Viroids and Satellites

By Ahmed Hadidi and Ricardo Flores

Viroids and Satellites describes plant diseases and their causal agents while also addressing the economic impact of these diseases. The book discusses various strategies for state-of-the-art methods for the detection and control of pathogens in their infected hosts and provides pivotal information from the discovery of viroids through the analysis of their molecular and biological properties, to viroid pathogenesis, host interactions, and RNA silencing pathways.

Students, researchers and regulators will find this to be a comprehensive resource on the topics presented.

• Provides coverage of the basic biological properties of disease, along with applied knowledge
• Features economic impacts, transmission, geographical distribution, epidemiology, detection, and control within each chapter
• Organizes viroid diseases by viroid taxonomy and viroid species

• Language: English
• Publisher: Academic Press
• Release date: Jul 18, 2017
• ISBN: 9780128017029

Book preview

satisfaction.

Section I

Viroids

Outline

Part I Viroids: Economic Significance

Part II Viroid Characteristics

Part III Viroid Diseases

Part IV Detection and Identification Methods

Part V Control Measures for Viroids and Viroid Diseases

Part VI Geographical Distribution of Viroids and Viroid Diseases

Part VII Special Topics

Part I

Viroids: Economic Significance

Outline

Chapter 1 Economic Significance of Viroids in Vegetable and Field Crops

Chapter 2 Economic Significance of Fruit Tree and Grapevine Viroids

Chapter 3 Economic Significance of Viroids in Ornamental Crops

Chapter 4 Economic Significance of Palm Tree Viroids

Chapter 1

Economic Significance of Viroids in Vegetable and Field Crops

Rosemarie W. Hammond,    U.S. Department of Agriculture, Beltsville, MD, United States

Abstract

Crop losses due to viroid infection occur in vegetable and field crops worldwide. Several viroids in the family Pospiviroidae infect these crops and economic losses range from minimal to severe depending upon the viroid/host combination, the host cultivar, the viroid strain and the environmental conditions. In this chapter, the impact of viroids in potato, tomato, cucumber, hop, and sweet pepper crops is summarized for each vegetable or field crop host and is followed by potential means of control to reduce losses caused by viroids.

Keywords

Potato; tomato; hop; vegetable; field crops; viroid

Introduction

Potato spindle tuber viroid (PSTVd) (Diener, 1971) was shown to be the causal agent of the potato spindle tuber disease described in the early 1920s in Irish Cobbler potato in North America (Martin, 1922). Members of the family Pospiviroidae cause disease in several other vegetable and field crops and the economic significance of viroid infection in these crops is a reflection of the symptoms they cause in their host that may affect crop quality and/or yield, their mode of transmission, their distribution and their ability to cause an epidemic (Randles, 2003). Although citrus exocortis viroid (CEVd) was detected in asymptomatic carrot, eggplant, and turnip in a survey of vegetable crops in Spain (Fagoaga and Duran-Vila, 1996), and PSTVd was detected in pepino (Solanum muricatum) (Mertelík et al., 2010; Puchta et al., 1990; Shamloul et al., 1997), the agronomic significance of those infections is currently unknown.

Potato

Potato (Solanum tuberosum L., family Solanaceae), the fourth most important food crop grown worldwide, after rice, wheat, and maize, is traditionally propagated from seed potatoes or from true seed harvested from potato fruits. In potato, the principal viroid pathogen is PSTVd; tomato chlorotic dwarf viroid has also been found in natural infections. Potato can be experimentally infected with Columnea latent viroid (Verhoeven et al., 2004), CEVd (Semancik et al., 1973), and pepper chat fruit viroid (PCFVd) (Verhoeven et al., 2009) resulting in tuber distortion and tuber growth reduction.

PSTVd is present worldwide in potato with multiple strains causing mild to severe symptoms (http://www.cabi.org/isc/datasheet/43659). The primary means of spread is mechanical transmission through contaminated cutting knives and farming equipment (Bonde and Merriam, 1951; Manzer and Merriam, 1961). PSTVd is also transmitted through true seed and pollen (Fernow et al., 1970; Singh et al., 1992). Transmission of PSTVd by aphids has been reported from plants coinfected with potato leafroll virus where PSTVd was transencapsidated in the virus particle (Querci et al., 1997; Syller et al., 1997).

Symptoms and yield loss from PSTVd infection in potato vary depending on the potato cultivar and environmental conditions, with little or no foliage symptoms under some environmental conditions, while tubers are elongated and may have severe growth cracks; yield loss may reach 64% due to reduced potato production (Diener, 1987; Pfannenstiel and Slack, 1980). In the Saco variety, a mild strain of PSTVd could result in a 17%–24% loss, while a severe strain would result in a 64% loss (Singh et al., 1971). Environmental conditions influence the yield loss as foliage symptoms of PSTVd in potato can become more severe if tubers are planted late in the season when temperatures are warm; high temperatures can also increase the viroid titer (Singh, 1983). PSTVd also reduces pollen viability and seed set in some potato cultivars (Grasmick and Slack, 1986).

Control of PSTVd in potato has been successful through strict quarantine measures with a zero tolerance for the presence of PSTVd and trade of certified, viroid-free seed potatoes. With these measures, PSTVd has essentially been eradicated from potato crops in North America and Western Europe (De Boer and DeHaan, 2005; Singh, 2014; Sun et al., 2004). PSTVd still poses significant problems for seed potato production in Russia and elsewhere (Owens et al., 2009). An economic impact assessment of the potential reintroduction of PSTVd into the European Union concluded that phytosanitary measures are economically justifiable to control the disease (EFSA Panel on Plant Health, 2011; Soliman et al., 2012).

Tomato

Tomato (Solanum lycopersicum L., family Solanaceae) is the second most important vegetable crop next to potato. The present world production is approximately 100 million tons of fresh fruit produced on 3.7 million hectares and in 144 countries (http://faostat3.fao.org/home/). Tomato is grown in both open fields and greenhouses for fresh market and processing. Viroids that naturally infect tomato include PSTVd, tomato apical stunt viroid, tomato planta macho viroid, Mexican papita viroid (now a strain of tomato planta macho viroid), tomato chlorotic dwarf viroid, Columnea latent viroid, and Indian tomato bunchy top viroid (a distinct strain of CEVd) (Singh et al., 2003). Common symptoms of viroid infection in tomato, which are dependent on viroid species and strain, cultivar, temperature, and light conditions, include chlorosis, bronzing, leaf distortion, reduced growth, heavy yield loss, and unmarketable fruit (Singh et al., 2003).

In general, pospiviroids are seed-transmitted in tomato and infection reduces pollen viability and seed germination rates in some cultivars (Benson and Singh, 1964; Hooker et al., 1978). Secondary mechanical spread of tomato apical stunt viroid in tomato greenhouse crops in Israel was found to be a result of the pollination activity of bumblebees (Antignus et al., 2007). Viroid infections in commercial tomato fields and in greenhouse-grown plants have been linked to imported seed or ornamentals (Batuman and Gilbertson, 2013; Van Brunschot et al., 2014; Verhoeven et al., 2012). As viroids are transmitted through tomato seed to varying extents and surface disinfection of seeds does not prevent transmission, recent seed testing and certification protocols for pospiviroids have been proposed for pre- and post-entry of tomato seed shipments. With the increased detection of tomato-infecting viroids in asymptomatic ornamentals (Chapter 3: Economic Significance of Viroids in Ornamental Crops), and since many growers may propagate tomatoes and ornamentals in the same greenhouses, increased grower vigilance should be practiced to avoid chance infections of cultivated crops.

Hop

Hop (Humulus lupulus L., family Cannabaceae) is a dioecious perennial climbing plant grown commercially worldwide for its use in the pharmaceutical and brewing industries. Traditionally the annual stems (vines/bines) are pruned continuously during the season to promote growth of selected vines and to control disease. After harvest, shoots are trimmed to soil level for the winter; in spring, new shoots arise from the rootstock. The female plant produces hop flowers, or cones, which contain resin glands that synthesize lupulin. Lupulin contains the essential oils and resins (alpha and beta acids) that impart flavor.

Hop stunt viroid (HSVd), the causal agent of hop stunt disease (Sano, 2003), and hop latent viroid (HLVd) (Barbara and Adams, 2003; Puchta et al., 1988) are significant pathogens in commercial hop fields (Pethybridge et al., 2008). Two recently reported viroids, apple fruit crinkle viroid (AFCVd) (Sano et al., 2004) and citrus bark cracking viroid (CBCVd) (Jakse et al., 2015), pose additional threats to the hop industry.

Hop stunt disease, first observed in the Fukushima province of Japan in the 1950s and 1960s (Shikata, 1987), has since been found in North America, South Korea, China, and Europe (Eastwell and Nelson, 2007; Eastwell and Sano, 2009; Guo et al., 2008; Radisek et al., 2012; Sano, 2003). The disease is characterized by a delay in emergence and early growth, shortened internodes, leaf curl and yellowing, small cone formation, and dry root rot; the severity of symptoms is dependent on the hop cultivar, may take years to appear, and may be more severe in warmer climates (Sasaki and Shikata, 1977).

The effect of HSVd on cone yield and brewing alpha acids can result in losses of 50%–70% (Sano, 2003). Losses of 50%–80% in hop production areas in the Northwest Yakima Valley, the United States, were observed in the hop cultivar Willamette Glacer, with a reduction in brewing alpha acid levels of 50%–70% (Eastwell and Nelson, 2007).

HLVd is widespread in all hop-growing regions worldwide. The impact of HLVd infection on yield is relatively minor as there are no severe symptoms associated with its presence (Barbara and Adams, 2003). The effects of HLVd on yield and quality appear to be cultivar dependent as cone yield was reduced by 27% and alpha acids were reduced by 31% in the hop cultivar Omega in the United Kingdom (Barbara et al., 1990).

In the Akita Prefecture of Japan, Sano et al. (2004) detected a strain of the AFCVd in symptomatic hops, with vine stunting and severe leaf curl and considerably lower alpha acid content in dried cones; the plants were negative for HSVd. The viroid appears to have spread over the major hop-producing regions of Japan and AFCVd-infected hops may have been introduced in infected mother stocks (Sano et al., 2004). It is not known if infection by AFCVd alone causes symptoms, as all hops examined were also infected with HLVd and most hops cultivated in Japan also were infected with hop latent virus and apple mosaic virus (Kanno et al., 1993).

In 2007, a severe stunting of hop was observed in several hop gardens in Slovenia, with symptoms similar to those caused by HSVd. The disease spread rapidly to other hop farms, and several hectares of hops were eradicated. In addition to hop mosaic virus, HLVd, and HSVd (Radisek et al., 2012), some manifestations of the disease symptoms were not characteristic of HSVd infection. Next-generation sequencing identified the putative causal agent of the disease as a novel strain of CBCVd, and was confirmed as such by biolistic inoculation of cloned cDNAs onto hop and the development of severe leaf malformations and stunting (Jakse et al., 2015). To date, this is the first and only report of CBCVd in hop.

As infected hop plants cannot be cured, control of viroid diseases includes the use of viroid-free planting stock and clean tools, cultural practices that limit bine pruning, and the adoption of dwarf cultivars that have been reported to exhibit some resistance to viroid infection (Barbara and Adams, 2003; Pethybridge et al., 2008; Sano, 2003; Takahashi, 1979).

Cucumber

Cucumber (Cucumus sativus L., family Cucurbitaceae) is a warm season vining plant primarily seed propagated and grown for its fruit. Pale fruit disease, with its distinctive symptom of pale green fruit was first reported in 1963 in The Netherlands and was later discovered in natural infections of cucumber elsewhere in the country (Van Dorst and Peters, 1974). Cucumber pale fruit disease was shown to be caused by a viroid, later designated a cucumber isolate of HSVd (Sano et al., 1984). In 2009, HSVd was discovered in Finland in greenhouse-grown cucumber exhibiting symptoms of yellow, bottle-shaped fruits and crumpled flowers (Lemmetty et al., 2011) and estimated yield losses to the grower were 2%–3%.

Pepper

Sweet (bell) pepper is a cultivar group in the species Capsicum annuum L., family Solanaceae, and is grown for its multicolored fruits for fresh market and processing. Sweet peppers are seed propagated, and both hybrid and open-pollinated varieties are grown. Experimental transmission of PSTVd to pepper was demonstrated by O’Brien and Raymer (1964); however, little or no resulting disease symptoms were observed. The first report of PSTVd naturally infecting pepper was made in New Zealand following evaluation of a diseased capsicum plant displaying subtle symptoms of wavy margins on the upper leaves with no significant effects on fruit production (Lebas et al., 2005). The occurrence of PSTVd in greenhouse-grown pepper was limited, however, due to the symptomless phenotype; infected pepper may serve as a source of inoculum where pepper and tomato are grown in the same greenhouse.

A new disease was observed in greenhouse-grown sweet pepper (cv. Jaguar) in The Netherlands and the pathogen, PCFVd, was proposed as a new pospiviroid species (Verhoeven et al., 2009). Symptoms of PCFVd in pepper included delayed fruit set, reduced fruit size and number, and reduced plant growth; it was also shown to be seed-transmitted. Mechanical inoculation revealed that PCFVd caused stem and petiole necrosis and stunting in tomato and small, distorted tubers in potato (Verhoeven et al., 2009). PCFVd was subsequently reported in pepper in Canada (Verhoeven et al., 2011), in a natural infection of field-grown tomato in Thailand (Reanwarakorn et al., 2011), and was intercepted in Australia in imported tomato seed from Thailand and Israel (Chambers et al., 2013). The crop losses associated with PCFVd in pepper are not yet known, however the destruction of PCFVd-infected tomato seed shipments impacts seed trade (Chambers et al., 2013).

Disease Management

No genetic resistance to viroids has been identified in these crops, and control measures include the use of clean planting stock, sanitary cultural practices, certification (Chapter 39: Quarantine and Certification for Viroids and Viroid Diseases), thermotherapy (Chapter 40: Viroid Elimination by Thermotherapy, Cold Therapy, Tissue Culture, In Vitro Micrografting or Cryotherapy), decontamination (Chapter 41: Decontamination Measures to Prevent Mechanical Transmission of Viroids), and engineered resistance (Chapter 42: Strategies to Introduce Resistance to Viroids).

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Chapter 2

Economic Significance of Fruit Tree and Grapevine Viroids

Ahmed Hadidi¹, Georgios Vidalakis² and Teruo Sano³,    ¹U.S. Department of Agriculture, Beltsville, MD, United States,    ²University of California, Riverside, CA, United States,    ³Hirosaki University, Hirosaki, Japan

Abstract

Fruit tree and grapevine viroids infect a large number of plant species and the economic significance of these viroids may vary according to the viroid or variant as well as to the host plant. Those of greatest economic importance are the viroids associated with apple scar skin, peach latent mosaic, avocado sunblotch, citrus exocortis, and citrus cachexia diseases. Certain citrus viroids have been utilized in producing dwarfed citrus trees in high density planting, which results in several beneficial economic effects. Most grapevine viroids are latent, however, the grapevine yellow speckle viroids have been implicated in vein banding disease.

Keywords

Economic significance; fruit tree viroids; pome and stone fruit viroids; persimmon viroids; citrus viroids; grapevine viroids

Introduction

Fruit trees and grapevine are important horticultural crops, responsible for tens of billions of dollars per year to the global economy, and comprising a major source of income for growers and allied businesses worldwide. Losses from viroid infections in these crops are difficult to measure unless infected hosts are visibly damaged. Viroids may be latent in some hosts yet have adverse effects that often go unnoticed. Whether viroid-infected fruit trees or grapevine show obvious detrimental effects or do not induce noticeable disease, viroid infections are responsible for significant economic losses to these crops. Table 2.1 lists viroids of fruit trees and grapevine and their alternative hosts. Specific variants of three citrus viroids may induce beneficial effects on citrus trees. Most grapevine viroids are latent and distributed worldwide. Only grapevine yellow speckle viroid 1 (GYSVd-1) and grapevine yellow speckle viroid 2 (GYSVd-2) can induce a yellow speckle symptom on grapevine leaves (Koltunow et al., 1989), which varies in intensity and may be absent under certain weather conditions.

Table 2.1

Fruit Tree and Grapevine Viroids and Their Natural Hosts

aSequences available online: http://www.ncbi.nlm.nih.gov/nuccore/; http://subviral.med.uottawa.ca

bSelected economically important hosts, with emphasis on fruit trees and grapevine, are listed.

cUnassigned members of new species.

Pome Fruit Viroids

Apple scar skin viroid (ASSVd) causes scar skin or dapple symptoms in apple fruits, especially in China, Japan, South Korea, and India. ASSVd causes serious yield losses in apple and affected fruits are significantly downgraded or unmarketable. ASSVd may be latent in many pear cultivars, which may be the source of viroid infection to adjacent apple trees. The viroid may also cause pear rusty skin and pear fruit crinkle diseases in China, pear fruit dimple disease in Japan, and variable fruit symptoms on cultivated and wild pear in Greece. Blemished pear fruits are reduced in quality and market value (Hadidi and Barba, 2011; Chapter 21: Apple Scar Skin Viroid).

Apple fruit crinkle viroid (AFCVd) causes crinkle and dappling symptoms on affected apple fruits. Moreover, it may cause brown necrotic areas in the flesh, fruit may drop early and/or fruits are smaller, and blister bark symptoms may appear in sensitive varieties (Koganezawa and Ito, 2011). AFCVd infection causes reduced yield and unmarketable fruits. The disease has been reported only from Japan, where the viroid also infects hop and persimmon. It causes major economic losses on hop plants by inciting severe stunting and reduction of alpha acids contents in the cones (see Chapter 22: Other Apscaviroids Infecting Pome Fruit Trees) but is symptomless in persimmon (Nakaune and Nakano, 2008).

Apple dimple fruit viroid (ADFVd) naturally infects apple (Di Serio et al., 2011) and fig (Chiumenti et al., 2014) with very limited incidence (Malfitano et al., 2004). Dimple fruit symptoms are observed only in red apple, in which the viroid may cause reduced yield and unmarketable fruits. Several apple cultivars such as Golden Delicious, Granny Smith, and others are symptomless. Pear seedlings infected with ADFVd are symptomless (see Chapter 22: Other Apscaviroids Infecting Pome Fruit Trees).

Pear blister canker viroid infects pear under natural conditions and the majority of pear cultivars are tolerant to infection and do not show bark symptoms (Flores et al., 2011). Sensitive infected trees show bark canker symptoms and quickly decline. The viroid also naturally infects wild pear and quince.

Stone Fruit Viroids

Peach latent mosaic viroid (PLMVd) causes disease in peach (see Chapter 29: Peach Latent Mosaic Viroid in Infected Peach), but it is latent in several stone fruit species: almond, pear, and wild pear (see Chapter 30: Peach Latent Mosaic Viroid in Temperate Fruit Trees Other Than Peach). Infected peach fruits are misshapen, discolored with cracked sutures and swollen roundish stones. Most PLMVd variants do not cause leaf symptoms in peach, however, some variants induce chlorotic or yellow mosaics or albino-variegated patterns, pink broken lines on petals, and possibly stem pitting. PLMVd infection causes yield reduction in peach fruits and fruits may become unmarketable. PLMVd in Japanese plum cv. Angeleno may cause spotted fruit disease (see Chapter 30: Peach Latent Mosaic Viroid in Temperate Fruit Trees Other Than Peach). The effect of PLMVd infection on yield and fruit quality has not yet been demonstrated in plum and other stone fruits, almond, and pears. PLMVd is very widely distributed.

Hop stunt viroid (HSVd) infects plum, peach, apricot, almond, and sweet cherry, and causes symptoms restricted to the fruit: dapple on plum and peach and yellow spots on apricot. Diseased sensitive plum cultivars were reported from Japan, South Korea, and China; some Japanese cultivars may produce fruits with yellowish red color and they may harden. Sensitive peach cultivars were reported from Japan. European Prunus cultivars are generally tolerant and may not show fruit symptoms. In Italy, however, some diseased plum cultivars may produce fruits with wine-red dappling or irregular reddish lines. Apricot cultivars in Spain produce fruits characterized by changes in their external appearance, which involves rugosity and loss of organoleptic characteristics (Amari et al., 2007). Yield, quality and marketable value of stone fruits with HSVd symptoms are reduced.

Mulberry, Pomegranate, and Fig Viroids

HSVd causes leaf vein clearing, yellow speckle, and deformation of mulberry leaves in Iran (Mazhar et al., 2014). The viroid is symptomless in pomegranate (Gorsane et al., 2010). HSVd and citrus exocortis viroid (CEVd) were identified in fig trees showing symptoms of fig mosaic disease (Yakoubi et al., 2007). Similarly, ADFVd was detected in fig accessions showing symptoms of fig viruses (Chiumenti et al., 2014).

Persimmon Viroids

Persimmon viroid 2 was reported from Japan by deep sequencing analysis of an American persimmon tree grafted onto a Japanese persimmon rootstock showing poor growth (Ito et al., 2013). However, the relationship between viroid infection and symptom expression has not yet been clarified, because not only persimmon viroid 2 but also multiple variants of a new unassigned closterovirus species, as well as AFCVd, citrus viroid VI, and persimmon latent viroid, were detected in the same tree.

Persimmon is also a natural host of three other apscaviroids in Japan: AFCVd, citrus viroid VI, and persimmon latent viroid (syn. persimmon viroid) (Nakaune and Nakano, 2008; Ito et al., 2013). They were identified in Japanese persimmons symptomatic and asymptomatic for fruit apex disorder. These viroids are graft transmissible from persimmon to persimmon.

Avocado Viroids

Avocado sunblotch viroid (ASBVd) causes a wide variety of symptoms on avocado fruits, twigs, and bark; and infected trees may be stunted. Trees with visible sunblotch symptoms often produce avocado fruits with reduced quality and yield (18%–30%) (Semancik, 2003a). A significant and dramatic reduction (95%) in fruit yield may also occur in some avocado trees in which ASBVd is latent (symptomless carriers) (Desjardins, 1987).

Potato spindle tuber viroid (PSTVd) was also reported to naturally infect avocado trees in Peru. PSTVd infection was latent, however, trees coinfected with ASBVd showed symptoms that included bunchy inflorescence, decrease in fruit size and number, and eventual decline and death of infected plants (Querci et al., 1995). It was suggested that PSTVd was introduced with the original avocado trees, about a century ago, mainly from Riverside, California (Bartolini and Salazar, 2003).

Citrus Viroids

Citrus viroids infect a large number of citrus species and citrus relatives; however, most of the infections have no noted effect on the host. Citrus viroids induce disease only when a specific viroid (or variant) infects a sensitive citrus host. On the other hand, specific variants of three citrus viroid species (i.e., citrus bent leaf viroid, HSVd, and citrus dwarfing viroid) may induce desirable economic effects (Duran-Vila and Semancik, 2003; Semancik, 2003b; Semacik et al., 1997; Vidalakis et al., 2010, 2011).

From the seven known citrus viroids only two, namely, CEVd and HSVd, have been associated with citrus diseases that can result in economic losses (Gumpf et al., 2014; Timmer et al., 2000). Recently, it has been reported that citrus bark cracking viroid, which does not cause any important citrus disease, is a highly aggressive pathogen on hop plants and causes major economic losses Jakse et al. (2015).

Exocortis and cachexia diseases, induced by CEVd and certain HSVd variants, respectively, are posing significant economic risks to global citrus production. Both diseases have been reported from all major citrus producing areas of the world, as well as in early citrus budwood registration programs, since their original descriptions in 1948 and 1950, respectively (Duran-Vila and Semancik, 2003). In addition, both exocortis and cachexia diseases can reduce tree performance of commercially popular and economically important citrus, such as trifoliate orange (Poncirus trifoliata (L.) Raf.) and mandarins (Citrus reticulata Blanco).

Exocortis is a bark scaling, stunting, and yield reducing disease of trees propagated on trifoliate and trifoliate hybrid rootstocks. These rootstocks, however, are tolerant to citrus tristeza virus and have replaced the tristeza-sensitive rootstock sour orange (Citrus aurantium L.) in many citrus producing areas of the world (Moreno et al., 2008). Roistacher et al. (1996) elegantly presented the economic consequences of citrus viroids in the transition from sour to the trifoliate orange rootstock in Belize. Viroid-infected trees showing decline and severe bark cracking generally yielded one-fourth box (10.2 kg) or less per tree compared to healthy trees, which yielded 40.8 kg. In addition, rootstocks showing severe bark cracking were predisposed to Phytophthora infections, as the pathogen could readily enter through the exposed vascular tissues and many trees died before the eighth year in the field. Overall, it was estimated that the economic loss in Belize in 1996 was $5678/ha, which corresponds to approximately $8685/ha in 2014. Cachexia infected mandarin, tangerine, or clementine trees are stunted, chlorotic with gum impregnations in the phloem, and reduced yield (Hashemian et al., 2009; Murcia et al., 2014; Timmer et al., 2000; Vernière et al., 2004, 2006).

Some citrus viroids are unique among plant pathogens in regard to the question of economic significance because they can be considered as genetic elements for the modification of host genome responses that result in desirable horticultural, production, environmental, labor, and ultimately economic benefits. Originally proposed by Cohen (1968) and Mendel (1968), the use of viroids as means of producing dwarfed citrus trees has been under continuous investigation and has been reviewed by Hutton et al. (2000) and Semancik (2003b) in detail. Specific variants of three citrus viroids are approved for commercial use in California, where experiments with navel orange trees (Citrus sinensis (L.) Osb.) on trifoliate rootstock and navel orange and clementine mandarin trees on Carrizo citrange (C. sinensis×P. trifoliata) rootstock in standard (6×6.7 m) and high density (3×6.7 m) plantings reduced the canopy volume by 33%–53.5%, and almost doubled the yield per land surface unit (Vidalakis et al., 2010, 2011).

While increased fruit production per land surface unit is an obvious economic benefit of dwarfed citrus trees in high density plantings, the cost of harvesting, pest management, and irrigation are also important economic factors (Fridley, 1977; Phillips, 1978). A high density planting of dwarfed citrus trees with small canopies will also be advantageous for Huanglongbing disease management programs. Visual inspection of dwarfed trees will be simpler without the need for tractors and platforms (Belasque et al., 2010). The effects of tree removal on fruit production are mitigated, as shown by the analysis of citrus groves at two density plantings (494 and 988 trees/ha). Even at the extreme tree loss rate of 30% per year, the higher density grove approached 35.5 tons/ha in year six while the lower density grove reached a maximum of 17.2 tons/ha (Stover, 2008).

In the face of serious challenges threatening citrus production globally, and in the absence of a true dwarf citrus this technology presents an interesting alternative: it can be used immediately for the development of a simple, flexible, and consumer acceptable citrus management system since they have low cost (natural agents and grafting) and low biological and commercial risk with no natural transmission vectors and no genetically engineered materials involved. Finally, the noncachexia variant of HSVd, is present in the 143-year-old Parent Navel tree in Riverside, California, suggesting that this RNA species does not have a deleterious effect on tree health (University of California, Riverside, routine testing since the 1950s). Is it possible that the superior performance of the Parent Navel tree since 1873 perhaps is associated to a certain degree with the presence of a nucleic acid element such as a viroid RNA?

Grapevine Viroids

There are at least six viroids reported to infect grapevines in nature (Table 2.1). Four of these, Australian grapevine viroid, grapevine latent viroid, HSVd (grapevine strain), and CEVd (grapevine strain), are latent and do not cause diseases in grapevine. Thus, they may be considered as economically unimportant. However, since HSVd can cause severe hop stunt disease on cultivated hops, their potential threats cannot be ignored (Kawaguchi-Ito et al., 2009). GYSVd-1 and GYSVd-2, however, have been implicated in the vein banding disease of grapevine, which is caused by coinfection with grapevine fanleaf virus or by the yellow speckle viroids alone (Martelli, 2014). With the exception of grapevine latent viroid, which was discovered recently in Xinjiang province, China in 2014 (Zhang et al., 2014), other grapevine viroids are distributed worldwide (Martelli, 2014). The incidences of HSVd and GYSVd-1 are extremely high in any of the grapevine producing areas. On the other hand, regional disparity can be seen in the incidence of Australian grapevine viroid, GYSVd-2 and CEVd; e.g., infection rate was relatively high, at 26%, 18.7%, and 9.3% in Tunisia, Iran, and India, respectively, but negligible in the other regions of the world (Adkar-Purushothama et al., 2014; Jiang et al., 2012). No information is available on the effect of any of the grapevine viroids on grape yield, vine vigor, and wine quality.

Acknowledgments

The senior author would like to thank Jon Hadidi BS, MBA, JD for his computer-related expertise.

References

1. Adkar-Purushothama CR, Kanchepalli PR, Sreenivasa MY, Zhang Z-X, Sano T. Detection, distribution, and genetic diversity of Australian grapevine viroid in grapevines in India. Virus Genes.