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Cercosporoid Diseases of Citrus

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Cercosporoid Diseases of Citrus Mycologia, 107(6), 2015, pp. 1151–1171. DOI: 10.3852/15-059 © 2015 by The Mycological Society of America, Lawrence, KS 66044-8897 Cercosporoid diseases of Citrus Feng Huang Z. fructicola and Z. fructigenum on Citrus in China and Institute of Biotechnology, Zhejiang University, Hangzhou Z. citri-griseum, which appears to have a wide host range 310058, China including Acacia, Citrus, Eucalyptus and Musa, as well as J.Z. Groenewald a global distribution. Key words: CBS-KNAW Fungal Biodiversity Centre, Uppsalalaan 8, citrus greasy spot, multigene phylogenetic 3584 CT, Utrecht, the Netherlands analyses, Mycosphaerella, Pseudocercospora, Zasmidium Li Zhu INTRODUCTION Institute of Biotechnology, Zhejiang University, Hangzhou 310058, China Several species of cercosporoid fungi have been asso- ciated with leaf and fruit spot diseases of Citrus spp. P.W. Crous1 (Pretorius et al. 2003), of which two are regarded as CBS-KNAW Fungal Biodiversity Centre, Uppsalalaan 8, 3584 CT, Utrecht, the Netherlands particularly serious. Greasy leaf spot, caused by Zasmi- Department of Plant Pathology and Microbiology, Forestry dium citri-griseum(sexual morph Mycosphaerella citri) and Agricultural Biotechnology Institute (FABI), University (Sivanesan 1984, Timmer and Gottwald 2000, Braun of Pretoria, Pretoria 0002, South Africa et al. 2014), and Phaeoramularia fruit and leaf spot, Microbiology, Department of Biology, Utrecht University, Padualaan 8, 3584 CH Utrecht, the Netherlands caused by Pseudocercospora angolensis (Seif 2000), which is also of quarantine concern in Europe (Quaedvlieg 1 Hongye Li et al. 2012, Crous et al. 2013). Institute of Biotechnology, Zhejiang University, Hangzhou In former years these genera were treated as asexual 310058, China morphs of the genus Mycosphaerella (Corlett 1991, Crous et al. 2004b), although recent phylogenetic stud‐ ies have shown that this complex consists of more than Abstract: Citrus leaves and fruits exhibiting disease 40 genera and that these asexual morphs represent symptoms ranging from greasy spot, yellow spot, small or large brown spot, black dot, and brown dot were genera in their own right (Crous et al. 2007, 2009b). sampled from Fujian, Guangdong, Guizhou, Hunan, Many of these represent important phytopathogenic Jiangxi, Yunnan, Zhejiang provinces and the Guangxi genera, including Cercospora (Crous et al. 2006, Groene- Zhuang Autonomous Region in China. In total 82 iso- wald et al. 2013), Passalora, Pseudocercospora (Crous et al. lates representing various cercosporoid genera were 2013), Ramularia (Braun 1995, 1998; Videira et al. isolated from these disease symptoms, which were sup- 2015), Septoria (Quaedvlieg et al. 2013, Verkley et al. plemented with eight Citrus cercosporoid isolates 2013), Zasmidium (Braun et al. 2013, 2014) and Zymo- collected from other countries. Based on a morpholo- septoria (Quaedvlieg et al. 2011, Stukenbrock et al. gical and phylogenetic study using sequence data from 2012), to name but a few. the nuclear ribosomal DNA’s ITS1-5.8S-ITS2 regions Several leaf spot diseases of citrus have been asso- (ITS), and partial actin (act), b-tubulin (tub2), 28S ciated with cercosporoid fungi in the past. Greasy leaf nuclear ribosomal RNA (28S rDNA) and translation spot of citrus originally was associated with Cercosporaci- elongation factor 1-a (tef1) genes, these strains were tri-grisea in Florida, although the fungus was isolated placed in the following genera: Cercospora, Pallidocerco‐ from brown leaf spot symptoms (Fisher 1961), in con- spora, Passalora, Pseudocercospora, Verrucisporota and Za‐ trast to the greasy leaf spots linked to Mycosphaerellacitri smidium. All isolates tended to be sterile, except the (Whiteside 1972). Presently this disease is still a major Zasmidium isolates associated with citrus greasy spot- problem in Florida and has also been reported from like symptoms, which subsequently were compared many other areas including Mexico, Central America, with phylogenetically similar isolates occurring on the Caribbean islands and Egypt (Mondal et al. 2004, Citrus and other hosts elsewhere. From these results Haggag 2012). At the same time similar diseases of four Zasmidium species were recognized on Citrus, citrus have been observed in Argentina, Australia and namely Z. indonesianum on Citrus in Indonesia, Japan (Tanaka and Yamada 1952, Marcó and White- side 1986, Timmer and Gottwald 2000). A different dis- ease, called citrus pseudo greasy spot was reported Submitted 25 Jun 2015; accepted for publication 25 Jun 2015. from Japan (Koizumi 1986, Furuya et al. 2012). 1 Corresponding authors. E-mail: [email protected], [email protected]. Although Yamada (1956) linked Mycosphaerella horii to cn citrus leaf spot in this country, the illustration suggests 1151 1152 MYCOLOGIA it could be a species of Didymella. Fisher (1961) orange, pomelo and tangerine (TABLE I). Collected sympto- reported Cercospora gigantea from grapefruit leaves in matic leaves, fruits and other citrus tissues were washed Florida, but an examination of the type specimen sug- with running water to remove the dust and were dried with gests this is probably a synonym of Corynespora citricola absorbent paper. To obtain the fungal strains, the dried (Pretorius et al. 2003). Crous and Braun (2003) tissues were surface-disinfected by scrubbing thoroughly (5 times) with a cotton ball dipped in 75% ethanol. After dry- reported Passalora citricola from leaves of Citrus (origin ing under a laminar flow hood, a small piece (3 6 3 mm) of unknown) and P. citrigena from leaf spots of Citrus sp. tissue was removed from the junction of infected and healthy occurring in Mexico. Several species of Cercospora, tissue and plated on 2% potato dextrose agar (PDA, accord- identified as C. penzigii, have been associated with leaf ing to Crous et al. 2009b) plates amended with 100 mg/mL spots on a range of Citrus spp. from Algeria, Argentina, ampicillin and streptomycin to inhibit bacterial growth and Azerbaijan, Bhutan, Caucasus, China, Cuba, Domini- incubated at 25 C. Emerging colonies were transferred to can Republic, India, Italy, Japan, Mexico, Papua New fresh PDA plates, and fertile colonies single-spored and Guinea, Senegal, South Africa, Swaziland, USA (FL, stored at 4 C (see Crous et al. 2009b) (TABLE II). Additional MS, TX) and Venezuela (Pretorius et al. 2003). Phylo- strains were obtained from the working collection of Pedro genetically, however, these isolates appear to represent Crous (CPC) housed at CBS, as well as the CBS culture col- unresolved species in the C. canescens, C. fagellaris and lection (Utrecht, the Netherlands). Cercospora sp. P species complexes (Groenewald DNA extraction, PCR amplification and sequencing.—Isolates et al. 2013). were cultured 7 d on PDA at 25 C, the mycelia harvested Citrus represents a significant and rapidly growing with a sterile blade and placed in centrifuge tubes. DNA global industry. Among all citrus-producing countries, was extracted with the Biospin Fungus Genomic DNA Extrac- China is regarded as one of the most important centers tion Kit (Bio-Flux, Bior Technology Co., China) and used for of origin of Citrus, having a citrus-growing history of PCR amplification. Six primer pairs were used to amplify par- more than 4000 y (Deng et al. 2008, Zhou and Ye tial sequences of nuclear ribosomal RNAs ITS1-5.8S-ITS2 2010). Presently citrus represents a significant industry regions (ITS), and partial actin (act), b-tubulin (tub2), 28S in more than nine provinces, autonomous regions and ribosomal RNA gene (28S rDNA) and translation elongation municipalities in China (Deng et al. 2008). The major factor 1-a (tef1)genes. Sequences of primers followed the cultivars grown here include grapefruit, kumquat, studies, ITS4/ITS5 (White et al. 1990), ACT-512F/ACT783-R lemon, mandarin, orange, pomelo and tangerine (Carbone and Kohn 1999), Bt2a (Glass and Donaldson ’ (Deng et al. 2008). All these cultivars suffer from citrus 1995) or T1 (O Donnell and Cigelnik 1997), /Bt2b (Glass and Donaldson 1995) or b-Sandy-R (Stukenbrock et al. greasy spot, which has been recorded under three dif- 2012), LSU1Fd (Crous et al. 2009a), /LR5 (Vilgalys and ferent names based on their different occurring symp- Hester 1990) and EF1-728F (Carbone and Kohn 1999), /EF- toms, including greasy spot (Huang 1943, Zhang and 2(O’Donnell et al. 1998). The amplified products were seq- Yin 1987), yellow spot (Yan 1984, Jiang et al. 2012) uenced in both directions and a consensus sequence deter- and small brown spot (Zhang and Yin 1987). mined (Sunny Biotechnology Co. Ltd, Shanghai, China) for In the present study we collected citrus materials the phylogenetic analyses. All sequences produced in this with a range of leaf spot symptoms throughout China study were submitted to GenBank (TABLE II). and supplemented this collection with Citrus isolates collected in other countries. We aimed to characterize Phylogenetic analyses.—Resulting sequences were used to iden- and compare the cercosporoid species associated with tify additional related sequences deposited in the NCBI Gen- citrus greasy spot in China and elsewhere with the con- Bank nucleotide databases using megablast queries and solidated species concept introduced by Quaedvlieg subjected to multiple sequences alignments with the online et al. (2014). Under this species concept, species are interface of MAFFT 6 (Katoh and Toh 2010) and manually corrected where necessary. Two datasets were constructed; recognized based on the combination of morphologi- the first using
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