Emergence and diversity of begomoviruses infecting solanaceous crops in East and Southeast Asia

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Emergence and diversity of begomoviruses infecting solanaceous crops in East and Southeast Asia Lawrence Kenyon ∗ , Wen-Shi Tsai, Su-Ling Shih, Li-Mei Lee AVRDC – The World Vegetable Center, PO Box 42, Shanhua, Tainan 74199, Taiwan, ROC

a r t i c l e

i n f o

Article history: Available online xxx Keywords: Geminiviridae Solanum lycopersicum Capsicum annuum Solanum melongena ssDNA virus Recombination

a b s t r a c t Over the past three decades diseases caused by whitefly-transmitted geminiviruses (begomoviruses) have emerged to be important constraints to the production of solanaceous crops, particularly tomato (Solanum lycopersicum) and peppers (Capsicum spp.), in many tropical and subtropical regions of the world. The most studied of these is Tomato yellow leaf curl virus (TYLCV), which has spread to many other areas from its likely origin in the Mediterranean basin region. The virus is usually associated with the polyphagous and virus-vectoring-efficient B-biotype of its vector whitefly (Bemisia tabaci). However, in Southeast and East Asia, a wide variety of distinct local begomovirus species have been identified from tomato and pepper crops over this period, and TYLCV was detected in Japan only in about 1996, China in 2006 and Korea in 2008, despite B-biotype whiteflies being present in several of the countries of the region since at least the early 1990s. Continental Southeast Asia appears to be a major center of diversity for begomoviruses and some species may have spread across the region; Tomato yellow leaf curl Thailand virus (TYLCTHV) appears to have spread from the Thailand–Myanmar region into southern China and is now displacing the local tomato-infecting species in Taiwan, and Tomato yellow leaf curl Kanchanaburi virus (TYLCKaV) appears to have spread from the Thailand–Vietnam region to Java, Indonesia. Since many of the native tomato- or pepper-infecting begomoviruses and associated satellite DNAs have also been detected in local weed species, it seems likely that their ancestors originated in these weed hosts, but with the expansion and intensification of tomato and pepper production in the region, there was selection for recombinant or mutant forms with greater virulence on tomato and/or pepper. Expansion and intensification of these crops may also have resulted in increased populations of local, and if present, B- or Q-biotype whiteflies, aiding the increase and spread of local begomovirus species. © 2013 Elsevier B.V. All rights reserved.

1. Introduction The Geminiviridae is a family of plant-infecting viruses that have a circular single-stranded DNA genomes and twinned icosahedral (geminate) particles. The family comprises four genera: Mastrevirus, Curtovirus, Topocuvirus and Begomovirus (Brown et al., 2012). Members of the genus Begomovirus infect dicotyledonous plants, are transmitted in a persistent manner by the whitefly Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) and can have either a mono- or bipartite genome. The monopartite begomoviruses previously were found only in the Old World, while the bipartite begomoviruses were predominantly located in the New World. However, there is evidence that some bipartite begomoviruses were present in Asia (Vietnam) prior to continental separation (Ha et al., 2008), and that monopartite viruses are emerging in Latin America through convergent evolution of bipartite viruses (Melgarejo et al., 2013). The International Committee on

∗ Corresponding author. Tel.: +886 6 5837801; fax: +886 6 5830009. E-mail address: [email protected] (L. Kenyon).

Taxonomy of Viruses (ICTV) species demarcation criteria is an 89% nucleotide identity threshold between full-length DNA-A component nucleotide sequences for begomovirus species (Brown et al., 2012), and strains of a species are defined by a 93% nucleotide identity threshold (Fauquet et al., 2008). The emergence of begomoviruses over the last 20–30 years as one of the most important groups of plant viruses affecting production of a variety of vegetable crops, particularly in the tropics and subtropics, has generally been associated with increases of populations of the vector whitefly, B. tabaci. Tomato leaf curl or tomato yellow leaf curl has become the most devastating viral disease of tomato worldwide (Hanssen et al., 2010). The disease is caused by a complex of mainly monopartite begomovirus species; of the begomovirus species recognized by the ICTV, over 40 have ‘tomato leaf curl’ as part of their name (Brown et al., 2012). The disease was first reported from the Jordan valley (now Israel) in the late 1930s and the causal agent there was identified as Tomato yellow leaf curl virus (TYLCV) in 1961. From the 1970s TYLCV spread from its origin in the Mediterranean basin region, first to neighboring countries and then starting in the 1980s, much more widely across tropical and subtropical regions of the world. Two different strains of the virus from

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Please cite this article in press as: Kenyon, L., et al., Emergence and diversity of begomoviruses infecting solanaceous crops in East and Southeast Asia. Virus Res. (2014), http://dx.doi.org/10.1016/j.virusres.2013.12.026

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Israel were identified, the Israel (IL) and the Mild (Mld) strain. Also, a related species, Tomato yellow leaf curl Sardinia virus (TYLCSV) became important in Italy in the late 1980s and subsequently in Spain. The spread of the two forms of TYLCV and of TYLCSV around the world has been well documented and analyzed (Lefeuvre et al., 2010; Navas-Castillo et al., 2011). The global emergence and spread of many begomoviruses, including TYLCV and TYLCSV, has been associated with the spread and increase of a more fecund and polyphagous whitefly biotype, referred to as the B-biotype (Seal et al., 2006). There has long been debate as to whether B. tabaci is a complex species or a species complex. Morphologically indistinguishable B. tabaci populations can have different host plant feeding preferences and virus transmission properties; this resulted in distinct populations being described as biotypes. By the early 2000s biotypes A to T had been described (Perring, 2001). The invasive Q-biotype, which was characterized by its increased resistance to many pesticides and tolerance to higher temperatures, was also associated with some of the spread and increase in begomoviruses such as TYLCV (Horowitz et al., 2007). The current approach to assessing the taxonomy of B. tabaci is to determine the degree of similarity between mitochondrial cytochrome oxidase subunit I (COI) gene sequences. Based on comparing 454 COI sequences, and with a threshold of 3.5% difference, Dinsdale et al. (2010) identified 24 constituent species within the B. tabaci complex. More recently, the number of constituent species identified increased to 31 and with this it was suggested that the threshold for difference in COI sequence should be increased to 4% (Lee et al., 2013). Based on this molecular phylogeny, the B-biotype and the Q-biotype are now often referred to as the Middle East-Asia Minor 1 (MEAM1) and Mediterranean (Med) cryptic species or haplotypes of B. tabaci, respectively. A further level of complexity in the virus–vector–host relationship is that the persistent transmission of TYLCV, and probably some other begomoviruses by B. tabaci depends on chaperonin GroEL homologs produced by endosymbiotic bacteria in the whiteflies (Diaz-Pendon et al., 2010). Zeidan et al. (1998) wrote that “Geminiviruses infecting tomatoes are rapidly spreading to regions where they were unknown before, threatening tomato production”, but then showed with the molecular sequence data available at the time that the isolates then present in Southeast and East Asia were distinct local begomovirus species and not the TYLCV or TYLCSV that were starting to appear in other parts of the world. Seven years later, Green et al. (2005) in an updated assessment of what was known of the diversity of begomoviruses of tomato and weeds in Asia, cataloged many more distinct begomovirus species having been identified in the region, and also the first identification of TYLCV in the region in Japan. Now, eight more years on, we here collate the recent and older information to provide an updated account of the emergence of begomoviruses infecting tomato, capsicum peppers and eggplant in East and Southeast Asia. We also use the available information to speculate as to what the main drivers for the emergence and diversity of these viruses across the region are.

2. Begomoviruses infecting solanaceous crops in Southeast Asia The first detection, identification and distribution of different begomovirus species from tomato, pepper and eggplant across the different countries of East and Southeast Asia is presented below for each country of the region and is summarized in Table 1. Based mainly on Zeidan et al. (1998) and Green et al. (2005), the earliest record of observing a disease of tomato, pepper and egg plant likely to be caused by begomovirus is also presented. To assess the diversity of the begomovirus species described below, nucleic

acid sequences of DNA-A components representative all the species were retrieved from GenBank (http://www.ncbi.nlm.nih.gov/), then aligned using the ClustalW facility, and a phylogenetic tree was constructed using the neighbor-joining method with 1000 bootstrap replications, using the MEGA5 package of programs (Tamura et al., 2011) (Fig. 1). 2.1. Cambodia (KHM) Tomato with leaf curl symptoms were observed in Cambodia pre-1989, but it was not until 2004 that a distinct monopartite virus was identified and named Tomato leaf curl Cambodia virus (ToLCKHV) with highest similarity to Tomato leaf curl Malaysia virus (ToLCMYV) (Green et al., 2005). Despite reports of severe leaf curl in tomato crops in some parts of Cambodia in recent years, there remain no published sequences of begomovirus from tomato in Cambodia. 2.2. China (CHA) A tomato disease probably caused by a begomovirus was first reported (though at low incidence) in China in 1965 in the tomatoproducing areas of the south, and later the virus causing disease in tomatoes in Guangxi province was identified as Tomato yellow leaf curl China virus (TYLCCNV) (Yin et al., 2001). Several other tomato-infecting begomoviruses were identified in the early 2000s. In Yunnan province, as well as TYLCCNV, Li et al. (2004) identified Tobacco curly shoot virus (TbCSV), Tobacco leaf curl Yunnan virus (TbLCYnV) and Tomato yellow leaf curl Thailand virus (TYLCTHV) infecting tomato. Although the isolates of TYLCTHV first identified in Thailand were bipartite, no DNA-B was detected associated with any of the tomato-infecting begomoviruses in China. Zhou et al. (2003) showed that TYLCCNV and begomovirus isolates from tobacco and some weeds in Yunnan were associated with three specific clades of betasatellites with which they had co-evolved. Isolates collected from Guangzhou were identified as Tomato leaf curl Taiwan virus (ToLCTV), and a distinct novel monopartite begomovirus, Tomato leaf curl Guangxi virus (ToLCGxV) was identified from tomato in Guanxi province in 2003 (Xu et al., 2007). In March 2006, a yellow mosaic disease was observed on tomato with disease incidence up 90% in fields of Sunqiao, Shanghai Province. This was subsequently identified as a strain of TYLCV with very high nucleic acid sequence homology to the Japanese “Tosa” strain, and the first incursion of TYLCV into China (Wu et al., 2006). The following year, an isolate of TYLCV was sequenced from the weedy “Dutch Eggplant” (Solanum aculeatissimum) in Shanghai province and found to be more closely related to TYLCV isolates from Africa and the Americas, suggesting a second distinct route into China (Yongping et al., 2008). By 2010 TYLCV had spread to be prevalent in at least six provinces of China, and by 2012 it had been detected in 11 provinces. The B-biotype of B. tabaci had been known in China since the mid 1990s, but the rapid spread of TYLCV after 2006 coincided with the arrival of the Q-biotype and was aided differentially by whitefly B- and Q-biotypes (Pan et al., 2012). Sequences of TYLCV from pepper and eggplant in Xinjiang province in 2011 have been deposited in GenBank as accessions JX456642 and JX456643 respectively, and TYLCV appears to be becoming more widespread in pepper production systems in southern provinces of China (Group R in Fig. 1). Zhang et al. (2010) identified a novel monopartite begomovirus from Hainan Island, Tomato leaf curl Hainan virus (ToLCHaV), and observed that it may have arisen by recombination between viruses related to Papaya leaf curl China virus (PaLCuCNV), Ageratum leaf curl virus (ALCuV) and Tomato leaf curl Vietnam virus (ToLCVV). Recently, several sequences labeled Pepper yellow leaf curl china virus (PYLCCNV) collected from peppers in China in 2010 were deposited in

Please cite this article in press as: Kenyon, L., et al., Emergence and diversity of begomoviruses infecting solanaceous crops in East and Southeast Asia. Virus Res. (2014), http://dx.doi.org/10.1016/j.virusres.2013.12.026

Countriesa

Cropb

Begomoc

AYVCNV

CHN

To Pe Eg To Pe Eg To To To To To To Pe To Pe To Pe Eg To Pe To Pe Eg

65 08 11 82 00 09 65 89 07 98 99 86 97 68 94 91 99 00 81 07 98 10 04

09

Countriesa

Cropb

ToLCGxV

ToLCHaV

CHN

To Pe Eg To Pe Eg To To To To To To Pe To Pe To Pe Eg To Pe To Pe Eg

03

08

IDN

PHL

TWN VNM

IDN

JPN KHM KOR LAO MMR MYS PHL THA

TWN VNM

ChiLCPKV

EpYVV

HYVMV

PaLCuCNV

PepYLCIV

PepLCV

PepLCYnV

03

TbLCJV

HYVV

TbLCTHV

01

09

TbLCYnV

ToLCCeV

03

ToLCCNV

ToLCGdV

02

03

08

03

05

TbCSV

03 00 97

00

89 07

97 06

05 05 07 99 03

ToLCHanV

ToLCHsV/RamMV

ToLCJaV

ToLCLV

ToLCMiV

ToLCMYV

ToLCPV

ToLCSuV

ToLCTV

ToLCVV

04

03

TYLCCNV

TYLCKaV

TYLCIDV

00

06 06

TYLCTHV

TYLCVV

02

TYLCV 06 11 11

98 09 09 96 ? 08

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THA

AYVV

98 99 97 06

97 06 01

91 08

01 00 10

10

81

05 07 98

04 10 04

07

a Countries: CHN, China; IDN, Indonesia; JPN, Japan; KHM, Cambodia; KOR, South Korea; LAO, Laos Peoples’ Democratic Republic; MMR, Myanmar; MYS, Malaysia; PHL, The Philippines; THA, Thailand; TWN, Taiwan; VMN, Vietnam. b Crops: To, tomato; Pe, capsicum peppers; Eg, eggplant. c ‘Begomo’ = first report of a leaf-curl type disease probably caused by a begomovirus.

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JPN KHM KOR LAO MMR MYS

AYVHuV

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Table 1 Year of first detection or identification of begomoviruses infecting tomato, pepper or eggplant from different countries of Southeast and East Asia. To decipher virus acronyms see main text and Supplementary Table S1.

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Fig. 1. Bootstrap consensus tree (1000 replicates) of 101 tomato and pepper-infecting begomoviruses from Southeast and East Asia inferred from DNA-A component nucleic acid sequences using the neighbor-joining method. Branches corresponding to partitions reproduced in less than 50% bootstrap replicates are collapsed. All positions containing gaps and missing data were eliminated. There were a total of 2507 positions in the final dataset. Evolutionary analyses were conducted in MEGA5 (Tamura et al., 2011). Sequences were downloaded from GenBank and details of each accession are given in Supplementary Table S1. Phylogenetic groupings A–F are referred to where appropriate in the text and may contain more than one related species.

GenBank. These are most closely related to TbLCYnV and Tobacco leaf curl Thailand virus (TbLCTHV) (Groups F and G in Fig. 1).

2.3. Indonesia (IDN) Tomato-infecting begomoviruses were first detected in tomato samples from Java and Sumatra in Indonesia in 1983. A distinct tomato-infecting begomovirus was detected in samples collected in 1998 in Lembang, Java, and given the name Tomato yellow leaf curl Indonesia virus (TYLCIDV) (Tsai et al., 2006a). From partial sequences from other samples, three distinct groups of begomovirus were detected in infected tomato samples from Java; those related to Ageratum yellow vein virus (AYVV), those forming the new species Tomato leaf curl Java virus (ToLCJaV), and those forming the new species Pepper yellow leaf curl Indonesia virus (PepYLCIV) (Sakamto et al., 2005). A betasatellite was required for AYVV to cause symptoms in tomato, ToLCJaV was generally also associated with a betasatellite, and there was evidence of recombination between AYVV and ToLCJaV (Kon et al., 2006). Only the DNA-A of PepYLCIV was detected infecting peppers and tomatoes in fields near Bogor, Java (Tsai et al., 2006b), though Sakata et al. (2008) showed that the DNA-B they identified in infected samples increased symptom severity in pepper and Nicotiana benthamiana plants. Identified from Sulawesi in 2006, Tomato leaf curl Sulawesi

virus (ToLCSuV) forms a phylogenetic group with PepYLCIV (Group U in Fig. 1). Since 2009, a strain of Tomato yellow leaf curl Kanchanaburi virus (TYLCKaV), very similar to that originally detected in Thailand, has started to emerge as an important threat to tomato and eggplant in Java (Fig. 2; unpublished results).

2.4. Japan (JPN) Low incidence disease of tomato and tobacco caused by begomovirus has been reported from various localities in Japan since the 1960s (Ueda et al., 2008), and a distinct species, Tobacco leaf curl Japan virus (TbLCJV) was identified from infected tomato samples (Shimizu and Ikegami, 1999). Soon afterwards, it was shown that known isolates of TbLCJV had a chimeric genome which may have arisen by recombination between ancestors of TbLCJV and the closely related species Honeysuckle yellow vein mosaic virus (HYVMV). Another recombinant isolate with a major component from HYVMV and a minor component from TbLCJV was also pathogenic on tomato (Kitamura et al., 2004). Phylogenetic analysis of these virus sequences with Eupatorium yellow vein virus (EpYVV) sequences revealed that they were separated into a discrete ‘Far East Asian clade’ distinct from all other begomoviruses (Group H in Figure 1). Sequences of TbLCJV grouped into the HYVMV sub-clade, which was distinct from the EpYVV sub-clade. However,

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importance of HYVV is unclear as TYLCV probably arrived at about this time and then spread rapidly to most regions of the southern Korean peninsula. Phylogenetic analysis of the sequences of TYLCV isolates from this region separated them into two groups; the ‘Masan’ group was most similar to the Japanese ‘Miyazaki’ group, and the ‘Jeju/Jeonju’ group was most similar to the Japanese ‘Tosa/Haruno’ group (Lee et al., 2010). A parallel study of isolates from the same area identified a third group with highest similarity to a group of isolates from China (Kim et al., 2011). Analysis of 16S rRNA sequences indicated that the Korean B. tabaci was most similar to the Q-biotype of B. tabaci from Iran and Nigeria, and since this biotype was present in Korea before the arrival of TYLCV, it was suggested that the TYLCV isolates were introduced to Korea via different routes, and then transmitted by local B. tabaci (Lee et al., 2010). 2.6. Laos Peoples’ Democratic Republic (LAO) There are apparently no early records of leaf curl-like disease in Laos. However, a distinct monopartite virus, Tomato leaf curl Laos virus (ToLCLV) was identified from a tomato sample collected in 1998 (Green et al., 2001). This was associated with a Tomato leaf curl betasatellite (Bull et al., 2004). Despite several recent reports of outbreaks of leaf curl of tomato in Laos, there are no other begomovirus sequences deposited in GenBank. Fig. 2. Direction and likely latest year of recent movement of native tomatoinfecting begomoviruses within Southeast Asia (TYLCKaV, Tomato yellow leaf curl Kanchanaburi virus; TYLCTHV, Tomato yellow leaf curl Thailand virus; ToLCHsV, Tomato leaf curl Hsinchu virus).

there was evidence for many recombination events between members of the Far East Asian clade, and some recombinants within the EpYVV sub-clade were isolated from diseased tomato (Ueda et al., 2008). Distinct from the Far East Asian clade of viruses, Ageratum yellow vein virus (AYVV-[Ishigaki]) strain and Ageratum yellow vein betasatellite (AYVB) were identified as causing severe leaf curling and yellowing of tomato plants on Ishigaki Island in 2005 (Andou et al., 2010). In 1996, while the indigenous tomato-infecting begomoviruses were being studied, a new leaf-curl disease was observed in glasshouse-grown tomato plants in Shizuoka and Aichi prefectures. The causal virus was quickly identified as having a nucleotide sequence similarity of 98% with a mild isolate of Tomato yellow leaf curl virus from Israel (TYLCV-Mld) (Kato et al., 1998). By 2004 TYLCV had spread to other prefectures and could be separated into three phylogenetic groups—Shizuoka (Sz), Aichi (Ai), Nagasaki (Ng)—with 99% identities within the groups. Both Sz and Ai were closely related to TYLCV-Mld, whereas Ng isolates were more closely related to TYLCV-IL. None of the isolates tested had a betasatellite (Ueda et al., 2004). Then, in 2003–2004 there was a sudden and severe outbreak of leaf curl in glasshouse-grown tomato in Shikoku, Kochi prefecture. Phylogenetic analysis of this new strain (TYLCV-[Tosa]) showed it to be more closely related to TYLCV-[Almeria] than TYLCV isolates Ng, Sz, or Ai, suggesting it to be a novel isolate of TYLCV newly introduced to Japan (Ueda et al., 2005). An outbreak of leaf curl on the subtropical island region of Okinawa in 2007 was probably caused by the domestic transportation of infected plants (Ueda et al., 2009). 2.5. South Korea (KOR) Tomato leaf curl was not reported from Korea until recently. Tomato samples collected in 2007 were identified as being infected with Tobacco leaf curl Korea virus (TbLCKV) (Lee et al., 2011), though they group closely with Honeysuckle yellow vein virus (HYVV) from Japan in the Far East Asian clade (Group H in Fig. 1). The

2.7. Myanmar (MMR) The only accessible record of a begomovirus infecting tomato in Myanmar was detected in a sample collected from Hmawbi Township in 1999 and is an apparently monopartite form of Tomato yellow leaf curl Thailand virus (TYLCTHV) (Green et al., 2001), which is generally isolated as a bipartite virus in Thailand and Taiwan (Group A in Fig. 1). 2.8. Malaysia (MYS) The earliest reports of leaf curl of tomato in Malaysia date to the mid-1980s, and a distinct monopartite begomovirus was identified from tomato samples collected in 1997 and named Tomato leaf curl Malaysia virus (ToLCMYV) (Green et al., 2001). This is most similar to ToLCLV from Lao (Group N in Fig. 1). Also present in GenBank is a begomovirus sequence from chilli pepper from 1997, Pepper leaf curl virus (PepLCV; AF414287) (Group D in Fig. 1), though there appears to be no publication associated with this. 2.9. Philippines (PHL) The report of a leaf curl disease transmitted by whiteflies and causing tomato yield losses of up to 80% in Bicol in 1968 (Retuerma et al., 1971) was probably the first record of a begomovirus disease in the Philippines. Diseased tomato samples from Luzon gave a positive reaction with antiserum to Tobacco leaf curl Japan virus (Osaki and Inouye, 1981), but it was not until the early 2000s that sequencing revealed the causal agent as a distinct monopartite begomovirus (Kon et al., 2002), which was subsequently named Tomato leaf curl Philippines virus (ToLCPV). Although the presence in the Philippines of begomovirus in capsicum peppers (and some weeds) had been confirmed using a DNA probe from TYLCTHV (Dolores and Pissawan, 1994), it was not until a diagnostic survey of tomatoes and peppers in Luzon, Cebu and Mindanao was conducted that the begomoviruses were identified (Tsai et al., 2011b). This survey was very brief and looked at relatively few samples, but it identified four distinct begomovirus species; ToLCPV in Luzon and Cebu on tomato and pepper, Tomato leaf curl Cebu virus (ToLCCeV) in all locations on both crops, Tomato leaf curl Mindanao virus

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(ToLCMiV) in Luzon and Mindanao on tomato, and Ageratum yellow vein virus (AYVV) on tomato in Mindanao. The high level of diversity within the ToLCMiV/AYVV group (Group O in Fig. 1) leads to GenBank separating out another species, Tomato leaf curl Cotabato virus (ToLCCoV). Concurrent with the survey, Sharma et al. (2011) detected several different strains of ToLCPV from the Laguna area of Luzon and identified that these were sometimes associated with a betasatellite. ToLCCeV and ToLCPV group together in phylogenetic analysis (Group S in Fig. 1) 2.10. Taiwan (TWN) A leaf curl disease caused by a virus serologically related to Tobacco leaf curl Japan virus (TbLCJV) was first observed in tomato in Taiwan in about 1981 (Green et al., 1987), but did not become widespread until about 1995 (Shih et al., 1995). When the virus was sequenced it was found to be a distinct monopartite begomovirus which was later named Tomato leaf curl Taiwan virus (ToLCTV; Genbank accession U88692) (Group I in Fig. 1). Subsequent surveying and sequencing classified the ToLCTV-Taiwan isolates into three strains (Tsai et al., 2011a). The strain A was common country-wide, whereas the strains B and C were restricted to East and West Taiwan, respectively. A second distinct tomatoinfecting begomovirus, Tomato leaf curl Hsinchu virus (ToLCHsV) was detected at very low frequency in the Hsinchu area of Taiwan in 2000 and 2001, but has not been detected in Taiwan subsequently (Tsai et al., 2011a). However, a genetically similar virus was detected in plants of Ramie (Boehmeria nivea L.) in China, and given the name Ramie mosaic virus (RamMV) (Group P in Fig. 1). The ToLCHsV/RamMV in China was found also to infect tobacco, but as yet has not been detected in tomato in the field in China. Since RamMV was detected infecting ramie in many provinces of China, it may be that ramie represents the original host of ToLCHsV (Li et al., 2010) and the virus spread from mainland China to Taiwan sometime before 2000 (Fig. 2). The third distinct begomovirus detected infecting tomato (in only two samples from Hsinchu in 2003) in Taiwan was identified as a recombinant with Ageratum yellow vein Hualien virus (AYVHuV) (Group O in Fig. 1) as the major component and ToLCTV strain B as the minor component (Tsai et al., 2011a). Having previously been detected in south China, Myanmar and Thailand (Attathom et al., 1994; Green et al., 2001; Li et al., 2004), the bipartite Tomato yellow leaf curl Thailand virus (TYLCTHV) (Group A in Fig. 1) was first detected in Taiwan in 2005 in the west-central tomato production area, suggesting it was then only a recent introduction to Taiwan from its likely origin somewhere in the Thailand-Myanmar-China region (Tsai et al., 2011a; Fig. 2). However, after 2005 TYLCTHV spread rapidly in West Taiwan and then in East Taiwan, often being detected in mixed infection with ToLCTV (Tsai et al., 2011a). Preliminary results from recent surveys indicate that TYLCTHV is tending to displace ToLCTV in many parts of Taiwan now. In 2007, TYLCTHV was detected causing relatively mild symptoms in some hot and sweet pepper (Capsicum spp.) cultivars in the field in Taiwan (Shih et al., 2010), indicating that pepper was as a natural host for TYLCTHV. No other begomovirus species has been detected infecting peppers in the field in Taiwan, and no begomovirus species has been detected infecting eggplant in Taiwan. 2.11. Thailand (THA) The earliest record of a virus causing leaf curling of tomato in Thailand is from 1978, and one of the earliest Asian tomatoinfecting begomoviruses to be characterized and fully sequenced was the bipartite Tomato yellow leaf curl Thailand virus (TYLCTHV) (Attathom et al., 1994; Rochester et al., 1994). Several strains of TYLCTHV (Group A in Fig. 1) were identified from different regions

of the country (Sawangjit et al., 2005a), and there was evidence of recombination between strains (Sawangjit et al., 2005b). When in 2001 samples from Kanchanaburi Province of tomato plants with leaf curl and yellowing, and of eggplant with yellow-mosaic, were tested, they were found to harbor a distinct novel bipartite begomovirus (Green et al., 2003), which was subsequently named Tomato yellow leaf curl Kanchanaburi virus (TYLCKaV) (Group T in Fig. 1). Knierim and Maiss (2007) were some of the first to use rolling circle amplification with Phi29 DNA polymerase of circular DNA molecules to identify and produce full-length clones of TYLCTHV and the monopartite Tobacco leaf curl Thailand virus (TbLCTHV) (Group F in Fig. 1) from tomato grown in a glasshouse in Bangkok. A sequence of Pepper leaf curl virus (PepLCV) from Thailand in 1999 is deposited in GenBank (AF134484) (Group D in Fig. 1). 2.12. Vietnam (VNM) The first begomovirus infecting tomato in Vietnam was identified from a sample collected in 1998 as monopartite, and was sufficiently distinct to be named Tomato leaf curl Vietnam virus (ToLCVV) (Green et al., 2001) (Group E in Fig. 1). Green et al. (2005) reported the detection of strains of the bipartite TYLCKaV in samples of tomato (GenBank DQ169054, DQ169055) and eggplant from southern provinces of Vietnam. Ha et al. (2008) then identified 16 distinct begomovirus species from crops and weeds in Vietnam, including TYLCKaV in eggplant, ToLCVV in tomato and a distinct novel species, Tomato yellow leaf curl Vietnam virus (TYLCVV), from tomato. From the diversity within the 16 species detected it was concluded that Southeast Asia and Vietnam in particular was a main center of diversity of begomoviruses and that bipartite (New World) begomoviruses had been present in the region before continental separation (Ha et al., 2008). Recently, two further distinct monopartite begomoviruses have been detected in Vietnam. Tomato leaf curl Hanoi virus (ToLCHanV) has apparently emerged through recombination with Papaya leaf curl China virus (PaLCuCNV) and Ageratum leaf curl virus (ALCuV), and Tomato leaf curl Hainan virus (ToLCHaV), which was recently identified in southern China but probably evolved from ToLCVV in Vietnam (Ha et al., 2011). Leaf curl started emerging as an important constraint to chilli pepper production in southern and central-coastal provinces of Vietnam in 2010, but the identity of the causal agent has not been published yet. With the prevalence of TYLCKaV in tomato and eggplant in the region, it is likely that this is the virus infecting peppers. 3. Factors possibly affecting the emergence and diversity of begomoviruses infecting solanaceous crops 3.1. Changes in cropping practices It is difficult to gauge the reliability of the statistics on the area planted to, and yield from, tomato, peppers and eggplants in the countries of Southeast and East Asia. From the estimates in the FAOSTAT production database (http://faostat.fao.org/), it appears that production of tomato in China has increased from about 5 million tons per annum in the early 1980s to over 50 million tons pa in 2011 (Fig. 3). Indonesia, the next largest producer in the region, has had a similar rate of increase in production, from about 100,000 tons pa in 1981 to nearly one million tons pa in 2011. There have been smaller increases in production in other countries of the region, and production in Japan appears to have gradually decreased over this period. The increase in production in each country has been through a combination of increased cropping area and increased yields per unit area, suggesting that cropping has become both more intensive and extensive. It seems likely that average field size

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Fig. 3. Changes in estimated total annual production of tomatoes (with 3-year moving averages) for the tomato producing countries of Southeast and East Asia for the period 1981 to 2011 (note that points for China are plotted against the 2nd (right-hand side) Y-axis since these are so much larger than all the other counties. Data from FAOSTAT (http://faostat.fao.org/) accessed in July 2013.

will have increased in some countries, but again, reliable data on this is elusive. Production of both chilli pepper and eggplant has followed similar trends to tomato in each of the countries of the region (FAOSTAT, accessed July 2013). It is difficult to obtain reliable data on what cultivars of tomato, pepper and eggplant were grown in most of these countries 30 years ago, and so it is difficult to determine how cultivar selection has changed since then. With the increasing importance of leaf curl in tomato over so much of the world, great effort has been made to identify resistance to tomato leaf curl and incorporate it into improved tomato cultivars. To date, five major genes for resistance or tolerance (Ty-1 to Ty-5) and many other more minor genes or QTLs have been identified from tomato wild relatives and some major genes have been incorporated into commercial cultivars in ˜ et al., 2010). In Taiwan, the different areas (reviewed by de la Pena Ty-2 resistance was identified in Solanum habrochaites using the then-prevalent ToLCTV (Hanson et al., 2000). This resistance was incorporated into some commercial cultivars released in Taiwan, though it is unclear what proportion of the Taiwan tomato crop came to carry this resistance. Unfortunately, it was quickly apparent that the Ty-2 resistance was not effective against TYLCTHV when it emerged in Taiwan in about 2005, and this is probably in part why TYLCTHV is displacing ToLCTV (Tsai et al., 2011a). With the arrival and spread of TYLCV in Japan, China and Korea, Ty genes have been, or are being incorporated into some of the commercial tomato cultivars for these countries, or cultivars carrying such resistance are being imported to these countries. The use of resistance to begomovirus infection is much less advanced in chilli pepper and eggplant in the region. Resistance to yellow mosaic of eggplant (probably caused by TYLCKaV) has been identified in Vietnam and is being incorporated into a commercial cultivar (S.J. de Hoop, personal communication). To our knowledge, there are as yet no commercial capsicum cultivars carrying resistance or tolerance to begomovirus infection. 3.2. Changes in vector whitefly populations Using DNA microsatellites to identify B. tabaci cryptic species, De Barro et al. (2008) suggested there was an association of the

invasion of Sumatra and Java, Indonesia, by a pepper-infecting begomovirus with an invasion sometime between 1994 and 1999 of B. tabaci, probably from central Thailand. The pepper-infecting begomovirus isolates [now classified as Pepper yellow leaf curl Indonesia virus (PepYLCIV)] had highest DNA-A sequence identity to Tomato yellow leaf curl Kanchanaburi virus (TYLCKaV) from Thailand, and unlike the spread of B- and Q-biotypes of B. tabaci in other parts of the world, the invading whitefly did not displace the local populations, but interbred with them and it was their alleles that subsequently spread rather than the individuals themselves. In Taiwan, the B-biotype has been present in the open field alongside the native populations for many years, while populations of the Q-biotype were detected only in glasshouse production systems, again often in combination with local biotypes (Hsieh et al., 2012). Although there is some suggestion that TYLCTHV is transmitted more efficiently than ToLCTV by individuals from the Taiwan B-biotype population, there have been no reports comparing the transmission efficiency of the B- or Qbiotypes with the local indigenous biotypes in Taiwan. Chu et al. (2006) reported that the exotic Q-biotype was probably imported into China from the Mediterranean region on ornamental crops in about 1999. Here, the Q-biotype (Med) performed better than the local ZHJ2 biotype (Asia II 1) on either uninfected or TYLCVinfected tomato plants, and association of the Q or ZHJ2 biotypes with TYLCV on cotton (a non-host of TYLCV), did not affect their fecundity and longevity. These results indicate that the alien Qbiotype whitefly, but not the indigenous ZHJ2 biotype, was likely to become the major vector of TYLCV (Li et al., 2011). Pan et al. (2012) showed that Q-biotype whiteflies acquired significantly more TYLCV DNA, reached the maximum viral load in a substantially shorter period of time, and exhibited significantly higher horizontal viral transmission frequency than B-biotype whiteflies. Consistent with the concomitant eruption of TYLCV in tomato fields of China following the rapid invasion of whitefly Q-biotype after its introduction in 2003, these results suggested that the epidemiology of TYLCV in China was aided differentially by the invasive biotype B and Q whiteflies through horizontal but not vertical transmission of the virus (Hsieh et al., 2007; Pan et al., 2012). The horizontal transmission significantly may increase the proportion of viruliferous

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whiteflies in a population of Q-biotype compared to in a population of B-biotypes. It is apparent that, study of the diversity and prevalence of vector whitefly populations has received greater attention in some countries of SE Asia than in others, so the coverage of knowledge is rather patchy. Also, because the situation has been observed to change so rapidly in some of the areas, ideally there would be continual monitoring of the whitefly populations across the region so more definite predictions and associations between virus emergence and specific whitefly populations could be made. 3.3. Virus evolution, recombination and component capture Duffy and Holmes (2008) using the then-published sequences of tomato-infecting begomoviruses estimated the mean genomic substitution rate to be 2.88 × 10−4 nucleotide substitutions per site per year (subs/site/year)—a rate in line with those estimated previously for mammalian ssDNA viruses and RNA viruses—although this rate could be confounded by frequent recombination within the virus genomes. These results suggested that the high evolutionary rate of begomoviruses is not primarily due to frequent recombination and may explain their ability to emerge in novel hosts. However, as indicated above, there is evidence for considerable recombination between the members of the distinct Far East Asian clade of begomoviruses in Japan, such that tomato-infecting isolates have been detected within each of the subclades (Ueda et al., 2008). Sawangjit et al. (2005b) found statistically significant evidence for recombination events between TYLCTHV isolates, including identifying regions of high homology to TYLCV, ToLCLV, and ToLCTV in different TYLCTHV isolates. Recombination analysis on the newly emerging Tomato leaf curl Hanoi virus (ToLCHanV) in Vietnam indicated that it has arisen through recombination between Papaya leaf curl China virus (PaLCuCNV) and Ageratum leaf curl virus (ALCuV) (Ha et al., 2011). It also appears likely that Tomato leaf curl Hainan virus (ToLCHaV) has evolved by recombination between ToLCHanV and ToLCVV (Zhang et al., 2010). On the other hand, recombination between the monopartite ToLCTV and the bipartite TYLCTHV has not been detected yet in Taiwan despite these two viruses often occurring as mixed infections in the field (Tsai et al., 2011a). Recombination analysis indicated that all but one of the 17 begomovirus isolates (comprising 4 discrete species) sequenced from samples of the perennial shrub, Sauropus androgynous (commonly known as star gooseberry) from Thailand were probably the product of one or more recombination events. Although not in the Solanaceae, the results indicated that S. androgynus plants act as natural hosts as well as potential nurseries for genetic recombination between begomovirus species and strains, several of which potentially also infect solanaceous plants (Shih et al., 2013). In Japan, using cloned TYLCV and Ageratum yellow vein betasatellite (AYVB) it was demonstrated that TYLCV could transreplicate with AYVB in Nicotiana benthamiana and tomato plants. A mixed infection of TYLCV and AYVB in tomato induced more severe symptoms of upward leaf curl, stunting, vein thickening, and swelling compared with TYLCV infection alone, and could be transmitted by vector whiteflies among plants. These results indicated that TYLCV possesses the potential to induce severe leaf curl by associating with AYVB (Ueda et al., 2012). Similarly, Blawid et al. (2008) showed that the monopartite viruses ToLCVV or TYLCVV were capable of replicating a betasatellite DNA and of transreplicating the DNA-B component of TYLCTHV. 4. Discussion and conclusion Although all the viruses mentioned in this review were identified from naturally infected plants in the field or glasshouse,

this does not necessarily mean all were present at high incidence or causing severe disease or significant loss in production. In 1998, Zeidan et al. reported that the whitefly-transmitted geminiviruses from Southeast and East Asia constitute a cluster of geminiviruses distinct from those of the Middle East, Southeast Europe and of the Americas. By 2005 many more begomovirus species native to the region had “emerged” and been identified, and TYLCV-IL and TYLCV-Mld had become established in Japan (Green et al., 2005). Now, as far as we can determine, including TYLCV, at least 36 distinct begomovirus species have been identified from tomato and/or pepper in Southeast and East Asia (Table 1). Although the peak period for identification of novel distinct species was in the early 2000s, this is probably a reflection of the increased interest in this group of viruses and the increased ease with which they could be identified by sequencing during this period, and cannot be used as any measure of the rate of evolution or emergence of this group of viruses. The great diversity of apparently local species and strains of monopartite begomoviruses and betasatellite molecules identified from the region supports the suggestion by Ha et al. (2008) that subcontinental Southeast Asia is a major center of diversity for these viruses. The frequent detection of many of these viruses or near relatives (including recombinant forms and satellite DNAs) in crop wild relatives and weed species in the region supports the hypothesis that the weeds and wild crop relatives act as reservoirs for the viruses and are where the viruses have evolved through mutation and recombination. Many of the ‘local’ begomovirus species have relatively localized geographic distributions; ToLCPV and ToLCCeV have only been detected in the Philippines, ToLCLV has only been detected in Laos, and ToLCSuV has only been detected in Sulawesi, Indonesia. This again suggests that these tomatoinfecting species have evolved and been selected for from ancestral species present in the native plant species of each location. However, it is also apparent that the two bipartite tomato-infecting species native to the subcontinent (TYLCTHV and TYLCKaV), are prevalent across a much wider area. As an aside, the great number of recombinant begomovirus isolates being detected in this region (as well as elsewhere in the world) is leading to complication in species delineation and naming; should a clearly recombinant DNA-A component with a sequence identity of less than 89% to any other DNA-A component be regarded as representing a novel begomovirus species and hence require a new species name? The expansion and intensification of cropping of tomato, pepper and eggplant (none of which originate in the region) in most of the countries of the region over the last 30–40 years coincides with increased populations of B. tabaci whiteflies (including in some locations the more polyphagous and virus-vectoring-efficient B- and Q-biotypes) and increased incidence of leaf curl diseases in these crops. Thus, it seems likely (though it is not possible to prove) that the intensification and expansion of cropping promoted increased populations of whiteflies, which resulted in greater spread of viruses from native vegetation into, and within, exotic crop species. At the same time, increased trade and movement of fresh produce and plant material spread native begomovirus species and local whitefly haplotypes within, and different strains of TYLCV and B- and Q-biotypes of B. tabaci into and within, the region. Thus, since the 2005 assessment (Green et al., 2005), TYLCTHV has spread into and started to displace the native ToLCTV in Taiwan (Tsai et al., 2011a), TYLCKaV has spread from the subcontinent to Java, Indonesia, and TYLCV strains have emerged to become major constraints to production in China (in 2006) and Korea (in 2008), though apparently nowhere else in the region. The prevalence of TYLCTHV and TYLCKaV over a wide area, including their spread into Taiwan and Java respectively, seems likely to be due in part to their greater aggression and virulence; TYLCTHV

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at least can overcome some of the leaf curl resistance commonly deployed. In conclusion, the major contributory factors for the emergence and spread of tomato, pepper and eggplant-infecting begomoviruses in Southeast and East Asia are probably expansion and intensification of production systems, leading to greater selection for more aggressive or crop-adapted begomovirus variants that have arisen through mutation, recombination, pseudo-recombination, and acquisition of satellite DNA molecules. Intensification of cropping systems probably also resulted in increased populations of indigenous and introduced whitefly cryptic species (haplotypes), increasing the incidence and rate of spread of the viruses. There has been introduction of begomovirus species from outside the region and spread of introduced and native species within it, probably through the movement, by humans, of infected plant materials. Some of the more recent changes in begomovirus species prevalence within an area may have been promoted by the deployment of tomato cultivars carrying some level of tolerance or resistance to only certain species of begomovirus, while climatic changes may have broadened the range of locations favorable for the vector whiteflies, and permitted the spread of the viruses to more northern latitudes and higher elevations. From this analysis, it is apparent that information on the prevalence and diversity of begomoviruses across South and Southeast Asia remains somewhat patchy, and is not being updated fast enough to keep pace with the evolving situation in the region. This even more is the case for the vector whitefly populations. In order to better understand the current (changing) situation and be able to develop strategies for the sustainable management of leaf curl diseases, the work initiated to more finely map the distribution of the different begomovirus genotypes (species) and the different whitefly haplotypes across the region needs to be greatly expanded. Also, the reactions of tomato lines carrying different combinations of resistance (Ty-) genes need to be assessed against the different begomovirus genotypes prevalent in more areas of the region so that tomato cultivars with the most appropriate Ty-gene or combination of Ty-genes can be selected or developed, and deployed in each location. Acknowledgements This work was in part funded through the German Federal Ministry for Economic Cooperation and Development (BMZ), Deutsche Gesellschaft für Internationale Zusammenarbeit (GIZ) GmbH project no. 81141863. The views expressed are not necessarily those of the BMZ/GIZ. We acknowledge the considerable input of Dr. Sylvia K. Green, formerly of AVRDC – The World Vegetable Center, in initiating the work on Begomoviruses in Asia. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/ j.virusres.2013.12.026. References Andou, T., Yamaguchi, A., Kawano, S., Kawabe, K., Ueda, S., Onuki, M., 2010. Ageratum yellow vein virus isolated from tomato plants with leaf curl on Ishigaki Island, Okinawa, Japan. Journal of General Plant Pathology 76 (4), 287–291. Attathom, S., Chiemsombat, P., Kositratana, W., Sae-Ung, N., 1994. Complete nucleotide sequence and genome analysis of bipartite tomato yellow leaf curl virus in Thailand. Kasetsart Journal, Natural Sciences 28, 632–639. Blawid, R., Van, D.T., Maiss, E., 2008. Transreplication of a Tomato yellow leaf curl Thailand virus DNA-B and replication of a DNAß component by Tomato leaf curl Vietnam virus and Tomato yellow leaf curl Vietnam virus. Virus Research 136 (1/2), 107–117.

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Please cite this article in press as: Kenyon, L., et al., Emergence and diversity of begomoviruses infecting solanaceous crops in East and Southeast Asia. Virus Res. (2014), http://dx.doi.org/10.1016/j.virusres.2013.12.026