Australasian Plant Pathology https://doi.org/10.1007/s13313-018-0592-6 REVIEW A review of the status of Avocado sunblotch viroid in Australia Andrew D. W. Geering1 Received: 20 June 2018 /Accepted: 23 August 2018 # Australasian Plant Pathology Society Inc. 2018 Abstract Avocado sunblotch viroid (ASBVd) can seriously impact both the yield and quality of avocado fruit and is also a serious impediment to international trade because of quarantine conditions imposed by importing countries. The Australian avocado industry was among the first in the world to adopt control measures for ASBVd, an outcome of distinguished research done by Australian scientists during the 1970–80s. The status of ASBVd in Australia has not been recently reviewed and much infor- mation is either not published or difficult to find. In this review, this information has been collated and comment made on historical distribution and prevalence, in order to guide future surveys and to allow evaluation of the success of the control programs. Keywords Avocado nursery voluntary accreditation scheme . ANVAS . Diagnosis . Biosecurity . Incursion pathway . Surveys Introduction although the disease was initially attributed to sunburn dam- age (Coit 1928) and then an infectious agent, probably a virus Only two subcellular pathogens of avocado (Persea americana) (Horne and Parker 1931; Whitsell 1952). The hypothesis for a are known to science, these being Avocado sunblotch viroid viral aetiology persisted for nearly 50 years, until three inde- (ASBVd; genus Avsunviroid)andPotato spindle tuber viroid pendent laboratories in Adelaide, Brisbane and Auckland, ob- (PSTVd; genus Pospiviroid). ASBVd is the most economically served the presence of viroid-like RNA in diseased plants important of the two with respect to the avocado industry, al- (Dale and Allen 1979; Palukaitis et al. 1979; Thomas and though PSTVd has a much wider host range and is primarily of Mohamed 1979), although infectivity of the RNA and fulfil- importance to the vegetable and ornamental plant industries ment of Koch’s Postulates were not demonstrated until 2 years (Owens and Verhoeven 2017). PSTVd has only ever been re- later (Allen et al. 1981). Other very significant outputs from corded infecting avocado in Peru (Querci et al. 1995), and this this research were the first entire nucleotide sequence for the unusual host-pathogen interaction is thought to be a conse- viroid (Symons 1981), elucidation of the replication cycle quence of the practice of intercropping avocados with potatoes, (Bruening et al. 1982; Hutchins et al. 1985, 1986; Forster which are an important reservoir of the viroid. ASBVd is present et al. 1988; Bonfiglioli et al. 1994) and development of rapid in Australia, Ghana, Greece, Israel, Mexico, Peru, South Africa, and sensitive molecular diagnostic methods (Allen and Dale, Spain, the United States of America and Venezuela (Kuhn et al. 1981;Palukaitisetal.1981). 2017; Lotos et al. 2018). New Zealand, which is the only coun- The economic impacts of ASBVd are manyfold. try that is currently allowed to export fresh avocado fruit to Apparently asymptomatic strains of the viroid can still re- Australia, has declared nationwide freedom from the pathogen duce yield of ‘Hass’ trees by 15–30%, and yield reductions (Pugh and Thomson 2009). are even greater for symptomatic strains, at 50–80% Australasian scientists were responsible for many (Saucedo-Carabez et al. 2014). Furthermore, about half of pioneering discoveries on ASBVd. Sunblotch disease was the fruit from symptomatic trees may be scarred and there- first described in the early twentieth century in California, fore significantly downgraded in quality. ASBVd is also an impediment to trade due to quarantine conditions imposed on the movement of fresh fruit due to the risk of transmit- * Andrew D. W. Geering ting the viroid in the seed. [email protected] Although ASBVd is known to occur in Australia, its status has not been recently reviewed. The aim of this paper is to 1 Queensland Alliance for Agriculture and Food Innovation, The University of Queensland, St. Lucia, QLD 4072, Australia provide comment on the geographical distribution and A. Geering prevalence of ASBVd in Australia in order to guide future industry established in south-east Queensland, with the plant- surveys and to assess the success of current control methods. ing of 100 seedling trees on the Blackall Range in 1930, the importation of the first named varieties (grafted ‘Fuerte’ and ‘Nabal’ trees) to Redlands Bay from California in 1931 and Origin of ASBVd and possible entry pathway then the planting of an orchard on Tamborine Mountain in into Australia 1933 (Anderson 1977;Whiley2000). In 1967, sunblotch disease was reported for the first Avocado is the only known natural host of ASBVd and a time in Australia, in a ‘Mexicola’ tree grown at the NSW logical corollary is that the viroid originated in the same loca- Department of Agriculture Tropical Fruit Research Station, tion as its host, which is the eastern and central highlands of Alstonville, NSW, which had been propagated using Mexico, through Guatemala to the Pacific coast of Central budwood that had been obtained from Wilson’sNursery America and the northern parts of South America (Ayala on Tamborine Mountain, Queensland, in 1962 (Trochoulias Silva and Ledesma, 2014). The avocado industry in southern and Allen 1970; T. Trochoulias pers. comm., now retired from California began using germplasm that was mainly sourced NSW Department of Primary Industries). This variety was from the cities of Atlixco and Santiago de Querétaro in being trialled as a dwarfing interstock and disease symp- Mexico but also from Guatemala (Whitsell 1952). toms were observed both on the ‘Mexicola’ mother tree The earliest anecdotal record of sunblotch disease was at and ‘Fuerte’ scions that had been grafted onto ‘Mexicola’. the West India Gardens Nursery, Altadena, California, in 1914 In 1973, sunblotch disease was observed at a second lo- (Whitsell 1952), which was owned by Frederick Popenoe. In cation in the avocado varietal collection at the CSIRO 1911, Popenoe sent his son Wilson and employee Carl Horticultural Research Station, Merbein, about 10 km Schmidt on a collecting mission to Atlixco, and they brought west of Mildura, Victoria. The infection at Merbein was back 41 accessions, one of which became the variety ‘Fuerte’, considered to have originated from a tree (AV-2) that had the mainstay of the infant Californian industry (Bost et al. been imported from California in 1948 and used as a root- 2013). In 1948, the California Avocado Society BCommittee stock (Allen, 1981). It is likely that AV-2 was the acces- on Foreign Exploration^ surveyed the Rodiles Grove of avo- sion code for ‘Mexicola’,asAllen(1976) stated that the cados near Atlixco, and observed sunblotch disease symptoms infection in Merbein could be traced back to a ‘Mexicola’ in 30 year-old ‘Fuerte-like’ seedling trees (Trask 1948; tree at Alstonville. Whitsell 1952). Credence should be given to these observa- tions, as the expedition members were very familiar with the disease in their home state. This circumstantial evidence sug- Historical records of ASBVd in Australia gests that ASBVd could have inadvertently been introduced to California from Mexico by the early botanical explorers. ASBVd appears to have always been very rare in Australia. However, it was not until 2009 that ASBVd was officially Initial characterization work was done with viroid isolates reported from Mexico (De La Torre et al. 2009) and contrary from trees that were held at research stations at Merbein or to historical anecdotal evidence, the only verified records of Alstonville and both stations have now closed down. At ASBVd are from Michoacán State, where the pathogen is Alstonville, only a single infected ‘Fuerte’ tree (isolate SB-2 common in ‘Hass’ avocados (De La Torre et al. 2009; in Allen and Dale (1981)) was retained for any length of time Saucedo-Carabez et al. 2014; Vallejo Pérez et al. 2017). in the varietal collection, and this tree was destroyed once During the period 1920–50, ASBVd became very common experimental work was complete in the early 1980s (R. N. in southern California and was considered the second most Allen pers. comm., now retired from Queensland important pathogen of avocado after Phytophthora Department of Agriculture and Fisheries (QDAF)). Viroid cinnamomi (Whitsell 1952). Consequently, avocado varieties isolate SB-1 was maintained in glasshouse-grown plants at that were sourced from California at this time were at high risk Merbein and at the Waite Institute, Adelaide (Bruening et al. of being infected, often asymptomatically (Wallace and Drake 1982; J. W. Randles pers. comm., now retired from University 1962). In 1924, sunblotch disease was recorded for the first of Adelaide). time outside of the USA, in Israel, and this was in ‘Fuerte’ and Three surveys for ASBVd have been undertaken in ‘Dickinson’ trees that had been imported from California Australia. The first of these surveys was undertaken by (Whitsell 1952; footnote 2 in Horne and Parker (1931)). Palukaitis et al. (1981) and focussed on the Tristates produc- Almost certainly ASBVd was introduced into Australia by a tion area, centred on Mildura and including orchards in the similar pathway and possibly at a similar time. Commercial Murray River irrigation areas of Victoria, New South Wales avocado production began in Australia in 1928 at Red Cliffs, and South Australia. ASBVd was only detected in two com- Victoria, with the planting of 25 imported trees from mercial orchards, in a single ‘Hass’ tree from Red Cliffs, California (Cadman and El-Zeftawi 1977). Shortly after, the Victoria, and two ‘Zutano AV35’ trees from Coomealla, NSW. A review of the status of Avocado sunblotch viroid in Australia The second survey was undertaken by Dale and Allen ASBVd has never been found in South Australia or (1981) and included orchards in northern NSW and south- Western Australia (R.