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. 2021 Dec 1;11(12):516. doi: 10.1007/s13205-021-03067-1

Occurrence of leek yellow stripe virus and onion yellow dwarf virus from edible Allium plants in the south Marmara region of Turkey

Hasan Tuna Tuzlali 1, Ali Karanfil 2, Savaş Korkmaz 2,✉
PMCID: PMC8636554  PMID: 34926113

Abstract

Among edible Allium plants (leek, onion, and garlic), leek yellow stripe (LYSV) and onion yellow dwarf virus (OYDV) are the most common viruses worldwide. While the presence of these two viruses in Turkey has previously been confirmed, only a few studies on their prevalence and genetic diversity have been performed. The aim of this study, conducted in the southern Marmara region of Turkey (SMR), was to identify the presence and genetic diversity of these viruses. Samples were collected from 494 plants exhibiting virus and virus-like symptoms. Samples were tested for the relevant viruses by double-antibody sandwich enzyme-linked immunosorbent assay and reverse transcription polymerase chain reaction (DAS-ELISA and RT-PCR, respectively). Tests revealed the presence of OYDV in 95 samples and LYSV in 52, whereas 33 samples were observed to have a combined infection. To examine the genetic diversity, 10 isolates from each virus were chosen from the infected samples. Using RT-PCR, the complete coat protein (CP) gene for LYSV and a partial sequence region of the nuclear inclusion b + CP gene for OYDV were amplified, cloned, and sequenced from the selected isolates. The sequence data were compared with the isolates in GenBank; it was determined that SMR LYSV and OYDV isolates show similarities over 77% with world isolates at the nucleotide and amino acid levels. Phylogenetic analyses showed that the LYSV and OYDV isolates had some diversity with isolates from different parts of the world, and the host had an important role in the phylogenetic relationships, particularly for LYSV.

Supplementary Information

The online version contains supplementary material available at 10.1007/s13205-021-03067-1.

Keywords: Virus, RT-PCR, Cloning, Similarity, Phylogenetic

Introduction

Plants of the Allium genus are cultivated in many parts of the world for both food and medicinal purposes (Rahman and Lowe 2006). Leek, garlic, and onion stand out as the most important species belonging to this genus (Li et al. 2010).

Phytopathogens are prominent in Allium-type plants, as pathogens commonly affect all cultivated agricultural products. Among these phytopathogens, viruses are of particular importance because they do not respond to chemical control and cause significant yield losses. Studies conducted worldwide have reported frequent infections of potyvirus species in addition to infections caused by tospovirus, carlavirus, and allexivirus species in leek, garlic, and onion cultivation (Dovas et al. 2001; Katis et al. 2012; Taglienti et al. 2018; Abraham et al. 2019).

Members of the potyvirus genus cause significant losses among plants of the Allium genus (Lot et al. 1998). Leek yellow stripe and onion yellow dwarf viruses (LYSV and OYDV, respectively), the two viruses first characterized among this group of viruses, have been reported to be frequently observed in areas in which these plants are cultivated (Winiarczyk et al. 2014; Fernández-Tabanera et al. 2018; Abraham et al. 2019). Therefore, LYSV and OYDV are the two most important plant pathogens of the potyvirus genus, causing economic losses in plants of the Allium genus.

In many worldwide studies, LYSV and OYDV infections have been reported from different countries, and detailed analyses have been conducted concerning their genetic diversity (Dovas et al. 2001; Fajardo et al. 2001; Bereda et al. 2015). However, the number of studies from Turkey that have investigated potyvirus infection in plants of the Allium genus is limited, and these studies have focused on identifying only LYSV and OYDV infections (Korkmaz and Cevik 2009; Fidan and Baloglu 2009; Santosa and Ertunc 2020). In addition, the Çanakkale, Balıkesir, and Bursa provinces that constitute the southern Marmara region of Turkey (SMR) are among the leading provinces in Turkey involved in the cultivation of onion and garlic, and literature reviews have revealed that no study has been conducted to determine the prevalence and genetic diversity of these potyviruses in these provinces. In this context, no study addressing the genetic diversity of SMR LYSV and OYDV isolates can be found. For these reasons, whether LYSV and OYDV infections are related to potyviruses was investigated by conducting surveys in commercial agricultural areas of SMR in which Allium species are cultivated. Molecular characterization of the isolates from the infected samples was performed, and their genetic diversity was investigated. This paper presents the most comprehensive study performed in Turkey to date.

Materials and methods

Sampling

Field studies were carried out in Bursa, Balıkesir, and the Çanakkale provinces of SMR in which Allium plants are cultivated. The survey areas were selected based on the farmer registration system data obtained from the district directorates of agriculture, the directions of the cultivators, and the opinions of the technical staff working in the relevant areas. Only samples from garlic, leek, and onion plants displaying virus and virus-like symptoms were collected based on the results from surveys conducted during the 2014 to 2017 production seasons as part of field studies.

Virus identification

Double antibody sandwich enzyme-linked immunosorbent assay (DAS-ELISA) tests were utilized to investigate OYDV and LYSV infections in the study samples. Tests were carried out with polyclonal antibodies specific to the target viruses. The tests were carried out based on the method reported by Clark and Adams (1977) in line with the recommendations of Bioreba (Switzerland) and Agdia (United States), which supplied the kits.

Furthermore, since both viruses were of the potyvirus genus, all positive samples were tested with specific primer pairs via reverse transcription-polymerase chain reaction (RT-PCR) to identify possible cross-reactions between them or with other potyviruses. First, total RNA was isolated from infected samples using the RNeasy Mini Kit (Qiagen, Canada). Complementary DNA (cDNA) was synthesized from the isolated total RNAs using PrimeScript cDNA synthesis kits (Takara, Japan). With the resulting cDNAs, tests were performed using the primer pair of 5 'TCA CTG CAT ATG CGC ACC AT 3' and 3 'GCA CCA TAC AGT GAA TTG AG 5' (1030 bp) sequences involving the complete coat protein (CP) gene and a part of the nuclear inclusion b (NIb) region, which were designed by Fajardo et al. (2001) for LYSV. The primers 5 'CAC CNT AYA TAG CRG ARA CAG CTC T 3' and 3'ACT GAA ATG CGC CAT TAT YTG YCT A 5' to amplify 602 bp of the NIb + CP region (Lee et al. 2005) for OYDV was also used.

Cloning and sequencing

Among the isolates obtained by the DAS-ELISA and RT-PCR tests, a total of 10 LYSV and 10 OYDV isolates were selected after considering the geographical origin and host from which they were obtained. CP-based molecular characterization was performed for the selected isolates to identify their genetic diversity.

In RT-PCR studies, 1030 bp amplicons of the complete CP gene and 602 bp amplicons of a part of the NIb + CP gene were obtained for LYSV and OYDV, respectively. These amplified target gene regions were cloned using pGEM®-T Easy Vector Systems (Promega, USA) by the TA cloning method, and the plasmid obtained for each isolate was sequenced bi-directionally with the primers M13F and M13R to confirm its identity.

Bioinformatics analyses

The raw sequence data obtained from sequencing were combined in CLC Main Workbench (V.7.7.3) software, and consensus sequences were deposited in NCBI GenBank (Supp. Table 1). The sequences of the world LYSV and OYDV isolates were taken from the GenBank database (Supp. Table 2 and 3). Similarities and phylogenetic relationships among the LYSV and OYDV Turkish isolates and their similarities and phylogenetic relationships with the world isolates were analyzed. The similarity rates were determined with Clustal W sequencing utilizing the sequence demarcation tool (SDT) V.1.2 (Muhire et al. 2014). Phylogenetic relationships of the isolates were investigated in MEGA 7 software with 1000 bootstrap values using the maximum likelihood method and Kimura 2 (K2) parameter model (Kumar et al. 2016).

Results

A total of 494 leek, garlic, and onion samples were collected during the field studies. Virus identification studies performed with the DAS-ELISA test found LYSV in 52 samples, OYDV in 95 samples, and combined infection of LYSV + OYDV in 33 samples (Table 1). Among the LYSV infections, 48 were observed in leek, three in onion, and one in garlic, whereas OYDV infections were identified in 18 leeks and 77 garlic plants. Twenty-one and 12 of the combined infections of LYSV and OYDV were in leek and garlic samples, respectively.

Table 1.

Result of virus identification tests based on the combining of DAS-ELISA and RT-PCR tests

Virus LYSV OYDV LYSV + OYDV
Province Çanakkale Balıkesir Bursa Çanakkale Balıkesir Bursa Çanakkale Balıkesir Bursa
Virus Leek 27/62 10/32 11/48 10/62 3/32 5/48 9/62 6/32 6/48
Onion 1/48 0/33 2/116 0/48 0/33 0/116 0/48 0/33 0/116
Garlic 0/40 1/98 0/17 26/40 41/98 10/17 3/40 8/98 1/17
Total 28/150 11/163 13/181 36/150 44/163 15/181 12/150 14/163 7/181
52/494 95/494 33/494
180/494
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Based on the DAS-ELISA test results, OYDV infection alone was identified in five onion samples, while mixed infection of LYSV + OYDV was present in two onion samples. However, no OYDV infection was identified among these samples by the RT-PCR tests. These results showed that 180 of the collected samples were infected with at least one virus in question based on the combination of DAS-ELISA and the RT-PCR tests (Table 1).

The most typical symptom seen in samples infected with LYSV was a yellow stripe on the leaves (Fig. 1a, b). Leaf yellowing and curling were observed in onions infected with LYSV (Fig. 1c, d), whereas garlic samples infected with OYDV had mosaics on their leaves, and some plants showed a slight leaf curl (Fig. 1e, f).

Fig. 1.

Fig. 1

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Some symptoms related with leek yellow stripe virus (LYSV) and onion yellow dwarf virus (OYDV) based on the virus identification analyses (a, b: yellow stripe symptoms on leek plants infected with LYSV, c, d: leaf yellowing and curling on onion plants infected with LYSV, e, f: mosaic and mild curling symptoms on garlic plants infected with OYDV)

After applying multiple sequence analyses to determine the genetic diversity of the LYSV isolates, the isolates were observed to exhibit a sequence similarity of 79% to 99% and 80% to 100% at the nucleotide and amino acid (nt and aa, respectively) levels. The similarity rates of these isolates when compared with world isolates were 78%–98% and 78%–100% at the nt and aa levels, respectively (Fig. 2 and Supp. Fig. 1).

Fig. 2.

Fig. 2

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The distribution of the pairwise identity scores of the complete coat protein genes of leek yellow stripe virus isolates at nucleotide level as calculated by the SDT software

The OYDV isolates were observed to exhibit a similarity of 76% to 99% and 83% to 100% at the nt and aa levels, respectively. The similarity rates of these isolates with world isolates were 77%–87% and 79%–94% at the nt and aa levels, respectively (Fig. 3 and Supp. Fig. 2).

Fig. 3.

Fig. 3

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The distribution of the pairwise identity scores of the partial coat protein genes of onion yellow dwarf virus isolates at nucleotide level as calculated by the SDT software

As a result of the phylogenetic analysis, the LYSV isolates were divided into two major groups. All members of the first group consisted of LYSV isolates obtained from garlic as hosts that were then distributed into two subgroups, whereas the second group was divided into two subgroups consisting of garlic and leeks (Fig. 4). In the second group, the isolates obtained from garlic and leeks were distributed in different subgroups. Isolates obtained from this study were observed in the phylogenetic tree to be in close relationships with each other based on their hosts of origin.

Fig. 4.

Fig. 4

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The phylogenetic tree of leek yellow stripe virus (LYSV) isolates constructed by the Maximum likelihood method using the nucleotide sequences of the complete coat protein genes. Scallion mosaic virus (ScaMV, AJ310208), wild onion symptomless virus (WoSV) (LC159495), narcissus yellow stripe virus (NYSV, KU516386), and shallot yellow stripe virus (SYSV, AM267479) related to LYSV were used as outgroup for construction of rooted phylogenetic tree

Phylogenetic analysis of the OYDV isolates revealed that the isolates were distributed in the phylogenetic tree in two major groups. Furthermore, five subgroups were identified in the phylogenetic tree (Fig. 5). In the subgroups of the first group, the isolates were found to be distributed according to their host of origin (onion and garlic), whereas in the second group, isolates with a different host of origin (onion, garlic, and leek) were found to be in the same subgroups. It was determined that the isolates from Turkey were distributed into two different main groups (I and II) and two subgroups (Ib and IIb).

Fig. 5.

Fig. 5

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The phylogenetic tree of onion yellow dwarf virus (OYDV) isolates constructed by the Maximum likelihood method using the nucleotide sequences of the partial coat protein genes. Scallion mosaic virus (ScaMV, AJ310208), wild onion symptomless virus (WoSV) (LC159495), narcissus yellow stripe virus (NYSV, KU516386), and shallot yellow stripe virus (SYSV, AM267479) related to OYDV were used as outgroup for construction of rooted phylogenetic tree

The genetic distances of all isolates used in the study were 0.1962 ± 0.0252 and 0.2476 ± 0.0394 for the LYSV and OYDV isolates, respectively (Supp. Table 4 and 5). The genetic distance of the LYSV isolates obtained from leeks was 0.0558 ± 0.0084, while it was 0.1986 ± 0.0262 for those obtained from garlic (Supp. Table 4). The genetic distances of OYDV isolates obtained from garlic, onion, and leek hosts were 0.2205 ± 0.0352, 0.2457 ± 0.0397, and 0.1704 ± 0.0270, respectively (Supp. Table 5). These calculations were also performed at the group and subgroup levels formed in the phylogenetic trees for the LYSV and OYDV isolates (Supp. Table 4 and 5).

Discussion

Virus identification studies performed within the scope of this study found the virus infection rate in the collected samples was 36.43%. Although all samples typically exhibited virus and virus-like symptoms, the resulting infection rate was relatively low. It is thought that two-thirds of the collected samples were not infected with the viruses in question and were instead infected with other viral diseases that affect Allium plants. Furthermore, Alliaceae plants are frequently reported to be infected with carlavirus, allexivirus, and phytoplasma infections in addition to potyvirus infections (Wylie et al. 2012; Abraham et al. 2019). In particular, the fact that the virus entities in question cannot be identified in any of the collected onion samples supports the idea that the observed symptoms may be caused by infections of other viruses and virus-like diseases (Baghalian et al. 2010; Gupta et al. 2017).

In the present study, LYSV and OYDV were found to extensively infect leeks and garlic, while LYSV infection was identified in only two onion plants. Based on the data in the literature, the infection rate of OYDV in onions is low, whereas its prevalence is higher in garlic (Shahraeen et al. 2008; Snihur et al. 2019). Therefore, garlic is considered the main host of OYDV in many countries. In fact, the host of origin of most of the OYDV isolates available in the GenBank database is garlic. Thus, the results obtained in this current study are compatible with previous studies.

Although OYDV infection based on DAS-ELISA test results was detected in seven onion plants, it is believed that the test may have cross-reacted with another potyvirus because the RT-PCR tests did not confirm this finding. According to Dovas et al. (2002), the RT-PCR test is reported to be more sensitive than the DAS-ELISA test for identifying LYSV and OYDV.

The sequence diversity was observed to be high among the LYSV and OYDV isolates. Furthermore, parallel to previous studies, we found that isolates obtained from different continents showed higher sequence similarity with each other, while isolates obtained from the same region exhibited very low sequence similarities (Arya et al. 2006; Sivaprasad et al. 2017). The similarity rates of LYSV and OYDV isolates among themselves and with world isolates have been observed to be very close to the threshold values required to be considered a new virus in potyvirus taxonomy (Adams et al. 2005). Low similarity rates obtained for LYSV and OYDV isolates were also obtained in studies on OYDV from Iran and LYSV from India (Baghalian et al. 2010; Gupta et al. 2017). In this context, findings reported from other studies support the results of the present study (Takaki et al. 2005).

LYSV and OYDV isolates are reported to be phylogenetically distributed into two major groups (Chen et al. 2001; Baghalian et al. 2010; Gupta et al. 2017). Phylogenetic analyses conducted within the scope of this study also revealed that the LYSV and OYDV isolates formed two major groups. Moreover, intergroup genetic distance values between the major groups were found to be significantly greater than the intragroup genetic distance values. Similar results were also obtained for the subgroups. These findings confirm the accuracy of the groups formed in the phylogenetic tree in parallel with data in the literature. LSYV leek isolates were found to be much more closely related to each other than LYSV garlic isolates based on genetic distance measurements at the host level. Garlic LSYV isolates were found in different major groups and subgroups in phylogenetic analyses. Host specialization of OYDV isolates was found to be less common than that of LYSV isolates, and isolates with a different host of origin in different subgroups were found.

Furthermore, the bioinformatics analyses revealed that the host plays an important role in the formation of major groups in phylogenetic relationships among LYSV isolates, whereas geographic origin does not play a role in the formation of major groups in phylogenetic relationships based on the gene regions used for both LYSV and OYDV isolates. In this context, it has been determined that isolates obtained from various continents, countries, and regions can be found in the same groups. Similar results have been reported in many studies on LYSV and OYDV isolates (Bereda et al. 2015; Gupta et al. 2017).

Conclusion

We believe it is necessary to conduct studies to investigate why LYSV and OYDV do not prefer onions, although they are cultivated in a manner similar to garlic (vegetative propagation material), and the host resistance and sources of infections for these viruses are the same. Moreover, high heterogeneity among both OYDV and LYSV isolates in terms of similarity exists; therefore, it is important to carry out additional bioinformatics analyses at the level of the complete genome with isolates obtained from different geographic origins and hosts for both viruses.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 119 KB) (115.5KB, docx)

Author contributions

SK: designed the study. HTT and AK: collected the samples and performed the laboratory tests. AK and SK: performed the bioinformatic analyses. All authors interpreted of results, drafted manuscript preparation, and approved the final version of the manuscript.

Declarations

Conflict of interest

The authors declare that they have no known competing financial interests or personal relationships that could have appearedto influence the work reported in this paper.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed consent

Informed consent was obtained from all individual participantsincluded in the study.

Contributor Information

Hasan Tuna Tuzlali, Email: tunatuzlali@comu.edu.tr.

Ali Karanfil, Email: alikaranfil@comu.edu.tr.

Savaş Korkmaz, Email: skorkmaz@comu.edu.tr.

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Supplementary Materials

Supplementary file1 (DOCX 119 KB) (115.5KB, docx)

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