Australasian Plant Pathology, 2002, 31, 385–390

Plant virus surveys on the island of New Guinea and adjacent regions of northern Australia R. I. DavisA,G, J. E. ThomasB, L. A. McMichaelB, R. G. DietzgenC, B. CallaghanC, A. P. JamesD, T. G. GunuaE and S. RahammaF A

Northern Australia Quarantine Strategy, Australian Quarantine and Inspection Service, Centre for Tropical Agriculture, PO Box 1054, Mareeba, Qld 4880, Australia. Present address: Secretariat of the Pacific Community, PMB Suva, Fiji Islands, South Pacific. B Queensland Horticulture Institute, Department of Primary Industries, Indooroopilly, Qld 4068, Australia. C Queensland Agricultural Biotechnology Centre, Department of Primary Industries, St Lucia, Qld 4072, Australia. D Bureau of Sugar Experiment Stations, PO Box 86, Indooroopilly, Qld 4068, Australia. E Bubia Agricultural Research Centre, Lae, Papua New Guinea. F Research Institute of Maize and Other Cereals, Maros, Ujung Pandang, Indonesia. G Corresponding author; email: [email protected] AP02047 RPe.altInDt. aivrusi uvreysofNwe Guiena ndnotrhernAustrali

Abstract. A series of plant virus surveys was undertaken in Papua (formerly Irian Jaya), Indonesia, Papua New Guinea, and Australia’s Torres Strait Islands, Gove and Cape York Peninsula from 1996 to 2000. Confirmed records included Chilli veinal mottle virus, Dasheen mosaic virus, Papaya ringspot virus, Passion fruit woodiness virus, Watermelon mosaic virus and Zucchini yellow mosaic virus. Peanut stripe virus (Bean common mosaic virus) was widespread in Papua and Fiji disease virus was recorded at one location in Papua New Guinea. The first records of Glycine mosaic virus outside Australia and of a natural infection of Passiflora latent virus in Passiflora foetida are reported.

Introduction The plant health status of the island of New Guinea, which comprises the Indonesian province of Papua (formerly Irian Jaya) to the west and most of Papua New Guinea (PNG) to the east, differs from that of Australia. A number of important insect pests and diseases of plants not present in Australia can be found in New Guinea. As these areas are also in proximity to Queensland’s extreme north, this entire region is of quarantine interest to Australia. In the early 1990s, surveys carried out by the Northern Australia Quarantine Strategy (NAQS) provided extensive checklists of plant pathogenic fungi in the Torres Strait/Cape York Peninsula region (Hyde and Alcorn 1993), the Western Province of PNG (Hyde and Philemon 1994) and Papua (Shivas et al. 1996). Comparatively little is known of the current plant virus disease status of Queensland’s extreme north and the island of New Guinea. Most of the confirmed plant virus records from this region are from PNG. These include descriptions of the physical properties, host range and mode of transmission of Watermelon mosaic virus (WMV, but named melon mosaic © Australasian Plant Pathology Society 2002

virus) in Cucurbita moschata (Van Velsen 1960), Cassia mosaic virus in Cassia spp. (Van Velsen 1961a), Chlorotic spot virus in Passiflora foetida (Van Velsen 1961b), Cowpea mosaic virus in Vigna sinensis (Van Velsen 1961c), a virus causing a chlorotic streak on leaves of Axonopus affinis (Van Velsen 1967a), a virus causing a streak on leaves of Hippeastrum vittatum (Van Velsen 1967b), and Centrosema mosaic virus (CenMV) in a number of legume hosts (Van Velsen and Crowley 1961, 1962). Using electron microscopy, large and small bacilliform virus particles (possibly those of a rhabdovirus and a badnavirus, respectively) were detected in taro (Colocasia esculenta) and Dasheen mosaic virus (DsMV) was identified in C. esculenta and Xanthosoma sp. (Shaw et al. 1979). Shaw (1984) listed numerous records of Fiji disease of sugarcane, caused by Fiji disease virus (FDV), based on observations of the characteristic leaf symptoms in sugarcane. More recently, Yam mild mosaic virus in yam, Hibiscus chlorotic ringspot virus in Abelmoschus manihot and Banana streak virus in banana were identified using molecular and/or serological methods (Fuji et al. 1999; Brunt and Spence 2000; Davis et al. 2000a).

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In Papua, two recent records of quarantine interest to Australia are Peanut stripe virus (PStV), a strain of Bean common mosaic virus, from Manokwari in the north-west (Akin and Sudarsono 1997) and Rice tungro bacilliform virus (RTBV) from Jayapura and Nabire in the north (Davis et al. 2000b). Local farmers believe these diseases to be widespread in Papua. Neither has been recorded in PNG. In far north Queensland, there are very few verified observations of plant viruses north of the main cropping areas near Cairns (J. Thomas, unpublished data). From 1996–2000, NAQS conducted plant virus disease surveys in far north Queensland, Papua and parts of PNG. Overseas surveys were undertaken in collaboration with the governments of either Indonesia or PNG. This paper reports the findings of these surveys and a survey in Australia’s Northern Territory (NT). Methods Surveys A survey of the Alotau district in PNG’s Milne Bay Province was conducted in 1996. In 1997 and 1999, surveys were conducted in the coastal regions of the Western Province of PNG immediately north of the Torres Strait, and in several locations across Papua. A survey undertaken in 1998 covered parts of the PNG side of the PNG/Papua border and sugarcane in, and near, the Ramu Sugar Ltd plantation in Morobe Province was surveyed in 2000. In Australia, more frequent surveys were undertaken in far north Queensland during these years, principally in areas of human activity. Parts of the Gove Peninsula, NT, were surveyed in 1997. Samples of young symptomatic leaves (about 1 g fresh weight) were collected, surface sterilised in the field in 1% available chlorine, finely chopped, desiccated over anhydrous CaCl2, and on completion of the surveys, stored at –20°C prior to testing. Samples were imported into Australia under AQIS biological material import permits 199810781, 99609609 and 200008612. Enzyme linked immunosorbent assay (ELISA) testing Plate trapped antigen (PTA)-ELISA (Mowat and Dawson 1987) was used to test legume leaf samples for viruses in the genus Potyvirus, and chilli (Capsicum annuum var. annuum) specimens for Potato virus Y (PVY). For cucurbit specimens collected before 1998, assays included double antibody sandwich (DAS)-ELISA (Clark and Adams 1977) for Cucumber mosaic virus (CMV), WMV and Zucchini yellow mosaic virus (ZYMV), and PTA-ELISA with biotin-streptavidin detection (Dietzgen and Herrington 1991) for CMV, Papaya ringspot virus (PRSV) and WMV. DAS-ELISA was used to test aroid specimens for DsMV, C. annuum for Chilli veinal mottle virus (ChiVMV) and cucurbit specimens collected after 1998 for CMV, ZYMV, PRSV and WMV. In all tests, samples were considered positive when the absorbance values (A410 nm) were greater than three times that of appropriate negative controls. Immunosorbent electron microscopy (ISEM) Copper grids (200 mesh) were incubated with antiserum (diluted 1/1000 in 0.05 M sodium phosphate buffer pH 7.0; PB) at room temperature for 2 h. An extract of leaf tissue, ground in the same buffer, was then incubated on the grids at room temperature for 2 h or overnight at 5°C. Grids were washed twice with PB, 5 min each wash between incubations. Subsequent decorating antibodies were diluted 1/30 in PB and the grids incubated at room temperature for 1–2 h. The grids were

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rinsed with distilled water and stained with 1% potassium phosphotungstic acid pH 7.0, before viewing under the electron microscope. ISEM was used to test for Glycine mosaic virus (GMV) in the case of one Crotalaria pallida leaf sample and for CMV, Passiflora latent virus (PLV) and Passion fruit woodiness virus (PWV) for P. foetida samples. Antisera The following antisera were used (source in parentheses): in PTA-ELISA, Potyvirus (AGDIA Cat No. 27200), CMV-TF (RIB Francki), PRSV (D. Purcifull), WMV, PVY [Department of Primary Industries, Queensland (DPIQ) collection]; in DAS-ELISA, DsMV (AGDIA Cat No. 48000), CMV-TF (RIB Francki), ChiVMV (DSMZ Cat No. As 0122), PRSV, ZYMV and WMV (Sanofi Cat Nos 51240, 51279, 51276, respectively); in ISEM, CMV-T (RIB Francki), PLV (G Pietersen) and PWV, GMV (DPIQ collection). RNA extraction and reverse transcription polymerase chain reaction (RT-PCR) For Arachis hypogea samples, RNA was extracted using the ‘leaf soak’ method of Thomson and Dietzgen (1995). Using the Superscript One-Step RT-PCR system (Life Technologies), 25 μL duplex RT-PCR reactions were set up containing 1 μL template (diluted 1:20 in sterile distilled water) and 400 nM each of primers specific for PStV and Peanut mottle virus (PeMoV) (Dietzgen et al. 2001). PCR was carried out in a Perkin Elmer Cetus DNA thermal cycler 480. The RT-PCR conditions were 72°C for 5 min, 48°C for 45 min, 94°C for 2 min, then 40 cycles of 94°C for 45 s, 54°C for 45 s, 72°C for 60 s, followed by a final cycle of 72°C for 10 min. RNA was extracted from samples of desiccated gall tissue from sugarcane leaves showing symptoms of Fiji disease using a slight modification of the ‘leaf soak’ method of Thomson and Dietzgen (1995). The samples were frozen with liquid nitrogen before grinding and a chloroform:isoamyl alcohol (24:1) extraction step completed the procedure. RT-PCR was carried out using the C.therm. Polymerase One-step RT-PCR System (Roche), and FDV-specific primers (Smith et al. 1992). All PCR and RT-PCR amplification products were separated by agarose gel electrophoresis, stained with ethidium bromide and visualised by UV illumination.

Results In this study, virus infection of 21 plant species in six different families was confirmed. A total of ten different viruses was identified to species level and 27 others from several legumes were assigned to the genus Potyvirus (Table 1). The approximate locations where viruses were found are presented in Fig. 1. At four locations in Papua, PStV was detected in peanut plants showing typical green veinbanding, mottle and blotch symptoms. Peanut stripe disease symptoms were not found in numerous peanut plantings surveyed on the PNG side of the PNG/Papua border. GMV was identified in PNG from a Crotolaria pallida plant. Potyvirus infection was confirmed by ELISA in a further eight different species showing mosaic symptoms. Potyviruses were widespread in all survey regions. FDV was detected in sugarcane plants growing in one commercial plantation (Ramu Sugar Ltd) and one nearby subsistence planting near Gusap in the Ramu Valley, PNG.

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Fig. 1. Approximate locations (䉱) of plant viruses listed in Table 1. Records from individual islands in the Torres Strait are omitted for clarity.

DsMV was detected in 11 of 30 aroid specimens collected (three C. esculenta, four Xanthosoma sp., three Alocasia sp. and one Amorphophallus sp.). Eight of these records were from Australia (Torres Strait, Cape York Peninsula and Gove). When cucurbit plantings were surveyed, PRSV was detected at three locations in PNG and two in Papua, ZYMV at three locations in Papua and two in PNG, and WMV was found at two locations each in Papua and PNG. Mixed infections of PRSV and ZYMV were found twice in PNG, and mixed infections of all three viruses were found four times (two in Papua and two in PNG). PWV infection of the common weed P. foetida was widespread in the Torres Strait Islands (nine records), and was also detected in Cape York Peninsula at three northern locations (Weipa, Umagico and Seisia). PLV was detected in P. foetida in the Torres Strait Islands and in Cape York Peninsula (one record for each region). In two samples from the Torres Strait region, a coinfection of PLV with PWV was recorded. ChiVMV was found in C. annuum at two different locations in Papua and a coinfection with PVY was detected in one leaf sample.

Discussion These surveys detected two plant viruses (PStV and FDV) on the island of New Guinea that are specifically ‘targeted’ by NAQS. PStV is an important pathogen of peanut crops in several Asian countries, including Indonesia (Saleh et al. 1989), but is absent from Australia. PStV was found in four widely separated locations in Papua, including two production regions adjacent to the PNG border. As PStV is transmitted at a relatively high rate in infected seed (up to 50%, Xu et al. 1991) as well as by aphids in a non-persistent manner, the risk of entry into PNG appears to be high. FDV is a major pathogen of sugarcane that has apparently been present in PNG for many years (Shaw 1984), and is also currently under quarantine containment in some of Australia’s sugarcane producing districts. Fiji disease-like symptoms were found (and FDV confirmed) on these surveys only in the north-east of the island of New Guinea. Fiji disease has never been recorded in Queensland north of Proserpine (R. C. Magarey, personal communication). As sugarcane is considered a major ‘target host plant’ on NAQS surveys,

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Table 1. Plant viruses recorded in far north Queensland and parts of the Gove Peninsula, Northern Territory in Australia, Papua in Indonesia, and Papua New Guinea Host plant Family Genus, species Araceae Alocasia sp.

Amorphophallus sp. Colocasia esculenta (taro) Xanthosoma sp. (taro)

Cucurbitaceae Cucurbita maxima (pumpkin)

Cucurbita moschata Trichosanthes cucumerina Fabaceae Arachis hypogaea (peanut)

Calopogonium mucunoides Centrosema pubescens Clitoria ternatea

Crotalaria anagyroides Crotalaria goreensis

Crotalaria lunata Crotalaria pallida Desmodium tortuosum Mucuna pruriens Passifloraceae Passiflora foetida

Poaceae Saccharum sp. Saccharum officinarum Solanaceae Capsicum annuum var. annuum (chilli)

NAQS Mareeba collection no.

Approximate locationA

Symptoms

VirusB

116 2093 2119 360 287, 288 2118 1704 60 280, 289

Hammond Is., TS, Australia Darnley Is., TS, Australia Mareeba, CYP, Australia Old Mawatta, WP, PNG Yirrkala, NT Australia Mareeba, CYP, Australia Merauke, Papua, Indonesia Sagarai, MBP, PNG Yirrkala, NT Australia

Feathery mosaic Feathery mosaic Feathery mosaic Mosaic Feathery mosaic Feathery mosaic Feathery mosaic Feathery mosaic Feathery mosaic

DsMV DsMV DsMV DsMV DsMV DsMV DsMV DsMV DsMV

808 1700 1889 9 428, 432, 1318, 1319, 1922 1402, 1790 1320, 1323 1322 1317 749 1820

Biak, Papua, Indonesia Merauke, Papua, Indonesia Mabaduan, WP, PNG Alotau, MBP, PNG Daru, WP, PNG

Mild mottle Mosaic Mosaic Mosaic Mosaic

ZYMV PRSV, ZYMV, WMV PRSV, ZYMV, WMV PRSV PRSV

Daru, WP, PNG Daru, WP, PNG Daru, WP, PNG Daru, WP, PNG Merauke, Papua, Indonesia Sorong, Papua, Indonesia

Mosaic Mosaic Mosaic Mosaic Mosaic Mosaic

ZYMV PRSV, ZYMV PRSV PRSV, WMV, ZYMV ZYMV PRSV, ZYMV, WMV

656 724 774, 775 794 1196 741 311 75, 76, 77 123 159 539, 1069 121, 1458 888 1100, 2091 1441 1594 1612 708 715 16 71, 78 2101 723 341 312 340

Jayapura, Papua, Indonesia Wamena, Papua, Indonesia Merauke, Papua, Indonesia Timika, Papua, Indonesia Bewani, SP, PNG Merauke, Papua, Indonesia Daru, WP, PNG Dauan Is., TS, Australia Mer Is., TS, Australia Thursday Is., TS, Australia Thursday Is., TS, Australia Hammond Is., TS, Australia Stephen Is., TS, Australia Darnley Is., TS, Australia Mabuiag Is., TS, Australia Karumba, CYP, Australia Mornington Is., CYP, Australia Wamena, Papua, Indonesia Wamena, Papua, Indonesia Alotau, MBP, PNG Dauan Is., TS, Australia Darnley Is., TS, Australia Wamena, Papua, Indonesia Parama, WP, PNG Daru, WP, PNG Parama, WP, PNG

Mottle/blotch Mottle/blotch Mottle/blotch Mottle/blotch Mosaic Mosaic Mottle Mosaic, crinkle, blister Mosaic Mottle Mosaic Mosaic Mosaic Mosaic Mosaic Mosaic Mosaic Feathery mosaic Mosaic Mottle Mosaic Mosaic Mosaic Strong mottle Mosaic Mosaic

PStVC PStV PStV PStV Potyvirus Potyvirus Potyvirus Potyvirus Potyvirus Potyvirus Potyvirus Potyvirus Potyvirus Potyvirus Potyvirus Potyvirus Potyvirus Potyvirus Potyvirus Potyvirus Potyvirus Potyvirus Potyvirus GMVD Potyvirus Potyvirus

835, 538 834 1457 866 2174 1963 872, 1070 2431 2137 2153 606, 1411 2008

Moa Is., TS, Australia Moa Is., TS, Australia Hammond Is., TS, Australia Horn Is., TS, Australia Yam Is., TS, Australia Yam Is., TS, Australia Thursday Is., TS, Australia Gabba Is., TS, Australia Umagico, CYP, Australia Seisia, CYP, Australia Weipa, CYP, Australia Mapoon, CYP, Australia

Mottle, ringspot Mosaic Mosaic Mottle, ringspot Ringspot Mottle, ringspot Mosaic, ringspot Mosaic Mosaic Mosaic Mosaic Mosaic

PWVD PWV PLVD PWV, PLV PWV PWV, PLV PWV PWV PWV PWV PWV PLV

2207 2209

Gusap, MP, PNG Gusap, MP, PNG

Fiji disease Fiji disease

FDVE FDV

1719 1793 1688

Jayapura, Papua, Indonesia Jayapura, Papua, Indonesia Merauke, Papua, Indonesia

Mosaic Mosaic, crinkle Mosaic

ChiVMV, PVY ChiVMV ChiVMV

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Table 1.

(Continued)

A

Abbreviations for locations are: CYP — Cape York Peninsula, Queensland; MB — Milne Bay Province; MP — Morobe Province; NT — Northern Territory; TS — Torres Strait, Queensland; WP — Western Province; SP — Sandaun Province. B Virus acronyms are: ChiVMV — Chilli veinal mottle virus; DsMV — Dasheen mosaic virus; FDV — Fiji disease virus; GMV — Glycine mosaic virus; PLV — Passiflora latent virus; PRSV — Papaya ringspot virus; PStV — Peanut stripe virus; PVY — Potato virus Y; PWV — Passion fruit woodiness virus; WMV — Watermelon mosaic virus; ZYMV — Zucchini yellow mosaic virus. C Positive for PStV and negative for Peanut mottle virus by RT-PCR. D Viruses identified by immunosorbent electron microscopy. E Positive for FDV in RT-PCR tests.

stands of cane and related species are always examined closely. The results reported here, therefore, suggest that FDV might also be absent from the small non-commercial sugarcane plantings that lie immediately to the north of Queensland’s disease-free production zone. Legumes showing virus-like symptoms were widespread in the survey regions. The record of GMV from Crotolaria pallida from PNG is the first for this virus from outside Australia. The legume samples that gave positive reactions for potyvirus by ELISA will be investigated further by cloning and sequencing of RT-PCR products obtained using potyvirus genus-specific degenerate primers. Sixteen legumes (eight C. pubescens, three C. mucunoides, two C. pallida one Glycine max, one D. tortuosum, and one Ormocarpum orientale) showed virus-like symptoms but tested negative for potyviruses. These may be infected with other viruses. For example, Van Velsen and Crowley (1961) reported widespread natural infection by the potexvirus CenMV in several legume genera, including Calopogonium, Centrosema, Crotolaria and Desmodium. DsMV is common in taro in countries neighbouring Australia (Zettler and Jackson 1979; Shaw et al. 1979; Pearson 1981). In Australia, DsMV had previously been detected in Alocasia, Colocasia, Xanthosoma and Dieffenbachia in south-east Queensland (Greber and Shaw 1986). The present study reports the presence of the virus in north Queensland and the NT, and for the first time, in an Amorphophallus sp. from PNG. The origin of DsMV found in Australia is not known. It may be endemic, or it may be that this virus is seen comparatively rarely in Australian aroids because it was introduced only occasionally with planting material in the past. Taro production is an emerging industry in far north Queensland and DsMV causes reductions in plant growth and corm yield of taro (Zettler et al. 1989). High losses in ornamentals in the genus Dieffenbachia have also been attributed to this disease (Chase and Zettler 1982). PWV causes a serious disease of passionfruit (Passiflora edulis and P. edulis × flavicarpa) in Australia, and is known to infect several other Passiflora spp. (Simmonds 1966; Teakle and Wildermuth 1967). In the present study, PWV was found in P. foetida in the Torres Strait region, and in the northern part of Cape York Peninsula. Further south on the Peninsula, passionfruit is grown to exploit a lucrative market for ‘out-of-season’ fruit (K. McGuffey, personal

communication). The weed species P. foetida and P. suberosa are significant sources of PWV in southern Queensland. The virus is a potential threat to commercial passionfruit production on Cape York Peninsula because both species can be found near crop plantings. This work reports for the first time, PLV from Cape York Peninsula and the Torres Strait region, and also PLV from naturally infected P. foetida. A number of other P. foetida samples from Papua, the Torres Strait region and Cape York Peninsula had obvious mosaic symptoms, but tested negative for CMV, PLV and PWV. The identity of viruses infecting these plants is currently under investigation. Although PRSV was found in cucurbits in Papua and PNG, it was likely to be the W (cucurbit-infecting) strain, as no ringspot-like symptoms were found on papaya in these surveys. Papaya ringspot disease, caused by the PRSV-P is an important disease of papaya under quarantine containment in south-east Queensland (Thomas and Dodman 1993). This strain also infects cucurbit species and it can be distinguished from the cucurbit-limited strain only by host range testing. This study has highlighted differences in the distribution of certain plant viruses across parts of the island of New Guinea and adjacent regions of northern Australia. The threat posed to Australia’s plant-based industries and the natural environment by plant viruses on the island of New Guinea is minimised by legislation prohibiting movement of plant material south from New Guinea and the Torres Strait Islands. This is enforced by AQIS officers stationed in all Torres Strait Island communities and on the mainland. Acknowledgements B. Waterhouse (NAQS) is gratefully acknowledged for identification of virus hosts. L. Loader (previously DPIQ) is acknowledged as collector of some aroid specimens. Some potyvirus and all DsMV ELISA testing was done by P. Cross (TASAG, Department of Primary Industry and Fisheries, Tasmania). The technical assistance of S. Jacobson and J. Parry is gratefully acknowledged. P. Bannink (Queensland Environmental Protection Agency) is thanked for providing the map used in Fig. 1. References Akin HM, Sudarsono (1997) Characterisation of peanut stripe virus (PStV) isolates originating from various provinces in Indonesia. Indonesian Journal of Tropical Agriculture 8, 13–20.

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Received 7 March 2002, accepted 17 June 2002

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