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Viruses of Kiwifruit (Actinidia Species)

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Viruses of Kiwifruit (Actinidia Species) 001_JPP_Review_221_colore 30-07-2013 16:52 Pagina 221 Journal of Plant Pathology (2013), 95 (2), 221-235 Edizioni ETS Pisa, 2013 221 INVITED REVIEW VIRUSES OF KIWIFRUIT (ACTINIDIA SPECIES) A.G. Blouin1, M.N. Pearson2, R.R. Chavan2, E.N.Y. Woo2, B.S.M. Lebas3, S. Veerakone3, C. Ratti4, R. Biccheri4, R.M. MacDiarmid1,2 and D. Cohen1 1The New Zealand Institute for Plant & Food Research Limited, Private Bag 92169, Auckland, New Zealand 2School of Biological Sciences, The University of Auckland, Private Bag 92019, Auckland, New Zealand 3Plant Health and Environment Laboratory, Ministry for Primary Industries, PO Box 2095, Auckland 1140, New Zealand 4Dipartimento di Scienze Agrarie, Area Patologia Vegetale, Viale G. Fanin 40, 40127 Bologna, Italy SUMMARY bark cracking and cane wilting. Pelargonium zonate spot virus (PZSV) has been detected in Italy associated with Kiwifruit (Actinidia deliciosa) was introduced to New severe symptoms on leaves and fruit. Zealand more than one hundred years ago and the New Zealand-raised cv. Hayward is now the dominant culti- var grown worldwide. Further accessions of kiwifruit INTRODUCTION seed and scionwood have been sourced from China for research and breeding. In one importation consign- In 1904, Isabel Fraser introduced the first kiwifruit ment, the first virus naturally infecting kiwifruit, Apple seed to New Zealand, and by 1910 the plants raised by a stem grooving virus (ASGV), was identified following friend, Alexander Allison, produced the first fruit out- symptoms observed in quarantined plants (2003). Since side China (Ferguson and Bollard, 1990). Actinidia deli- that time a further 12 viruses have been identified in ki- ciosa cv. Hayward was selected around 1925 and ki- wifruit. We classify these 13 viruses into three groups. wifruit production started in New Zealand by 1930 The first group comprises the non-specialist viruses (Ferguson and Bollard, 1990). The original name ‘Chi- and includes Alfalfa mosaic virus (AMV) and Cucumber nese gooseberry’ was replaced by ‘kiwifruit’ when the mosaic virus (CMV) both members of the family Bro- first fruit were exported to the USA in 1959 (Ferguson moviridae. The group also includes a further five viruses and Bollard, 1990). The name ‘kiwifruit’ is now often that appear to have limited effect on kiwifruit: two to- used for all species within the genus Actinidia. Until bamoviruses, Ribgrass mosaic virus (RMV) and Turnip 2000 A. deliciosa ‘Hayward’ was the cultivar of choice, vein clearing virus (TVCV); a tombusvirus, Cucumber and almost all the international trade in kiwifruit was of necrosis virus (CNV); a novel potexvirus; and Apple this one cultivar. When facing overproduction in the stem gooving virus (ASGV, genus Capillovirus). Most of early 1990s, the New Zealand industry innovated and the viruses classified in this first group are cosmopolitan assessed the commercial potential of another species, and sometimes orchard weeds provide reservoirs for in- Actinidia chinensis (Ferguson and Huang, 2007). fection. A. deliciosa has fruit with green flesh and hairy skin, The second group comprises the kiwifruit-adapted while A. chinensis has smooth-skinned fruit and, usually, viruses. This group includes three novel viruses. i.e. two yellow flesh. Other differences include fruit flavour, vitiviruses, Actinidia virus A (AcVA) and Actinidia virus flower size, shoot hairiness, geographic distribution, B (AcVB), and a citrivirus closely related to Citrus leaf chromosome number, and leaf shape (Ferguson and blotch virus (CLBV). In addition, preliminary evidence Bollard, 1990). The introduction of the yellow-fleshed of a novel virus belonging to the Closteroviridae family A. chinensis cv. Hort16A, marketed under the Zespri has been obtained. Gold Kiwifruit brand, changed the industry by offering The third group of viruses induces disease in ki- a product that complemented, rather than competed wifruit. To date only two viruses have caused significant with, cv. Hayward resulting in increased consumption damage to kiwifruit within commercial orchards. In (Anonymous, 2012). Since 2000, most newly planted or- New Zealand, Cherry leaf roll virus (CLRV) has been chards in New Zealand have been A. chinensis and cv. detected on kiwifruit associated with symptoms includ- Hort16A now represents about 26% of the New ing leaf spots, fruit malformation, reduction in yield, Zealand export of kiwifruit (Anonymous, 2012). Other yellow-fleshed A. chinensis have now been commer- cialised in a number of countries, including cvs Jintao or ENZAGold™. About 30% of kiwifruit planted in China is now A. chinensis (Ferguson and Seal, 2008). Corresponding author: A.G. Blouin The success of the yellow and, subsequently, a red- Fax: +64.9.9257001 E-mail: [email protected] fleshed A. chinensis, combined with the need to intro- 001_JPP_Review_221_colore 30-07-2013 16:52 Pagina 222 222 Viruses of kiwifruit Journal of Plant Pathology (2013), 95 (2), 221-235 Fig. 1. Kiwifruit production worldwide past 20 years (after Belrose Inc., 2012). Data from world kiwifruit review 2012 based on predicted production for 2012. Production for 1999-2002 is in dark grey with a total production of 1,152,578 tons. The predicted production for 2009-2012 is in light grey with a total of 1,862,487 tons. duce novelty into the market, has intensified breeding all cv. Hort16A plantings in New Zealand, and possibly programmes in New Zealand, Italy and China. This in other producing countries, could be removed be- breeding activity has resulted in more plant movement cause of the cultivar’s vulnerability to the disease between countries. Despite the development of new va- (Anonymous, 2012; Young, 2012) resulting in an urgent rieties, ‘Hayward’ is still the predominant fruit traded need for new resistant cultivars. internationally, comprising an estimated 90–95% of the Although there were some reports of virus-like symp- worldwide kiwifruit market (Ferguson and Seal, 2008). toms, no viruses were identified in kiwifruit before International kiwifruit production is concentrated in 2003. The first indication of a kiwifruit-infecting virus relatively few countries. The top four countries are Chi- comes from New Zealand quarantine records in 1983. na, Italy, New Zealand and Chile, which collectively Gary Wood, from the then Department of Industrial produce more than 80% of the world’s kiwifruit crop; and Scientific Research (DSIR, New Zealand), docu- the top ten producing countries represent more than mented local lesions observed on Chenopodium quinoa 96% of the world supply (Anonymous, 2012) (Fig. 1). after sap inoculation of kiwifruit imported from China Commercial production of kiwifruit in China has in- and held in quarantine. The infected kiwifruit plants creased steadily over the past two decades; now, China were either destroyed or died during thermotherapy (G. is the biggest producer, with more than 25% of the Wood, personal communication). world’s production. This has contributed to the 62% in- In the 1980s, as Italy was becoming an important ki- crease in total world production over the past 10 years wifruit producer with the second greatest area planted (Anonymous, 2012). worldwide, there were no records of viruses infecting Disease pressure is a new concept for the kiwifruit the crop. Caciagli and Lovisolo (1987) surveyed com- industry. Some fungal diseases were reported previously, mercial orchards for potential viral diseases and collect- such as Armillaria novae-zelandii in New Zealand ed samples from 100 symptomless A. deliciosa and one (Horner, 1992); Phomopsis sp. in Greece (Elena, 2009); plant of A. deliciosa that showed chlorotic mottling. The Cadophora melinii in Italy (Prodi et al., 2008); and verti- extracts from these plants were mechanically inoculated cillium wilt of gold kiwifruit in Chile (Auger et al., into four herbaceous indicators (C. quinoa, C. amaranti- 2009). To date, these pathogens tend to be localised. color, Nicotiana glutinosa and N. clevelandii). None of The recent detection of a virulent strain of the 404 inoculated indicator plants displayed symptoms. Pseudomonas syringae pv. actinidiae in Italy and New Additionally, the authors challenged young A. deliciosa Zealand (Ferrante and Scortichini, 2010; Everett et al., plants with 17 common viruses from Italy, including Al- 2011) has had disastrous consequences for the produc- falfa mosaic virus (AMV) and Cucumber mosaic virus tion of A. chinensis cv. Hort16A. Some anticipate that (CMV). Only three viruses, Tobacco necrosis virus 001_JPP_Review_221_colore 30-07-2013 16:52 Pagina 223 Journal of Plant Pathology (2013), 95 (2), 221-235 Blouin et al. 223 (TNV), Tobacco rattle virus (TRV) and CMV, induced identified in kiwifruit was detected by leaf symptoms, symptoms on the inoculated leaves of the kiwifruit, and transmission electron microscopy (TEM) and mechani- only CMV moved systemically. The authors concluded cal transmission to herbaceous indicators, and identified that kiwifruit may be resistant to virus infections. by DAS-ELISA, RT-PCR and sequencing of amplicons. A few years later, during a survey in the Fujian Other kiwifruit from the same consignment were subse- Province in China, Lin and Gao (1995) identified one quently studied further and new viruses were identified. plant showing a “mosaic disease” attributed to an To date, the viruses discovered in kiwifruit can be di- unidentified virus. Nitta and Ogasawara (1997) report- vided in three groups. The first group comprises AMV, ed evidence of a graft-transmissible
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