As described above, samples from suspected alternate hosts were identified morphologically and phylogenetically to validate the presence of the same rust pathogens with Meliosma tree-infecting rusts. In addition, we referred to the literature from neighboring countries (China, Japan, and Taiwan) that reported on the alternate hosts of the four rust species to determine the primary and alternate hosts in Korea.
3. Results and Discussion
Utilizing ITS and LSU rDNA sequences, our molecular phylogenetic analysis generated a well-resolved phylogenetic tree (Figure 1), revealing four distinct clades within the genus Neophysopella. Three of these clades originated from M. myriantha. The primary clade, identified as N. vitis, contained the majority of Korean samples. This clade also featured rust samples from two other host plants, Parthenocissus tricuspidata and P. quinquefolia. The second clade was grouped with N. meliosmae-myrianthae samples found in M. myriantha in Japan. Additionally, it encompassed rust samples affecting three separate Vitis species (V. amurensis Rupr., V. flexuosa Thunb., and V. vinifera L.), serving as intermediate hosts in Korea. The third clade consisted of seven Korean samples and an N. meliosmae sample of Japan, without including rust samples from other hosts, suggesting that this species is autoecious. Finally, rust samples originating from M. oldhamii in Korea formed a strongly supported clade (99% BS value in both ML and ME) with an N. hornotina sample from M. arnottiana (Wight) Walp. in Japan, further indicating its autoecious nature.
The cox3 mtDNA gene displayed high amplification efficiency for Neophysopella species, compared to the ITS or LSU rDNA regions. Additionally, this gene showed high specificity for rust fungi without contamination from host plants or other organisms. Notably, the cox3 gene sequences, previously unexplored for a phylogenetic study of Neophysopella species, supported their substantial distinctiveness (Figure 2). The strong BS values for their respective groupings in both ML and ME analyses further corroborated the accuracy of their delimitations. Consequently, using cox3 in phylogenetic analysis is an essential advancement in providing a new tool for species identification within this genus.
Comprehensive histological and microscopic investigations were carried out for the rust-infected leaves and stems of Meliosma myriantha and M. oldhamii. All rust species parasitic to the two trees have been confirmed as members of the genus Neophysopella (Pucciniales), given that they exhibited the type 7 of spermogonia [20], Aecidium-type aecia, uredinia surrounded by paraphyses, and telia arranged in vertical rows [10]. Detailed morphological examinations identified four distinct species of Neophysopella, corroborating the phylogenetic differentiation among the four Neophysopella spp. parasitic to Meliosma spp. Among these, N. hornotina (Figure 3 and Figure 4) was found to infect only M. oldhamii, whereas three Neophysopella species, N. meliosmae (Figure 5 and Figure 6), N. meliosmae-myrianthae (Figure 7 and Figure 8), and N. vitis (Figure 9 and Figure 10), were parasitic on M. myriantha.
On Meliosma species, the early symptoms caused by rust pathogens are indistinguishable, making it hard to distinguish them at the initial infections. However, as the disease progresses, distinctions can be made based on where the rust species forms spermogonia and aecia on different tree parts, such as the leaf, petiole, or stem. And in the case of leaves, whether the structures appear on the upper or/and lower surface is also a key character. The spermogonia of N. hornotina, N. meliosmae, and N. vitis were amphigenous, while the ones of N. meliosmae-myrianthae were epiphyllous. Aecia were hypophyllous in N. meliosmae-myrianthae and N. vitis and mostly hypophyllous in N. hornotina, while mostly epiphyllous in N. meliosmae. In addition, the spermogonia and aecia of N. hornotina and N. meliosmae were previously found to occur on leaves and petioles, but the present study discovered that they sometimes develop spermogonia and aecia on the stem, leading to localized swelling and deformation.
The two host plants (M. myriantha and M. oldhamii) are widely distributed in the southwestern areas of Korea. However, our field observations indicated that N. hornotina is confined to a specific region (Wanju-gun) of Jeollabuk-do, whereas the distribution of N. vitis broadly aligns with one of M. myriantha. We found several M. myriantha leaves exhibiting symptoms of two or three rust species, but such samples were excluded from the current study to prevent misidentification arising from the mixed infection. Further research is needed to verify whether these rust species co-infect a single plant.
The four species bear considerable morphological resemblance, yet they exhibit some unique traits, especially for the aecial structures. N. hornotina is notably characterized by its significantly larger aeciospores compared to the other three species, and these spores feature a thicker wall on both sides and at the apex. N. meliosmae, on the other hand, is uniquely identified by the larger size of its urediniospores compared to the rest. Another distinctive feature of N. meliosmae-myrianthae is the development of a thick wall at the spore apex. In addition, our study is the first to provide detailed descriptions of the spermogonia and spermatia for all rust species using scanning electron microscopy. Detailed morphometric data for each species and their spore stages are provided in the section Taxonomy below.
The present study revealed that all four rust species develop spermatia and aeciospores on Meliosma spp., but it also illustrated different spore types forming on each alternate host plant of all four rust species, confirming that they are macrocyclic (Figure 11). Further, N. meliosmae and N. hornotina were autoecious species, completing their life cycle on Meliosma spp., respectively, while N. meliosmae-myrianthae and N. vitis are heteroecious species, as documented in previous studies [4,5,7]. Notably, we discovered a few additional plants serving as alternate hosts for these Neophysopella species near the infected Meliosma trees in Korea. As a result, the present study uncovered that Vitis amurensis, V. flexuosa, and V. vinifera plants are alternate host plants for N. meliosmae-myrianthae in Korea. As mentioned previously in Na et al. [11], N. vitis completes its life cycle by forming uredinial and telial stages on Parthenocissus tricuspidata and P. quinquefolia.
Our study provides a comprehensive view of the rust pathogens affecting M. myriantha and M. oldhamii in Korea. Moreover, the high resolution of a cox3-based phylogenetic tree for Neophysopella offers a novel tool for accurate species delineation. The findings lay the groundwork that could enhance our understanding of the epidemiology and ecosystems of these rust diseases, thereby contributing to the health and conservation of M. myriantha, M. oldhamii, and potentially other host plants affected by these rust pathogens.
4. Taxonomy
This study provides detailed taxonomic and ecological descriptions of four Neophysopella species in Korea: N. hornotina, N. meliosmae, N. meliosmae-myrianthae, and N. vitis.
Neophysopella hornotina (Cummins) Jing X. Ji & Kakish., Mycological Progress 18(6): 863 (2019) [MB#829731] (Figure 3 and Figure 4).
Description: Symptoms of spermogonial and aecial stages appeared as chlorotic spots on upper leaf surfaces (Figure 3A,B). The spermogonia were amphigenous, pale yellow, densely grouped, and conical in shape (type 7), 92–115 μm wide, and 80–124 μm high (Figure 3E and Figure 4A–C). Spermatia were oblong or elliptical in shape and measured 5–6 μm long and 2–3 μm wide (Figure 4D). Aecia were hypophyllous, subcuticular, and rarely petiolicolous, surrounding the spermogonia, typically Aecidium-type with peridia, and measured 200–360 μm in diameter (Figure 3C–G). Aeciospores were hyaline, mostly subglobose to broadly ellipsoid but often angular, and measured 28.7–43.9 × 22.7–35 µm (av. 33.7 × 29.1 µm) (Figure 4F) with a verrucose wall of 0.8–6.1 µm thick at the side but 4.1–15.8 μm thick apically (Figure 4H). The uredinia (Figure 3G–I) and telia (Figure 3J) developed on the lower surface of the leaf, appearing as small, scattered, or densely clustered structures on discolored angular spots restricted within the leaf veins. The uredinia were hypophyllous, pale yellow, densely surrounded by paraphyses, and measured 80–160 μm in diameter. The paraphyses were oblong to cylindrical, light chest-brown, moderately or strongly incurved, and measured 26.8–63.1 μm long and 10.9–20 μm wide with a hyaline wall that was dorsally 3.3–12.4 μm thick (Figure 4I,K). The urediniospores were obovoid, oblong, or ellipsoid, pale yellow, and measured 22.7–29.4 × 16.7–22.5 µm (av. 26.6 × 20.4 µm) (Figure 4J) with an echinulate wall of 0.8–1.4 µm thick (Figure 4L). The telia were pale chestnut-brown, hypophyllous, and subepidermal. The teliospores developed in 2–5 layers, variable in shape but mostly angular, yellow to brown, thin-walled, and measured 7.3–21.7 × 8.9–17.6 μm (av. 12.1 × 11.8 µm) (Figure 4M).
Life cycle: Autoecious, completing a life cycle solely on Meliosma oldhamii (Figure 11).
Distribution in Korea: Jeollabuk-do (Wanju-gun).
Note: The morphological characteristics and molecular phylogenetic data corresponded to the reference details for Neophysopella hornotina [4]. Interestingly, our in-field observations revealed that the development of its spermogonia or aecia stage on Meliosma oldhamii stems led to localized swelling and deformation. The rust agent affecting M. oldhamii was initially described as Aecidium hornotinum Cummins in 1937 [21], and later, the name was recombined as Neophysopella hornotina [10]. In Korea, the rust agent on M. oldhamii was previously considered Aecidium meliosmae-myrianthae [13]. However, due to the lack of a detailed description or preserved samples in an herbarium, it remains uncertain whether A. meliosmae-myrianthae affects M. oldhamii in Korea. To our knowledge, this is the first report of N. hornotina in Korea. In Japan, it has been confirmed that this pathogen affects both M. oldhamii and M. tenuis Maxim. [4], although N. hornotina has not yet been found on M. tenuis in Korea.
Neophysopella meliosmae (Kusano) Jing X. Ji & Kakish., Mycological Progress 18 (6): 863 (2019) [MB#830299] (Figure 3 and Figure 4).
Description: Symptoms of spermogonial and aecial stages appeared on upper leaf surfaces and stems (Figure 5A–G). The spermogonia were amphigenous, and rarely caulogenous, petiolicolous, pale yellow, densely grouped, subcuticular, and conical in shape (type 7), 95–174 μm wide, and 89–145 μm high (Figure 5A–C,E). The spermatia were oblong or elliptical in shape and measured ca. 2–3 μm wide and 5 μm long (Figure 6D). Aecia were epiphyllous, and rarely caulogenous, petiolicolous, surrounding the spermogonia, typically Aecidium-type with peridia, and measured 240–330 μm in diameter (Figure 5A–G and Figure 6E,G). Aeciospores were hyaline, mostly subglobose to broadly ellipsoid but often angular, and measured 21.9–32.9 × 16.7–23.2 µm (average 28.0 × 18.6 µm) with a verrucose wall of 0.8–1.4 μm thick (Figure 6F,H). The uredinia and telia developed on the lower surface of the leaf, appearing as small, scattered, or densely clustered structures on discolored angular spots restricted within the leaf veins (Figure 5H–J). The uredinia were hypophyllous, pale yellow, and measured 40–160 μm in diameter, densely surrounded by paraphyses. The paraphyses were oblong to cylindrical, chest-brown, moderately or strongly incurved, and measured 31.1–51.9 μm long and 9.7–26.5 μm wide with a hyaline wall that was dorsally 5.7–11.7 μm thick (Figure 5I and Figure 6I,K). The urediniospores were obovoid, oblong, or ellipsoid, pale yellow, and measured 25.2–36.8 × 16.7–23.4 µm (average 32.7 × 20.1 µm) with an echinulate wall of 1.7–3.2 µm thick (Figure 6J,L). The telia were pale chestnut-brown, hypophyllous, and subepidermal. The teliospores developed in 2–4 layers, variable in shape but mostly angular, yellow to brown, thin-walled, and measured 12.3–21.2 × 8.2–15.9 μm (av. 16.1 × 11.5 µm) (Figure 5J and Figure 6M,N).
Life cycle: Autoecious, completing the life cycle solely on Meliosma myriantha (Figure 11).
Distribution in Korea: Gyeongsangnam-do (Changwon-si, Geoje-si, Gimhae-si), Jeollanam-do (Gangjin-gun, Suncheon-si).
Note: By their unique morphological characteristics and distinct phylogenetic position, the specimens have been identified as Neophysopella meliosmae [5,22]. This species was also characterized by the appearance of aecial stages on the upper leaf surfaces. In some cases, when the stems of M. myriantha were affected by the spermogonia or aecia stage, the infection expanded locally and caused deformation. Described initially as Phakopsora meliosmae Kusano in 1904 [23], the species was later reclassified as Neophysopella meliosmae [10]. To our knowledge, this is the first report of N. meliosmae in Korea.
Neophysopella meliosmae-myrianthae (Henn. and Shirai) Jing X. Ji & Kakish., Mycological Progress 18 (6): 863 (2019) [MB#829730] (Figure 5 and Figure 6).
Description: The spermogonia were epiphyllous, densely grouped, subcuticular, and conical in shape (type 7), 82–125 μm wide and 67–89 μm high (Figure 7C and Figure 8A–C). The spermatia were oblong or elliptical in shape and measured ca. 2 μm wide and 4 μm long (Figure 8D). Aecia were hypophyllous, typically Aecidium-type with peridia, and measured 140–330 μm in diameter (Figure 7A,B,D,E and Figure 8E,G). The aeciospores were hyaline, mostly angularly subglobose to broadly ellipsoid, and measured 13.2–18.8 × 11.1–15.8 µm (average 15.7 × 13.4 µm), with a wall of 0.7–1.5 μm thick (1.7–6.7 μm thick at apical part), evenly covered by verrucose (Figure 8E,F,H). The uredinia and telia developed on the lower surface of the leaf, appearing as small, scattered, or densely clustered structures on discolored angular spots restricted within the leaf veins (Figure 7F–H). The uredinia were hypophyllous, pale yellow, densely surrounded by paraphyses, and measured 130–330 μm in diameter. The paraphyses were cylindrical, pale yellow to chest-brown, weakly to moderately incurved, and measured 25.9–56.7 μm long and 7.7–16.0 μm wide with a hyaline wall that was dorsally 1.6–4.7 μm thick (Figure 7G and Figure 8I,K). The urediniospores were obovoid, ellipsoid, pale yellow, and measured 14.5–26.2 × 11.1–14.5 µm (average 20.3 × 12.9 µm) with an echinulate wall of 0.9–1.9 µm thick (Figure 8J,L). The telia were pale yellow to chestnut-brown, hypophyllous, and subepidermal. The teliospores developed in 2–5 layers, variable in shape but mostly angular, yellow to brown, thin-walled, and measured 7.2–25.8 × 6.4–15.2 μm (av. 18.4 × 11.3 µm) (Figure 7H and Figure 8M,N).
Life cycle: Heteroecious, forming spermogonial and aecial stages on Meliosma myriantha, but uredinial and telia stages on Vitis amurensis, V. flexuosa, and V. vinifera (Figure 11).
Distribution in Korea: Jeollanam-do (Gangjin-gun), Jeollabuk-do (Jeonju-si, Wanju-gun).
Note: Although the disease symptoms of this rust species were mainly similar to those of N. vitis, a key difference was the formation of its spermogonia only on the leaves. The causal agent was first designated as Aecidium meliosmae-myrianthae [24], and later combined under Neophysopella meliosmae-myrianthae [10]. The present study discovered Vitis amurensis, V. flexuosa, and V. vinifera as the alternate hosts of N. meliosmae-myrianthae, in addition to various Vitis species previously listed in other Asian countries (Bangladesh, China, Indonesia, Jamaica, Japan, Malaysia, Myanmar, Philippines, Taiwan, Thailand, USA). It includes Cissus adnata Roxb., V. betulifolia Diels & Gilg., V. coignetiae Pulliat ex Planch., V. ficifolia Bunge., V. labrusca L., V. quinquangularis Rehd., V. romanetii Roman., and V. rotundifolia Michx. [7]. In Korea, A. meliosmae-myrianthae was previously attributed to the rust agent on M. myriantha [14]. However, the details covering the collection date, geographic location, and mycological and pathological characteristics have not been recorded, and no herbarium specimen exists for reference. This study is the first official report of N. meliosmae-myrianthae in Korea, grounded on its authentic herbarium materials with detailed mycological data.
Neophysopella vitis (P. Syd.) Jing X. Ji & Kakish., Mycological Progress 18 (6): 863 (2019) [MB#829736] (Figure 7 and Figure 8).
Description: Symptoms of spermogonial and aecial stages appeared as chlorotic spots on upper leaf surfaces (Figure 9A,B). The spermogonia were amphigenous, densely grouped, subcuticular, and conical in shape (type 7), 62–113 μm wide and 56–90 μm high (Figure 9C,D and Figure 10A–C). The spermatia were oblong or elliptical in shape and measured ca. 1.5 μm wide and 4 μm long (Figure 10D). Aecia were hypophyllous, typically Aecidium-type with peridia, and measured 270–370 μm in diameter (Figure 9D,E and Figure 10E,G). Aeciospores were hyaline, angularly subglobose to broadly ellipsoid, and measured 12.1–16.8 × 16.5–23.5 µm (average 14.7 × 19.7 µm), with a wall of 0.8–1.5 μm thick, evenly covered by verrucose (Figure 10E,F,H). The uredinia and telia developed on the lower surface of the leaf, appearing as small, scattered, or densely clustered structures, exhibiting discolored angular spots restricted within the leaf veins, both on the upper and lower sides of the leaves (Figure 9F–H). The uredinia were hypophyllous, pale yellow, densely surrounded by paraphyses, and measured 100–240 μm in diameter. The paraphyses were cylindrical, pale yellow, moderately to strongly incurved, and measured 26.6–91.2 μm long and 8.8–15.2 μm wide with a hyaline wall that was dorsally 3.4–8.8 μm thick (Figure 9G and Figure 10I,K). The urediniospores were obovoid, ellipsoid, yellow, and measured 15.5–26.6 × 10.9–16.5 µm (average 20.0 × 14.7 µm) with an echinulate wall of 0.9–2.0 µm thick (Figure 10J,L). The telia were pale chestnut-brown, hypophyllous, and subepidermal. The teliospores developed in 2–5 layers, variable in shape but mostly angular, brown, thin-walled, and measured 6.9–17.9 × 6.8–12.4 μm (av. 11.1 × 8.8 µm) (Figure 9H and Figure 10M).
Life cycle: Heteroecious, forming spermogonial and aecial stages on Meliosma myriantha, but uredinial and telia stages on Parthenocissus tricuspidata and P. quinquefolia (Figure 11).
Distribution in Korea: Busan (Buk-gu), Gyeongsangnam-do (Changwon-si, Geoje-si, Hadong-gun, Hamyang-gun, Namhae-gun, Sacheon-si, Sancheong-gun), Jeju-do (Jeju-si), Jeollanam-do (Gangjin-gun, Hwasun-gun, Jangseong-gun, Suncheon-si, Wando-gun), Jeollabuk-do (Buan-gun, Gochang-gun, Jeongeup-si, Jeonju-si, Jinan-gun, Imsil-gun, Wanju-gun), Gyeonggi-do (Yongin-si).
Note: Most of the collected samples from M. myriantha were identified as N. vitis. It shares similar symptoms with N. meliosmae-myrianthae, with the unique characteristic of N. vitis being the production of its spermogonia on both leaf surfaces. The causal agent was initially described as Phakopsora vitis P. Syd. in 1899 [25] and has since been reclassified under the genus Neophysopella [10]. In addition to its two uredinial and telial hosts confirmed in Korea, Parthenocissus tricuspidata and P. quinquefolia [11], several other species of Parthenocissus, including P. heterophylla, and P. semicordata, have been documented as alternate hosts of N. vitis in Japan, China, Taiwan, and Nepal [7].
5. Conclusions
This study provides comprehensive morphological and phylogenetic information on rust diseases affecting Meliosma myriantha and M. oldhamii trees in Korea, pinpointing four distinct Neophysopella species as the causal agents. Notably, N. hornotina and N. meliosmae are documented in Korea for the first time. In addition, we completed the life cycles of the four rust species in Korea by specifying each alternate host plant for two heteroecious species (N. meliosmae-myrianthae and N. vitis) but also provided detailed morphological descriptions for each spore stage. Groundbreaking phylogenetic tools, including the cox3 gene, enhance the species delineation of Neophysopella. The study fills critical knowledge gaps and paves the way for the future disease management and conservation of Meliosma species.
Author Contributions
Conceptualization, D.H.N., H.-D.S. and Y.-J.C.; investigation, D.H.N., J.S.L., H.-D.S. and Y.-J.C.; visualization, D.H.N.; writing—original draft preparation, D.H.N. and Y.-J.C.; writing—review and editing, D.H.N., J.S.L., H.-D.S. and Y.-J.C.; supervision, Y.-J.C. All authors have read and agreed to the published version of the manuscript.
Funding
This research was supported by the National Academy of Agricultural Science grant (PJ0149560112022) from the Rural Development Administration, Korea.
Data Availability Statement
The data generated during the current study are available from the corresponding author on request.
Conflicts of Interest
The authors declare no conflict of interest.
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Figure 1.
Maximum-likelihood tree of Neophysopella species inferred from a concatenated alignment of ITS and LSU rDNA sequences. The numbers above/below the branches represent support values (ML BS/ME BS) over 70%. The rust specimens sequenced in the present study are shown in bold. The scale bar equals the number of nucleotide substitutions per site.
Figure 1.
Maximum-likelihood tree of Neophysopella species inferred from a concatenated alignment of ITS and LSU rDNA sequences. The numbers above/below the branches represent support values (ML BS/ME BS) over 70%. The rust specimens sequenced in the present study are shown in bold. The scale bar equals the number of nucleotide substitutions per site.
Figure 2.
Maximum-likelihood tree of Neophysopella species inferred from a concatenated alignment of cox3 mtDNA sequences. The numbers above/below the branches represent support values (ML BS/ME BS) over 70%. The scale bar equals the number of nucleotide substitutions per site.
Figure 2.
Maximum-likelihood tree of Neophysopella species inferred from a concatenated alignment of cox3 mtDNA sequences. The numbers above/below the branches represent support values (ML BS/ME BS) over 70%. The scale bar equals the number of nucleotide substitutions per site.
Figure 3.
The rust disease caused by Neophysopella hornotina on Meliosma oldhamii. (A,B) Symptoms appeared on the upper leaf surface. (C) Spermogonia and aecia on the upper leaf surface. (D) Spermogonia and aecia on the stem. (E) Spermogonia on the lower leaf surface. (F) Aecia on the lower leaf surface. (G,H) Uredinia and telia on the lower leaf surface. Red arrows indicate uredinia (I,J) Close-up of uredinia (I) and telia (J) on the lower leaf surface. Red circle indicates telia.
Figure 3.
The rust disease caused by Neophysopella hornotina on Meliosma oldhamii. (A,B) Symptoms appeared on the upper leaf surface. (C) Spermogonia and aecia on the upper leaf surface. (D) Spermogonia and aecia on the stem. (E) Spermogonia on the lower leaf surface. (F) Aecia on the lower leaf surface. (G,H) Uredinia and telia on the lower leaf surface. Red arrows indicate uredinia (I,J) Close-up of uredinia (I) and telia (J) on the lower leaf surface. Red circle indicates telia.
Figure 4.
Neophysopella hornotina on Meliosma oldhamii observed under a DIC microscope (two columns on the left) and a scanning electron microscope (two columns on the right). (A–D) Spermogonium (A–C) and spermatia (D). (E–H) Aecium (E,G) and aeciospores (F,H). (I–L) Uredinium (I,K) and urediniospores (J,L). (M) Telia with teliospores.
Figure 4.
Neophysopella hornotina on Meliosma oldhamii observed under a DIC microscope (two columns on the left) and a scanning electron microscope (two columns on the right). (A–D) Spermogonium (A–C) and spermatia (D). (E–H) Aecium (E,G) and aeciospores (F,H). (I–L) Uredinium (I,K) and urediniospores (J,L). (M) Telia with teliospores.
Figure 5.
The rust disease caused by Neophysopella meliosmae on Meliosma myriantha. (A,B) Symptoms appeared on the upper leaf surface. (C) Spermogonia and aecia on the upper leaf surface. (D–G) Spermogonia and aecia on the stem. (H) Uredinia and telia on the lower leaf surface. Red circles indicate uredinia (I,J) Close-up of uredinia (I) and telia (J) on the lower leaf surface.
Figure 5.
The rust disease caused by Neophysopella meliosmae on Meliosma myriantha. (A,B) Symptoms appeared on the upper leaf surface. (C) Spermogonia and aecia on the upper leaf surface. (D–G) Spermogonia and aecia on the stem. (H) Uredinia and telia on the lower leaf surface. Red circles indicate uredinia (I,J) Close-up of uredinia (I) and telia (J) on the lower leaf surface.
Figure 6.
Neophysopella meliosmae on Meliosma myriantha observed under a DIC microscope (two columns on the left) and a scanning electron microscope (two columns on the right). (A–D) Spermogonium (A–C) and spermatium (D). (E–H) Aecium (E,G) and aeciospores (F,H). (I–L) Uredinium (I,K) and urediniospores (J,L). (M,N) Telia with teliospores.
Figure 6.
Neophysopella meliosmae on Meliosma myriantha observed under a DIC microscope (two columns on the left) and a scanning electron microscope (two columns on the right). (A–D) Spermogonium (A–C) and spermatium (D). (E–H) Aecium (E,G) and aeciospores (F,H). (I–L) Uredinium (I,K) and urediniospores (J,L). (M,N) Telia with teliospores.
Figure 7.
The rust disease caused by Neophysopella meliosmae-myrianthae on Meliosma myriantha (A–E) and Vitis vinifera (F–H). (A,B) Symptoms appeared on the lower leaf surface. (C) Spermogonia on the upper leaf surface. (D,E) Aecia on the lower leaf surface. (F) Uredinia on the lower leaf surface. (G) Close-up of uredinia on the lower leaf surface. (H) Telia on the lower leaf surface.
Figure 7.
The rust disease caused by Neophysopella meliosmae-myrianthae on Meliosma myriantha (A–E) and Vitis vinifera (F–H). (A,B) Symptoms appeared on the lower leaf surface. (C) Spermogonia on the upper leaf surface. (D,E) Aecia on the lower leaf surface. (F) Uredinia on the lower leaf surface. (G) Close-up of uredinia on the lower leaf surface. (H) Telia on the lower leaf surface.
Figure 8.
Neophysopella meliosmae-myrianthae on Meliosma myriantha (A–H) and Vitis vinifera (I–N) observed under a DIC microscope (two columns on the left) and a scanning electron microscope (two columns on the right). (A–D) Spermogonium (A–C) and spermatia (D). (E–H) Aecium (E,G) and aeciospores (F,H). (I–L) Uredinium (I,K) and urediniospores (J,L). (M,N) Telia with teliospores.
Figure 8.
Neophysopella meliosmae-myrianthae on Meliosma myriantha (A–H) and Vitis vinifera (I–N) observed under a DIC microscope (two columns on the left) and a scanning electron microscope (two columns on the right). (A–D) Spermogonium (A–C) and spermatia (D). (E–H) Aecium (E,G) and aeciospores (F,H). (I–L) Uredinium (I,K) and urediniospores (J,L). (M,N) Telia with teliospores.
Figure 9.
The rust disease caused by Neophysopella vitis on Meliosma myriantha (A–E) and Parthenocissus tricuspidata (F–H). (A,B) Symptoms appeared on the upper leaf surface. (C) Spermogonia on the upper leaf surface. (D,E) Spermogonia and aecia on the lower leaf surface. (F) Symptoms appeared on the upper leaf surface. (G) Close-up of uredinia on the lower leaf surface. (H) Telia on the lower leaf surface.
Figure 9.
The rust disease caused by Neophysopella vitis on Meliosma myriantha (A–E) and Parthenocissus tricuspidata (F–H). (A,B) Symptoms appeared on the upper leaf surface. (C) Spermogonia on the upper leaf surface. (D,E) Spermogonia and aecia on the lower leaf surface. (F) Symptoms appeared on the upper leaf surface. (G) Close-up of uredinia on the lower leaf surface. (H) Telia on the lower leaf surface.
Figure 10.
Neophysopella vitis on Meliosma myriantha (A–H) and Parthenocissus tricuspidata (I–M) observed under a DIC microscope (two columns on the left) and a scanning electron microscope (two columns on the right). (A–D) Spermogonium (A–C) and spermatium (D). (E–H) Aecium (E,G) and aeciospores (F,H). (I–L) Uredinium (I,K) and urediniospores (J,L). (M) Telia with teliospores.
Figure 10.
Neophysopella vitis on Meliosma myriantha (A–H) and Parthenocissus tricuspidata (I–M) observed under a DIC microscope (two columns on the left) and a scanning electron microscope (two columns on the right). (A–D) Spermogonium (A–C) and spermatium (D). (E–H) Aecium (E,G) and aeciospores (F,H). (I–L) Uredinium (I,K) and urediniospores (J,L). (M) Telia with teliospores.
Figure 11.
Life cycles of four rust species parasitic on Meliosma oldhamii and M. myriantha in Korea. (A) Autoecious and macrocyclic life cycle of Neophysopella hornotina on M. oldhamii. (B) Macrocyclic life cycles of three rust species parasitic on M. myriantha, including Neophysopella meliosmae (autoecious on M. oldhamii), N. meliosmae-myrianthae (heteroecious between M. myriantha and Vitis spp.), and N. vitis (heteroecious between M. myriantha and Parthenocissus spp.).
Figure 11.
Life cycles of four rust species parasitic on Meliosma oldhamii and M. myriantha in Korea. (A) Autoecious and macrocyclic life cycle of Neophysopella hornotina on M. oldhamii. (B) Macrocyclic life cycles of three rust species parasitic on M. myriantha, including Neophysopella meliosmae (autoecious on M. oldhamii), N. meliosmae-myrianthae (heteroecious between M. myriantha and Vitis spp.), and N. vitis (heteroecious between M. myriantha and Parthenocissus spp.).
Table 1.
Herbarium specimens of Neophysopella species used in this study.
| Herbarium Specimen | Host Plant | Rust Species | Stage | Date | Geographic Origin | GenBank Acc. No. |
|---|---|---|---|---|---|---|
| ITS/LSU/cox3 | ||||||
| KSNUH1868 | Meliosma myriantha | N. meliosmae | S+A | Jun. 2022 | Samgeo-dong, Geoje-si | OR436895/OR436830/OR466550 |
| KSNUH 1870 | Meliosma myriantha | N. meliosmae | S+A | Jun. 2022 | Dongbu-myeon, Geoje-si | OR436896/OR436831/OR466551 |
| KSNUH 1872 | Meliosma myriantha | N. meliosmae | S+A | Jun. 2022 | Dongbu-myeon, Geoje-si | OR436897/OR436833/OR466554 |
| KSNUH 1875 | Meliosma myriantha | N. meliosmae | S+A | Jun. 2022 | Daecheong-dong, Gimhae-si | OR436891/OR436836/OR466552 |
| KSNUH 1877 | Meliosma myriantha | N. meliosmae | S+A | Jun. 2022 | Cheonseon-dong, Seongsan-gu, Changwon-si | OR436892/OR436838/OR466556 |
| KSNUH 1997 | Meliosma myriantha | N. meliosmae | U+T | Oct. 2022 | Seongjeon-myeon, Gangjin-gun | OR436893/OR436864/OR466553 |
| KSNUH 1998 | Meliosma myriantha | N. meliosmae | U+T | Oct. 2022 | Seungju-eup, Suncheon-si | OR436894/OR436865/OR466555 |
| KSNUH 1856 | Meliosma myriantha | N. meliosmae-myrianthae | S+A | Jun. 2022 | Gui-myeon, Wanju-gun | OR431849/OR436879/OR466565 |
| KSNUH 1857 | Meliosma myriantha | N. meliosmae-myrianthae | S+A | Jun. 2022 | Gui-myeon, Wanju-gun | OR431850/OR436880/OR466566 |
| KSNUH 1860 | Meliosma myriantha | N. meliosmae-myrianthae | S+A | Jun. 2022 | Gui-myeon, Wanju-gun | OR431851/OR436884/OR466572 |
| KSNUH 1945 | Meliosma myriantha | N. meliosmae-myrianthae | S+A | Jul. 2022 | Seongjeon-myeon, Gangjin-gun | OR431844/OR436852/OR466567 |
| KSNUH 1850 | Meliosma myriantha | N. vitis | S+A | May 2022 | Halla Arboretum, Jeju-si | OR436784/OR436873/OR466519 |
| KSNUH 1851 | Meliosma myriantha | N. vitis | S+A | May 2022 | Gosan Recreational Forest, Wanju-gun | OR436785/OR436874/OR466542 |
| KSNUH 1852 | Meliosma myriantha | N. vitis | S+A | Jun. 2022 | Yongbok-dong, Wansan-gu, Jeonju-si | OR436787/OR436876/OR466507 |
| KSNUH 1853 | Meliosma myriantha | N. vitis | S+A | Jun. 2022 | Jeonju Arboretum, Jeonju-si | OQ161600/OQ161599/OR466502 |
| KSNUH 1854 | Meliosma myriantha | N. vitis | S+A | Jun. 2022 | Mt. Naejangsan, Jeongeup-si | OR436788/OR436877/OR466529 |
| KSNUH 1855 | Meliosma myriantha | N. vitis | S+A | Jun. 2022 | Gui-myeon, Wanju-gun | OR436789/OR436878/OR466543 |
| KSNUH 1858 | Meliosma myriantha | N. vitis | S+A | Jun. 2022 | Jungin-dong, Wansan-gu, Jeonju-si | OR436790/OR436881/OR466520 |
| KSNUH 1859 | Meliosma myriantha | N. vitis | S+A | Jun. 2022 | Gui-myeon, Wanju-gun | OR436792/OR436883/OR466521 |
| KSNUH 1861 | Meliosma myriantha | N. vitis | S+A | Jun. 2022 | Gui-myeon, Wanju-gun | OR436793/OR436885/OR466545 |
| KSNUH 1862 | Meliosma myriantha | N. vitis | S+A | Jun. 2022 | Macheon-myeon, Hamyang-gun | OR436794/OR436886/OR466513 |
| KSNUH 1863 | Meliosma myriantha | N. vitis | S+A | Jun. 2022 | Cheongam-myeon, Hadong-gun | OR436795/OR436887/OR466523 |
| KSNUH 1864 | Meliosma myriantha | N. vitis | S+A | Jun. 2022 | Sangju-myeon, Namhae-gun | OR436796/OR436888/OR466531 |
| KSNUH 1865 | Meliosma myriantha | N. vitis | S+A | Jun. 2022 | Sanam-myeon, Sacheon-si | OR436797/OR436889/OR466532 |
| KSNUH 1866 | Meliosma myriantha | N. vitis | S+A | Jun. 2022 | Sanam-myeon, Sacheon-si | OR436798/OR436890/OR466541 |
| KSNUH 1867 | Meliosma myriantha | N. vitis | S+A | Jun. 2022 | Hwamyeong-dong, Buk-gu, Busan | OR436799/OR436829/OR466530 |
| KSNUH 1869 | Meliosma myriantha | N. vitis | S+A | Jun. 2022 | Samgeo-dong, Geoje-si | OQ304336/OQ283684/OR466525 |
| KSNUH 1871 | Meliosma myriantha | N. vitis | S+A | Jun. 2022 | Dongbu-myeon, Geoje-si | OR436800/OR436832/OR466503 |
| KSNUH 1873 | Meliosma myriantha | N. vitis | S+A | Jun. 2022 | Dongbu-myeon, Geoje-si | OR436801/OR436834/OR466509 |
| KSNUH 1874 | Meliosma myriantha | N. vitis | S+A | Jun. 2022 | Nambu-myeon, Geoje-si | OR436802/OR436835/OR466510 |
| KSNUH 1876 | Meliosma myriantha | N. vitis | S+A | Jun. 2022 | Cheonseon-dong, Seongsan-gu, Changwon-si | OR436803/OR436837/OR466546 |
| KSNUH 1932 | Meliosma myriantha | N. vitis | S+A | Jun. 2022 | Seosam-myeon, Jangseong-gun | OR436805/OR436847/OR466526 |
| KSNUH 1933 | Meliosma myriantha | N. vitis | S+A | Jun. 2022 | Asan-myeon, Gochang-gun | OR436806/OR436848/OR466549 |
| KSNUH 1936 | Meliosma myriantha | N. vitis | S+A | Jul. 2022 | Seungju-eup, Suncheon-si | OR436807/OR436849/OR466504 |
| KSNUH 1938 | Meliosma myriantha | N. vitis | S+A | Jul. 2022 | Yongdang-dong, Suncheon-si | OQ304333/OQ283683/OR466535 |
| KSNUH 1940 | Meliosma myriantha | N. vitis | S+A | Jul. 2022 | Wando-eup, Wando-gun | OQ304334/OQ283686/OR466524 |
| KSNUH 1942 | Meliosma myriantha | N. vitis | S+A | Jul. 2022 | Hwasun-eup, Hwasun-gun | OR436808/OR436850/OR466506 |
| KSNUH 1943 | Meliosma myriantha | N. vitis | S+A | Jul. 2022 | Seongjeon-myeon, Gangjin-gun | OR436809/OR436851/OR466537 |
| KSNUH 1946 | Meliosma myriantha | N. vitis | S+A | Jul. 2022 | Jinseo-myeon, Buan-gun | OR436810/OR436853/OR466527 |
| KSNUH 1947 | Meliosma myriantha | N. vitis | S+A | Jul. 2022 | Sangseo-myeon, Buan-gun | OR436811/OR436854/OR466511 |
| KSNUH 1948 | Meliosma myriantha | N. vitis | S+A | Jul. 2022 | Gosan Recreational Forest, Wanju-gun | OR436812/OR436855/OR466540 |
| KSNUH 1949 | Meliosma myriantha | N. vitis | S+A | Jul. 2022 | Jeongcheon-myeon, Jinan-gun | OR436813/OR436856/OR466548 |
| KUS-F 32828 | Meliosma myriantha | N. vitis | S | May 2022 | Gosan Recreational Forest, Wanju-gun | OR436783/OR436872/OR466547 |
| KUS-F 32868 | Meliosma myriantha | N. vitis | S+A | May 2022 | Mt. Seongsusan, Imsil-gun | OR436786/OR436875/OR466539 |
| KUS-F 32944 | Meliosma myriantha | N. vitis | S+A | Jun. 2022 | Mt. Seongsusan, Imsil-gun | OR436791/OR436882/OR466508 |
| KUS-F 32985 | Meliosma myriantha | N. vitis | S+A | Jun. 2022 | Gamgyo-ri, Sangseo-myeon, Buan-gun | OR436804/OR436839/OR466544 |
| KSNUH 1878 | Meliosma oldhamii | N. hornotina | S+A | May 2022 | Gosan Recreational Forest, Wanju-gun | OR436826/OR436841/OR466558 |
| KSNUH 1879 | Meliosma oldhamii | N. hornotina | S+A | Jun. 2022 | Gui-myeon, Wanju-gun | OR436821/OR436844/OR466517 |
| KSNUH 1880 | Meliosma oldhamii | N. hornotina | S+A | Jun. 2022 | Gui-myeon, Wanju-gun | OR436822/OR436845/OR466562 |
| KSNUH 1993 | Meliosma oldhamii | N. hornotina | U+T | Oct. 2022 | Mt. Moaksan, Gui-myeon, Wanju-gun | OR436824/OR436863/OR466559 |
| KUS-F 32625 | Meliosma oldhamii | N. hornotina | U+T | Nov. 2021 | Gosan Recreational Forest, Wanju-gun | OR436825/OR436840/OR466557 |
| KUS-F 32912 | Meliosma oldhamii | N. hornotina | S+A | Jun. 2022 | Daea Arboretum, Wanju-gun | OR436827/OR436842/OR466563 |
| KUS-F 32918 | Meliosma oldhamii | N. hornotina | S+A | Jun. 2022 | Sanggwan-myeon, Wanju-gun | OR436828/OR436843/OR466564 |
| KUS-F 32951 | Meliosma oldhamii | N. hornotina | S+A | Jun. 2022 | Soyang-myeon, Wanju-gun | OR436823/OR436846/OR466560 |
| KSNUH 1523 | Parthenocissus quinquefolia | N. vitis | U | Sep. 2021 | Jeonju Arboretum, Jeonju-si | OM423803/OM420272/OR466514 |
| KSNUH 1719 | Parthenocissus quinquefolia | N. vitis | U | Oct. 2021 | Banwol-dong, Deokjin-gu, Jeonju-si | OM423804/OM420263/OR466500 |
| KSNUH 1724 | Parthenocissus quinquefolia | N. vitis | U | Oct. 2021 | Songcheon-dong, Deokjin-gu, Jeonju-si | OM423805/OM420266/OR466518 |
| KSNUH 0955 | Parthenocissus tricuspidata | N. vitis | U | Oct. 2020 | Chahwang-myeon, Sancheong-gun | OR436819/OR436869/OR466534 |
| KSNUH 1600 | Parthenocissus tricuspidata | N. vitis | U | Oct. 2021 | Jeonju Arboretum, Jeonju-si | OM423808/OM420262/OR466505 |
| KSNUH 1621 | Parthenocissus tricuspidata | N. vitis | U | Oct. 2021 | Hwaseo-myeon, Sangju-si | OR436820/OR436870/OR466538 |
| KSNUH 1660 | Parthenocissus tricuspidata | N. vitis | U | Oct. 2021 | Pogok-eup, Cheoin-gu, Yongin-si | OR436782/OR436871/OR466522 |
| KSNUH 1720 | Parthenocissus tricuspidata | N. vitis | U | Oct. 2021 | Banwol-dong, Deokjin-gu, Jeonju-si | OM423809/OM420264/OR466512 |
| KSNUH 1722 | Parthenocissus tricuspidata | N. vitis | U | Oct. 2021 | Ua-dong, Deokjin-gu, Jeonju-si | OM423810/OM420265/OR466501 |
| KSNUH 1963 | Parthenocissus tricuspidata | N. vitis | U | Aug. 2022 | Mt. Moaksan, Wanju-gun | OR436814/OR436859/OR466516 |
| KSNUH 1979 | Parthenocissus tricuspidata | N. vitis | U | Sep. 2022 | Jungin-dong, Wansan-gu, Jeonju-si | OR436815/OR436861/OR466517 |
| KSNUH 2002 | Parthenocissus tricuspidata | N. vitis | U+T | Oct. 2022 | Seongjeon-myeon, Gangjin-gun | OR436816/OR436866/OR466528 |
| KUS-F 30853 | Parthenocissus tricuspidata | N. vitis | U | Oct. 2018 | Mt. Sarabongsan, Jeju-si | OM423807/OM420270/OR466533 |
| KUS-F 31465 | Parthenocissus tricuspidata | N. vitis | U+T | Nov. 2019 | Mt. Sarabongsan, Jeju-si | OR436817/OR436867/OR466515 |
| KUS-F 31487 | Parthenocissus tricuspidata | N. vitis | U+T | Nov. 2019 | Mt. Sarabongsan, Jeju-si | OR436818/OR436868/OR466536 |
| KSNUH 1962 | Vitis amurensis | N. meliosmae-myrianthae | U | Aug. 2022 | Mt. Moaksan, Wanju-gun | OR431846/OR436858/OR466570 |
| KSNUH 1961 | Vitis flexuosa | N. meliosmae-myrianthae | U | Aug. 2022 | Mt. Moaksan, Wanju-gun | OR431845/OR436857/OR466568 |
| KSNUH 1973 | Vitis vinifera | N. meliosmae-myrianthae | U | Aug. 2022 | Jeonju Arboretum, Jeonju-si | OR431847/OR436860/OR466569 |
| KSNUH 1989 | Vitis vinifera | N. meliosmae-myrianthae | U+T | Oct. 2022 | Iseo-myeon, Wanju-gun | OR431848/OR436862/OR466571 |
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Na, D.H.; Lee, J.S.; Shin, H.-D.; Choi, Y.-J. Taxonomy, Phylogeny, and Life Cycle of Four Neophysopella Species on Meliosma myriantha and M. oldhamii in Korea. Forests 2023, 14, 1934. https://doi.org/10.3390/f14101934
AMA Style
Na DH, Lee JS, Shin H-D, Choi Y-J. Taxonomy, Phylogeny, and Life Cycle of Four Neophysopella Species on Meliosma myriantha and M. oldhamii in Korea. Forests. 2023; 14(10):1934. https://doi.org/10.3390/f14101934
Chicago/Turabian StyleNa, Dong Hwan, Jae Sung Lee, Hyeon-Dong Shin, and Young-Joon Choi. 2023. "Taxonomy, Phylogeny, and Life Cycle of Four Neophysopella Species on Meliosma myriantha and M. oldhamii in Korea" Forests 14, no. 10: 1934. https://doi.org/10.3390/f14101934
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