dsRNA-Mediated Pest Management of Tuta absoluta Is Compatible with Its Biological Control Agent Nesidiocoris tenuis

Abstract

RNAi-mediated insect pest management has recently shown promising results against the most serious pest of tomato, the tomato leafminer, Tuta absoluta. This study aimed to investigate whether dsRNA (dsTa-αCOP) designed to target the T. absoluta-αCOP gene could cause adverse effects to its biocontrol agent, the mirid predator, Nesidiocoris tenuis. Oral exposure of N. tenuis to dsRNA (dsNt-αCOP) designed to target N. tenuis-αCOP resulted in a 61%, 67% and 55% reduction in its transcript level in comparison to the sucrose, dsGFP and dsTa-αCOP treatments, respectively. In addition, significantly higher mortality of 57% was recorded in dsNt-αCOP-treated N. tenuis when compared to the sucrose (7%), dsGFP (10%) and dsTa-αCOP (10%) treatments. Moreover, the predation rate of ~33–39 Ephestia kuehniella eggs per N. tenuis adult dramatically reduced to almost half in the surviving dsNt-αCOP-treated N. tenuis. This worst-case exposure scenario confirmed for the first time that the RNAi machinery is functional in this species and that the risk of exposure through the oral route is possible. In contrast, dsTa-αCOP did not cause any sub-lethal effects to N. tenuis upon oral exposure. Oral exposure of T. absoluta to dsTa-αCOP resulted in 50% mortality. In the context of a biosafety risk assessment of RNAi-mediated insect management, investigating the effects on non-target organisms is essential in order to include this method as part of an integrated pest management strategy. Based on our laboratory assays, RNAi-mediated control is compatible with the biological control of T. absoluta by its natural enemy N. tenuis, adding the RNAi approach in the armoire of integrated pest management of T. absoluta.

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“…Furthermore, the increasing public acceptance and safety record (Kleter, 2020;Papadopoulou et al, 2020) continue to provide evidence for their adoption in the management of insect pests (Khalid et al, 2017;Sinisterra-Hunter and Hunter, 2018;ISAAA, 2019;Jalaluddin et al, 2019;Samada and Tambunan, 2020). Our results further support the concept of using RNAi to improve the management of T. absoluta (Camargo et al, 2016;Rahmani and Bandani, 2021;Sarmah et al, 2021) and other lepidopteran pests (Ni et al, 2017;Bramlett et al, 2020;Yan et al, 2020a). The capacity to use RNAi to reduce T. absoluta through exogenously treated leaves, plants, or diets with bacterial-expressed dsRNA provides ample evidence for moving forward toward commercialization of RNAi biopesticides for the management of this economically devastating lepidopteran pest.…”

“…Modern agricultural biotechnologies are the most likely solution to growing demands for food, feed, and fibers, providing safer, more specific management of pathogens and pests (Adeyinka et al, 2020;Bramlett et al, 2020;Kunte et al, 2020;Raybould and Burns, 2020;Yan et al, 2020a,b;Sarmah et al, 2021). Furthermore, the increasing public acceptance and safety record (Kleter, 2020;Papadopoulou et al, 2020) continue to provide evidence for their adoption in the management of insect pests (Khalid et al, 2017;Sinisterra-Hunter and Hunter, 2018;ISAAA, 2019;Jalaluddin et al, 2019;Samada and Tambunan, 2020).…”

“…Efforts to develop botanical pesticides, like citrus peel extract have met with limited success (Senthil-Nathan, 2013;Miresmailli and Isman, 2014;Campolo et al, 2017). Development of alternative methods for pest control like RNAi biopesticides provide highly specific pesticides that do not harm parasitoids, pollinators, or predators (Chen et al, 2018;Niu et al, 2018;Christiaens et al, 2020;Fletcher et al, 2020;Kunte et al, 2020;Taning et al, 2020;Yan et al, 2020a,b;Sarmah et al, 2021). Research also shows that RNAi biopesticides can be exogenously applied in liquid sprays (Dalakouras et al, 2016;Koch et al, 2016;McLoughlin et al, 2018;Dubrovina et al, , 2020Jalaluddin et al, 2019;Mezzetti et al, 2020) or bound with a carrier-like clay or nanotubes in sprays (Worrall et al, 2019;Fletcher et al, 2020) or applied in water or clay pellets as a soil treatment (Ghosh et al, 2018) or as plant-expressed silencing, which has met with significant success in field crops (Younis et al, 2014;Bramlett et al, 2020;Das and Sherif, 2020;Veillet et al, 2020).…”

“…Application of RNAi to manage insect pests or viral pathogens is widely supportive of integrated pest management strategies and shows great potential (Bramlett et al, 2020;Christiaens et al, 2020;Das and Sherif, 2020). Sarmah et al (2021) report that while Tuta absoluta is sensitive to RNAi treatments demonstrating significantly increased mortality when ingesting the dsRNA made to the alphaCOP (αCOP) (Coatomer subunit alpha protein) mRNA transcript, there was no significant increase in mortality when treated individuals were fed on by the mirid predator Nesidiocoris tenuis (Hemiptera: Miridae). Thus, they concluded that RNAi-mediated control of T. absoluta would be a safe addition to biological control programs as it would not negatively affect the pest's natural enemies (Sarmah et al, 2021).…”

RNA interference in Pardosa pseudoannulata, an important predatory enemy against several insect pests, through ingestion of dsRNA‐expressing Escherichia coli

“…Although the RNAi‐mediated insect management was expected to be a sequence‐specific technology, silencing genes in non‐target species have been reported (Davidson and McCray Jr., 2011). Thus, the biosafety assessment of RNAi‐based pesticides is necessary as part of an integrated pest management strategy, especially in the beneficial insects as pollinators of Bombus and predators as Nesidiocoris (Zotti et al ., 2018; Sarmah et al ., 2021; Taning et al ., 2021a; 2021b). These reports supplied helpful information for our further application of the RNAi in the protection and utilization of these spiders.…”