Actinidia Is a Natural Host to a Wide Range of Plant Viruses

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1 Actinidia Is a Natural Host to a Wide Range of Plant Viruses M.N. Pearson 1, D. Cohen 2, R. Chavan 1 and A. Blouin 2 1 School of Biological Sciences, The University of Auckland, Private Bag , Auckland, New Zealand 2 The New Zealand Institute for Plant & Food Research Ltd., Private Bag , Auckland, New Zealand Keywords: Vitivirus, Potexvirus, Alfalfa mosaic virus, Apple stem grooving virus, Citrus leaf blotch virus, Cucumber mosaic virus, Cucumber necrosis virus, Ribgrass mosaic virus Abstract At the 6 th International Symposium on Kiwifruit in 2006 we reported the presence of Apple stem grooving virus, Ribgrass mosaic virus (Tobamovirus) and a nm flexuous virus in Actinidia accessions from China. The flexuous virus was subsequently sequenced and shown to be closely related to Citrus leaf blotch virus (Flexiviridae). Although to date no obvious virus problems have been reported in commercial crops further examination of kiwifruit germplasm has detected additional viruses, both spherical and filamentous, from a range of virus families and genera. These include Alfalfa mosaic virus, Cucumber mosaic virus, Cucumber necrosis virus, a Potexvirus and two novel Vitiviruses. The biological properties of the viruses from kiwifruit and their phylogenetic relationships with similar viruses from other hosts will be described, and the possible implications for the kiwifruit industry discussed. INTRODUCTION At the 2006 Kiwifruit Symposium we reported the detection of Apple stem grooving virus (ASGV) in Actinidia chinensis from China held in quarantine in Auckland, New Zealand, plus a Tobamovirus, a Flexivirus (previously described as a carlavirus-like virus), and several other sap-transmissible virus-like agents in A. chinensis and A. deliciosa (Pearson et al., 2007). The identification of ASGV (Clover et al., 2003) was the first definitive identification of a virus from Actinidia although there were previous publications describing viral-like symptoms in China (Lin and Gao, 1995) and viral-like symptoms in Actinidia deliciosa grafted on to A. polygama rootstocks in Japan (Nitta and Ogasawara, 1997). Since 2006 we have further characterized the Tobamovirus and Flexivirus plus several additional viruses from plants showing a range of viral-like symptoms (Fig. 1). METHODS Mechanical Inoculation of Herbaceous Indicators Leaf extracts in 0.1 M sodium phosphate buffer, ph 7.5, plus 5% PVP (Sweet, 1975) were mechanically inoculated to the herbaceous indicator species Chenopodium quinoa, Nicotiana benthamiana, N. clevelandii, N. glutinosa, N. occidentalis and Phaseolus vulgaris. Virus Identification Symptomatic Actinidia and herbaceous indicators were examined for viruses using a range of techniques including transmission electron microscopy, enzyme labeled immuno-sorbent assay (ELISA) using commercially available antisera, reverse transcription polymerase chain reaction (RT-PCR) and sequencing using a range of generic and specific primers (Chavan et al., 2009) and high-resolution tandem mass spectrometry of coat proteins (Blouin et al., 2010). Proc. VII th IS on Kiwifruit Eds.: G. Costa and A.R. Ferguson Acta Hort. 913, ISHS

2 RESULTS Tobamovirus The Tobamovirus previously detected in both A. chinensis and A. deliciosa (Pearson et al., 2007) has been sequenced and shown to a strain of Ribgrass mosaic virus (RMV) (Chavan et al., 2009). RMV is a common and widespread virus which infects Plantago spp. and a range of cruciferous hosts (Gibbs, 1999; Heinze et al., 2006). Flexivirus The Flexivirus previously detected in both A. chinensis and A. deliciosa (Pearson et al., 2007) has been sequenced and shown to be closely related to Citrus leaf blotch virus. The virus also reacts with an antiserum to Citrus leaf blotch in ELISA (antiserum kindly supplied by Dr Richard Lee, USDA, Riverside, California). Alfalfa Mosaic Virus and Cucumber Mosaic Virus AMV was detected in A. guilinensis and both AMV and CMV were detected in A. glaucophylla and A. fortunatii by ELISA using commercially available antisera. Partial coat protein gene sequence of AMV isolates from A. glaucophylla and A. fortunatii are very similar to isolates from lupin, carrot, pepper and tomato. Vitivirus Two novel Vitiviruses, tentatively named Actinidia virus A and Actinidia virus B (AcVA and AcVB) were identified from A. chinensis following transmission to Nicotiana occidentalis where they produced different symptoms. Infection of AcVA alone showed large necrotic local lesions and the systemically infected plants were stunted with very small leaves. Single infection of AcVB induced chlorotic local lesions with ringspots. The systemic leaves showed strong chlorosis but the overall shape and height of the plant remained comparable to those of the uninfected plants. The viruses can be transmitted to A. deliciosa by grafting but are mostly asymptomatic. Sequence data from both replicase and coat protein genes indicates the two viruses are distinct from each other and members of the Vitivirus including the grapevine vitiviruses Grapevine virus A and Grapevine virus B. Potexvirus A novel Potexvirus, Actinidia virus X, was identified from A. chinensis following transmission to N. benthamiana and subsequently maintained in N. occidentalis. The most closely related are Asparagus virus 3 (AV-3), Scallion virus X (ScaVX) and Narcissus mosaic virus (NMV) which show ~75% aa similarity in the replicase and ~60% aa similarity in CP. When A. chinensis seedlings were mechanically infected, systemic spread was detected but virus titre in the leaves rapidly fell and could not be detected at 2 months post inoculation. Cucumber Necrosis Virus CNV was detected by MAF Biosecurity NZ in Actinidia held in quarantine using generic Tombusvirus primers. DISCUSSION To date we have identified nine distinct viruses in Actinidia germplasm originating from China representing eight different virus genera (Table 1). Researchers at the University of Bologna have also detected CMV and an as yet uncharacterized flexuous virus (C. Ratti, pers. commun.). In general, symptoms observed on A. chinensis have been relatively minor; some symptoms appear in early spring and fade by summer while others cannot be observed until summer. Currently we have very little information on the biological properties (host range, disease symptoms, vectors, etc.) of the viruses isolated from Actinidia species and consequently it is not possible to predict the precise effects of 468

3 the various viruses on different Actinidia species and cultivars. However, based on the known properties of other species in the same genus assumptions can be made about the likely modes of transmission and the breadth of host range. The two viruses with the greatest potential to spread are the two aphid transmitted viruses CMV and AMV. Both of these viruses have a worldwide distribution and consequently do not constitute a biosecurity risk. These viruses were found on noncommercial Actinidia species and symptoms on A chinensis have been very mild. Both viruses have very wide host ranges and are transmitted by multiple aphid species and therefore it would be impossible to protect kiwifruit crops from infection. However, given their universal distribution any significant effect on kiwifruit would probably have been noticed by now. Of the remaining viruses, Apple stem grooving virus, Ribgrass mosaic virus, Citrus leaf blotch virus, and Potexviruses have no known natural vectors, limiting spread to infected plant material, grafting, and mechanical transmission by means such as pruning. Citrus leaf blotch is seed transmissible at a rate of ~2.5% in citrus (Guerri et al., 2004) but there is no evidence of seed transmission in Actinidia in tests on more than 200 seedlings grown from fruit collected from an infected plant. Cucumber necrosis virus is transmitted through the soil by a fungus (Olpidium spp.) but even if the vector is present, spread would be slow. A. chinensis infected with the Vitiviruses show a wide range of symptoms, the most visible are observed in spring. However, half of the infected plants do not show any viral symptoms. Vitiviruses are spread by aphids or mealybugs and typically require helper viruses for transmission from and to the natural host. So far the natural vectors of the novel Vitiviruses have not been identified, but the detection of the viruses has only been made on graft material imported from China. As we commented previously (Pearson et al., 2007) viruses are common in most crops, particularly vegetatively propagated species, and consequently it is not surprising to find a range of different viruses in Actinidia. There is a report of dieback associated with ASGV in Russia (Grin ko, 2008) but this is appeared to be a complex disease syndrome and ASGV may be only one contributing factor. So far we have not observed virus-like symptoms associated with disease in commercial crops. However, the effects of viruses on crops can range from insignificant (e.g., latent viruses) to severe and often differ between host species or cultivars. Also the effects of mixed virus infections may be additive. Consequently, it is generally desirable to prevent virus infection and spread where possible. In particular we would recommend virus testing of imports and new cultivars before release and distribution. ACKNOWLEDGEMENTS The authors wish to thank Zespri Innovation and the KRIP fund (Plant & Food Research) for funding this work. Literature Cited Blouin, A.G., Greenwood, D.R., Chavan, R.R., Pearson, M.N., Clover, G.R.G., Macdiarmid, R.M. and Cohen, D A generic method to identify plant viruses by high resolution tandem mass spectrometry of their coat proteins. J. Virol. Methods 63: Chavan, R.R., Pearson, M.N. and Cohen, D Partial characterization of a novel Tobamovirus infecting Actinidia chinensis and A. deliciosa (Actinidiaceae) from China. Eur. J. Plant Pathol. 124: Clover, G.R.G., Pearson, M.N., Elliot, D.R., Tang, Z., Smales, T.E. and Alexander, B.J.R Characterization of a strain of Apple stem grooving virus in Actinidia chinensis from China. Plant Pathol. 52: Gibbs, A Evolution and origins of Tobamoviruses. Philosoph. Trans. Roy. Soc. London B 354: Grin ko, N.N Virus aetiology of Chinese Actinidia dieback. Zashchita i Karantin 469

4 Rastenii 6: Guerri, J., Pina, J.A., Vives, M.C., Navarro, L. and Moreno, P Seed transmission of Citrus leaf botch virus: implications in quarantine and certification programs. Plant Disease 88(8): Heinze, C., Lesemann, D.-E., Ilmberger, N., Willingman, P. and Adam, G The phylogenetic structure of the cluster of tobamovirus species serologically related to Ribgrass mosaic virus (RMV) and the sequence of Streptocarpus flower break virus (SFBV). Arch. Virol. 151: Lin, Y. and Gao, R Survey and identification of Actinidia spp. diseases in Fujian, China. J. Fujian Agri. Univ. 24:49-53 (in Chinese). Nitta, H. and Ogagawara, S A new, graft transmitted, disease of kiwifruit. Acta Hort. 444: Sweet, J.B Soil borne viruses occurring in nursery soils and infecting some ornamental species of Rosaceae. Ann. Appl. Biol. 79: Tables Table 1. Summary of viruses identified from Actinidia spp. and general biological properties of viruses in the genus. Virus name Genus Typical biological properties of genus Natural host range Transmission Apple stem grooving virus Capillovirus narrow mechanical Alfalfa mosaic virus Alfamovirus wide mechanical, aphids Actinidia virus X Potexvirus limited mechanical Actinidia vitivirus A Vitivirus narrow mechanical, mealy bugs & scale Actinidia vitivirus B Vitivirus narrow mechanical, mealy bugs & scale Citrus leaf blotch virus Citrivirus narrow mechanical, seed (in citrus) Cucumber mosaic virus Cucumovirus very wide mechanical, aphids Cucumber necrosis virus Tombusvirus narrow mechanical, soil fungus Ribgrass mosaic virus Tobamovirus narrow mechanical 470

5 Figures Fig. 1. Virus-associated symptoms on Actinidia chinensis. 471

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