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Phyllosticta Citriasiana Sp. Nov., the Cause of Citrus Tan Spot of Citrus Maxima in Asia

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Phyllosticta Citriasiana Sp. Nov., the Cause of Citrus Tan Spot of Citrus Maxima in Asia Fungal Diversity Phyllosticta citriasiana sp. nov., the cause of Citrus tan spot of Citrus maxima in Asia Wulandari, N.F.1,2,3, To-anun, C1., Hyde, K.D.4,2, Duong, L.M.5, de Gruyter, J.6*, Meffert, J.P.6, Groenewald, J.Z.7 and Crous, P.W.7 1Department of Plant Pathology, Faculty of Agriculture, Chiang Mai University, Chiang Mai, 51200, Thailand 2Mushroom Research Centre, 128 Moo 3, Pha Dheng, T. Papae, Mae Taeng, Chiang Mai 50150, Thailand 3Microbiology Division, Research Centre for Biology, Indonesian Institute of Sciences, Cibinong Science Centre Jl. Raya Jakarta-Bogor KM 46, Cibinong 16911, Indonesia 4School of Science Mae Fah Luang University, 333 M. 1. T. Tasud Muang District, Chiang Rai 57100, Thailand 5Microbiology & Biotechnology Department Hanoi National University of Education 136 Xuanthuy, Caugiay, Hanoi, Vietnam 6Plant Protection Service, P.O. Box 9102, 6700 HC, Wageningen, The Netherlands 7CBS Fungal Biodiversity Centre, P.O. BOX 85167, 3508 AD, Utrecht, The Netherlands Wulandari, N.F., To-anun, C., Hyde, K.D., Duong, L.M., de Gruyter, J., Meffert, J.P., Groenewald, J.Z. and Crous, P.W. (2009). Phyllosticta citriasiana sp. nov., the cause of Citrus tan spot of Citrus maxima in Asia. Fungal Diversity 34: 23-39. Guignardia citricarpa, the causal agent of Citrus Black Spot, is subject to phytosanitary legislation in the European Union and the U.S.A. This species is frequently confused with G. mangiferae, which is a non-pathogenic, and is commonly isolated as an endophyte from citrus fruits and a wide range of other hosts. Recently, necrotic spots similar to those caused by G. citricarpa were observed on fruit of Citrus maxima intercepted in consignments exported from Asia. In these spots, pycnidia and conidia of a Guignardia species closely resembling G. citricarpa were observed, and therefore measures were taken for the consignments in line with the European Union legislation for G. citricarpa. To determine the identity of the causal organism on this new host, fungal isolates were subjected to DNA sequence analysis of the internal transcribed spacer region (ITS1, 5.8S, ITS2), translation elongation factor 1-alpha (TEF1) and actin genes. A combined phylogenetic tree resolved three species correlating to G. citricarpa, G. mangiferae and a previously undescribed species, Phyllosticta citriasiana sp. nov., closely related to G. citricarpa. Morphologically P. citriasiana can be distinguished from G. citricarpa by having larger conidia, longer conidial appendages, and in not producing any diffuse yellow pigment when cultivated on oatmeal agar (OA). Furthermore, it is distinguishable from G. mangiferae by having smaller conidia, with a narrower mucoid sheath. In culture, colonies of P. citriasiana can also be distinguished from G. citricarpa and G. mangiferae by being darker shades of grey and black on OA, malt extract agar (MEA), potato-dextrose agar, and cornmeal agar. Furthermore, cultures of P. citriasiana achieved optimal growth after 2 weeks at 21–27°C, and ceased to grow at 30–33°C. In contrast, colonies of G. citricarpa and G. mangiferae achieved optimal growth at 27–30°C, and ceased to grow at 30–36°C. Colonies of P. citriasiana also grew faster than those of G. citricarpa and G. mangiferae on OA and MEA. Phyllosticta citriasiana appears to be a harmful pathogen of Citrus maxima, causing a tan spot on fruit, underlining the need for further surveys and research to determine its distribution and host range. Key words: Citrus Black Spot, Guignardia, quarantine, molecular phylogeny, Phyllosticta, systematics. Article Information Received 15 November 2008 Accepted 15 December 2008 Published online 1 January 2009 *Corresponding author: J. (Hans) de Gruyter; e-mail: [email protected] Introduction Glienke-Blanco et al., 2002; Rodrigues et al., 2004; Huang et al., 2008; Sánchez Márquez et Where known, anamorphs of Guignardia al., 2008; Thongkantha et al., 2008). Many (Botryosphaeriaceae) reside in Phyllosticta Guignardia species cause leaf blotch and black (Van der Aa, 1973; Punithalingam, 1974; Van spots on fruits of various plants (Raabe et al., der Aa and Vanev, 2002). Guignardia species 1981; Glienke-Blanco et al., 2002). Few have often been recorded as endophytes, plant studies, however, have focused on the phylo- pathogens and saprobes (Baayen et al., 2002; genetic relationships among Guignardia and 23 Phyllosticta species, and uncertainty remains citricarpa were observed on fruit of Citrus pertaining to species boundaries and host maxima, intercepted in consignments exported ranges of most taxa (Okane et al., 2001; from Asia. In these spots, pycnidia and conidia Baayen et al., 2002; Crous et al., 2006). of a Guignardia species, closely resembling G. Species of Guignardia are commonly known citricarpa, were observed and therefore, mea- only from their anamorphs. The identification of sures were taken for the consignments in line Phyllosticta anamorphs is highly problematic, as with the EU legislation for Guignardia citri- few characters are available to separate different carpa. species. Sometimes a single difference in coni- By testing several PCR methods deve- dial morphology, such as the thickness of the loped for detection of G. citricarpa on lesions mucoid layer surrounding the conidium, or ap- of Citrus maxima and isolates at the Dutch pendage shape and size, resulted in authors Plant Protection Service, the real-time PCR describing different species. Van der Aa and method developed by Van Gent-Pelzer et al. Vanev (2002) revised the 2936 taxa described (2007) failed to provide any amplification, in the genus Phyllosticta, accepting 141 spe- which was due to sequence divergence in the cies. Many other Phyllosticta species were ITS region. Therefore, a conventional PCR combined into genera such as Ascochyta, assay is normally recommended for the diag- Coleophoma, Fusicoccum, Leptodothiorella, nosis of G. citricarpa on C. maxima fruit. This Phoma and Phomopsis, to name but a few. was confirmed in a comparative study with a Recent studies on Guignardia and Phyl- conventional PCR assay developed by Bonants losticta have illustrated the confusion that still et al. (2003) on isolates obtained from C. exists surrounding species concepts in literature. maxima (I.R. Heurneman-van Brouwershaven, For instance, both Guignardia endophyllicola unpubl. data). and G. mangiferae have been linked to P. capi- To determine the identity of the Guignar- talensis as anamorph (Okane et al., 2001). This dia species associated with tan spot of Citrus matter was resolved by Baayen et al. (2002), maxima fruit intercepted from Asia, fungal who successfully used ITS DNA sequence data isolates were subjected to DNA sequence to show that G. endophyllicola was conspecific analysis of the internal transcribed spacer with G. mangiferae. To date the ITS domain has (ITS1, 5.8S, ITS2) region and partial transla- chiefly been used for species discrimination in tion elongation factor 1-alpha (TEF1) and actin this group (Everett and Rees-George, 2006), and (ACT) gene sequences. Further aims were to further work remains to determine if a multi- investigate the species boundaries of Asian gene phylogenetic approach would not resolve isolates compared to isolates identified as G. more cryptic taxa. citricarpa and G. mangiferae, and to determine Citrus Black Spot, caused by Guignardia which genes are useful in distinguishing iso- citricarpa (anamorph Phyllosticta citricarpa) is lates of Guignardia at the species level. regulated as a quarantine pest in the European Union and the U.S.A. It occurs in a number of Material and Methods countries in Southeast Asia, Africa, South America, and Australia, and can be dissemina- Isolates ted by means of infected fruit or vegetative Cultures were obtained from the CBS plant material. Two distinct Guignardia species Fungal Biodiversity Centre (CBS), Utrecht, are associated with citrus, namely the pathogen The Netherlands, and the Plant Protection G. citricarpa, and the endophyte G. mangiferae Service (PD), Wageningen, The Netherlands. (Meyer et al., 2001; Baayen et. al., 2002; To supplement the dataset with more species, Everett & Rees-George, 2006; Baldassari et al., single ascospore and conidial isolates were 2008). Based on the ITS sequences, several respectively made from Guignardia and PCR detection methods have been developed Phyllosticta fruiting bodies occurring on leaves for detection of G. citricarpa (Bonants et al., and fruit of diverse host plants (Table 1). 2003; Meyer et al., 2006; Peres et al., 2007; Colonies were established on 2 % malt extract Van Gent-Pelzer et al., 2007). Recently, agar plates (MEA; Sigma-Aldrich Chemie, necrotic spots similar to those caused by G. Zwijndrecht, The Netherlands) by using the 24 Fungal Diversity techniques as explained in Cheewangkoon et Cultures were grown on 2% tap-water al. (2008). agar supplemented with sterile pine needles (WAP) (Crous et al., 2006), for microscopic Molecular phylogeny examination. Preparations were mounted in DNA extraction was done using the cotton-blue lactophenol or clear lactic acid, and UltraClean™ Microbial DNA Kit (MO Bio, studied by means of a light microscope (× 1000 Carlsbad, CA, USA) according to manufac- magnification). The 95 % confidence intervals turer’s protocol. The primers V9G (de Hoog were derived from 30 observations of spores and Gerrits van den Ende, 1998) and ITS4 formed on WAP, with extremes given in (White et al., 1990) were used to amplify the parentheses. All cultures obtained in this study internal transcribed spacer region (ITS) of the are maintained in the culture collection of the nuclear ribosomal RNA operon, including the CBS (Table 1). Colony colours (surface and 3’ end of the 18S rRNA, the first internal reverse) were assessed after growth on four transcribed spacer region, the 5.8S rRNA gene; different media, potato-dextrose agar (PDA), the second internal transcribed spacer region cornmeal agar (CMA), MEA and oatmeal agar and the 5’ end of the 28S rRNA gene. To (OA, Gams et al., 2007) using the colour charts resolve taxa in the G. mangiferae and G.
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