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Article

Phytophthora Species from Xinjiang Wild Apple Forests in China

by
Xiaoxue Xu
1,
Wenxia Huai
1,
Hamiti
2,
Xuechao Zhang
3 and
Wenxia Zhao
1,*
1
The Key Laboratory of National Forestry and Grassland Administration on Forest Protection, Research Institute of Forest Ecology Environment and Protection, Chinese Academy of Forestry, Beijing 100091, China
2
Forest Bureau of Emin County, Xinjiang Uygur Autonomous Region, Emin 834600, China
3
Institute of Agricultural Sciences of Ili Kazakh Autonomous Prefecture, Yining 835000, China
*
Author to whom correspondence should be addressed.
Forests 2019, 10(10), 927; https://doi.org/10.3390/f10100927
Submission received: 28 August 2019 / Revised: 2 October 2019 / Accepted: 17 October 2019 / Published: 21 October 2019
(This article belongs to the Special Issue Phytophthora Infestations in Forest Ecosystems)
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Abstract

:
Phytophthora species are well-known destructive forest pathogens, especially in natural ecosystems. The wild apple (Malus sieversii (Ledeb.) Roem.) is the primary ancestor of M. domestica (Borkh.) and important germplasm resource for apple breeding and improvement. During the period from 2016 to 2018, a survey of Phytophthora diversity was performed at four wild apple forest plots (Xin Yuan (XY), Ba Lian (BL), Ku Erdening (KE), and Jin Qikesai (JQ)) on the northern slopes of Tianshan Mountain in Xinjiang, China. Phytophthora species were isolated from baiting leaves from stream, canopy drip, and soil samples and were identified based on morphological observations and the rDNA internal transcribed spacer (ITS) sequence analysis. This is the first comprehensive study from Xinjiang to examine the Phytophthora communities in wild apple forests The 621 resulting Phytophthora isolates were found to reside in 10 different Phytophthora species: eight known species (P. lacustris being the most frequent, followed by P. gonapodyides, P. plurivora, P. gregata, P. chlamydospora, P. inundata, P. virginiana, and P. cactorum) and two previously unrecognized species (P. sp. CYP74 and P. sp. forestsoil-like). The highest species richness of Phytophthora occurred at BL, followed by XY. P. lacustris was the dominant species at BL, XY, and JQ, while P. gonapodyides was the most common at KE. In the present paper, the possible reasons for their distribution, associated implications, and associated diseases are discussed.

1. Introduction

Xinjiang wild apple (Malus sieversii (Ledeb.) Roem.), the wild ancestor of the domesticated apple, is mainly distributed in the Tian Shan mountains in Central Asia, including the Ili River Valley in northwest China’s Xinjiang Uygur Autonomous Region and southeast and east Kyrgyzstan [1,2,3]. It is the dominant species in the relict wild fruit wood forests of inner Eurasia and is protected as a vulnerable species among the endangered rare germplasm resources of China [4,5,6]. However, the wild populations of M. sieversii have experienced a dramatic decrease in recent years, and symptoms of the decline can be observed in many wild apple forests. Affected trees show higher canopy loss, branch dieback, bark and cambium necrosis, and growth reduction. Similar to other countries in Central Asia, several abiotic and biotic factors negatively affect the health status of wild apple forests in China [7], including environmental and climate impacts, insect pests, cambium feeders such as Agrilus mali Matsumura, and infection by pathogenic fungi [8,9,10,11,12,13] (Figure 1).
The presence of Phytophthora species in forests and natural ecosystems is considered to be an important biotic factor responsible for the decline, dieback, and mortality of trees [14]. Belonging to the class Oomycetes, or “water molds”, in the kingdom Chromista, these fungus-like organisms can cause root rot, bark cankers, and diseases leading to the decline and dieback of a wide range of plant species worldwide [15]. Over the past two decades, numerous surveys have shown that many known and previously unknown Phytophthora species are present in a variety of natural and semi-natural forests and river systems in Europe, America, Australia, South Africa, and more recently, Asia [16]. Some of these Phytophthora species, including P. cactorum, P. cinnamomi, and P. plurivora, have shown strong involvement in the decline and dieback of forests, while the exact role in forest ecosystems of many other species, such as P. cryptogea, P. chlamydospora, and P. gonapodyides, is unclear [16]. In a recent study, P. plurivora was found to cause damage to the fine roots and stems of M. sieversii in the declining wild fruit forests of Xinjiang Province, China [17]. However, the findings described in that report were based on a limited number of samples. Furthermore, the distribution and ecological roles of P. plurivora and other Phytophthora species in wild apple forests are still unknown.
In June to October 2016–2018, a survey of Phytophthora diversity was performed at four plots in wild apple forests on the northern slope of Tianshan Mountain in Xinjiang using baiting assays from rhizosphere soil, streams, and canopy drip. This study presents the results of this survey related to the Phytophthora species associated with the decline or dieback of Malus sieversii.

2. Material and Methods

2.1. Study Area

The study was carried out in wild apple forests on the northern slopes of Tianshan Mountain in Xinjiang, China. We chose Xin Yuan (XY) (83°33′ E, 43.25′ N), Ba Lian (BL) (82°50′ E, 43°15′ N), Ku Erdening (KE) (82°51′ E, 43°13′ N), and Jin Qikesai (JQ) (83°25′ E, 43°18′ N) as the studied trap plots, as these locations are where the wild apple trees mostly live [18] (Figure 2). In these four plots, the decline of wild apple trees in XY is the most serious. A total of 10 stream sites that flow though the declining wild apple trees were set at each of the 4 areas; 10 canopy drip sites under the declining wild apple trees were set at each of the 4 areas. Fifteen soil sites under the declining trees were set at XY and at BL. In total, 40 stream sites, 40 forest sites, and 30 soil sampling sites were set in these 4 plots to investigate the presence of Phytophthora in the wild apple forests.

2.2. Sampling and Phytophthora Isolation

This research used stream, canopy drip, and soil sampling baiting [19,20,21,22] at the 4 plots from 2016 to 2018. All isolates of Phytophthora spp. were recovered from sites by baiting with leaves of wax (Fraxinus chinensis Roxb). The baiting leaves were placed in the surveyed sites for 1 week, retrieved, and brought to the laboratory from June to October each year. Pieces of approximately 2 mm² were cut from the margins of the brown spots and plated in CARP+. Colonies of suspected Phytophthora species growing from plated baits were transferred to CARP (CARP+ without Benlate and hymexazol) to confirm purity and then to CMA for characterization and storage [23].

2.3. Classical Identification of Isolates

Morphospecies were first identified by colony patterns in V8 agar (V8A). Colony growth patterns of 7 day old cultures grown at 20 °C in the dark in V8A and morphological features of sporangia, oogonia, antheridia, chlamydospores, hyphal swellings, and aggregations were studied, described, and photographed. The formation of sporangia was stimulated by flooding small V8A disks (0.5 mm diameter) with sterile water at room temperature, and this was observed by microscope after 12, 24, 48, and 72 hours. The results were compared with those of known isolates and species descriptions present in the literature [24].

2.4. Molecular Identification of Isolates

DNA isolation and amplification was carried out. For all Phytophthora isolates obtained in this study, mycelial DNA was extracted from pure cultures grown in corn meal agar (CMA). DNA extraction and amplification were performed in accordance with Huai et al. [25], using the primer pairs ITS6 (5′-GAA GGT GAA GTC GTA ACA AGG-3′) [26] and ITS4 (5′-TCC TCC GCT TAT TGA TAT GC-3′) [27] to amplify both ITS1 and ITS2 regions, including the 5.8S rDNA. The PCR reaction was conducted in a 25 μL reaction mixture consisting of 12.5 μL of 2× Taq Master Mix, 9.5 μL of double-distilled H2O (both supplied by TIANGEN Biotech, Beijing, China), 0.75 μL of rDNA internal transcribed spacer (ITS) primers or 0.25 μL of Btub or EF1a primer (all primers were sourced from Sangon Biotech, Shanghai, China), and 1.5 μL of DNA template. The PCR thermal cycling program was as follows: initial denaturation at 95 °C for 3 min, followed by 35 cycles consisting of denaturation at 95 °C for 1 min, annealing at 58 °C for 30 s, extension at 72 °C for 1 min, and a final extension at 72 °C for 10 min.
Sequence data were initially assembled using STADEN Package 2.0.0. and compared with other closely related species, including some undescribed taxa obtained from GenBank [28].

2.5. Phylogenetic Analysis

Sequences were aligned using MEGA version 6.0. No further editing was done on the alignment to ensure reproducibility and to prevent the introduction of bias. Sequences were concatenated for phylogenetic analyses. Isolates represented each of the known species; the undescribed taxa obtained in this study were compiled into a single data set, and Maximum Likelihood (ML) analysis was performed using MEGA version 6.0. The bootstrap support values were obtained with 1000 bootstrap replicates for each. To ensure general reproducibility, the analysis was repeated using MrBayes to build a Bayesian tree. DANMAN 8 was also used to align multiple sequences to compare the sequences of the same species.

3. Results

3.1. Phytophthora Species Identification

In total, 621 Phytophthora isolates were recovered from this study: 261 from BL, 199 from XY, 121 from KE, and 40 from JQ. Most isolates were recovered from streams and rivers. A total of 597 isolates were from stream baiting, 15 were from soil sampling, and nine were from canopy drip.
Ten morphospecies were identified on the basis of colony patterns and micromorphological features. The features of the sporangium were recorded and photographed. There were two unknown Phythphthora taxa. One was P. sp. CYP74, which is heterothallic, and no oogonia were observed. Another one was P. sp. forestsoil-like which is self-sterile. Species identification was confirmed by comparing ITS rDNA sequences. ITS sequence data were obtained for all isolates, and their identities were confirmed by conducting a BLAST search in GenBank. The results of morphological observations were consistent with ITS analysis; 578 isolates were of eight known species, which, in order of frequency, were P. lacustris, P. gonapodyides, P. plurivora, P. gregata, P. chlamydospora, P. inundata, P. virginiana, and P. cactorum. In addition, 43 isolates of two unknown species were identified; in order of frequency, these were P. sp. CYP74 and P. sp. forestsoil-like (Table 1).

3.2. Phylogenetic Analysis

The aligned ITS dataset consisted of approximately 913 characters. Phylogenetic analysis of Bayes and ML trees revealed sequences that were grouped within four of the 10 main clades of the genus Phytophthora [29,30] ascribed to 10 different species (Table 2). Several isolates corresponded to known species as follows: P. cactorum—clade 1; P. plurivora—clade 2; P. lacustris, P. gonapodyides, P. chlamydospora, P. gregata and P. inundata—clade 6; P. virginiana—clade 9.
The phylogenetic analysis revealed two undescribed Phytophthora taxa, P. sp. CYP74 and P. sp. forestsoil-like, both from clade 6 (Figure 3). P. sp. CYP74 was found to be similar to P. mississippiae and P. ornamentata. Compared with the isolate P. sp. CYP74, the ITS sequence identity of P. mississippiae and P. omamentata was shown to be 99.66%. P. sp. forestsoil-like was found to be similar to P. sp. forestsoil-like (TW55), which was reported in Taiwan [24], with an ITS sequence identity of 96.38%.

3.3. The Distribution of Phytophthora Species

In this research, four plots with varying Phytophthora diversity were investigated (Figure 4). Ba Lian (BL), with nine species, had the greatest diversity, and Jin Qikesai (JQ) had the least diversity with five species. P. lacustris was the most widespread species and the main species at JQ and BL (70% and 69%). It also accounted for the largest proportion at XY, followed by P. gonapodyides. Overall, these two species were the most common in the wild apple forests. The third most common species, with 35 strains, was P. sp. CYP74; this species was baited at all plots and was predominantly found at XY and BL. P. cactorum and P. virginiana were only found at BL, and P. inundata was only found at XY.

4. Discussion

The results of this study provide the first record of the broad range of Phytophthora spp. associated with the wild apple forest ecosystem in Northwest China. Ten Phytophthora species belonging to clades 1, 2, 6, and 9 were isolated in the wild apple forests, including eight species reported for the first time in Xinjiang and two previously unrecognized species. P. cactorum, P. plurivora, P. lacustris, P. gonapodyides, P. gregata, and P. sp. CYP74 were caught in the forest stands. P. plurivora, P. lacustris, P. gonapodyides, P. chlamydospora, P. gregata, P. inundata, P. sp. CYP74, P. sp. forestsoil-like, and P. virginiana were caught in the natural rivers. The present work indicates the diversity and distribution of Phytophthora in Xinjiang wild apple forests.
From clade 6, P. lacustris and P. gonapodyides were caught in 4 plots from June to October. The number of these two species took up 88.6% of all Phytophthora species in this survey. In particular, P. lacustris represented more than half of the total number of strains. P. lacustris and P. gonapodyides were obtained from canopy drip samples, soil samples, and mostly stream samples. These species often co-exist in river systems in the temperate regions of North America, Europe, and Asia [20,31,32]. P. lacustris, which like P. gonapodyides belongs to clade 6, is widely distributed globally. Initially identified as a saprotroph that infects plant detritus, it has now been shown to cause significant damage to fine roots and weak-to-moderate bark lesions in Alnus glutinosa and Prunus persica in Portugal, Italy, and Turkey, among other places [33,34,35,36,37]. Samples in previous research on this species were from soil, trees, and roots, while in the present study, they were mostly taken from streams, with a few collected by canopy drip and from the soil by baiting. In the present study, P. lacustris was acquired from all four site plots, demonstrating that a large number of P. lacustris live in the wild apple forests of Xinjiang, especially in the riparian habitats of streams. P. gonapodyides was described in 1927 as a global species, appearing in almost every Phytophthora survey and demonstrating weak pathogenicity [32,38,39,40,41,42,43].
P. gregata was obtained from stream samples at BL in July and stream, soil samples at XY in September. It was reported in China in 2013 by stream baiting [20] and was shown to cause significant reduction of shoot and root growth but was not found to kill plants [44].
The present survey is the first report of P. inundata in China but was previously reported as a pathogen of shrubs and trees in Europe and South America [45] and the cause of Viburnum latent infection in Australia and Virginia [46]. All Phytophthora species have the potential to disturb natural ecosystems, particularly those of exotic origin, provided that environmental conditions are conducive to disease development [14,32,47].
P. chlamydospora was caught at BL in August by stream baiting and stream samples at XY in September. It has been recovered in Europe, North America, Argentina, and Taiwan from cankers on trees, roots, and foliage of horticultural nursery stock [16,24,48,49].
In this research, we baited two undescribed species: P. sp. CYP74, which is heterothallic like P. mississippiae, and P. sp. forestsoil-like, which is self-sterile like P. sp. forestsoil-like (TW55), reported in Taiwan in 2017 [24]. Detailed information for these two species will be shown in future studies.
P. plurivora from clade 2 is known to be a serious pathogen of many forest trees, including oak, beech, and Alnus glutinosa seedlings. This species can cause dieback and root loss and is most frequently associated with cankers in Europe, North America, and Asia [31,32,33,50,51,52,53,54,55]. Via the examination of plant tissues and soil samples, it has been reported to cause cankers in wild apple forests in Xinjiang [17], corroborating its discovery in stream water and soil samples in the present study.
From clade 1, we collected P. cactorum at BL by canopy drip in September. First described in 1886, this clade1a species is similar to the notorious pathogenic species P. infestans, which can cause damping-off of seedlings, fruits, leaf stems, and roots, as well as collar and crown rot and stem canker on an extremely wide host range of more than 200 species from 160 generas of plants, including many fruits, ornamental plants, and forest trees. It has been reported to be the cause of aerial cankers on European beech trees and is a major problem in apple orchards, causing the death of apple trees [56]. A previous study of staple crops in Xinjiang showed that P. cactorum was isolated from the fruits, root crowns, and diseased soils of strawberry, safflower, apple, and pear plants [47]. The present study represents the first time that P. cactorum has been found in the forest system in Xinjiang. It may have spread to the forests from nearby farms and is a probable reason for the decline in apple trees [15,57,58,59].
In clade 9, P. virginiana was obtained at BL by stream baiting in July. It was first isolated from irrigation water at several ornamental nurseries in 2013 in Virginia [60]. No pathogenicity of this species has yet been detected.
In this study, all plots were situated in areas of declining wild apple trees. Although the diversity of Phytophthora was different at different plots, it may be related to the population density of wild apple forests and human activities. We will set some survey plots in healthy stands and investigate the pathogenicity of these Phytophthora species in future studies to confirm their effects on this wild apple forest ecological system and better understand the reasons for its decline.

5. Conclusions

1) This first extensive survey demonstrated 10 Phytophthora species in a Xinjing wild apple forest ecosystem. Discussing the potential pathogenicity of these Phytophthora, this is a basic study to find out the reasons why the wild apple trees have declined.
2) P. lacustris and P. gonapodyides are the most widespread species, and BL has the highest number of Phytophthora species. Two undescribed species were also detected in this research. These results form a foundation for the study of the genetic diversity of Phytophthora.

Author Contributions

Conceptualization, W.Z. and W.H.; methodology, X.X.; formal analysis, X.X.; investigation, X.Z.; resources, H.; writing—original draft preparation, X.X.; writing—review and editing, W.H.; supervision, W.Z.; project administration, W.Z.; funding acquisition, W.Z. and W.H.

Funding

This research was funded by National Key R&D Program of China, grant number 2016YFC0501503 and National Natural Science Foundation of China, No. 31470649. The APC was funded by National Key R&D Program of China, 2016YFC0501503.

Acknowledgments

The authors are grateful to the Zhongsheng Li and Jinlong Zhang for material support, Jiaqing Jiang for strains saved during this work. In particular, thank Krishan Andradige for his kind encouragements and supports.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Declining symptoms of wild apple forests in Xinjiang.
Figure 1. Declining symptoms of wild apple forests in Xinjiang.
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Figure 2. The four plots located in Xinyuang, Gongliu county, China.
Figure 2. The four plots located in Xinyuang, Gongliu county, China.
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Figure 3. A phylogram based on ITS sequence data indicating the placement of clade 6 and the undescribed Phytophthora taxa recovered in this study. The topological structures of Bayes and Maximum likelihood (ML) trees are the same. Bootstrap support is given above the line. Numbers above the branches represent the bootstrap support based on the maximum likelihood analysis.
Figure 3. A phylogram based on ITS sequence data indicating the placement of clade 6 and the undescribed Phytophthora taxa recovered in this study. The topological structures of Bayes and Maximum likelihood (ML) trees are the same. Bootstrap support is given above the line. Numbers above the branches represent the bootstrap support based on the maximum likelihood analysis.
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Figure 4. The Phytophthora species distribution at four plots.
Figure 4. The Phytophthora species distribution at four plots.
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Table
Table 1. The information of 621 Phytophthora strains relating to clades, species, methods, numbers, and plots including Xin Yuan (XY), Ba Lian (BL), Ku Erdening (KE), and Jin Qikesai (JQ).
Table 1. The information of 621 Phytophthora strains relating to clades, species, methods, numbers, and plots including Xin Yuan (XY), Ba Lian (BL), Ku Erdening (KE), and Jin Qikesai (JQ).
CladeSpeciesPlotMethodNumber
clade1aP. cactorumBLcanopy drip1
clade2cP. plurivoraBLsoil1
XYsoil2
XYstream3
KEstream5
clade6bP. lacustrisBLstream175
BLcanopy drip2
BL soil4
XYstream84
XYcanopy drip1
XY soil1
KEstream48
JQstream28
P. gonapodyidesBLstream56
XYstream74
XY canopy drip5
XYsoil3
KEstream63
JQstream7
P. chlamydosporaBLstream3
XYstream3
P. gregataBLstream2
XYstream4
XYsoil1
P. inundataXYstream1
P. sp. CYP74BLstream13
XYstream15
XYcanopy drip2
KEstream3
JQstream2
P. sp. forestsoil-likeBLstream3
KEstream2
JQstream3
clade9aP. virginianaBLstream1
Table
Table 2. GenBank number and rDNA internal transcribed spacer (ITS) clade of 10 Phytophthora species in Xinjiang wild apple forests.
Table 2. GenBank number and rDNA internal transcribed spacer (ITS) clade of 10 Phytophthora species in Xinjiang wild apple forests.
SpeciesIsolate No.ITS CladeGenbank Number
Phytophthora cactorum8BLL31MN175469
Phytophthora plurivora1KEX3(6)2MN175458
Phytophthora lacustris4GLX9(3) 6MN175455
8KEX3(2)6MN175463
Phytophthora gregata9XYX6(5)6MN175456
7XYT6(2)6MN175459
Phytophthora gonapodyides9XYX7(2)6MN175457
2KEX5(5)6MN175462
Phytophthora sp. CYP74 1KEX9(1)6MN175460
15XYX2(1)6MN175465
Phytophthora chlamydospora9XYX5(4)6MN175461
5BLX9(2)6MN175466
Phytophthora sp. forestsoil-like1BLX1(7)6MN175464
8JQX4(1)6MN175468
Phytophthora inundata15XYX3(1)6MN209784
Phytophthora virginiana1BLX1(3)9MN175467

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Xu, X.; Huai, W.; Hamiti; Zhang, X.; Zhao, W. Phytophthora Species from Xinjiang Wild Apple Forests in China. Forests 2019, 10, 927. https://doi.org/10.3390/f10100927

AMA Style

Xu X, Huai W, Hamiti, Zhang X, Zhao W. Phytophthora Species from Xinjiang Wild Apple Forests in China. Forests. 2019; 10(10):927. https://doi.org/10.3390/f10100927

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Xu, Xiaoxue, Wenxia Huai, Hamiti, Xuechao Zhang, and Wenxia Zhao. 2019. "Phytophthora Species from Xinjiang Wild Apple Forests in China" Forests 10, no. 10: 927. https://doi.org/10.3390/f10100927

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