Abstract
Phytoseiulus persimilis is one of the most important biological control agents of spider mites. Multiple studies have been conducted on factors affecting its reproduction, but limited research on related molecular mechanisms has been carried out. In this study, RNA interference of three genes, ribosomal protein L11 (RpL11), ribosomal protein S2 (RpS2), and transformer-2 (tra-2), to newly emerged females were performed through oral delivery of double-stranded RNA, and knockdown of target genes was verified using qRT-PCR analysis. When RpL11 or RpS2 was interfered, 42 and 30% P. persimilis individuals either laid no egg or had no egg hatched, whereas the remaining females had their oviposition duration reduced by 31.8 and 49.9%, fecundity reduced by 48.1 and 67.8%, and egg hatching rate reduced by 20.4 and 22.4%, respectively. In addition, offspring sex ratios were significantly male biased especially at low fecundities. When tra-2 was interfered, no significant difference in fecundity was detected, but egg hatching rate reduced by 30.6%. This study verified the possibility of RNA interference in Phytoseiidae through oral delivery, and indicated that RpL11 and RpS2 are involved in egg formation, whereas tra-2 is involved in embryo development in P. persimilis. Phytoseiid mites have different sex determination pathways compared to insects. The present study provides data and evidence at molecular biological level for future research on reproduction and sex determination of phytoseiid mites.
Similar content being viewed by others
References
Amano H, Chant DA (1978) Some factors affecting reproduction and sex ratios in two species of predacious mites, Phytoseiulus persimilis Athias-Henriot and Amblyseius andersoni (Chant) (Acarina: Phytoseiidae). Can J Zool 56:1593–1607. https://doi.org/10.1139/z78-221
Bopp D, Saccone G, Beye M (2014) Sex determination in insects: variations on a common theme. Sex Dev 8:20–28. https://doi.org/10.1159/000356458
Cramton SE, Laski FA (1994) string of pearls encodes Drosophila ribosomal protein S2, has Minute-like characteristics, and is required during oogenesi. Genetics 137:1039–1048. https://doi.org/10.1101/gad.8.15.1853
Croft BA, Croft MB (1996) Intra- and interspecific predation among adult female phytoseiid mites (Acari: Phytoseiidae): effects on survival and reproduction. Environ Entomol 25(4):853–858. https://doi.org/10.1093/ee/25.4.853
Filia AG, Bain SA, Ross L (2015) Haplodiploidy and the reproductive ecology of arthropods. Curr Opin Insect Sci 9:36–43. https://doi.org/10.1016/j.cois.2015.04.018
Fraulo AB, Mcsorley R, Liburd OE (2008) Effect of the biological control agent Neoseiulus californicus (Acari: Phytoseiidae) on arthropod community structure in north Florida strawberry fields. Fla Entomol 91(3):436–445. https://doi.org/10.1653/0015-4040(2008)91[436:eotbca]2.0.co;2
Gadsby MC (1982) Dispersal in Phytoseiulus persimilis Athias-Henriot (Acarina: Phytoseiidae) and its importance to biological control programs. Dissertation, University of British Columbia
Gardner A, Ross L (2014) Mating ecology explains patterns of genome elimination. Ecol Lett 17:1602–1612. https://doi.org/10.1111/ele.12383
Gempe T, Beye M (2011) Function and evolution of sex determination mechanisms, genes and pathways in insects. Bioessays 33(1):52–60. https://doi.org/10.1002/bies.201000043
Geuverink E, Rensink AH, Rondeel I, Beukeboom LW, van de Zande L, Verhulst EC (2017) Maternal provision of transformer-2 is required for female development and embryo viability in the wasp Nasonia vitripennis. Insect Biochem Mol Biol 90:23–33. https://doi.org/10.1016/j.ibmb.2017.09.007
Gotoh T, Tsuchiya A (2008) Effect of multiple mating on reproduction and longevity of the phytoseiid mite Neoseiulus californicus. Exp Appl Acarol 44(3):185–197. https://doi.org/10.1007/s10493-008-9143-0
Hoy MA (1979) Parahaploidy of the arrhenotokous predator, Metaseiulus occidentalis (Acarina: Phytoseiidae) demonstrated by x-irradiation of males. Ent Exp Appl 26:97–104. https://doi.org/10.1111/j.1570-7458.1979.tb02903.x
Hoy MA, Waterhouse RM, Wu K et al (2016) Genome sequencing of the phytoseiid predatory mite Metaseiulus occidentalis reveals completely atomized Hox Genes and superdynamic intron evolution. Genome Biol Evol 8(6):1762–1775. https://doi.org/10.1093/gbe/evw048
Huang Z, Bian G, Xi Z, Xie X (2017) Genes important for survival or reproduction in Varroa destructor identified by RNAi. Insect Sci. https://doi.org/10.1111/1744-7917.12513
Jiang X, Lv J, Wang E, Xu X (2019) Spermatophore producing process and sperm transfer in Phytoseiulus persimilis. Exp Appl Acarol 77(1):11–25. https://doi.org/10.1007/s10493-018-0333-0
Kurscheid S, Valle MR, Bruyeres AG (2009) Evidence of a tick RNAi pathway by comparative genomics and reverse genetics screen of targets with known loss-of-function phenotypes in Drosophila. BMC Mol Biol 10:26. https://doi.org/10.1186/1471-2199-10-26
Lambertsson A (1998) The Minute genes in Drosophila and their molecular functions. Adv Genet 38:69–134. https://doi.org/10.1016/s0065-2660(08)60142-x
Lenteren JCV (2011) The state of commercial augmentative biological control: plenty of natural enemies, but a frustrating lack of uptake. Biocontrol 57(1):1–20. https://doi.org/10.1007/s10526-011-9395-1
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(–∆∆Ct) method. Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262
Lv J, Zhang B, Jiang X, Wang E, Xu X (2018) Quantitative impact of mating duration on reproduction and offspring sex ratio of Phytoseiulus persimilis (Acari: Phytoseiidae). J Integr Agr 17(0):60345–60347. https://doi.org/10.1016/s2095-3119(18)61974-4
Marygold SJ, Roote J, Reuter G et al (2007) The ribosomal protein genes and Minute loci of Drosophila melanogaster. Genome Biol 8(10):R216. https://doi.org/10.1186/gb-2007-8-10-r216
McMurtry JA, Huffaker CB, Vrie MVD (1970) Ecology of tetranychid mites and their natural enemies: A review: I. Tetranychid enemies: Their biological characters and the impact of spray practices. Hilgardia 40(11):331–390. https://doi.org/10.3733/hilg.v40n11p331
McMurtry JA, Oatman ER, Phillips PA, Wood CW (1978) Establishment of Phytoseiulus persimilis (Acari: Phytoseiidae) in Southern California. Entomophaga 23:175–179. https://doi.org/10.1007/BF02371725
Nachman G, Zemek R (2003) Interactions in a tritrophic acarine predator-prey metapopulation system V: Within-plant dynamics of Phytoseiulus persimilis and Tetranychus urticae (Acari: Phytoseiidae, Tetranychidae). Exp Appl Acarol 29(1/2):35–68. https://doi.org/10.1023/a:1024273327807
Nagelkerke CJ, Sabelis MW (1998) Precise control of sex allocation in pseudo-arrhenotokous phytoseiid mites. J Evolut Biol 11(6):649–684. https://doi.org/10.1046/j.1420-9101.1998.11060649.x
Opit GP, Nechols JR, Margolies DC (2004) Biological control of two spotted spider mites, Tetranychus urticae Koch (Acari: Tetranychidae), using Phytoseiulus persimilis Athias-Henriot (Acari: Phytoseidae) on ivy geranium: assessment of predator release ratios. Biol Control 29(3):445–452. https://doi.org/10.1016/j.biocontrol.2003.08.007
Palma AD, Alberti G (2001) Fine structure of the female genital systemin phytoseiid mites with remarks on egg nutrimentary development, sperm-access system, sperm transfer, and capacitation (Acari, Gamasida, Phytoseiidae). Exp Appl Acarol 25:525–591. https://doi.org/10.1023/A:1014741808835
Pomerantz AF, Hoy MA (2015) RNAi-mediated knockdown of transformer-2 in the predatory mite Metaseiulus occidentalis via oral delivery of double-stranded RNA. Exp Appl Acarol 65(1):17–27. https://doi.org/10.1007/s10493-014-9852-5
Reynaud E, Bolshakov VN, Barajas V, Kafatos FC, Zurita M (1997) Antisense suppression of the putative ribosomal protein S3A gene disrupts ovarian development in Drosophila melanogaster. Mol Gen Genet 256:462–467. https://doi.org/10.1007/s004380050590
Sabelis MW, Nagelkerke CJ, Breeuwer JAJ (2002) Sex ratio control in arrhenotokous and pseudo-arrhenotokous mites. In Hardy I C W (ed) Sex ratios: concepts and research methods. Cambridge, Cambridge University Press, pp 235–253. https://doi.org/10.1017/cbo9780511542053.012
Sarno F, Ruiz MF, Eirin-Lopez JM, Perondini AL, Selivon D, Sanchez L (2010) The gene transformer-2 of Anastrepha fruit flies (Diptera, Tephritidae) and its evolution in insects. BMC Evol Biol 10(1):140. https://doi.org/10.1186/1471-2148-10-140
Shukla JN, Palli SR (2012) Sex determination in beetles: production of all male progeny by parental RNAi knockdown of transformer. Sci Rep-UK 2:602. https://doi.org/10.1038/srep00602
Song Q, Gilbert LI (1997) Molecular cloning, developmental expression, and phosphorylation of ribosomal protein S6 in the endocrine gland responsible for insect molting. J Biol Inorg Chem 272(7):4429–4435. https://doi.org/10.1074/jbc.272.7.4429
Toyoshima S, Amano H (1998) Effect of prey density on sex ratio of two predacious mites, Phytoseiulus persimilis and Amblyseius womersleyi (Acari: Phytoseiidae). Exp Appl Acarol 22:709–723. https://doi.org/10.1023/A:1006093424452
Toyoshima S, Nakamura M, Nagahama Y, Amano H (2000) Process of egg formation in the female body cavity and fertilization in male eggs of Phytoseiulus persimilis (Acari: Phytoseiidae). Exp Appl Acarol 24:441–451. https://doi.org/10.1023/A:1006484621449
Tsunoda T (1994) Mating behavior of the predacious mite, Amblyseius womersleyi Schicha (Acari: Phytoseiidae). Appl Entomol Zool 29:141–147. https://doi.org/10.1303/aez.29.141
Wu K, Hoy MA (2014) Oral delivery of double-stranded RNA induces prolonged and systemic gene knockdown in Metaseiulus occidentalis only after feeding on Tetranychus urticae. Exp Appl Acarol 63(2):171–187. https://doi.org/10.1007/s10493-014-9772-4
Zhang X, Lv J, Hu Y (2015) Prey preference and life table of Amblyseius orientalis on Bemisia tabaci and Tetranychus cinnabarinus. PLoS ONE 10:e0138820. https://doi.org/10.1371/journal.pone.0138820
Zhou X, Liao W, Liao J, Liao P, Lu H (2015) Ribosomal proteins: functions beyond the ribosome. J Mol Cell Biol 7(2):92–104. https://doi.org/10.1093/jmcb/mjv014
Acknowledgements
This study was supported by the National Key R & D Program of China (Grant No. 2017YFD0200400), the National Natural Science Foundation of China (Grant Nos. 31701850, 31872028) and co-innovation project of CAAS and SDAAS ‘Key technologies on regional green agricultural development and integrated demonstration’. We thank Ms. Hu Yi for the rearing of Tetranychus urticae and Ms. Gong Tao, Zhuo Yuli, Lu Qin for their assistance in the experiments.
Author information
Authors and Affiliations
Corresponding authors
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Sijia, B., Jiale, L., Juan, X. et al. RNAi mediated knockdown of RpL11, RpS2, and tra-2 led to reduced reproduction of Phytoseiulus persimilis. Exp Appl Acarol 78, 505–520 (2019). https://doi.org/10.1007/s10493-019-00403-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10493-019-00403-2