Molecular Basis of Mutual Benefits Between Cucurbit Chlorotic Yellows Virus (CCYV) Transmission and Imidacloprid Resistance in Bemisia Tabaci”

doi:10.21203/rs.3.rs-1469019/v1

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Molecular Basis of Mutual Benefits Between Cucurbit Chlorotic Yellows Virus (CCYV) Transmission and Imidacloprid Resistance in Bemisia Tabaci”

https://doi.org/10.21203/rs.3.rs-1469019/v1

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Increased insecticide resistance among insect vectors and arboviruses results in significant economic losses to agricultural production and poses a continuous threat to human health. To date, many studies have been conducted on how virus-infected host plants indirectly and plant virus directly change the physiological characteristics of insect vectors. However, the relationship between the insecticide resistance of the insect vector and the virulence of the viral pathogen has not received sufficient attention. Here, we investigated the effect of Cucurbit chlorotic yellows virus (CCYV), a plant virus transmitted by whitefly (Bemisia tabaci) in a semi-persistent manner, on the tolerance of B. tabaci to the neonicotinoid imidacloprid. We found CCYV enhanced the tolerance of B. tabaci to imidacloprid. The CYP6CM1 gene was significantly up-regulated in viruliferous susceptible B. tabaci compared with non-viruliferous B. tabaci after an acquisition access period of 10 d, including its upstream regulators. Silencing the CYP6CM1 gene by RNA interference reduced the ability of B. tabaci to acquire CCYV compared with the control. Additionally, imidacloprid-resistant B. tabaci outperformed sensitive adults in terms of virus transmission ability. These results suggest that CCYV enhances the ability of imidacloprid-sensitive B. tabaci to resist adverse external factors (insecticides). In turn, B. tabaci resistance affects virus transmission. Thus, to a certain extent, the plant virus and insect vector establish a mutually beneficial relationship that facilitates virus transmission.

Cucurbit chlorotic yellows virus (CCYV)

Bemisiatabaci

Resistance

Imidacloprid

CYP6CM1

Virus transmission

the relationship between the insecticide resistance of the insect vector and the virulence of the viral pathogen has not received sufficient attention.
This research aims to reveal the correlation between the virus transmission ability and insecticide resistance of Bemisia. tabaci.
Cucurbit chlorotic yellows virus (CCYV), a plant virus transmitted by whitefly (B. tabaci) in a semi-persistent manner, enhanced the tolerance of B. tabaci to imidacloprid.
Additionally, imidacloprid-resistant B. tabaci outperformed sensitive adults in terms of virus transmission ability.
The plant virus and insect vector establish a mutually beneficial relationship that facilitates virus transmission.

Viral pathogen-induced plant diseases show a global distribution, and severely affect crop yield and the global economy (He and Krainer, 2020). Insect-borne viruses account for the majority of plant viruses, and are efficiently transmitted by insect vectors (Eigenbrode et al., 2018). The current prevention and control strategies of plant viruses are mainly focused on controlling the corresponding vectors. Therefore, insecticides play a critical role in ensuring food security worldwide. However, the overuse of insecticides in the field has led to the emergence of insecticide resistance among insect vectors. The tobacco whitefly (Bemisia tabaci) is known to transmit more than 200 plant viruses, and is thus considered a super pest worldwide (De Barro et al., 2011; Polston et al., 2014). Synthetic insecticides used to control B. tabaci include organophosphorus, pyrethroids, insect growth regulators, nicotinoids, and neonicotinoids. Among these, neonicotinoids have been used continuously, which has led to the emergence of high-level resistance to this class of chemical insecticides in the whitefly, making whitefly management difficult (Ahmad et al., 2002; Horowitz et al., 2002; Nauen and Denholm, 2005). Recently, we showed that the ability of B. tabaci to transmit Cucurbit chlorotic yellows virus(CCYV)is closely and intrinsically linked to resistance to imidacloprid a neonicotinoid.

CCYV (genus Crinivirus) was first reported by Okuda et al. (2010) and is transmitted in a semi-persistent manner specifically by B. tabaci (Li et al., 2016). CCYV causes the fading and yellowing of the entire leaf, except the leaf veins (which remain green), resulting in serious yield losses. In recent years, CCYV has been reported in many countries in North America and East Asia (Kwak et al., 2021; Kavalappara et al., 2021; Chynoweth et al., 2021; Hernandez et al., 2021; Abrahamian et al., 2012), and the extent and scope of its damage is ever expanding.

Recently, we found that the ability of B. tabaci to transmit CCYV is associated with overexpression of CYP6CM1, a gene belonging to the cytochrome P450 family, which is closely related to imidacloprid resistance (Karunker et al., 2008; Yang et al., 2013; Li et al., 2015). The cAMP-response element binding protein (CREB) transcription factor regulates the expression of CYP6CM1 via the mitogen-activated protein kinase (MAPK) signaling pathway (Yang et al., 2020) (Fig. 1). In this study, we investigated whether CCYV changes the tolerance of B. tabaci to imidacloprid at the genetic level, thus facilitating its transmission. This research aims to reveal the correlation between the virus transmission ability and insecticide resistance of B. tabaci, which may provide a new hypothesis for the further investigation of insect-virus coevolution.

2.1 Plants, insects, and virus

Cucumber (Cucumis sativus L. cv. Bojie-107) and cotton (Gossypium hirsutum L. cv. Zhongmian-49) plants were grown in pots (diameter = 10 cm; height = 12 cm) in separate insect-proof cages (60 cm ⋅ 40 cm ⋅ 80 cm), which were placed in a greenhouse under controlled conditions: long-day photoperiod (16 h light/8 h dark); 28 ± 0.5°C temperature; 60–70% relative humidity. The colony of B. tabaci Mediterranean (MED; formerly biotype Q) cryptic species was maintained on cucumber plants, which was not exposed to any insecticide during the culture period and served as a sensitive population in this experiment. The purity of B. tabaci MED was monitored every 2–3 generations using reverse transcription PCR (RT-PCR) and sequencing of mtCOI gene (Khasdan et al., 2005; Shatters et al., 2009) with sequence-specific primers (Annexes). B. tabaci MED was a multi-generation population reared in the presence of imidacloprid (as the resistant population). The CCYV-infected cucumber plants were maintained in the laboratory for two years. Cucumber plants were used for virus clone maintenance and transmission assays. Cotton is a suitable host for B. tabaci but not for CCYV; therefore, it was used for the retention time experiment in transmission assays. Viruliferous B. tabaci adults were collected from CCYV-infected plants and transferred to virus-free cucumber plants for inoculation.

2.2 Imidacloprid bioassay of non-viruliferous and viruliferous B. tabaci

Three-day-old non-viruliferous B. tabaci adults were collected from virus-free plants and placed on CCYV-infected plants. After feeding for 10 d, a total of 20 B. tabaci individuals were chosen for the imidacloprid bioassay, which was performed using the leaf dip method (Houndété et al., 2010). The cucumber leaf discs (35 cm in diameter) were dipped for 10 s in 50 mg/L imidacloprid (pesticide registration no.: PD20131915; product standard no.: GB/T28143-2011; dosage form: emulsifiable oil; imidacloprid 5%). Subsequently, the leaf discs were air-dried, and placed in a Petri dish (diameter = 35 mm) containing 1% agar. The mortality rate of B. tabaci was determined after 48 h by counting the number of dead insects (i.e., insects that showed no movement or abnormal movement). Experiments were repeated 12 times.

2.3 Resistant B. tabaci colonies

The LC₅₀ of imidacloprid was determined using the leaf dip method, as described above. The calculated LC₅₀ value was then used to screen the resistant colonies of B. tabaci. Total RNA was extracted using the TaKaRa RNAiso Plus Kit (Cat# 9109, Lot# AL42064A), according to the manufacturer’s instructions. Then, cDNA was synthesized using the TaKaRa Reverse Transcription Kit (Cat# RR047A, Lot# AL21113A). To detect the expression of the resistance gene CYP6CM1, quantitative real-time PCR (qRT-PCR) was performed using TaKaRa TB GreenR Premix Ex Taq™ II (Cat# RR820A, Lot# AJF2612A), according to the manufacturer’s instructions.

2.4 Expression analysis of CYP6CM1 and its upstream regulators in B. tabaci

Non-viruliferous B. tabaci adults were collected from healthy plants and placed on CCYV-infected and healthy plants for 1, 5, 10, 15, and 20 d. Then, 80 B. tabaci adults were selected for each experiment. To determine the expression level of CYP6CM1, total RNA extraction and qRT-PCR were performed as described above, with five replicates. According to Yang et al. (2020), the effect of CCYV on the upstream regulatory factors was investigated. Imidacloprid-resistant and imidacloprid -sensitive non-viruliferous B. tabaci adults were placed on healthy and CCYV-infected cucumber plants for 1 and 10 d, respectively. Experimental methods and total RNA extraction were performed as described above. Four replicates were performed for this experiment.

2.5 RNA interference (RNAi) and qRT-PCR

The cDNA templates of B. tabaci samples were amplified by PCR, cloned into the pMDTM18-T vector (TaKaRa, Code NO.6011), and confirmed by sequencing. Double-stranded RNAs (dsCYP6CM1, dsGFP) were synthesized by in vitro transcription using the T7 RNAi Transcription Kit (TR102) (Vazyme), and fed to B. tabaci at a concentration of 40 µg/mL using the membrane feeding method, as described by Li et al. (2015). The effects of RNAi on the expression of the target gene in B. tabaci were analyzed by qRT-PCR after feeding for 3 d. This experiment was performed in triplicate. Then, the silenced B. tabaci were fed on CCYV-infected cucumber plants for 1 and 3 h. CCYV mRNA molecules were quantified by qRT-PCR. Relative gene expression levels were calculated using the 2^− ΔΔCt method, with Actin as the internal reference. Eight replicates were performed for each group.

2.6 Virus transmission assays

To determine the acquisition access period (AAP), non-viruliferous resistant and sensitive B. tabaci adults were starved for 2 h, and placed on CCYV-infected cucumber plants in an insect-proof cage. The insects were collected after 1, 2, 6, 24, and 48 h of feeding.

To determine the retention time, resistant and sensitive B. tabaci adults were placed on CCYV-infected cucumber plants, and collected after 3 d. Then, after 2 h of starvationt, the B. tabaci adults were released onto cotton plants (non-host of CCYV), and collected after 1, 3, 6, 9, and 15 d of feeding.

Sixteen replicates were performed for each experiment. A mixed sampling of male and female B. tabaci adults was used in both experiments, with 20 adults per tube (Li et al., 2016; Lei et al., 2021). Then, CCYV mRNA in insects was detected by qRT-PCR.

2.7 Statistical analyses

Data were statistically analyzed using Student’s t-test. Statistical analyses were performed in IBM SPSS Statistics 20.0, and graphs were generated using GraphPad Prism 8.0.2. The LC₅₀ value (of imidacloprid), toxicity regression equation, and R² value were calculated using the Probit function. Data were expressed as mean ± standard error (SE).

3.1 Bioassays

The imidacloprid tolerance of B. tabaci was measured by the leaf dip method after 10 d of AAP (Fig. 2a). Viruliferous B. tabaci exhibited significantly lower corrected mortality rate than non-viruliferous B. tabaci (t = 2.131, df = 22, P = 0.045) (Fig. 2b). This indicates that CCYV improves the tolerance of B. tabaci to imidacloprid.

3.2 Screening of resistant B. tabaci

Under long-term imidacloprid treatment, the tolerance of B. tabaci to imidacloprid gradually increased. The expression level of CYP6CM1 was approximately 30-fold higher in resistant B. tabaci than in sensitive B. tabaci (Fig. 3a). According to the classification of resistance classes (Yan et al., 2012), the adults of B. tabaci screened in this study showed moderate resistance to imidacloprid, with a resistance multiplicity of 11.30 compared with the LC₅₀ value of sensitive B. tabaci (Table 1).

Table 1

Toxicity regression equation and resistance multiplicity.
B. tabaci type^†	Toxicity regression equation	R²	LC₅₀ (mg/L)	95% CI (mg/L)^‡	Resistance multiplicity
Resistant (R_n)	Y = -9.621 + 3.521X	0.933	540.398	490.845–629.279	11.300
Resistant (R₁)	Y = -4.427 + 1.921X	0.878	198.579	164.053–233.764	4.160
Sensitive (S₀)	Y = -3.805 + 2.266X	0.913	47.769	32.813–58.680	-
^†S₀, susceptible B. tabaci population; R₁, first-generation resistant population; R_n, resistant population cultured for multiple generations. ^‡CI, confidence interval.

3.3 Effects of CCYV on the expression of CYP6CM1 in B. tabaci

The CYP6CM1 gene was first up-regulated and then down-regulated in viruliferous B. tabaci (Fig. 3b). No significant difference was observed in the expression of CYP6CM1 between viruliferous and non-viruliferous B. tabaci after 1 d of feeding (t_1d = 0.873, df = 8, P = 0.247) and 5 d of feeding (t_5d = 1.862, df = 8, P = 0.076). The expression of CYP6CM1 showed an increasing trend in viruliferous B. tabaci. At 10 and 15 d, the CYP6CM1 gene was significantly up-regulated in viruliferous B. tabaci compared with the non-viruliferous group (t_10d = 12.870, df = 8, P < 0.001; t_15d = 7.243, df = 8, P < 0.001). However, CYP6CM1 expression was down-regulated in viruliferous B. tabaci at 20 d, and the difference in its expression between the two groups was not significant (t_20d = 2.175, df = 8, P = 0.062), probably because of the senescence or death of adults. This indicates that CCYV affects the sensitivity of B. tabaci to imidacloprid by altering the expression of the CYP6CM1 gene.

3.4 Effects of CCYV on the upstream regulators of CYP6CM1

No difference was detected in the expression of the ERK gene between non-viruliferous and viruliferous B. tabaci, regardless of their resistance to imidacloprid, at both 1 and 10 d after feeding (Fig. 4a and 4b) (St_1d = 0.502, df = 6, P = 0.633; St_10d = 1.758, df = 6, P = 0.261). Although the p38 gene showed no difference in expression between resistant and sensitive B. tabaci at 1 d (St_1d = 0.847, df = 6, P = 0.429), it was significantly up-regulated in viruliferous adults compared with non-viruliferous B. tabaci at 10 d (Fig. 4c and 4d ) (St_10d = 4.993, df = 6, P = 0.002). The transcription factor genes CREB showed similar expression profiles, with significant up-regulation at 10 d in sensitive viruliferous B. tabaci (Fig. 4e and 4f) (St_1d = 1.431, df = 6, P = 0.202; St_10d = 5.587, df = 6, P = 0.001). The expression level of CYP6CM1 was significantly up-regulated at 10 d in susceptible B. tabaci (Fig. 5a and 5b) (St_1d = 1.800, df = 6, P = 0.122; St_10d = 24.020, df = 6, P < 0.001).. Therefore, we speculated that the effect of resistance on B. tabaci is greater than that of CCYV.

3.5 Effects of silencing CYP6CM1 on the acquisition of CCYV by B. tabaci

When dsCYP6CM1 and dsGFP were fed to B. tabaci at a concentration of 40 µg/mL by membrane feeding, the effect of dsCYP6CM1 on CYP6CM1 expression was significantly higher than that of dsGFP (t = 38.850, df = 4, P < 0.001) (Fig. 6a). The silenced B. tabaci were placed on CCYV-infected cucumber plants to acquire the virus, and were collected after 1 and 3 h of feeding. We found that the silencing of CYP6CM1 significantly decreased the amount of virus acquired by B. tabaci (t_1h = 2.299, df = 14, P = 0.037; t_3h = 3.110, df = 14, P = 0.0076) (Fig. 6b). These results suggest that the CYP6CM1 expression affects the virulence acquisition of B. tabaci.

3.6 Comparison of virus acquisition and retention

The ability of insect vectors to transmit the virus could be determined by measuring virulence acquisition and retention. We compared the differences in virulence acquisition and retention between resistant and sensitive B. tabaci. Resistant B. tabaci acquired significantly more copies of the virus than sensitive B. tabaci after non-viruliferous vectors were placed on CCYV-infected plants for 2 h and 6 h (t_2h = 2.365, df = 26, P = 0.026; t_6h = 2.940, df = 26, P = 0.030). We found that acquired virus copies no longer changed at 24 and 48 h for either resistant or sensitive B. tabaci (Fig. 7a). This indicated that, for the semi-persistent virus like CCYV, complete virus acquisition was possible from 24 to 48 h for B. tabaci. We investigated the virulence retention capacity of resistant and sensitive B. tabaci on cotton (a non-host of CCYV). When viruliferous B. tabaci were fed on cotton for 1 and 3 d, the resistant B. tabaci lost the virus more readily than sensitive adults, as indicated by a significant decrease in virulence retention capacity (t_1d = 2.716, df = 30, P = 0.011; t_3d = 3.240, df = 30, P = 0.003). At 9 d, the virus titer in resistant B. tabaci decreased significantly compared with that in sensitive adults (t_9d = 3.646, df = 30, P = 0.001) (Fig. 7b). These results suggest that resistant B. tabaci possess a higher ability to acquire but lower ability to retain the virus compared with sensitive adults.

Insecticide resistance is a common problem that prevents effective pest control; however, little attention has been given to the relationship between insect vector-mediated transmission of plant viruses and insecticide resistance (Rivero et al., 2010). In recent years, related studies have gradually emerged. Wan et al. (2020) found that spinosad-resistant western flower thrips (Frankliniella occidentalis) showed a significant increase in Tomato spotted wilt orthotospovirus (TSWV) acquisition and replication, thus promoting the spread of the virus. There have also been reports of microbe-mediated insecticide sensitivity. For example, the symbiotic bacteria or gut microbiota of wheat aphid Sitobion miscanthi and Rhagoletis pomonella are reportedly associated with detoxification (Li et al., 2020; Lauzon et al., 2003).

This raised the question whether insect vector-borne viruses and insect vectors exist in a mutually beneficial relationship over the long term? In this study, we found that CCYV reduced the susceptibility of B. tabaci to imidacloprid (Fig. 1). This result is similar to the findings of Liu et al. (2020), who showed that the infection of B. tabaci with Tomato yellow leaf curl virus (TYLCV) increased its tolerance to the insecticide Flupyradifurone, while viruliferous B. tabaci exhibited significantly higher LC₅₀ to this insecticide. The reduced susceptibility of B. tabaci to imidacloprid is probably caused by CCYV promoting the expression of the imidacloprid resistance gene CYP6CM1 (Fig. 2). Further investigation revealed that CCYV also affects the expression of the upstream regulators of CYP6CM1 in sensitive populations (Fig. 3). Genes including p38 (which encodes a MAPK family protein) and CREB (which encodes a transcription factor that regulates CYP6CM1 expression) were significantly up-regulated when B. tabaci acquired CCYV for 10 d. However, no difference was observed in the expression of CYP6CM1 between the treatment and control groups in the resistant populations (Fig. 4, Fig. 5). Therefore, we speculated that the effect of B. tabaci resistance on its regulatory factors is much more than that of CCYV.

In addition, we silenced CYP6CM1 to investigate the effect of the resistance gene on the virulence acquisition of B. tabaci. Interference CYP6CM1 decreased the virulence acquisition (Fig. 6). This indicates that the resistance gene CYP6CM1 is related to the virulence acquisition of the B. tabaci; however, the underlying mechanism needs further investigation. We also compared the virulence acquisition and retention capacity of resistant and sensitive B. tabaci. The results showed that resistant B. tabaci acquired a higher amount of the virus RNA than sensitive B. tabaci within the same time period (Fig. 7a). This is probably because resistant B. tabaci require more energy to replenish the energy spent on enhancing insecticide resistance and feeding. However, the ability of resistant B. tabaci to retain virulence was weaker than that of sensitive B. tabaci (Fig. 7b). Considering the semi-persistent transmission of CCYV, resistant B. tabaci could spread the virus to other hosts faster than sensitive B. tabaci.

In conclusion, our results suggest that there is a mutually beneficial relationship between CCYV and its vectors, as indicated by two main findings: (1) CCYV up-regulated the expression of the resistance gene CYP6CM1, and enhanced the tolerance of B. tabaci to imidacloprid; (2) resistant B. tabaci outperformed sensitive B. tabaci in terms of virulence transmission ability. Nonetheless, it remains unclear how CCYV regulates the expression of resistance genes in B. tabaci. Further research is needed to address this limitation. The yearly increase in insecticide resistance and the widespread outbreaks of viral diseases also need to be discussed from an evolutionary perspective. An in-depth understanding of the interactions between vector insects and plant viruses can help model the synergistic evolution of insecticide resistance, which will assist in better pest control, a matter that requires constant attention in the future.

Author contribution

FY, JL and MY conceived and designed the experiment; MY, HH, ZZ, BZ, CZ (Chaoqiang Zhu), WY performed the investigation; MY and ZZ analyzed the data; MY and FY wrote the original draft; FY, JL and CZ (Chenchen Zhao) reviewed and edited the document. All authors contributed to the manuscript.

Acknowledgements

This research was funded by the National Natural Science Foundation of China (Project No. 31901886, 31871973, 31471776 ). We thank the anonymous reviewers for the constructive scientific reviews of this manuscript.

Conflict of Interest Statement The authors declare no competing interests.

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19 Mar, 2022

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Molecular Basis of Mutual Benefits Between Cucurbit Chlorotic Yellows Virus (CCYV) Transmission and Imidacloprid Resistance in Bemisia Tabaci”

Status:

Version 1

Abstract

Figures

Key Message

1 Introduction

2 Materials And Methods

2.1 Plants, insects, and virus

2.5 RNA interference (RNAi) and qRT-PCR

2.6 Virus transmission assays

2.7 Statistical analyses

3 Results

3.1 Bioassays

3.6 Comparison of virus acquisition and retention

Discussion

Declarations

References

Supplementary Files

Status:

Version 1