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Occurrence, distribution, and management of tomato yellow leaf curl virus in China


Tomato yellow leaf curl virus (TYLCV), belonging to the genus Begomovirus in the family Geminiviridae, is the most damaging virus for global tomato production. This virus has become one of the most studied plant viral pathogens because of its huge economic importance. Since it was firstly identified in Shanghai, China, in 2006, it has been spread to most parts of the country. The widespread occurrence, rapid spread to new regions, and enormous damage to tomato production, makes it an important agricultural pathogen in China. TYLCV has been characterized extensively at the molecular level. This review is focused on the occurrence and distribution of all TYLCV isolates in China, providing valuable information for further epidemiological studies. In addition, management strategies for TYLCV are also proposed, with the ultimate goal to prevent and control the further occurrence of this viral disease.

An introduction to geminiviruses and tomato yellow leaf curl virus (TYLCV)

Geminiviridae is the largest plant virus family. Geminiviruses are non-enveloped plant viruses with small circular single-stranded (ss) DNA genomes of 2.5 to 3.0 kilobases (kb) in a monopartite or bipartite arrangement encapsidated in twinned virions. Based on their genome features, insect vector, and host range, geminiviruses are divided into fourteen genera, and the genus Begomovirus is the largest genus, containing 445 virus species to date (Fiallo-Olivé et al. 2021). Begomoviruses have small genomes, composed of one (monopartite) or two (bipartite) DNA molecules of about 2.7 kb with similar genome structures and encoding 6–8 multifunctional typical proteins (Fiallo-Olivé et al. 2021; Devendran et al. 2022). TYLCV is a monopartite begomovirus and one of the most devastating plant pathogens worldwide. The symptoms of TYLCV in infected tomato plants include yellowing, chlorosis and leaf curling of young leaves, stunted growth, and marked reduction of leaf size (Fig. 1a, b), which causes up to 100% yield loss in tomato. The widespread occurrence and tremendous spread rate to new regions make it an important pathogen with enormous economic importance worldwide (Prasad et al. 2020).

Fig. 1
figure 1

Disease symptoms caused by tomato yellow leaf curl virus (TYLCV) and genome organization of TYLCV. a Disease symptoms induced by TYLCV in Solanum lycopersicum plants in the field. b Specific DNA bands detected in infected tomato plants by PCR using TYLCV-specific primers. Lanes 1 and 2 indicate DNA extracted from two independent TYLCV-infected S. lycopersicum plants. M: DNA ladder marker, NC: negative control using DNA extracted from uninfected tomato plants. c Schematic representation of TYLCV genomic organization. Open reading frames encoded on the virion-sense (V) strand and complementary-sense (c) strand are denoted (V1, V2, C1, C2, C3, and C4); the new ORFs V3 and C5 have been identified recently (Gong et al. 2021). d Disease symptoms induced in Nicotiana benthamiana (Nb), S. lycopersicum (Sl), and Arabidopsis thaliana (At) plants agroinoculated with mock (empty vector) or the infectious clones of TYLCV. Plants were photographed at 25 days post inoculation (dpi). Bars = 9 cm. e Western blot analysis of total proteins from (d) with anti-TYLCV-coat protein (CP) antibodies. Ponceau S staining of the large Rubisco subunit (RbcL) served as the loading control. Note: The TYLCV Beijing isolate (GenBank Accession No. MN432609) was used in this figure

The first report of tomato yellow leaf curl disease (TYLCD) came from the Jordan Valley of Israel in the 1950s, and it was first called ‘tomato yellow top’ (Cohen and Harpaz 1964). According to a study in 1986, the populations of whiteflies increased correlating with the occurrence of TYLCD (Cohen and Berlinger 1986). In 1988, the viral particles of TYLCV isolated from tomato and datura plants were observed with typical twinned structures, resembling those known for geminiviruses (Czosnek et al. 1988). In 1991, it was found that TYLCV has a circular ssDNA molecule as its genomic component (Navot et al. 1991). Since then, different strains of this virus have been identified around the globe (Cohen and Harpaz 1964; Lefeuvre et al. 2010; Oh et al. 2013; Hosseinzadeh et al. 2014; Mabvakure et al. 2016; Pérez-Padilla et al. 2020). With the outspread of TYLCV in Jordan, Lebanon, Sudan, Tunisian, and other countries, interest in this virus has increased for researchers. So far, more than 550 articles related to TYLCV can be found in PubMed (, demonstrating its scientific and economic importance.

TYLCV encodes six canonical viral proteins (the virion-sense strand contains two ORFs, V1 and V2, and the complementary-sense strand encompasses four ORFs, C1, C2, C3, and C4) (Fig. 1c). The coat protein (CP) encoded by the V1 ORF is required for the packaging of the viral DNA and the spread by insect vectors (Wei et al. 2017; Fondong et al. 2013). The V2 ORF encodes the V2 protein, which is an RNA silencing suppressor of transcriptional gene silencing (TGS) and post-transcriptional gene silencing (PTGS) (Glick et al. 2008; Wang et al. 2014, 2018, 2020). The replication-associated protein (Rep) encoded by the C1 ORF is essential for reprograming the cell cycle and mediating rolling circle replication (RCR) of the viral genome (Hanley-Bowdoin et al. 2013; Basak 2016). The C2 ORF encodes the transcription activator protein (TrAP) and can also suppress TGS, PTGS, protein ubiquitination, and jasmonic acid (JA) signaling (Lozano-Duran et al. 2011; Luna et al. 2012; Rosas-Diaz et al. 2016). The replication-enhancing protein (REn) is encoded by the C3 ORF and is vital for viral replication by interacting with POLA2, a subunit of DNA polymerase α, and POLD2, a subunit of DNA polymerase δ. The viral C3 protein may selectively mediate the effective recruitment of DNA polymerase δ over ε to enhance geminivirus replication (Wu et al. 2021). Geminivirus C4 displays a broad diversity of functions during the viral infection, both within and between geminiviruses (Medina-Puche et al. 2021). TYLCV C4 protein also has multiple roles in causing disease symptoms, participating in the viral movement, and repressing host DNA methylation and RNA silencing (Rojas et al. 2001; Kon et al. 2007; Luna et al. 2012; Guo et al. 2022). Recently, several studies have shown that geminiviruses, including TYLCV, encode additional small proteins with different subcellular localization patterns and virulence functions (Gong et al. 2021, 2022; Li et al. 2021a, b; Chiu et al. 2022; Zhao et al. 2022). Among these small proteins, the V3 protein of TYLCV is a Golgi- and partially endoplasmic reticulum (ER)-localized protein, which functions as an RNA silencing suppressor and a viral cellular movement protein (Gong et al. 2021, 2022). The TYLCV C5 protein is considered as a pathogenicity determinant and RNA silencing suppressor (Zhao et al. 2022).

TYLCV has a very diverse host range and it is reported to cause severe epidemics in Phaseolus vulgaris and solanaceous plants (Navas-Castillo et al. 1999). Notably, the infectious clone of TYLCV can effectively infect model plants Nicotiana benthamiana and Arabidopsis thaliana under laboratory conditions (Fig. 1d, e), which helps accelerate the studies of the biology of TYLCV and its interactions with both plant and vector.

TYLCV infection dramatically reduces plant productivity, resulting in substantial economic losses, and 20–100% yield loss depending on the plant growth stage at the time of infection (Levy and Lapidot 2008). Because of the economic importance of TYLCV and its devastating and widespread nature, efforts have been made to study TYLCV pathogenesis and develop tolerant or resistant plants.

Occurrence and distribution of TYLCV in China

Geographical distribution

Although TYLCV quickly became a devastating pathogen of tomato in the tropics, subtropics, and warm temperate regions shortly after it was first discovered, in China, however, there was no report on this virus before 2006. Wu et al. (2006) firstly observed that a yellow mosaic disease appeared on tomato plants with 90% disease incidence during March 2006 in fields of Sunqiao, Shanghai, China, and then confirmed that TYLCV isolate SH2 (GenBank Accession No. AM282874.1) caused this viral disease. Since then, multiple TYLCV isolates have been reported in China. Based on the published articles and annotated sequences, 99 species of geminiviruses with over 1600 isolates in total had been isolated, identified, and characterized in China by the end of 2021 (Li et al. 2022). Among them, TYLCV is the geminivirus with the highest number of isolates: 415 isolates with full-length nucleic acid sequences and distributed in most provinces of China have been identified so far (Table 1 and Additional file 1: Table S1), further demonstrating that this viral pathogen is a huge threat to agriculture because of its widespread incidence and tremendous rate of spread.

Table 1 Geographical distribution of TYLCV isolates in China

The top 5 provinces with the highest number of TYLCV isolates are Yunnan Province (119 isolates), Shandong Province (76 isolates), Henan Province (31 isolates), Beijing (29 isolates), and Hebei Province (21 isolates) (Additional file 2: Table S2). Of note, Yunnan, Shandong, and Henan are important provinces with the largest scale of tomato cultivation in China. Therefore, it is expected that most TYLCV isolates are isolated and identified in these provinces. TYLCV is also present in provinces where geminivirus species are rare (Li et al. 2022). For example, in Beijing, Shanxi, and Shaanxi, TYLCV is the dominant geminivirus species. In short, TYLCV has been spread over most provinces of China in recent 16 years (Table 1).

Host plants

A major challenge in controlling any pathogen is its maintenance in alternate hosts. TYLCV has a very diverse host range, and it has been detected in 49 species belonging to 16 families (Papayiannis et al. 2011). In China, TYLCV infects 25 species of plants, which include 14 species of cash crop plants and 11 species of non-cash plants (Additional file 3: Table S3). Fourteen species of cash crop plants include Solanum lycopersicum (tomato), Capsicum annuum (pepper), Vigna unguiculata (cowpea), Capsicum frutescens (millet pepper), Nicotiana tabacum (tobacco), Phaseolus vulgaris (kidney bean), Cucurbita moschata (pumpkin), Malus domestica (apple), Abutilon theophrasti (abutilon), Gossypium hirsutum (cotton), Abelmoschus esculentus (okra), Agastache rugosa (herba agastaches), and Solanum melongena (eggplant). Among these, the most affected plant is tomato, from which a total of 360 isolates of TYLCV have been identified, accounting for 85% of all isolates. Tomato, native to South America, belongs to the Solanaceae family and is one of the most important fruits and vegetable crops globally. There is a high tomato production in China. For example, in 2019, 62,869,500 tons of tomatoes were produced from tomato fields covering a total of 1,086,800 hm2, accounting for 34.78% and 21.60% of the world's total harvested area and annual production, respectively (Zeng et al. 2021). Despite the high yield, demand far exceeds tomato production in China. One of the most important causes of yield loss affecting tomato is TYLCD, and TYLCV is one of the most important pathogens causing the disease. In addition, TYLCV can also combine with other viruses to form a disease complex, leading to enhanced symptoms on hosts. For example, the synergistic infection of TYLCV and tomato chlorosis virus (ToCV) results in a high disease severity index and causes dramatic losses (Li et al. 2022).

There are 9 isolates of TYLCV identified in pepper in three provinces in China, indicating that pepper is also a primary host of TYLCV in China. TYLCV also infects multiple weeds, including Acalypha australis, Alcea rosea, Agastache rugosa, Abelmoschus esculentus, and Viola prionantha (Additional file 3: Table S3). These weeds are considered alternate hosts, which provide a storehouse of inoculum during the growing season as well as crop-free periods, and must be taken into consideration when devising control strategies.

Of note, the damaging TYLCD is caused by many other begomoviruses in addition to TYLCV globally. In China, there are over 20 geminivirus species that can damage tomato in the field (Fig. 2) (Cui et al. 2004; Li et al. 2004, 2020, 2022; Xie et al. 2013a, b; Yan et al. 2021). Interestingly, tomato yellow leaf curl China virus (TYLCCNV) is a typical monopartite geminivirus associated with a tomato yellow leaf curl China betasatellite (TYLCCNB) in the field (Cui et al. 2004; Hu et al. 2020). Infection by TYLCCNV alone in tobacco or tomato plants fails to induce any apparent symptoms (Cui et al. 2004), while TYLCCNB is required for inducing dwarfing, leaf curling, yellow mosaic patterns, and stem distortion symptoms in tobacco or tomato plants infected by this virus complex. In most conditions, there is no satellite associated with the infection of TYLCV (Yan et al. 2021).

Fig. 2
figure 2

Phylogenetic tree based on the full-length nucleic acid sequences of the geminivirus species from China that can infect tomato in the field. Numbers on the nodes suggest the percentage of bootstrap support from 1000 replicates

Transmission of TYLCV

TYLCV is transmitted between plants by an insect vector, Bemisia tabaci (commonly known as whitefly), in a persistent-circulative or persistent-propagative manner (Gottlieb et al. 2010; He et al. 2020). Whitefly is a cryptic species complex composed of 35 putative cryptic species (Luan et al. 2014). They attack more than 600 plant species and cause damage to plants through direct feeding and transmission of plant viruses (Boykin and De Barro 2014; Xia et al. 2021). Within this complex, the putative Middle East-Asia Minor 1 (MEAM1) and Mediterranean species (MED), known formerly as the ‘B biotype’ and ‘Q biotype’, respectively, are economically important pests that cause severe crop losses through direct feeding and transmission of plant viruses (Navas-Castillo et al. 2011). MED has a higher ability to develop insecticide resistance than other species, while MEAM1 is characterized by high fecundity and a broad host range (Ghanim et al. 2014). B. tabaci first appeared in China in the late 1940s. However, the first expansion of B. tabaci did not caused great harm until the appearance of the B biotype in the mid-1990s (Luo et al. 2002). A new biotype of whitefly with a higher ability to develop insecticide resistance, named the Q biotype, was first found in Yunnan Province of China in 2003 and rapidly expanded throughout China (Chu et al. 2007; Pan et al. 2011). Although B and Q biotype rapidly invaded the entire country, TYLCV was not identified until 2006 in China. Due to the almost simultaneous emergence of TYLCV and Q biotype, some studies hypothesized that the two exist in a stronger reciprocal relationship than TYLCV and B biotype and demonstrated that TYLCV was indirectly mutualistic to the Q biotype (Pan et al. 2013). In addition, there is a significant difference in the accumulation of viruses between viruliferous Q-infected leaves and viruliferous B-infected leaves at 7 days after the initial inoculation, with the former being higher than the latter (Shi et al. 2014). Similarly, Q biotypes have been confirmed to be the predominant pathogenic vector of TYLCD in China and are responsible for TYLCD outbreaks in America (Gilbertson et al. 2015). These results offer an orientation for TYLCV management and TYLCD prevention.

During the last 20 years, the transovarial transmission of TYLCV has been reported in two invasive species of the B. tabaci complex (B and Q biotype whiteflies) (Fiallo-Olivé et al. 2020). However, the study of transovarial transmission of TYLCV by seven whitefly species indigenous to China showed that TYLCV virions were detected in eggs of all these species except one and in nymphs of two species but in none of the ensuing adults of all the species. These results suggest that these indigenous whiteflies cannot transmit TYLCV transovarially (Guo et al. 2019). Transovarial transmission is a feature of the circulative propagative plant virus. Many studies have also focused on the potential replication of TYLCV in its vector. Although there was controversy around this topic, He et al. recently provided evidence of the replication of TYLCV in the whitefly vector (He et al. 2020). Their findings revealed that TYLCV has evolved to induce and recruit insect DNA synthesis machinery to support its replication in vector salivary glands (He et al. 2020), which provides insights into how a plant virus may evolve to infect and replicate in an insect vector.

Interestingly, seed transmission has previously been reported in some RNA viruses, but geminiviruses have not previously been described as seed-borne viruses. In 2013 and 2014, TYLCV was detected in young tomato plants derived from fallen fruits of TYLCV-infected tomato plants in Korea (Kil et al. 2016), indicating TYLCV-IL could be transmitted via seeds, and tomato plants germinated from TYLCV-infected seeds might be an inoculum source of TYLCV. However, this finding was then revisited with a different result by a different laboratory in other tomato-growing areas. Pérez-Padilla et al. showed that TYLCV DNA was detected in tomato and N. benthamiana seeds collected from plants naturally or experimentally infected with TYLCV-IL, supporting its seed-borne nature (Pérez-Padilla et al. 2020). While the significant reduction in TYLCV DNA load after surface disinfection of tomato seeds suggests that the virus can be the contaminant of the seed coat, transmission assays carried out with seven tomato genotypes and more than 3,000 tomato plants revealed no evidence of seed transmission from "surface-disinfected" or untreated seed for two Mediterranean isolates of TYLCV-IL (Pérez-Padilla et al. 2020). Supporting this finding, Tabein et al. (2021) also found no evidence for the tomato seed transmissibility of tomato yellow leaf curl Sardinia virus (TYLCSV), one of the agents inducing the TYLCD. Therefore, TYLCV-IL is seed-borne but is not seed transmitted in tomato or N. benthamiana, suggesting that transmission through seed is not a general property of TYLCV.

Diagnosis of TYLCV

Early detection and precise diagnosis of TYLCV is a crucial step for preventing the possible spread of infectious disease and minimizing losses. The application of sensitive and specific detection methods is fundamental for managing TYLCV. The traditional method of identifying TYLCV is through visual observation of symptoms. This is often possible only after major damage has already been done to the crop, and a trained person can screen numbers of plants in the field by walking along the plant rows. However, symptom-based diagnosis of TYLCV is unreliable as asymptomatic infection often occurs at early stages, on one hand, and other plant viruses might cause similar symptoms, on the other hand. It is also crucial to accurately confirm the viral species infecting the plants. Currently, various methods have been developed to detect TYLCV, mainly by identifying the presence of viral protein such as the coat protein (CP) of TYLCV (protein-based detection) or by testing the presence of TYLCV DNA (nucleic acid-based detection) (Fig. 3).

Fig. 3
figure 3

Schematics of the protein- and nucleic acid-based diagnosis of geminiviruses, including TYLCV. ELISA, enzyme-linked immunosorbent assay; PCR, polymerase chain reaction; RCA, rolling circle amplification; LAMP, loop-mediated isothermal amplification; RPA, recombinase polymerase amplification; NGS, next-generation sequencing

Protein-based detection of TYLCV

Serological methods, such as enzyme-linked immunosorbent assay (ELISA), are based on the reliable detection of the CP of TYLCV using polyclonal or monoclonal antibodies. In the ELISA test, plant samples are immobilized to a solid surface. If TYLCV is present in the sample, the coat protein of TYLCV will interact with the primary antibody, which is then complexed into a secondary antibody conjugated with a reporter molecule, commonly an enzyme, to enable the detection of the virus by producing the chromogenic products (Fig. 3). In this approach, a high-quality TYLCV-specific antibody is a prerequisite for the sensitive and specific detection of TYLCV. Antibodies have been raised for TYLCV, and different types of ELISA such as dot-ELISA and direct tissue blot immunoassay have been developed to detect TYLCV from field tomato and whitefly samples. The developed dot-ELISA can be used to detect TYLCV from tissue crude extract diluted at 1:5,120 (w/v, g/mL) and viruliferous whitefly homogenate diluted at 1:128 (individual whitefly/μL) (Xie et al. 2013a, b). Due to their simplicity and low cost, ELISA is the most suitable method for the high-throughput analysis of samples in a short time.

Nucleic acid-based detection of TYLCV

Detection methods based on the nucleic acids of TYLCV can be classified into polymerase chain reaction (PCR) and isothermal amplification, such as rolling circle amplification (RCA), loop-mediated isothermal amplification (LAMP), and recombinase polymerase amplification (RPA). In the past decade, high-throughput sequencing technologies, also known as next-generation sequencing (NGS), have revolutionized the discovery and characterization of geminiviruses (Fig. 3). A few of such methods are described here.

The PCR technique is the most popular technique used in the molecular characterization of TYLCV. After amplification of DNA regions in TYLCV using specific primers, subsequent DNA sequencing can be used to confirm TYLCV infection. The PCR method is highly sensitive and suitable for routine detection of TYLCV in laboratories. It can also be used to detect TYLCV from both tomato plants and whiteflies without extraction or purification of nucleic acids (Atzmon et al. 1998). However, using the PCR-based detection method for in-field diagnosis is a challenge as it requires expensive and specific equipment.

RCA is an isothermal amplification process that has led to a revolution in the diagnosis of TYLCV and related geminiviruses (Haible et al. 2006). It uses the DNA polymerase of bacteriophage phi29 to synthesize multiple copies of circular DNA molecules in a nonspecific manner. After annealing of primers to the single-stranded circular molecule, the polymerase reaches the primer binding site, displaces the newly synthesized strand, and goes on with DNA synthesis for several rounds at 30 °C (Johne et al. 2009). This mechanism produces a long concatemeric single-stranded DNA, which can be subsequently digested with the single-cutting restriction enzyme to yield fragments of full-genome length of TYLCV, cloned, and sequenced (Yang et al. 2014, 2017). As specific primer sequences are not required for this technique, RCA enables the detection of unknown geminiviruses. In addition, RCA has a higher sensitivity than PCR and can be used to detect geminivirus from dried plant samples (Shepherd et al. 2008).

LAMP is another isothermal amplification process conducted at a constant temperature of 60–65 °C. It uses the strand displacement and auto-cycling activity of Bacillus stearothermophilus (Bst) DNA polymerase. In the LAMP method, two inner primers and two outer primers are required to generate loops and displace newly generated strands. With the help of two different loop primers, more DNA products could be synthesized, and the resulting products can be visualized by agarose gel electrophoresis and/or a naked-eye system. LAMP has been used to detect TYLCV, maize streak virus, and several other begomoviruses, such as squash leaf curl virus, tomato leaf curl Bangalore virus, and tomato leaf curl New Delhi virus (Fukuta et al. 2003; Kuan et al. 2010; Tembo et al. 2020). The major limitation of the LAMP method is primer design.

RPA amplifies target DNA by using recombinase, DNA polymerase, and single-stranded DNA binding protein (SSB). In the RPA assay, SSB binds the primers and scans for the target sequences. The primers recombine with the target, and the polymerase extends the 3’ end of the invading primer using the opposite strand as a template. Exponential amplification is achieved by the cyclic repetition of this process (Lobato and O'Sullivan 2018). RPA-based assays have been developed to detect TYLCV from crude extracts (Londono et al. 2016). Coupled to a portable lateral flow device, RPA can detect 0.5 pg of TYLCV DNA after 30 min at 37 °C without specialized equipment (Zhou et al. 2022).

NGS is a promising technique for identifying geminiviruses without prior knowledge or sequence information of the virus (Wu et al. 2010). In response to virus infection, the host plant employs the antiviral RNA silencing machinery to generate virus-derived small interfering RNAs, which can be assembled into contigs covering partial or complete virus genomes. Following further cloning and sequencing, NGS allows rapid and simultaneous detection of all known or unknown viral sequences present in a sample (Yang et al. 2021). In the past years, NGS has been successfully used to rapidly identify TYLCV and unknown geminiviruses from different hosts, including woody plants, such as mulberry mosaic dwarf-associated virus and apple geminivirus (Liang et al. 2015; Ma et al. 2015).

TYLCV management

Since TYLCV is an obligate intracellular parasite, the plant disease caused by this virus is incurable in field conditions, and management of TYLCV is a major concern worldwide (Rojas et al. 2018). Therefore, the success in management of TYLCV disease is dependent on good agricultural practices before, during, and after the growing season.

Before planting

Before planting or transplanting, it is critical to use virus-free and insect-free transplants and, if possible, resistant varieties. Growing resistant varieties is ideal and eco-friendly to control TYLCV disease. Six quantitative trait loci, namely Ty-1/3, Ty-2, Ty-4, ty-5, and Ty-6, have been identified from wild tomato species (Lapidot et al. 2014, 2015; Caro et al. 2015; Yan et al. 2021). These resistance genes/loci have been introduced into commercially acceptable cultivars during the past decades via traditional breeding methods and have played vital roles in rendering plant resistant to TYLCV and several begomoviruses. However, they are ineffective against the entire suit of tomato-infecting begomoviruses, and resistance might be overcome by TYLCV-betasatellite disease complexes (Voorburg et al. 2020).

After selecting the variety and source of planting material, it is important to determine the planting dates and field location. In general, when viral infection of plants occurs at their early developmental stages, the disease symptoms caused by TYLCV will be more severe, and the yield loss will be higher. If the population information of whitefly and virus pressure of TYLCV is available, new planting can be established when the population of whitefly and sources of TYLCV inoculum are at the lowest levels. When possible, protected culture and row covers can be used to exclude whiteflies, especially for high-value vegetable crops grown in greenhouses. Furthermore, growing plants with adequate nutrition and water is helpful in improving soil health, plant immunity, and yield.

During the growing season

As the severity of the disease caused by TYLCV is correlated with the host, the titer of virus inoculum, and the population of whiteflies, it is vital to inspect the field frequently during the growing season. The population of whiteflies in protected cultures and the open field could be monitored using yellow sticky cards. At present, the application of insecticides is the most commonly used approach to control the population of insect vectors. However, one of the problems with using insecticides is the emergence of insect vector populations with insecticide resistance (Horowitz et al. 2004; Gilbertson et al. 2015). This is well documented for the supervector B. tabaci in China (Gilbertson et al. 2015). Thus, rotation of insecticides with different modes of action during a growing season is recommended to minimize the development of insecticide resistance in vector. An alternative approach for controlling insect vectors is to release biocontrol reagents such as predators, parasitoids, and fungi to reduce vector populations.

Roguing is a practice that involves the removal of TYLCV-infected plants during the growing season. This can reduce sources of virus inoculum and is most helpful in slowing down the spread of TYLCV if the incidence of the virus is low. To avoid releasing viruliferous whiteflies, rogued plants should be immediately sealed in whitefly-proof containers and destroyed.

After harvest

After harvest, it is critical to destroy infected plants properly. To eliminate or reduce the initial inoculum sources in a defined region, extensive sanitation should also be carried out to eliminate or reduce the initial inoculum sources. As weeds often serve as reservoir hosts of TYLCV, removing weeds in and around fields is critical. Crop rotation with non-host of TYLCV or whitefly can be used to combat TYLCV and whitefly pressure. A host-free period is advised to reduce virus inoculum or vector populations when possible. Host-free periods have successfully managed TYLCV in the Dominican Republic (Rojas et al. 2018).

In short, integrated pest management (IPM) is a general and valuable strategy to reduce economic losses and epidemics caused by TYLCV below an acceptable threshold. Therefore, the above TYLCV management is mainly based on two principles: one is to prevent TYLCV from entering the plants by using resistant plant varieties or using virus-free planting materials, and the other is to use prophylaxis practices to restrain TYLCV spread by eliminating reservoirs, surveillance, and control of whiteflies (Rubio et al. 2020).

Conclusion and future perspectives

TYLCV poses a serious threat to tomato production throughout the world's temperate regions. Because of the widespread distribution and the rapid global spread of this viral pathogen, TYLCD is expected to be a continuous challenge to tomato production in China and the rest of the globe. The largest number of TYLCV isolates identified in most provinces of China and many parts of the globe indicates that no region is immune to this pathogen, and stronger efforts to control its spread need to be made. Therefore, there is an urgent requirement for devising more efficient control measures based on the recent progress in the study of TYLCV. Future research must focus on developing plant resistance using cutting-edge techniques such as specific clustered regularly interspaced palindromic repeats (CRISPR)/Cas9 system and reliable RNA interference (RNAi) technology and applying and mining wild tomato resistance germplasm sources. With the development of CRISPR/Cas genome editing systems and the exploration and function identification of plant susceptibility genes to TYLCV, transgene-free resistant tomato plants generated by CRISPR/Cas in which susceptibility genes have been edited would offer a promising opportunity for the prevention and control of TYLCV in the field. At the same time, whiteflies are carriers of TYLCV, understanding of the tripartite interactions of plant-TYLCV-whitefly is important for effective field controlling method, and efforts to control the whitefly populations will be beneficial to control this disease and increase tomato yield. Like Bt crops, insecticidal proteins that are lethal to whiteflies can be expressed in plants using transgene technology, which would be a significant breakthrough. Controversially, although transgenic plants have proved efficient against viral infection, concerns about transgenic food safety by consumers hamper their applicability. Therefore, the government should develop a comprehensive program to improve public understanding of transgene technology and promote acceptability of transgenic crops.

Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.



Arabidopsis thaliana

Bst :

Bacillus stearothermophilus




Coat protein


Enzyme-linked immunosorbent assay


Endoplasmic reticulum


Integrated pest management


Jasmonic acid


Loop-mediated isothermal amplification


Middle East-Asia Minor 1


Mediterranean species


Nicotiana benthamiana


Next-generation sequencing


Open reading frame


Polymerase chain reaction


Post-transcriptional gene silencing


Rubisco subunit


Replication associated protein


Rolling circle amplification


Rolling circle replication


Replication enhancing protein


RNA interference


Recombinase polymerase amplification


Solanum lycopersicum


Single-stranded DNA binding protein


Transcriptional gene silencing


Tomato chlorosis virus


Transcription activator protein


Tomato yellow leaf curl China betasatellite


Tomato yellow leaf curl China virus


Tomato yellow leaf curl disease


Tomato yellow leaf curl virus




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We thank our colleagues in China who work on TYLCV research for their input in proofreading the detailed information of each TYLCV isolate. We thank Dr. Rosa Lozano-Durán for her valuable suggestions and English editing of the manuscript. We apologize that, due to space constraints, we have not been able to cite all published works that underlie the development of this field.


This work was supported by grants from the National Key Research and Development Program of China (2021YFD1400400) to Fangfang Li, and the National Natural Science Foundation of China (31720103914) to Xueping Zhou.

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XZ and FL designed the research; FL, RQ, XY and PG analysed the data; FL, RQ, XY and XZ wrote the paper. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Xueping Zhou.

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Supplementary Information

Additional file 1: Table S1

. Information of all tomato yellow leaf curl virus isolates in China

Additional file 2: Table S2

. Distribution of all tomato yellow leaf curl virus isolates in China

Additional file 3: Table S3

. The host plants of all tomato yellow leaf curl virus isolates in China

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Li, F., Qiao, R., Yang, X. et al. Occurrence, distribution, and management of tomato yellow leaf curl virus in China. Phytopathol Res 4, 28 (2022).

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