Miha Humar, University of Ljubljana, Slovenia 米哈·胡马尔，卢布尔雅那大学，斯洛文尼亚
REVIEWED BY 审稿人
Ram Pal, Ram Pal，
National Research Centre For Orchids (ICAR), India 印度兰花国家研究中心（ICAR）
Nakkeeran S., Nakkeeran S.，
Tamil Nadu Agricultural University, India 印度泰米尔纳德农业大学
RECEIVED 06 March 2023 收到 2023 年 3 月 6 日
ACCEPTED 06 October 2023 接受日期 2023 年 10 月 6 日
published 05 January 2024 发表日期 2024 年 1 月 5 日
CITATION 引用
Bag TK, Dutta P, Hubballi M, Kaur R, Mahanta M, Chakraborty A, Das G, Kataky M and Waghunde R (2024) Destructive Phytophthora on orchids: current knowledge and future perspectives. Bag TK，Dutta P，Hubballi M，Kaur R，Mahanta M，Chakraborty A，Das G，Kataky M 和 Waghunde R（2024）兰科植物的毁灭性疫霉：现有知识与未来展望。
Front. Microbiol. 14:1139811. 《前沿微生物学》 14:1139811。
doi: 10.3389/fmicb.2023.1139811
Destructive Phytophthora on orchids: current knowledge and future perspectives 兰科植物的毁灭性疫霉病：现有知识与未来展望
Tusar Kanti Bag ^(1**){ }^{1 *}, Pranab Dutta ^(2**){ }^{2 *}, Manjunath Hubballi ^(3){ }^{3}, Ravpreet Kaur ^(1){ }^{1}, Madhusmita Mahanta ^(2){ }^{2}, Ardhendu Chakraborty ^(4){ }^{4}, Gitasree Das ^(5){ }^{5}, Madhusmita Kataky ^(6){ }^{6} and Rajesh Waghunde ^(7){ }^{7} Tusar Kanti Bag ^(1**){ }^{1 *} ，Pranab Dutta ^(2**){ }^{2 *} ，Manjunath Hubballi ^(3){ }^{3} ，Ravpreet Kaur ^(1){ }^{1} ，Madhusmita Mahanta ^(2){ }^{2} ，Ardhendu Chakraborty ^(4){ }^{4} ，Gitasree Das ^(5){ }^{5} ，Madhusmita Kataky ^(6){ }^{6} 和 Rajesh Waghunde ^(7){ }^{7}^(1){ }^{1} Division of Plant Pathology, Indian Agricultural Research Institute, New Delhi, India, ^(2){ }^{2} CPGSAS, CAU (Imphal) Umiam, Imphal, India, ^(3){ }^{3} Department of Plant Pathology, College of Horticulture Bagalkot, Bagalkot, Karnataka, India, ^(4){ }^{4} Krishi Vigyan Kendra, Khowai, Tripura, India, ^(5){ }^{5} Department of Plant Pathology, Assam Agricultural University, Jorhat, Assam, India, ^(6){ }^{6} Krishi Vigyan Kendra-Kamrup, Azara, Assam Agricultural University, Guwahati, Assam, India, ^(7){ }^{7} College of Agriculture, Navsari Agricultural University, Bharuch, Gujarat, India ^(1){ }^{1} 植物病理学系，印度农业研究学院，新德里，印度， ^(2){ }^{2} CPGSAS，CAU（英帕尔）乌米亚姆，英帕尔，印度， ^(3){ }^{3} 植物病理学系，园艺学院巴格尔科特，巴格尔科特，卡纳塔克邦，印度， ^(4){ }^{4} 农业科技中心，科瓦伊，特里普拉，印度， ^(5){ }^{5} 植物病理学系，阿萨姆农业大学，乔尔哈特，阿萨姆，印度， ^(6){ }^{6} 农业科技中心-卡姆鲁普，阿扎拉，阿萨姆农业大学，古瓦哈蒂，阿萨姆，印度， ^(7){ }^{7} 农业学院，纳瓦萨里农业大学，巴鲁奇，古吉拉特，印度
Abstract 摘要
Anton de Bary first coined the genus, Phytophthora, which means “plant destroyer”, viewing its devastating nature on potatoes. Globally plants have faced enormous threat from Phytophthora since its occurrence. In fact, a century ago, Phytophthora palmivora was first reported on Dendrobium maccarthiae in Sri Lanka. Since then, members of beautiful flowering crops of the family Orchidaceae facing the destructive threat of Phytophthora. Several Phytophthora species have been recorded to infect orchids with economic loss worldwide. To date, orchids are attacked by 12 species of Phytophthora. Five Phytophthora species (P. palmivora, P. nicotianae, P. cactorum, P. multivesiculata, P. meadii) are the major pathogenic Oomycetous Chromista" rather than true fungi frequently occurred on Orchidaceae. Phytophthora palmivora (having ~32 orchid host genera in 15 countries), Phytophthora nicotianae (having ∼15\sim 15 orchid host genera in 16 countries), Phytophthora cactorum (having ∼43\sim 43 orchid host genera in 6 countries), Phytophthora multivesiculata (having 2 orchid host genera in 5 countries) and Phytophthora capsici (having 2 orchid host genera in all Vanilla growing countries) are potential destroyers of Orchidaceae. Most of them are water loving Oomycetes cause disease in moist environments (> 80% RH) at 16-28^(@)C16-28^{\circ} \mathrm{C}. In artificially constructed orchidaria, anthropogenic factors are mostly contributed to the dissemination Phytophthora diseases in addition to many other factors. Water management, clean cultivation, and agro-chemicals are the major options for effective management of orchid Phytophthora, as the eco-friendly management options like development of resistant hybrids/cultivars, biological disease management, transgenic approaches, RNAi technology remained in the infant stage. In this review, we intended to highlight the insight of Phytophthora diseases associated with the orchid disease with reference to the historical aspect of the diseases, symptoms and signs, the pathogens, taxonomy, geographic distribution, host range within the Orchidaceae, pathogen identification, molecular diagnostics, mating types and races, management options and strategies and future perspectives. Anton de Bary 首先提出了属名 Phytophthora，意为“植物毁灭者”，这是基于它对马铃薯的毁灭性影响。自出现以来，全球植物一直面临着 Phytophthora 的巨大威胁。事实上，一个世纪前，Phytophthora palmivora 首次在斯里兰卡的 Dendrobium maccarthiae 上被报道。从那时起，兰科中美丽的观赏作物一直面临着 Phytophthora 的破坏性威胁。目前已记录有几种 Phytophthora 物种在全球范围内感染兰花，造成经济损失。到目前为止，兰花已受到 12 种 Phytophthora 的侵害。其中五种 Phytophthora 物种（P. palmivora、P. nicotianae、P. cactorum、P. multivesiculata、P. meadii）是经常发生在兰科植物上的主要病原性卵菌类生物，而不是真正的真菌。 红火疫霉（在 15 个国家有约 32 个兰科寄主属），烟草疫霉（在 16 个国家有 ∼15\sim 15 个兰科寄主属），苹果腐疫霉（在 6 个国家有 ∼43\sim 43 个兰科寄主属），多囊疫霉（在 5 个国家有 2 个兰科寄主属）和辣椒疫霉（在所有香草种植国家有 2 个兰科寄主属）是兰科植物的潜在破坏者。它们大多数是喜欢水分的卵菌，在湿度高于 80%的潮湿环境中引发病害。在人工建造的兰科植物园中，人为因素除了许多其他因素外，也促进了疫霉病的传播。水管理、清洁栽培和农用化学品是有效管理兰科植物疫霉病的主要措施，而环保的管理方法如抗病杂交种/品种的开发、生物病害管理、转基因方法和 RNAi 技术仍处于初级阶段。 在本篇综述中，我们旨在结合病害的历史方面、症状与病征、病原体、分类、地理分布、兰科植物中的寄主范围、病原体鉴定、分子诊断、交配型和小种、防治措施与策略以及未来展望，来突出与兰科植物病害相关的疫霉病的见解。
Introduction 引言
Orchids are economically highly valued ornamental flowering plants belonging to one of the largest plant families, Orchidaceae. These are traded commercially across the globe in the form of ornamental plants, cut flowers, and potted plants (Hinsley et al., 2018). As per the recent report, the total number of species is approximately 29,199 (Govaerts et al., 2017), and approximately 1, 25, 000 hybrid orchids are registered in the world (Jangyukala and Hemanta, 2021). They exhibit huge diversity with respect to the size, shape, and color of the flower. Furthermore, these are also popular for their durability and exquisite appearance. The value of the global orchid industry is approximately 400 billion US dollars (DITP News, 2015). 兰花是经济价值很高的观赏开花植物，属于最大的植物科之一——兰科（Orchidaceae）。它们以观赏植物、切花和盆栽的形式在全球范围内进行商业交易（Hinsley 等，2018）。根据最新报告，兰花的物种总数约为 29,199 种（Govaerts 等，2017），全球约有 125,000 种杂交兰花被注册（Jangyukala 和 Hemanta，2021）。它们在花的大小、形状和颜色方面表现出极大的多样性。此外，它们也因其耐久性和精美的外观而广受欢迎。全球兰花产业的价值约为 4000 亿美元（DITP 新闻，2015）。
The advancement in commercial orchid production technology has increased the trade of orchid cut-flowers and potted plants several times around the world. However, the commercial production of orchids is challenged by an array of biotic as well as abiotic stresses across the globe. The biotic stresses comprise thrips, scale insects, mites, cockroaches, snails, slugs, nematodes, bacteria, fungi, and viruses, which infect the crop at different stages of production (Jensen, 1959; Farr et al., 1989; Hu et al., 1993; Uchida and Sipes, 1998). The two most important bacterial species infecting orchids are Acidovorax avenae subsp. cattleyae (Syn: Pseudomonas cattleyae), inciting bacterial brown spot disease (Miller, 1990), and Pectobacterium chrysanthemi (Syn: Erwinia chrysanthemi), inciting bacterial soft rot (Chan et al., 2005; Cating et al., 2008). Among the fungal diseases, black rot caused by species of Phytophthora and Pythium, anthracnose caused by species of Colletotrichum, Fusarium rots (Foster, 1955; Srivastava et al., 2018), 商业兰花生产技术的进步使兰花切花和盆栽植物的贸易在全球范围内增加了几倍。然而，全球范围内的兰花商业生产面临着一系列生物和非生物胁迫的挑战。生物胁迫包括蓟马、蚧虫、螨虫、蟑螂、蜗牛、蛞蝓、线虫、细菌、真菌和病毒，它们在生产的不同阶段感染作物（Jensen，1959；Farr 等，1989；Hu 等，1993；Uchida 和 Sipes，1998）。感染兰花的两种最重要的细菌种类是酸菌属亚种卡特兰酸菌（学名：假单胞菌属卡特兰酸菌），引起细菌性褐斑病（Miller，1990），以及欧文氏菌属金盏花欧文氏菌（学名：欧文氏菌属金盏花菌），引起细菌性软腐病（Chan 等，2005；Cating 等，2008）。在真菌病害中，由疫霉属和腐霉属物种引起的黑腐病，由刺盘孢属物种引起的炭疽病，以及镰刀菌腐烂病（Foster，1955；Srivastava 等，2018）
flower spot (Botrytis sp.), and rusts are considered to be important. Major black rot caused by Phytophthora is known to be one of the most deadly diseases in orchids. The very name Phytophthora was described as a plant destructor or plant destroyer by de Bary (1876). There have been 116 species in total in the genus Phytophthora, infecting a range of crops across the globe. Several Phytophthora species have been recorded to inflict economic losses worldwide by the infection of orchids (Uchida, 1994; Erwin and Ribeiro, 1996; Orlikowski and Szkuta, 2006; Cating et al., 2009). Although the nature of the damage and economic losses depend on the growth stages and organs of infected orchid crops, global data on the intensity of the diseases in different countries and the actual losses incurred by different Phytophthora diseases on orchids have remained obscure. Furthermore, consolidated information on various aspects of the destructive Phytophthora diseases on orchids is lacking in the literature. This review aimed to highlight recent developments in Phytophthora diseases associated with orchids regarding symptoms and signs, the pathogens, taxonomy, geographic distribution, host range within the Orchidaceae, and management strategies, along with future perspectives. 花斑病（灰葡萄孢属），以及锈病被认为是很重要的病害。由疫霉属引起的严重黑腐病是兰花中最致命的病害之一。疫霉属这一名称由德巴利（1876）描述为植物破坏者或植物毁灭者。到目前为止，疫霉属共有 116 个种，感染全球多种作物。一些疫霉属物种已被记录在案，由于感染兰花而给全球带来经济损失（Uchida，1994；Erwin 和 Ribeiro，1996；Orlikowski 和 Szkuta，2006；Cating 等，2009）。尽管损害的性质和经济损失取决于感染兰花的生长阶段和器官，但关于不同国家疾病严重程度以及不同疫霉病对兰花造成的实际损失的全球数据仍然不明确。此外，关于兰花上破坏性疫霉病的各种方面的综合信息在文献中仍然缺乏。 这篇综述旨在突出与兰花相关的疫霉病的最新进展，包括症状和病征、病原体、分类、地理分布、兰科植物中的寄主范围以及防治策略，并展望未来的发展方向。
Historical perspective of Phytophthora species infecting Orchidaceae 感染兰科植物的疫霉属物种的历史背景
There are several species of Phytophthora recorded among the various members of the family Orchidaceae. However, a brief historical aspect of important species of Phytophthora infecting orchids is enumerated below: 在兰科植物的各种成员中，已记录有多个疫霉属物种。然而，以下简要列举了感染兰花的重要疫霉属物种的历史背景：
The first record of Phytophthora infection on Dendrobium maccarthiae was reported from Ceylon (presently Sri Lanka) in 1921, in ibid which constitutes the oldest literature. The fungus was identified as Phytophthora palmivora (Petch, 1921) and reported to be responsible for the wilt disease of D. maccarthiae in Ceylon by Gadd (1924). Later, it was reported by Schwarz (1927) that several indigenous and imported orchid varieties from India and the Philippines were attacked by Phytophthora in Java (presently Indonesia). The disease was named black heart and leaf rot of orchids as characterized by the rotting of the heart and leaves with the final discoloration of affected areas and drooping of foliage (Figure 1; Supplementary File 1). Several species in Orchidaceae, viz., Cattleya sp., Dendrobium crumenatum, Grammatophyllum speciosum, Oncidium sp., Phalaenopsis amabilis, Phalaenopsis schilleriana, Vanda coerulea, and Vanda limbata, were invaded by this fungus. The strains of the fungus varied significantly in cultural characteristics and virulence with reference to their hosts. Initially, this rot disease was believed to be caused by the tropical fungus Phytophthora omnivora de Bary, which was considered synonymous with Phytophthora faberi, but later on, the fungus was identified as P. palmivora by Ashby (1929a). Interestingly, a contemporary agronomist, Kopp (1930), described a disease of Vanilla (family: Orchidaceae) in Reunion that resulted in black lesions and rot on the stems, leaves, and pods. These spots contained abundant Phytophthora sporangia similar to those of P. palmivora Butler (=P. faberi Maubl. at that time). It might be the same lineage that caused the pod rot in Cocoa. Subsequently, Kevorkian (1940) documented that Phytophthora spp. caused the wet rot of Cattleya and Vanda rhizomes in the northeastern Caribbean island of Puerto Rico. However, the name “Black rot of orchids” was first coined by Rossetti (1943) while giving an account of a disease of Cattleya and Vanda in Puerto Rico and Stanhopea saccata in an unnamed locality. The name black rot is used to designate a disease caused by Dendrobium maccarthiae 上的 Phytophthora 感染的首次记录是在 1921 年从锡兰（现斯里兰卡）报告的，在同一篇文献中是最早的文献。该真菌被鉴定为 Phytophthora palmivora（Petch，1921），并由 Gadd（1924）报告为导致锡兰 D. maccarthiae 萎蔫病的原因。后来，Schwarz（1927）报告说，来自印度和菲律宾的几种本地和引进的兰花品种在爪哇（现印度尼西亚）受到了 Phytophthora 的侵害。这种疾病被命名为兰花的黑心病和叶腐病，其特征是心部和叶片腐烂，最终导致感染区域变色和叶片下垂（图 1；补充文件 1）。几种兰科植物，如 Cattleya 属、Dendrobium crumenatum、Grammatophyllum speciosum、Oncidium 属、Phalaenopsis amabilis、Phalaenopsis schilleriana、Vanda coerulea 和 Vanda limbata，都受到了这种真菌的侵袭。该真菌的菌株在培养特性及对寄主的致病性方面存在显著差异。 最初，这种腐烂病被认为是由热带真菌 Phytophthora omnivora de Bary 引起的，该真菌被认为与 Phytophthora faberi 是同义词，但后来 Ashby（1929a）将其鉴定为 P. palmivora。有趣的是，同时代的一位农学家 Kopp（1930）描述了留尼汪岛上的香草（兰科）的一种疾病，该疾病导致茎、叶和豆荚出现黑色病斑和腐烂。这些病斑中含有大量类似 P. palmivora Butler（当时称为 P. faberi Maubl.）的 Phytophthora 孢子囊。这可能是导致可可豆腐烂的同一谱系。随后，Kevorkian（1940）记录了在波多黎各东北部的加勒比海岛屿上，Phytophthora spp. 引起的卡特兰和万代兰块茎的湿腐病。然而，“兰花黑腐病”这一名称最早由 Rossetti（1943）提出，他在描述波多黎各的卡特兰和万代兰疾病以及一个未命名地点的 Stanhopea saccata 疾病时使用了这一名称。名称“黑腐病”用于指代由
pythiaceous fungi of more than one species, mainly including the genera Pythium or Phytophthora (Limber, 1946). The symptoms of P. palmivora (Bult.) were adequately described on mature plants of Vanda orchids, and it was reported that P. palmivora was a parasite of orchids in Singapore (Thompson, 1959). The pathogenicity of P. palmivora in the Orchidaceae was first experimentally proven by Richard B. Hine, who was working as a plant pathologist at the University of Hawaii, USA. He demonstrated that plants in the orchid genera Dendrobium, Cattleya, Epidendrum, Paphiopedilum, and Vanda were susceptible to P. palmivora (Bult.) when inoculated with suspensions of zoospores or mycelium on wounded leaves. However, a natural infection of Cattleya and Vanda by P. palmivora in the field was reported in Hawaii (Hine, 1962). Thereafter, several scientific reports confirmed that PP. palmivora (Bult.) is the leading orchid pathogen in various countries around the globe (Thompson, 1958, 1959; Forsberg, 1985; Alfieri et al., 1994; Ann, 1995; Simone and Burnett, 1995; Hong et al., 1998; Yeh et al., 1998; Portales, 2004; Purwantara et al., 2004; Sangchote et al., 2004; Bag, 2006; Orlikowski and Szkuta, 2006; dos Santos, 2012; Rahman et al., 2014; Khairum et al., 2016). 致病疫霉属的多种真菌，主要包括疫霉属或疫病菌属（Limber，1946）。P. palmivora（Bult.）的症状在石斛兰属的成熟植株上得到了充分描述，并有报道指出 P. palmivora 是新加坡兰科植物的寄生菌（Thompson，1959）。P. palmivora 在兰科植物中的致病性最初是由在美国夏威夷大学工作的植物病理学家 Richard B. Hine 通过实验验证的。他证明当用游动孢子或菌丝的悬浮液接种在受伤的叶片上时，石斛兰属、卡特兰属、石斛属、兜兰属和石斛兰属的植物都容易感染 P. palmivora（Bult.）。然而，在夏威夷的田间，有报道指出 Cattleya 和 Vanda 自然感染了 P. palmivora（Hine，1962）。此后，多项科学报告证实了 PP 。 palmivora（Bult。）是全球多个国家的主要兰科植物病原体（Thompson，1958，1959；Forsberg，1985；Alfieri 等，1994；Ann，1995；Simone 和 Burnett，1995；Hong 等，1998；Yeh 等，1998；Portales，2004；Purwantara 等，2004；Sangchote 等，2004；Bag，2006；Orlikowski 和 Szkuta，2006；dos Santos，2012；Rahman 等，2014；Khairum 等，2016）。
Phytophthora nicotianae Breda de Haan 辣椒疫霉菌
The black rot disease on the Laelia orchid was reported to be caused by Phytophthora parasitica Dastur (=P. nicotianae Breda de Haan) in Buenos Aires (Argentina) by Rossetti (1943) who first brought it to the attention of the scientific community. Vine blight and fruit rot of Vanilla (V. fragrans) caused by Phytophthora parasitica were further reported in Puerto Rico (Cibes and Childers, 1949). Subsequently, Phytophthora parasitica was repeatedly confirmed as a phytopathogen of orchids in predominant orchid-growing countries (Chen and Hsieh, 1978; Takahito et al., 1979; Forsberg, 1985; Wey, 1988; Uchida and Aragaki, 1991; Uchida, 1994; Ann, 1995; Zhang et al., 2006; Tao et al., 2011a; Daly et al., 2013). 兰属兰花上的黑腐病最早由 Rossetti（1943）在布宜诺斯艾利斯（阿根廷）报道，该病由寄生疫霉（Phytophthora parasitica Dastur= P. nicotianae Breda de Haan）引起，他首次将这一问题引起科学界的注意。随后，Cibes 和 Childers（1949）在波多黎各报道了由寄生疫霉引起的香草（V. fragrans）的枝枯病和果实腐烂病。此后，寄生疫霉被反复确认为主要兰花种植国家的兰花病原菌（Chen 和 Hsieh，1978；Takahito 等，1979；Forsberg，1985；Wey，1988；Uchida 和 Aragaki，1991；Uchida，1994；Ann，1995；Zhang 等，2006；Tao 等，2011a；Daly 等，2013）。
