柑橘疮痂病研究进展
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摘要
柑橘疮痂病(Citrus scab)是柑橘上的重要真菌病害,为害新梢、幼叶和果实,影响柑橘生长发育,果实产量和商品价值。在柑橘上,Elsino?属中的3个种可引起疮痂病,即由Elsino?fawcettii引起的普通疮痂病(Citrus Scab,CS);由E. australis引起的甜橙疮痂病(Sweet Orange Scab,SOS)和最近在柠檬上分离的1个新种E. citricola。由于离体条件下这些病菌生长极其缓慢,国内对柑橘疮痂病的研究主要局限在病害的化学防治方面。关于柑橘疮痂病的病原种类、病菌的遗传和致病性变异、致病机制和病害快速检测等方面的研究均相对匮乏。然而最近国外在这些方面却取得较为显著的进展。本文就柑橘疮痂病的病原菌种类、地理分布和快速检测、病菌毒素的合成、防治等方面作了详细介绍,以期满足读者对柑橘疮痂病的全方位了解。
Citrus(Citrus spp.), cultivated in tropical and subtropical regions, is one of the most important fruit in the world. China is the largest country for citrus cultivation and production. By 2016, China's citrus planting area was 2 556 700 hectares, with a production of 3 618 800 tons. Cultivated citrus plants often suffer economic losses from bacterial, fungal and viral diseases. Among all diseases found in citrus, citrus scab disease has been recognized as one of the most important diseases worldwide. Citrus scab disease was first reported in Florida in the 1880 s. Currently, this disease is distributed in the world citrus producing areas except the countries in the Mediterranean region. The first record of citrus scab disease in China can be traced back to the 1920 s, and now citrus scab diseases occur in all citrusproducing areas of China. Citrus of mandarin, lemon, and pomelo are usually more seriously affected.In generally, pathogenic fungi causing citrus scab disease include two species belong to the genus Elsino?: Elsino? fawcettii Bitancourt and Jenkins(anamorph: Sphaceloma fawcettii Jenkins) and Elsino?australis Bitancourt and Jenkins(anamorph: Sphaceloma australis Bitancourt and Jenkins). E. fawcettii causes citrus scab(formerly sour orange scab or common scab) on the fruits, leaves and twigs of many susceptible citrus cultivars, including lemons(C. limon(L.) Burm. F.), grapefruit(C. paradisi Macf.),satsuma(C. unshiu Marc.) and many tangerines(C. reticulate Blanco) and their hybrids. Severely affected leaves, twigs and fruits are often deformed into scab, and the fruit's acceptability and value for the fresh market was reduced due to the external blemishes. E. australis causes sweet orange scab, mainly affecting the fruit and rarely affecting the leaves of sweet orange [C. sinensis(L.) Osbeck] and some mandarin(C. reticulate Blanco) cultivars. Compared to E. fawcettii, erumpent scab pustules caused by E. australis tend to have a flatter cork appearance. E. fawcettii is widely distributed, while the distribution of E. australis is limited to humid citrus-growing areas in Southern America, such as Argentina, Bolivia, Brazil, Ecuador, Paraguay and Uruguay, and has recently been reported in some regions in the United States, such as Florida, Texas, Louisiana, Mississippi, Arizona, and California. Recently, a new pathotype, natsudaidai pathotype of E. australis on Citrus natsudaidai Hayata was reported in Korea. It is nonpathogenic to sweet orange. In addition, a strain from lemon in Brazil has recently been identified as a new species Elsino? citricola Fan, Barreto & Crous, sp. nov. Similar to citrus scab, E. citricola affects the leaves, twigs and fruits with the similar symptoms to those caused by E. fawcettii, but the geographical distribution and host range are unknown. As a fungus of the genus Elsino?, E. fawcettii produces a red or yellow water-insoluble pigments named‘elsinochrome'in the culture medium. Elsinochrome belongs to photosensitizing reagents which absorbs light energy and reacts with oxygen molecules to produce active oxygen species(ROS), such as superoxides(O2-), hydrogen peroxide(H2 O2), hydroxyl radical(OH·) and singlet oxygen(1 O2). ROS could cause damage to the cell membranes and electrolyte leakage from the cells. Elsinochrome is a non-host selective toxin which synthesized via the polyketide pathway and toxic to citrus cells and other plant cells. It has been proven that the type I fungal polyketide synthase encoding gene(EfPKS1) of E. fawcettii is involved in elsinochrome synthesis.Deletion of EfPKS1 completely abolished elsinochrome synthesis, and this function was restored by reintroducing EfPKS1 into △EfPKS1 restored this function. Under laboratory conditions, the synthesis of elsinochrome is regulated by a variety of environmental and physiological factors. Among them, light is not only an indispensable factor for toxicity, but also a factor for elsinochrome production. In addition,alkaline conditions are also beneficial for the production of elsinochrome. The genes required for the biosynthesis of secondary metabolites in filamentous fungi often reside in a cluster. The gene cluster response for elsinochrome synthesis was predicted, based on this prediction, its synthetic pathway of was inferred. In Elsino? spp., elsinochrome synthesis and sporulation are closely linked. EfPKS1 or TSF1 deletion mutant of E. fawcettii not only loses the synthesis of elsinochrome, but also loses its ability to sporulate. Symptom-based diagnosis is the most economical, rapid, and commonly used method for diagnosis of citrus scab. In general, citrus scabs can be diagnosed based on typical symptoms. However,symptoms may change due to host varieties, stage of the infected organs, and field environmental factors. In addition, the symptoms of citrus canker and Botrytis-injury, insect damages, as well as wind damage and other mechanical damage are similar to citrus scab, which makes it difficult to distinguish.Elsino? spp. grows very slowly in vitro, and it is difficult to identify Elsino? spp. based on the morphological characteristics. Host range, pathogenicity and molecular method such as ITS sequence analysis,Amplified Fragment Length Polymorphism(AFLP) and random amplified polymorphic DNA(RAPD)can effectively distinguish these species and pathogenic types, but it takes time and labor, and requires a large amount of experimental space. Fortunately, specific primer pairs for E. fawcettii, E. australis and natsudaidai pathotype of E. australis based on PCR rapid molecular diagonosis were developed by Korea scientists. Although existing diagnostic techniques cannot distinguish the pathotype of E. fawcettii.Citrus scab can severely affect the growth of leaves and twigs, and causes fruitlet-dropping. Moreover,it can cause serious external blemishes on fruit and reduce their economic value. The disease must be controlled before the diseased fruit is destined for the fresh market. Integrated control strategies including planting disease-free seedlings, removing diseased shoots, strengthening the management of orchards and timely spraying protection. Citrus scab is manageable with appropriate fungicides spraying that achieve sustained profitability. Generally, scab control requires two or three fungicide applications.The first spray is usually applied at the beginning of new shoot germination in early spring, followed by a second application just at the time of the petals almost fallen, and a third application approximately 3 weeks thereafter. Effective fungicides registries for citrus scab control include copper fungicides such as Bordeaux mixture, copper hydroxide; benzimidazole fungicides such as thiophanate-methyl; ergosterol synthesis inhibitors, such as diniconazole, difenoconazole and myclobutanil; strobilurins, such as azoxystrobin; and the other fungicides, such as mancozeb, chlorothalonil, etc.. However, long-term use of the same systemic action mechanism of fungicides is likely to lead to the emergence fungicide-resistant biotype of E. fawcettii. For example, benomyl resistant strains were widely distributed in Florida as early as 1985, and it was also reported in Japan and New Zealand. However, the resistance of E. fawcettii in China to any fungicides remains unclear. Both E. fawcettii and E. australis are listed in regulated pests of EU, and E. australis is a regulated pest in the United States. A recent survey for the presence of E. australis in China was failed to confirm it existence. In order to prevent invasion of E. australis companying with the importation of citrus fruit, we recommend including E. australis in the list of pests that are prohibited from entering China, and implement quarantine to prevent disease input and to protect the safety of citrus production and export in China.
Citrus(Citrus spp.), cultivated in tropical and subtropical regions, is one of the most important fruit in the world. China is the largest country for citrus cultivation and production. By 2016, China's citrus planting area was 2 556 700 hectares, with a production of 3 618 800 tons. Cultivated citrus plants often suffer economic losses from bacterial, fungal and viral diseases. Among all diseases found in citrus, citrus scab disease has been recognized as one of the most important diseases worldwide. Citrus scab disease was first reported in Florida in the 1880 s. Currently, this disease is distributed in the world citrus producing areas except the countries in the Mediterranean region. The first record of citrus scab disease in China can be traced back to the 1920 s, and now citrus scab diseases occur in all citrusproducing areas of China. Citrus of mandarin, lemon, and pomelo are usually more seriously affected.In generally, pathogenic fungi causing citrus scab disease include two species belong to the genus Elsino?: Elsino? fawcettii Bitancourt and Jenkins(anamorph: Sphaceloma fawcettii Jenkins) and Elsino?australis Bitancourt and Jenkins(anamorph: Sphaceloma australis Bitancourt and Jenkins). E. fawcettii causes citrus scab(formerly sour orange scab or common scab) on the fruits, leaves and twigs of many susceptible citrus cultivars, including lemons(C. limon(L.) Burm. F.), grapefruit(C. paradisi Macf.),satsuma(C. unshiu Marc.) and many tangerines(C. reticulate Blanco) and their hybrids. Severely affected leaves, twigs and fruits are often deformed into scab, and the fruit's acceptability and value for the fresh market was reduced due to the external blemishes. E. australis causes sweet orange scab, mainly affecting the fruit and rarely affecting the leaves of sweet orange [C. sinensis(L.) Osbeck] and some mandarin(C. reticulate Blanco) cultivars. Compared to E. fawcettii, erumpent scab pustules caused by E. australis tend to have a flatter cork appearance. E. fawcettii is widely distributed, while the distribution of E. australis is limited to humid citrus-growing areas in Southern America, such as Argentina, Bolivia, Brazil, Ecuador, Paraguay and Uruguay, and has recently been reported in some regions in the United States, such as Florida, Texas, Louisiana, Mississippi, Arizona, and California. Recently, a new pathotype, natsudaidai pathotype of E. australis on Citrus natsudaidai Hayata was reported in Korea. It is nonpathogenic to sweet orange. In addition, a strain from lemon in Brazil has recently been identified as a new species Elsino? citricola Fan, Barreto & Crous, sp. nov. Similar to citrus scab, E. citricola affects the leaves, twigs and fruits with the similar symptoms to those caused by E. fawcettii, but the geographical distribution and host range are unknown. As a fungus of the genus Elsino?, E. fawcettii produces a red or yellow water-insoluble pigments named‘elsinochrome'in the culture medium. Elsinochrome belongs to photosensitizing reagents which absorbs light energy and reacts with oxygen molecules to produce active oxygen species(ROS), such as superoxides(O2-), hydrogen peroxide(H2 O2), hydroxyl radical(OH·) and singlet oxygen(1 O2). ROS could cause damage to the cell membranes and electrolyte leakage from the cells. Elsinochrome is a non-host selective toxin which synthesized via the polyketide pathway and toxic to citrus cells and other plant cells. It has been proven that the type I fungal polyketide synthase encoding gene(EfPKS1) of E. fawcettii is involved in elsinochrome synthesis.Deletion of EfPKS1 completely abolished elsinochrome synthesis, and this function was restored by reintroducing EfPKS1 into △EfPKS1 restored this function. Under laboratory conditions, the synthesis of elsinochrome is regulated by a variety of environmental and physiological factors. Among them, light is not only an indispensable factor for toxicity, but also a factor for elsinochrome production. In addition,alkaline conditions are also beneficial for the production of elsinochrome. The genes required for the biosynthesis of secondary metabolites in filamentous fungi often reside in a cluster. The gene cluster response for elsinochrome synthesis was predicted, based on this prediction, its synthetic pathway of was inferred. In Elsino? spp., elsinochrome synthesis and sporulation are closely linked. EfPKS1 or TSF1 deletion mutant of E. fawcettii not only loses the synthesis of elsinochrome, but also loses its ability to sporulate. Symptom-based diagnosis is the most economical, rapid, and commonly used method for diagnosis of citrus scab. In general, citrus scabs can be diagnosed based on typical symptoms. However,symptoms may change due to host varieties, stage of the infected organs, and field environmental factors. In addition, the symptoms of citrus canker and Botrytis-injury, insect damages, as well as wind damage and other mechanical damage are similar to citrus scab, which makes it difficult to distinguish.Elsino? spp. grows very slowly in vitro, and it is difficult to identify Elsino? spp. based on the morphological characteristics. Host range, pathogenicity and molecular method such as ITS sequence analysis,Amplified Fragment Length Polymorphism(AFLP) and random amplified polymorphic DNA(RAPD)can effectively distinguish these species and pathogenic types, but it takes time and labor, and requires a large amount of experimental space. Fortunately, specific primer pairs for E. fawcettii, E. australis and natsudaidai pathotype of E. australis based on PCR rapid molecular diagonosis were developed by Korea scientists. Although existing diagnostic techniques cannot distinguish the pathotype of E. fawcettii.Citrus scab can severely affect the growth of leaves and twigs, and causes fruitlet-dropping. Moreover,it can cause serious external blemishes on fruit and reduce their economic value. The disease must be controlled before the diseased fruit is destined for the fresh market. Integrated control strategies including planting disease-free seedlings, removing diseased shoots, strengthening the management of orchards and timely spraying protection. Citrus scab is manageable with appropriate fungicides spraying that achieve sustained profitability. Generally, scab control requires two or three fungicide applications.The first spray is usually applied at the beginning of new shoot germination in early spring, followed by a second application just at the time of the petals almost fallen, and a third application approximately 3 weeks thereafter. Effective fungicides registries for citrus scab control include copper fungicides such as Bordeaux mixture, copper hydroxide; benzimidazole fungicides such as thiophanate-methyl; ergosterol synthesis inhibitors, such as diniconazole, difenoconazole and myclobutanil; strobilurins, such as azoxystrobin; and the other fungicides, such as mancozeb, chlorothalonil, etc.. However, long-term use of the same systemic action mechanism of fungicides is likely to lead to the emergence fungicide-resistant biotype of E. fawcettii. For example, benomyl resistant strains were widely distributed in Florida as early as 1985, and it was also reported in Japan and New Zealand. However, the resistance of E. fawcettii in China to any fungicides remains unclear. Both E. fawcettii and E. australis are listed in regulated pests of EU, and E. australis is a regulated pest in the United States. A recent survey for the presence of E. australis in China was failed to confirm it existence. In order to prevent invasion of E. australis companying with the importation of citrus fruit, we recommend including E. australis in the list of pests that are prohibited from entering China, and implement quarantine to prevent disease input and to protect the safety of citrus production and export in China.
引文
[1]SCRIBNER F L.Notes on the orange leaf scab[J].Bulletin of the Torrey Botanical Club,1886,13(10):181-183.
[2]HYUN J W,TIMMER L W,LEE S C,YUN S H,KO S W,KIM K S.Pathological characterization and molecular analysis of Elsino?isolates causing scab diseases of citrus in Jeju island in Korea[J].Plant Disease,2007,85(9):1013-1017.
[3]REINKING O A.Diseases of economic plants in Southern China[J].Phillippine Agriculturist,1919,8:109-134.
[4]李红叶.柑橘病害发生与防治彩色图说[M].北京:中国农业出版社,2011LI Hongye.Occurrence and control of citrus diseases[M].Beijing:China Agriculture Press,2011.
[5]HOU X,KEVIN H D,LI H.Pathotypes and genetic diversity of Chinese collections of Elsino?fawcettii causing citrus scab[J].Journal of Integrative Agriculture,2014,13(6):1293-1302.
[6]CHUNG K R.Elsino?fawcettii and Elsino?australis:The fungal pathogens causing citrus scab[J].Molecular Plant Pathology,2011,12(2):123-135.
[7]TIMMER L W,GARNSEY S M,GRAHAM J H.Compendium of citrus diseases[M].American Phytopathological Society,2000.
[8]TIMMER L W,PRIEST M,BROADBENT P,TAN M K.Morphological and pathological characterization of species of Elsinoe?causing scab diseases of citrus[J].Phytopathology,1996,86(10):1032-1038.
[9]FAN X,BARRETO R,GROENEWALD J,BEZERRA J,PEREIRA O,CHEEWANGKOON R,MOSTERT L,TIAN C,CROUS P W.Phylogeny and taxonomy of the scab and spot anthracnose fungus Elsino?(Myriangiales,Dothideomycetes)[J].Studies in Mycology,2017,87:1-41.
[10]BITANCOURT A,JENKINS A E.Perfect stage of the sweet orange fruit scab fungus[J].Mycologia,1936,28(5):489-492.
[11]BITANCOURT A A,JENKINS A.Elsino?fawcettii,the perfect stage of the citrus scab fungus[J].Phytopathology,1936,26(4):393-395.
[12]HAWKSWORTH D L.A new dawn for the naming of fungi:Impacts of decisions made in melbourne in july 2011 on the future publication and regulation of fungal names[J].IMA Fungus,2011,2(2):155-162.
[13]TAYLOR J W.One fungus=one name:DNA and fungal nomenclature twenty years after PCR[J].IMA Fungus,2011,2(2):113-120.
[14]ROSSMAN A Y,CROUS P W,HYDE K D,HAWKSWORTHD L,APTROOT A,BEZERRA J L,BHAT J D,BOEHM E,BRAUN U,BOONMEE S.Recommended names for pleomorphic genera in Dothideomycetes[J].IMA Fungus,2015,6(2):507-523.
[15]ROSSMAN A Y,ALLEN W C,CASTLEBURY L A.New combinations of plant-associated fungi resulting from the change to one name for fungi[J].IMA Fungus,2016,7(1):1-7.
[16]DNN W,EHC M K,HYDE K D.Towards incorporating anamorphic fungi in a natural classification-checklist and notes for2011[J].Mycosphere,2012,3(2):1-88.
[17]JENKINS A E.Lima bean scab caused by Elsino?[J].Journal of Agricultural Research,1931,42:13-23.
[18]WHITESIDE J O.Biological characteristics of Elsino?fawcettii pertaining to the epidemiology of sour orange scab[J].Phytopathology,1975,65(10):1170-1175.
[19]KIM K W,HYUN J W.Nonhost-associated proliferation of intrahyphal hyphae of citrus scab fungus Elsino?fawcettii:Refining the perception of cell-within-a-cell organization[J].Micron,2007,38(6):565-571.
[20]WHITESIDE J O.Pathogenicity of two biotypes of Elsino?fawcettii to sweet orange and some other cultivars[J].Phytopathology,1978,68:1128-1131.
[21]HYUN J W,YI S H,MACKENZIE S J,TIMMER L W,KIM KS,KANG S K,KWON H M,LIM H C.Pathotypes and genetic relationship of worldwide collections of Elsino?spp.Causing scab diseases of citrus[J].Phytopathology,2009,99(6):721-728.
[22]WEISS U,MERLINI L,NASINI G.Naturally occurring perylenequinones[J].Progress in the Chemistry of Organic Natural Products,1987,52:1-71.
[23]WEISS U,ZIFFER H,BATTERHAM T,BLUMER M,HACK-ENG W,COPIER H,SALEMINK C.Pigments of Elsino?species:I.Pigment production by Elsino?species;isolation of pure elsinochromes A,B,and C[J].Canadian Journal of Microbiology,1965,11(1):57-66.
[24]LIAO H L,CHUNG K R.Cellular toxicity of elsinochrome phytotoxins produced by the pathogenic fungus,Elsino?fawcettii causing citrus scab[J].New Phytologist,2010,177(1):239-250.
[25]LIAO H L,CHUNG K R.Genetic dissection defines the roles of elsinochrome phytotoxin for fungal pathogenesis and conidiation of the citrus pathogen Elsino?fawcettii[J].Molecular PlantMicrobe Interactions,2008,21(4):469-479.
[26]MA L,HONG T,LI C,ZHANG Y,WANG Z H,JI W Z.Photodynamic inhibitory effects of three perylenequinones on human colorectal carcinoma cell line and primate embryonic stem cell line[J].World Journal of Gastroenterology,2003,9(3):485-490.
[27]KENNEDY J,AUCLAIR K,KENDREW S G,PARK C,VED-ERAS J C,HUTCHINSON C R.Modulation of polyketide synthase activity by accessory proteins during lovastatin biosynthesis[J].Science,1999,284(5418):1368-1372.
[28]WANG L Y,HUEYJIUNN B,KUANGREN C,LIAO H L.Factors affecting the production of elsinochrome phytotoxin by the citrus scab pathogen,Elsino?fawcettii[J].Open Mycology Journal,2009,3(3):1-8.
[29]HYUN J W,PERES N A,YI S Y,TIMMER L W,KIM K S,KWON H M,LIM H C.Development of PCR assays for the identification of species and pathotypes of Elsino?causing scab on citrus[J].Plant Disease,2007,91(7):865-870.
[30]WHITESIDE J O.Detection of benomyl-tolerant strains of Elsino?fawcettii in florida citrus groves and nurseries[J].Plant Disease,1980,64(9):871-872.
[31]IEKI H.Emergence of benzimidazole-resistant strains of Elsino?fawcetti Jenkins in citrus orchards in Japan[J].Annals of the Phytopathological Society of Japan,2009,60(4):501-506.
[32]TYSON J L,FULLERTON R A.First report of benomyl resistance in Elsino?fawcettii in new Zealand citrus orchards[J].Australasian Plant Pathology,2001,30(1):69-69.
[33]侯欣.中国柑橘疮痂病菌的种类和变异研究[D].杭州:浙江大学,2013.HOU Xin.Species and variation of Chinese collections of Elsino?spp.causing scab diseases of citrus[D].Hangzhou:Zhejiang University,2013.
[34]王明爽,孟幼青,候欣,祝增荣,李红叶.值得重视的两种柑橘真菌性病害[J].植物检疫,2017(1):65-68.WANG Mingshuang,MENG Youqing,HOU Xin,ZHUZengrong,LI Hongye.Two citrus fungal diseases worthy of attention[J].Plant Quarantine,2017(1):65-68.
[2]HYUN J W,TIMMER L W,LEE S C,YUN S H,KO S W,KIM K S.Pathological characterization and molecular analysis of Elsino?isolates causing scab diseases of citrus in Jeju island in Korea[J].Plant Disease,2007,85(9):1013-1017.
[3]REINKING O A.Diseases of economic plants in Southern China[J].Phillippine Agriculturist,1919,8:109-134.
[4]李红叶.柑橘病害发生与防治彩色图说[M].北京:中国农业出版社,2011LI Hongye.Occurrence and control of citrus diseases[M].Beijing:China Agriculture Press,2011.
[5]HOU X,KEVIN H D,LI H.Pathotypes and genetic diversity of Chinese collections of Elsino?fawcettii causing citrus scab[J].Journal of Integrative Agriculture,2014,13(6):1293-1302.
[6]CHUNG K R.Elsino?fawcettii and Elsino?australis:The fungal pathogens causing citrus scab[J].Molecular Plant Pathology,2011,12(2):123-135.
[7]TIMMER L W,GARNSEY S M,GRAHAM J H.Compendium of citrus diseases[M].American Phytopathological Society,2000.
[8]TIMMER L W,PRIEST M,BROADBENT P,TAN M K.Morphological and pathological characterization of species of Elsinoe?causing scab diseases of citrus[J].Phytopathology,1996,86(10):1032-1038.
[9]FAN X,BARRETO R,GROENEWALD J,BEZERRA J,PEREIRA O,CHEEWANGKOON R,MOSTERT L,TIAN C,CROUS P W.Phylogeny and taxonomy of the scab and spot anthracnose fungus Elsino?(Myriangiales,Dothideomycetes)[J].Studies in Mycology,2017,87:1-41.
[10]BITANCOURT A,JENKINS A E.Perfect stage of the sweet orange fruit scab fungus[J].Mycologia,1936,28(5):489-492.
[11]BITANCOURT A A,JENKINS A.Elsino?fawcettii,the perfect stage of the citrus scab fungus[J].Phytopathology,1936,26(4):393-395.
[12]HAWKSWORTH D L.A new dawn for the naming of fungi:Impacts of decisions made in melbourne in july 2011 on the future publication and regulation of fungal names[J].IMA Fungus,2011,2(2):155-162.
[13]TAYLOR J W.One fungus=one name:DNA and fungal nomenclature twenty years after PCR[J].IMA Fungus,2011,2(2):113-120.
[14]ROSSMAN A Y,CROUS P W,HYDE K D,HAWKSWORTHD L,APTROOT A,BEZERRA J L,BHAT J D,BOEHM E,BRAUN U,BOONMEE S.Recommended names for pleomorphic genera in Dothideomycetes[J].IMA Fungus,2015,6(2):507-523.
[15]ROSSMAN A Y,ALLEN W C,CASTLEBURY L A.New combinations of plant-associated fungi resulting from the change to one name for fungi[J].IMA Fungus,2016,7(1):1-7.
[16]DNN W,EHC M K,HYDE K D.Towards incorporating anamorphic fungi in a natural classification-checklist and notes for2011[J].Mycosphere,2012,3(2):1-88.
[17]JENKINS A E.Lima bean scab caused by Elsino?[J].Journal of Agricultural Research,1931,42:13-23.
[18]WHITESIDE J O.Biological characteristics of Elsino?fawcettii pertaining to the epidemiology of sour orange scab[J].Phytopathology,1975,65(10):1170-1175.
[19]KIM K W,HYUN J W.Nonhost-associated proliferation of intrahyphal hyphae of citrus scab fungus Elsino?fawcettii:Refining the perception of cell-within-a-cell organization[J].Micron,2007,38(6):565-571.
[20]WHITESIDE J O.Pathogenicity of two biotypes of Elsino?fawcettii to sweet orange and some other cultivars[J].Phytopathology,1978,68:1128-1131.
[21]HYUN J W,YI S H,MACKENZIE S J,TIMMER L W,KIM KS,KANG S K,KWON H M,LIM H C.Pathotypes and genetic relationship of worldwide collections of Elsino?spp.Causing scab diseases of citrus[J].Phytopathology,2009,99(6):721-728.
[22]WEISS U,MERLINI L,NASINI G.Naturally occurring perylenequinones[J].Progress in the Chemistry of Organic Natural Products,1987,52:1-71.
[23]WEISS U,ZIFFER H,BATTERHAM T,BLUMER M,HACK-ENG W,COPIER H,SALEMINK C.Pigments of Elsino?species:I.Pigment production by Elsino?species;isolation of pure elsinochromes A,B,and C[J].Canadian Journal of Microbiology,1965,11(1):57-66.
[24]LIAO H L,CHUNG K R.Cellular toxicity of elsinochrome phytotoxins produced by the pathogenic fungus,Elsino?fawcettii causing citrus scab[J].New Phytologist,2010,177(1):239-250.
[25]LIAO H L,CHUNG K R.Genetic dissection defines the roles of elsinochrome phytotoxin for fungal pathogenesis and conidiation of the citrus pathogen Elsino?fawcettii[J].Molecular PlantMicrobe Interactions,2008,21(4):469-479.
[26]MA L,HONG T,LI C,ZHANG Y,WANG Z H,JI W Z.Photodynamic inhibitory effects of three perylenequinones on human colorectal carcinoma cell line and primate embryonic stem cell line[J].World Journal of Gastroenterology,2003,9(3):485-490.
[27]KENNEDY J,AUCLAIR K,KENDREW S G,PARK C,VED-ERAS J C,HUTCHINSON C R.Modulation of polyketide synthase activity by accessory proteins during lovastatin biosynthesis[J].Science,1999,284(5418):1368-1372.
[28]WANG L Y,HUEYJIUNN B,KUANGREN C,LIAO H L.Factors affecting the production of elsinochrome phytotoxin by the citrus scab pathogen,Elsino?fawcettii[J].Open Mycology Journal,2009,3(3):1-8.
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