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Apple Scar Skin Viroid
C H A P T E R
21 Apple Scar Skin Viroid Ahmed Hadidi1, Marina Barba2, Ni Hong3 and Vipin Hallan4 1
U.S. Department of Agriculture, Beltsville, MD, United States 2CREAResearch Centre for Plant Protection and Certification, Rome, Italy 3 Huazhong Agricultural University, Wuhan, China 4CSIR-Institute of Himalayan Bioresource Technology, Palampur, Himachal Pradesh, India
INTRODUCTION Apple scar skin disease was first reported from China in the 1930s (Ohtsuka, 1935, 1938), then from Japan in 1953 (Ushirozawa et al., 1968). The viroid etiology of the disease was suggested in the 1980s (Koganezawa, 1985, 1986) and its causal agent, apple scar skin viroid (ASSVd) from Japan and China, was purified, cloned, and sequenced (Hashimoto and Koganezawa, 1987; Puchta et al., 1990).
TAXONOMIC POSITION AND NUCLEOTIDE SEQUENCE Apple scar skin viroid (Hashimoto and Koganezawa, 1987) is the type species of the genus Apscaviroid, family Pospiviroidae (Owens et al., 2012; Chapter 13: Viroid Taxonomy). Table 21.1 describes nucleotide sequence information of known ASSVd variants that infect apple, pear, apricot, peach, sweet cherry, and Himalayan wild cherry. Most deletions, insertions, and changes among variants of the viroid occur in regions corresponding to the pathogenicity and left terminal domains of ASSVd (i.e., Puchta et al., 1990; Shamloul et al., 2004; Yang et al., 1992; Zhu et al., 1995).
Viroids and Satellites. DOI: http://dx.doi.org/10.1016/B978-0-12-801498-1.00021-8
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TABLE 21.1 Characteristics, Size, and Sequence of ASSVd Variants From Naturally Infected Pome and Stone Fruit Trees Variant
Size (nt)
Remarks
Reference
Scar skin from Japan
330
From apple (reference variant)
Hashimoto and Koganezawa (1987)
Scar skin from China
329
From apple; differs from apple reference variant (Hashimoto and Koganezawa, 1987) at 4 nt positions
Puchta et al. (1990)
Scar skin from China
330
From apple; differs from another Chinese variant (Puchta et al., 1990) in one base insertion; differs from the apple reference variant at 3 nt positions
Yang et al. (1992)
Dapple apple from Canada
331
Shares 97% sequence identity with apple reference variant
Zhu et al. (1995)
Dapple apple from South Korea
331
Shares over 99% sequence identity with the apple reference variant; differs at one site, and 1 nt is inserted
Lee et al. (2001)
Dapple apple from India
330 or 331
Variants share 94% 100% sequence identity with each other. Two variants are identical to a Chinese variant; six variants share 99% sequence identity with a Korean variant. Two variants are similar to a Chinese and a Japanese variants
Walia et al. (2009)
Symptomless pear from China
330
Differs from apple reference variant at 4 nt positions
Zhu et al. (1995)
Pear rusty skin from China
334
Shares 92% sequence identity with apple reference variant and differs at 25 nt positions
Zhu et al. (1995)
Pear fruit dimple from Japan
330
Differs from apple reference variant at 3 nt positions
Osaki et al. (1996)
Pear fruit crinkle from China
333
Shares 95% sequence identity with apple reference variant and differs at 19 nt positions. Shares 92% sequence identity with pear rusty skin reference variant and differs at 27 nt positions. Differs from pear fruit crinkle reference variant at 6 nt sites
Shamloul et al. (2004)
(Continued)
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TABLE 21.1
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(Continued)
Variant
Size (nt)
Remarks
Reference
Variants from apple and pear, from Iran
329 334
Variants form a cluster distinct from other variants
Yazarlou et al. (2012)
Variants from apple, pear, apricot and peach from China
315 330 (apple)
From Xinjiang Province; variants from apple, pear, peach, and apricot share 98%, 89%, 98%, 98% sequence identity, respectively, with apple scar skin variant from China (Puchta et al., 1990)
Wang et al. (2012)
250 327 (pear) 330 (apricot) 330 332 (peach)
Variants from sweet cherry from Greece
327 340
Differ from apple reference variant at up to 29 positions
Kaponi et al. (2010, 2013)
Variants from Himalayan wild cherry from India
330
Variants share 91% 98% sequence identity with sweet cherry variants from Greece and differ at 10 30 positions; differ from the apple reference variant at up to 18 positions
Walia et al. (2012)
ECONOMIC SIGNIFICANCE Apple scar skin disease in apple caused severe losses in China in the 1950s, especially in the Liadong peninsula area and several provinces (Liu et al., 1957), where thousands of trees were affected and apple fruits were rendered unmarketable. Recently, the disease has become problematic for the production of cultivar “Red Fuji” in China, which became the main apple cultivar after it was introduced from Japan (N. Hong, unpublished). In Japan in the 1970s, the disease was observed in major apple growing areas, however, it was sporadic; diseased fruits lost their market value (Koganezawa et al., 2003). The disease was also reported from several regions in South Korea (Lee et al., 2001; Kim et al., 2010), as well as from the Indian State of Himachal Pradesh (Walia et al., 2009). Affected fruits are significantly downgraded. Many pear trees in China and Japan are infected latently with ASSVd (Hadidi and Barba, 2011). These trees may be the source of viroid infection to apple trees that eventually will develop scar skin and/or dapple symptoms (Liu et al., 1957, 1962, 1985; Ohtsuka, 1935). Also, latently infected, cultivated or wild pear trees in Greece may infect susceptible
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pear cultivars and induce fruit symptoms (Kyriakopoulou et al., 2003). ASSVd infection in pear trees causes pear rusty skin and pear fruit crinkle diseases in China (Chen et al., 1987; Shamloul et al., 2003, 2004; Zhu et al., 1995), pear fruit dimple disease in Japan (Osaki et al., 1996), and diseased pear in Greece (Kyriakopoulou and Hadidi, 1998; Kyriakopoulou et al., 2001, 2003). Blemished fruit are reduced in value and become unmarketable.
SYMPTOMS The expression of apple scar skin and/or dapple apple fruit symptoms may be related to the apple cultivar (Koganezawa et al., 2003). Scar skin symptoms appear on cultivars such as “Ralls Janet,” “Indo,” and “Golden Delicious,” while dapple symptoms generally appear on red-skinned cultivars such as “Jonathan,” “Red Gold,” and “Red Fuji.” Both types of symptoms may appear on “Starking Delicious” and “Red Delicious.” Fig. 21.1 shows dapple apple symptoms on “Red Fuji” during the fruit coloring stage. The dappling symptoms become less obvious every subsequent year while the scar skin symptoms become more
FIGURE 21.1 Dapple apple symptoms on apple cultivar “Red Fuji” fruit caused by ASSVd. Source: Courtesy WenXing Xu.
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pronounced (Yamaguchi and Yanase, 1976). Fig. 21.2 shows scar skin symptoms on “Golden Delicious.” Leaf roll or leaf epinasty symptoms may develop, under certain conditions, on certain apple cultivars such as “Stark’s Earliest,” “Sugar Crab,” and “Ralls Janet” (Chen et al., 1988a; Ito and Yoshida, 1993; Liu et al., 1957; Skrzeczkowski et al., 1993). Pear rusty skin disease symptoms are restricted to the fruit of Chinese pears such as cultivar “Muoli.” Similar disease symptoms were observed on fruit of the Italian cultivar “Passacrassana” grafted on quince rootstocks in central Italy (Kyriakopoulou et al., 2001). Pear fruit crinkle disease is characterized by crinkling symptoms on fruit of the Chinese pear cultivars “Xuehuali” and “Yali” in Hebei Province (Shamloul et al., 2004). Pear fruit dimple disease symptoms in Japan are restricted to fruits of the Japanese pear cultivars “Nitaka” and “Yoshino” (Ohtsu et al., 1990). Symptoms of ASSVd infection on Greek pear cultivars and wild pears are also observed on fruit and include russet, scarring, and cracking (Kyriakopoulou et al., 2001). ASSVd-infected bean leaves develop interveinal chlorotic symptoms whether inoculated with ASSVd infectious transcripts or with viroidliferous whiteflies (Walia et al., 2015).
FIGURE 21.2
Scar skin symptoms on apple cultivar “Golden Delicious” fruit.
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HOST RANGE ASSVd naturally infects apple, wild apple (Malus sylvestris), pear, wild pear (Pyrus amygdaliformis), apricot, and sweet cherry trees (Hadidi and Barba, 2011), as well as peach (Wang et al., 2012) and Himalayan wild cherry (Prunus cerasoides) trees (Walia et al., 2012). Grafting experiments showed that the viroid also infects species of Malus, Pyrus, Sorbus, Chaenomeles, Cydonia, and Pyronia (Desvignes et al., 1999). Using genetic engineering approaches (see ’’Section Transmission’’) Walia et al. (2014) extended the host range of ASSVd to herbaceous hosts which include cucumber, tomato, garden pea, eggplant, Nicotiana benthamiana, N. tabacum, N. glutinosa, Chenopodium quinoa, and C. amaranticolor.
TRANSMISSION ASSVd is transmitted by grafting to apple (Chen et al., 1988b; Kim et al., 2006) and pear seedlings (Chen et al., 1988b), by razor slashing of apple seedlings with viroid RNA (Koganezawa, 1985; Koganezawa et al., 1982), and by using (viroid-contaminated) pruning tools dipped in crude sap of infected stem to both lignified stems and green shoots of apple trees and seedlings (Kim et al., 2006). However, it was not transmitted by knife cutting to Japanese pear (Osaki et al., 1996). ASSVd may spread naturally from infected trees to uninfected neighboring trees (Desvignes et al., 1999; Ohtsuka, 1935; Ushirozawa et al., 1968). The mechanism of this transmission is unclear but it may be due to root grafting. The viroid is transmitted in Greece by grafting onto infected wild pear, traditional pear, and other pome fruit rootstocks and spreads through the use of infected propagation material (Kyriakopoulou et al., 2001). ASSVd is seed borne in apple (Hadidi et al., 1991; Kim et al., 2006), but viroid transmission from apple seeds to seedlings was reported to be negative (Desvignes et al., 1999; Howell et al., 1995). However, Kim et al. (2006) showed that seedlings germinated from ASSVd-positive apple seeds demonstrated a 7.7% infection rate. ASSVd in oriental pear was either not seed transmitted or transmitted at a low rate (Hurtt and Podleckis, 1995). ASSVd is transmitted by agroinfection of ASSVd recombinant constructs to apple and pear seedlings (Zhu et al., 1998) and to nine herbaceous plant species by mechanical inoculation of in vitro ASSVd dimeric transcripts and to a lesser degree by dimeric DNA plasmids or sap inoculation (Walia et al., 2014).
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Recently it has been shown that ASSVd is transmitted by the greenhouse whitefly Trialeurodes vaporariorum to herbaceous plant species such as bean and cucumber (Walia et al., 2015). Both viroid RNA and DNA forms were identified in viruliferous insects. The viroid transfer efficiency was enhanced with the help of Cucumis sativus phloem protein 2 (CsPP2), which is known to translocate viroid RNAs. This PP2/ ASSVd complex is stably present in the viroid infected cucumber plants (Walia et al., 2015).
GEOGRAPHICAL DISTRIBUTION AND EPIDEMIOLOGY Fig. 21.3 shows the geographical distribution of ASSVd worldwide. Apple scar skin disease in apple is prevalent in China and Japan (Hadidi and Barba, 2011). The disease was also reported from South Korea (Kim et al., 2010), India (Behl et al., 1998; Thakur et al., 1995; Walia et al., 2009), and Iran (Yazarlou et al., 2012). It was also reported from the United States, Canada, and the United Kingdom, but its incidence is rare in these countries; it is extremely rare in Italy, France, and Germany (Hadidi and Barba, 2011). It was recently reported from Argentina (Nome et al., 2012). Dapple apple disease was reported from the United States, Canada, the United Kingdom, China, and Japan (Hadidi and Barba, 2011), and South Korea (Kim et al., 2006, 2010; Lee et al., 2001). Many pear trees in China are latently infected with ASSVd (Liu et al., 1962; Zhu et al.,
FIGURE 21.3
Geographical distribution of ASSVd worldwide.
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1995). In the early 1960s nearly 90% of the pear trees were viroidinfected in China (Liu et al., 1962). ASSVd-infected pear fruits with rusty skin or fruit crinkle symptoms have been reported repeatedly from China during the last three decades (Chen et al., 1987; Shamloul et al., 2003, 2004; Zhu et al., 1995). About 14% of pear trees from several provinces in China were positive for ASSVd infection (Hong et al., 2012). The incidence of ASSVd-infected pear trees in Namyangju and Ulsan regions in South Korea were 1.2% and 1.4%, respectively (Kim et al., 2010). Pear fruit dimple diseased trees infected with ASSVd were found in “Niitaka” and “Yoshino” cultivars in Chiba, Ibaraki, and Oita prefectures in Japan, and the viroid was thought to spread by grafting (Osaki et al., 1996). ASSVd in pear fruits affected with rusty skin-like symptoms was reported from central Italy (Kyriakopoulou et al., 2001). In Greece, several pear cultivars and wild pear trees were found infected with ASSVd (Kyriakopoulou et al., 2001). ASSVd was reported from apricot and peach in China (Wang et al., 2012; Zhao and Niu, 2008), sweet cherry in Greece (Kaponi et al., 2010, 2013), and Himalayan wild cherry in India (Walia et al., 2012).
DETECTION Field and greenhouse biological indexing of ASSVd from apple or pear trees has been described (Hadidi and Barba, 2011). These assays may need 2 3 years for developing fruit symptoms in the field or 2 3 months for apple indicators to develop leaf epinasty and curling in the greenhouse. Greenhouse indexing of ASSVd from pear trees can be done by biological indexing followed by molecular hybridization (Hurtt et al., 1992). ASSVd may be detected in infected tissues by standard, return, twodimensional, or bidirectional polyacrylamide gel electrophoretic analysis of the extracted RNAs (Hanold et al., 2011; Chapter 34: Gel Electrophoresis). Unlike biological indexing, these assays are rapid, and easy to perform. ASSVd variants may also be detected by different methods of molecular hybridization (Hadidi and Yang, 1990; Hadidi et al., 1990; Hurtt et al., 1992; Kyriakopoulou and Hadidi, 1998; Kyriakopoulou et al., 2001; Podleckis et al., 1993; Walia et al., 2014; Zhu et al., 1998; Chapter 35: Molecular Hybridization Techniques for Detecting and Studying Viroids). Different methods of RT-PCR (Hadidi and Candresse, 2003; Hadidi et al., 2011; Kim et al., 2010; Kumar et al., 2013; Chapter 36: Viroid Amplification Methods: RT-PCR, Real- Time RT-PCR, and RTLAMP) are very sensitive for detecting ASSVd and other viroids from
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different plant species (Hadidi et al., 2011). ASSVd was also detected by nucleic acid sequence-based amplification with electrochemiluminescence (NASB-ECL) (Kim et al., 2006). Microarrays and next-generation sequencing have not yet been applied for detecting ASSVd, however, they have been used for detecting other viroids (Chapter 37: Detection and Identification of Viroids by Microarrays and Chapter 38: Application of Next-Generation Sequencing Technologies to Viroids).
CONTROL Quarantine programs in many developed countries require ASSVd assays for imported pome fruit germplasm to prevent its introduction and/or spread to local susceptible plant species. Moreover, pome and stone fruit trees are among plants covered by certification schemes in many countries (Roy, 2011); thus, nursery stocks of apple, pear, and other host species must be propagated from mother trees indexed as free of ASSVd (Barba et al., 2003). ASSVd-infected trees in orchards should be removed to avoid possible spread of the viroid to neighboring trees by root grafting or other means. The standard thermotherapy treatment (70 days exposure at 38 C) was successful in obtaining ASSVd-free apple plants (Howell et al., 1998). About 90% of plants were ASSVd-free when the thermotherapy treatment (48 days at 37 C) was preceded by keeping apple plants dormant for 3 months at 4 C in cool chambers (Desvignes et al., 1999). The viroid was successfully eliminated from infected pear by in vitro therapy and apical meristem culture (Postman and Hadidi, 1995). Dipping ASSVd-contaminated pruning tools in 2% sodium hypochlorite solution, (Clorox regular bleach production contains 6.0% solution of sodium hypochlorite), prevented viroid transmission (Kim et al., 2006).
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Jelkmann, W. (Eds.), Virus and Virus-Like Diseases of Pome and Stone Fruits. APS Press, St. Paul, MN, pp. 407 413. Shamloul, A.M., Yang, X., Han, L., Hadidi, A., 2004. Characterization of a new variant of apple scar skin viroid associated with pear fruit crinkle disease. J. Plant. Pathol. 86, 249 256. Shamloul, A.M., Yang, X., Han, L., Hadidi, X., 2003. Pear fruit crinkle. In: Hadidi, A., Flores, R., Randles, J.W., Semancik, J.S. (Eds.), Viroids. CSIRO Publishing, Collingwood, VIC, pp. 327 329. Skrzeczkowski, L.J., Howell, W.E., Mink, G.I., 1993. Correlation between leaf epinasty symptoms on two apple cultivars and results of cRNA hybridization for detection of apple scar skin viroid. Plant Dis. 77, 919 921. Thakur, P.D., Ito, T., Sharma, J.N., 1995. Natural occurrence of a viroid disease of apple in India. Indian J. Virol. 11, 73 75. Ushirozawa, K., Tojo, Y., Takemae, S., Sekiguchi, A., 1968. Studies on apple scar skin disease (1) On transmission experiments. Bull. Nagano Hort. Res. Stn. Jpn. 9, 1 12 (in Japanese with English summary). Walia, Y., Dhir, S., Bhadoria, S., Hallan, V., Zaidi, A.A., 2012. Molecular characterization of apple scar skin viroid from Himalayan wild cherry. Forest Pathol. 42, 84 87. Walia, Y., Dhir, S., Ram, R., Zaidi, A.A., Hallan, V., 2014. Identification of the herbaceous host range of apple scar skin viroid and analysis of its progeny variants. Plant Pathol. 63, 684 690. Walia, Y., Dhir, S., Zaidi, A.A., Hallan, V., 2015. Apple scar skin viroid naked RNA is actively transmitted by the whitefly Trialeurodes vaporariorum. RNA Biol. 12 (10), 1 8. Walia, Y., Kumar, Y., Rana, T., Bhardwaj, P., Ram, R., Thakur, P.D., et al., 2009. Molecular characterization and variability analysis of apple scar skin viroid in India. J. Gen. Plant Pathol. 75, 307 311. Wang, Y., Zhao, Y., Niu, J., 2012. Molecular identification and sequence analysis of the apple scar skin viroid (ASSVd) isolated from four kinds of fruit trees in Xinjiang province of China. Mol. Pathogens 3, 12 18. Yamaguchi, A., Yanase, H., 1976. Possible relationship between the causal agent of dapple apple and scar skin. Acta Hortic. 67, 249 254. Yang, X., Hadidi, A., Hammond, R.W., 1992. Nucleotide sequence of apple scar skin viroid reverse-transcribed in host extracts and amplified by the polymerase chain reaction. Acta Hortic. 309, 305 309. Yazarlou, A., Jafarpour, B., Habili, N., Randles, J.W., 2012. First detection and molecular characterization of new apple scar skin viroid variants from apple and pear in Iran. Australasian Plant Dis. Notes. 7, 99 102. Zhao, Y., Niu, J.X., 2008. Apricot is a new host of apple scar skin viroid. Australasian Plant Dis. Notes. 3, 98 100. Zhu, S.F., Hadidi, A., Hammond, R.W., Yang, X., Hansen, A.J., 1995. Nucleotide sequence and secondary structure of pome fruit viroids from dapple diseased apples, pear rusty skin diseased pears and apple scar skin symptomless pears. Acta Hortic. 386, 554 559. Zhu, S.F., Hammond, R.W., Hadidi, A., 1998. Agroinfection of pear and apple with dapple apple viroid results in systemic infection. Acta Hortic. 472, 613 616.
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21 Apple Scar Skin Viroid Ahmed Hadidi1, Marina Barba2, Ni Hong3 and Vipin Hallan4 1
U.S. Department of Agriculture, Beltsville, MD, United States 2CREAResearch Centre for Plant Protection and Certification, Rome, Italy 3 Huazhong Agricultural University, Wuhan, China 4CSIR-Institute of Himalayan Bioresource Technology, Palampur, Himachal Pradesh, India
INTRODUCTION Apple scar skin disease was first reported from China in the 1930s (Ohtsuka, 1935, 1938), then from Japan in 1953 (Ushirozawa et al., 1968). The viroid etiology of the disease was suggested in the 1980s (Koganezawa, 1985, 1986) and its causal agent, apple scar skin viroid (ASSVd) from Japan and China, was purified, cloned, and sequenced (Hashimoto and Koganezawa, 1987; Puchta et al., 1990).
TAXONOMIC POSITION AND NUCLEOTIDE SEQUENCE Apple scar skin viroid (Hashimoto and Koganezawa, 1987) is the type species of the genus Apscaviroid, family Pospiviroidae (Owens et al., 2012; Chapter 13: Viroid Taxonomy). Table 21.1 describes nucleotide sequence information of known ASSVd variants that infect apple, pear, apricot, peach, sweet cherry, and Himalayan wild cherry. Most deletions, insertions, and changes among variants of the viroid occur in regions corresponding to the pathogenicity and left terminal domains of ASSVd (i.e., Puchta et al., 1990; Shamloul et al., 2004; Yang et al., 1992; Zhu et al., 1995).
Viroids and Satellites. DOI: http://dx.doi.org/10.1016/B978-0-12-801498-1.00021-8
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TABLE 21.1 Characteristics, Size, and Sequence of ASSVd Variants From Naturally Infected Pome and Stone Fruit Trees Variant
Size (nt)
Remarks
Reference
Scar skin from Japan
330
From apple (reference variant)
Hashimoto and Koganezawa (1987)
Scar skin from China
329
From apple; differs from apple reference variant (Hashimoto and Koganezawa, 1987) at 4 nt positions
Puchta et al. (1990)
Scar skin from China
330
From apple; differs from another Chinese variant (Puchta et al., 1990) in one base insertion; differs from the apple reference variant at 3 nt positions
Yang et al. (1992)
Dapple apple from Canada
331
Shares 97% sequence identity with apple reference variant
Zhu et al. (1995)
Dapple apple from South Korea
331
Shares over 99% sequence identity with the apple reference variant; differs at one site, and 1 nt is inserted
Lee et al. (2001)
Dapple apple from India
330 or 331
Variants share 94% 100% sequence identity with each other. Two variants are identical to a Chinese variant; six variants share 99% sequence identity with a Korean variant. Two variants are similar to a Chinese and a Japanese variants
Walia et al. (2009)
Symptomless pear from China
330
Differs from apple reference variant at 4 nt positions
Zhu et al. (1995)
Pear rusty skin from China
334
Shares 92% sequence identity with apple reference variant and differs at 25 nt positions
Zhu et al. (1995)
Pear fruit dimple from Japan
330
Differs from apple reference variant at 3 nt positions
Osaki et al. (1996)
Pear fruit crinkle from China
333
Shares 95% sequence identity with apple reference variant and differs at 19 nt positions. Shares 92% sequence identity with pear rusty skin reference variant and differs at 27 nt positions. Differs from pear fruit crinkle reference variant at 6 nt sites
Shamloul et al. (2004)
(Continued)
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TABLE 21.1
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(Continued)
Variant
Size (nt)
Remarks
Reference
Variants from apple and pear, from Iran
329 334
Variants form a cluster distinct from other variants
Yazarlou et al. (2012)
Variants from apple, pear, apricot and peach from China
315 330 (apple)
From Xinjiang Province; variants from apple, pear, peach, and apricot share 98%, 89%, 98%, 98% sequence identity, respectively, with apple scar skin variant from China (Puchta et al., 1990)
Wang et al. (2012)
250 327 (pear) 330 (apricot) 330 332 (peach)
Variants from sweet cherry from Greece
327 340
Differ from apple reference variant at up to 29 positions
Kaponi et al. (2010, 2013)
Variants from Himalayan wild cherry from India
330
Variants share 91% 98% sequence identity with sweet cherry variants from Greece and differ at 10 30 positions; differ from the apple reference variant at up to 18 positions
Walia et al. (2012)
ECONOMIC SIGNIFICANCE Apple scar skin disease in apple caused severe losses in China in the 1950s, especially in the Liadong peninsula area and several provinces (Liu et al., 1957), where thousands of trees were affected and apple fruits were rendered unmarketable. Recently, the disease has become problematic for the production of cultivar “Red Fuji” in China, which became the main apple cultivar after it was introduced from Japan (N. Hong, unpublished). In Japan in the 1970s, the disease was observed in major apple growing areas, however, it was sporadic; diseased fruits lost their market value (Koganezawa et al., 2003). The disease was also reported from several regions in South Korea (Lee et al., 2001; Kim et al., 2010), as well as from the Indian State of Himachal Pradesh (Walia et al., 2009). Affected fruits are significantly downgraded. Many pear trees in China and Japan are infected latently with ASSVd (Hadidi and Barba, 2011). These trees may be the source of viroid infection to apple trees that eventually will develop scar skin and/or dapple symptoms (Liu et al., 1957, 1962, 1985; Ohtsuka, 1935). Also, latently infected, cultivated or wild pear trees in Greece may infect susceptible
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pear cultivars and induce fruit symptoms (Kyriakopoulou et al., 2003). ASSVd infection in pear trees causes pear rusty skin and pear fruit crinkle diseases in China (Chen et al., 1987; Shamloul et al., 2003, 2004; Zhu et al., 1995), pear fruit dimple disease in Japan (Osaki et al., 1996), and diseased pear in Greece (Kyriakopoulou and Hadidi, 1998; Kyriakopoulou et al., 2001, 2003). Blemished fruit are reduced in value and become unmarketable.
SYMPTOMS The expression of apple scar skin and/or dapple apple fruit symptoms may be related to the apple cultivar (Koganezawa et al., 2003). Scar skin symptoms appear on cultivars such as “Ralls Janet,” “Indo,” and “Golden Delicious,” while dapple symptoms generally appear on red-skinned cultivars such as “Jonathan,” “Red Gold,” and “Red Fuji.” Both types of symptoms may appear on “Starking Delicious” and “Red Delicious.” Fig. 21.1 shows dapple apple symptoms on “Red Fuji” during the fruit coloring stage. The dappling symptoms become less obvious every subsequent year while the scar skin symptoms become more
FIGURE 21.1 Dapple apple symptoms on apple cultivar “Red Fuji” fruit caused by ASSVd. Source: Courtesy WenXing Xu.
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pronounced (Yamaguchi and Yanase, 1976). Fig. 21.2 shows scar skin symptoms on “Golden Delicious.” Leaf roll or leaf epinasty symptoms may develop, under certain conditions, on certain apple cultivars such as “Stark’s Earliest,” “Sugar Crab,” and “Ralls Janet” (Chen et al., 1988a; Ito and Yoshida, 1993; Liu et al., 1957; Skrzeczkowski et al., 1993). Pear rusty skin disease symptoms are restricted to the fruit of Chinese pears such as cultivar “Muoli.” Similar disease symptoms were observed on fruit of the Italian cultivar “Passacrassana” grafted on quince rootstocks in central Italy (Kyriakopoulou et al., 2001). Pear fruit crinkle disease is characterized by crinkling symptoms on fruit of the Chinese pear cultivars “Xuehuali” and “Yali” in Hebei Province (Shamloul et al., 2004). Pear fruit dimple disease symptoms in Japan are restricted to fruits of the Japanese pear cultivars “Nitaka” and “Yoshino” (Ohtsu et al., 1990). Symptoms of ASSVd infection on Greek pear cultivars and wild pears are also observed on fruit and include russet, scarring, and cracking (Kyriakopoulou et al., 2001). ASSVd-infected bean leaves develop interveinal chlorotic symptoms whether inoculated with ASSVd infectious transcripts or with viroidliferous whiteflies (Walia et al., 2015).
FIGURE 21.2
Scar skin symptoms on apple cultivar “Golden Delicious” fruit.
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HOST RANGE ASSVd naturally infects apple, wild apple (Malus sylvestris), pear, wild pear (Pyrus amygdaliformis), apricot, and sweet cherry trees (Hadidi and Barba, 2011), as well as peach (Wang et al., 2012) and Himalayan wild cherry (Prunus cerasoides) trees (Walia et al., 2012). Grafting experiments showed that the viroid also infects species of Malus, Pyrus, Sorbus, Chaenomeles, Cydonia, and Pyronia (Desvignes et al., 1999). Using genetic engineering approaches (see ’’Section Transmission’’) Walia et al. (2014) extended the host range of ASSVd to herbaceous hosts which include cucumber, tomato, garden pea, eggplant, Nicotiana benthamiana, N. tabacum, N. glutinosa, Chenopodium quinoa, and C. amaranticolor.
TRANSMISSION ASSVd is transmitted by grafting to apple (Chen et al., 1988b; Kim et al., 2006) and pear seedlings (Chen et al., 1988b), by razor slashing of apple seedlings with viroid RNA (Koganezawa, 1985; Koganezawa et al., 1982), and by using (viroid-contaminated) pruning tools dipped in crude sap of infected stem to both lignified stems and green shoots of apple trees and seedlings (Kim et al., 2006). However, it was not transmitted by knife cutting to Japanese pear (Osaki et al., 1996). ASSVd may spread naturally from infected trees to uninfected neighboring trees (Desvignes et al., 1999; Ohtsuka, 1935; Ushirozawa et al., 1968). The mechanism of this transmission is unclear but it may be due to root grafting. The viroid is transmitted in Greece by grafting onto infected wild pear, traditional pear, and other pome fruit rootstocks and spreads through the use of infected propagation material (Kyriakopoulou et al., 2001). ASSVd is seed borne in apple (Hadidi et al., 1991; Kim et al., 2006), but viroid transmission from apple seeds to seedlings was reported to be negative (Desvignes et al., 1999; Howell et al., 1995). However, Kim et al. (2006) showed that seedlings germinated from ASSVd-positive apple seeds demonstrated a 7.7% infection rate. ASSVd in oriental pear was either not seed transmitted or transmitted at a low rate (Hurtt and Podleckis, 1995). ASSVd is transmitted by agroinfection of ASSVd recombinant constructs to apple and pear seedlings (Zhu et al., 1998) and to nine herbaceous plant species by mechanical inoculation of in vitro ASSVd dimeric transcripts and to a lesser degree by dimeric DNA plasmids or sap inoculation (Walia et al., 2014).
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Recently it has been shown that ASSVd is transmitted by the greenhouse whitefly Trialeurodes vaporariorum to herbaceous plant species such as bean and cucumber (Walia et al., 2015). Both viroid RNA and DNA forms were identified in viruliferous insects. The viroid transfer efficiency was enhanced with the help of Cucumis sativus phloem protein 2 (CsPP2), which is known to translocate viroid RNAs. This PP2/ ASSVd complex is stably present in the viroid infected cucumber plants (Walia et al., 2015).
GEOGRAPHICAL DISTRIBUTION AND EPIDEMIOLOGY Fig. 21.3 shows the geographical distribution of ASSVd worldwide. Apple scar skin disease in apple is prevalent in China and Japan (Hadidi and Barba, 2011). The disease was also reported from South Korea (Kim et al., 2010), India (Behl et al., 1998; Thakur et al., 1995; Walia et al., 2009), and Iran (Yazarlou et al., 2012). It was also reported from the United States, Canada, and the United Kingdom, but its incidence is rare in these countries; it is extremely rare in Italy, France, and Germany (Hadidi and Barba, 2011). It was recently reported from Argentina (Nome et al., 2012). Dapple apple disease was reported from the United States, Canada, the United Kingdom, China, and Japan (Hadidi and Barba, 2011), and South Korea (Kim et al., 2006, 2010; Lee et al., 2001). Many pear trees in China are latently infected with ASSVd (Liu et al., 1962; Zhu et al.,
FIGURE 21.3
Geographical distribution of ASSVd worldwide.
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1995). In the early 1960s nearly 90% of the pear trees were viroidinfected in China (Liu et al., 1962). ASSVd-infected pear fruits with rusty skin or fruit crinkle symptoms have been reported repeatedly from China during the last three decades (Chen et al., 1987; Shamloul et al., 2003, 2004; Zhu et al., 1995). About 14% of pear trees from several provinces in China were positive for ASSVd infection (Hong et al., 2012). The incidence of ASSVd-infected pear trees in Namyangju and Ulsan regions in South Korea were 1.2% and 1.4%, respectively (Kim et al., 2010). Pear fruit dimple diseased trees infected with ASSVd were found in “Niitaka” and “Yoshino” cultivars in Chiba, Ibaraki, and Oita prefectures in Japan, and the viroid was thought to spread by grafting (Osaki et al., 1996). ASSVd in pear fruits affected with rusty skin-like symptoms was reported from central Italy (Kyriakopoulou et al., 2001). In Greece, several pear cultivars and wild pear trees were found infected with ASSVd (Kyriakopoulou et al., 2001). ASSVd was reported from apricot and peach in China (Wang et al., 2012; Zhao and Niu, 2008), sweet cherry in Greece (Kaponi et al., 2010, 2013), and Himalayan wild cherry in India (Walia et al., 2012).
DETECTION Field and greenhouse biological indexing of ASSVd from apple or pear trees has been described (Hadidi and Barba, 2011). These assays may need 2 3 years for developing fruit symptoms in the field or 2 3 months for apple indicators to develop leaf epinasty and curling in the greenhouse. Greenhouse indexing of ASSVd from pear trees can be done by biological indexing followed by molecular hybridization (Hurtt et al., 1992). ASSVd may be detected in infected tissues by standard, return, twodimensional, or bidirectional polyacrylamide gel electrophoretic analysis of the extracted RNAs (Hanold et al., 2011; Chapter 34: Gel Electrophoresis). Unlike biological indexing, these assays are rapid, and easy to perform. ASSVd variants may also be detected by different methods of molecular hybridization (Hadidi and Yang, 1990; Hadidi et al., 1990; Hurtt et al., 1992; Kyriakopoulou and Hadidi, 1998; Kyriakopoulou et al., 2001; Podleckis et al., 1993; Walia et al., 2014; Zhu et al., 1998; Chapter 35: Molecular Hybridization Techniques for Detecting and Studying Viroids). Different methods of RT-PCR (Hadidi and Candresse, 2003; Hadidi et al., 2011; Kim et al., 2010; Kumar et al., 2013; Chapter 36: Viroid Amplification Methods: RT-PCR, Real- Time RT-PCR, and RTLAMP) are very sensitive for detecting ASSVd and other viroids from
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different plant species (Hadidi et al., 2011). ASSVd was also detected by nucleic acid sequence-based amplification with electrochemiluminescence (NASB-ECL) (Kim et al., 2006). Microarrays and next-generation sequencing have not yet been applied for detecting ASSVd, however, they have been used for detecting other viroids (Chapter 37: Detection and Identification of Viroids by Microarrays and Chapter 38: Application of Next-Generation Sequencing Technologies to Viroids).
CONTROL Quarantine programs in many developed countries require ASSVd assays for imported pome fruit germplasm to prevent its introduction and/or spread to local susceptible plant species. Moreover, pome and stone fruit trees are among plants covered by certification schemes in many countries (Roy, 2011); thus, nursery stocks of apple, pear, and other host species must be propagated from mother trees indexed as free of ASSVd (Barba et al., 2003). ASSVd-infected trees in orchards should be removed to avoid possible spread of the viroid to neighboring trees by root grafting or other means. The standard thermotherapy treatment (70 days exposure at 38 C) was successful in obtaining ASSVd-free apple plants (Howell et al., 1998). About 90% of plants were ASSVd-free when the thermotherapy treatment (48 days at 37 C) was preceded by keeping apple plants dormant for 3 months at 4 C in cool chambers (Desvignes et al., 1999). The viroid was successfully eliminated from infected pear by in vitro therapy and apical meristem culture (Postman and Hadidi, 1995). Dipping ASSVd-contaminated pruning tools in 2% sodium hypochlorite solution, (Clorox regular bleach production contains 6.0% solution of sodium hypochlorite), prevented viroid transmission (Kim et al., 2006).
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