Abstract
The rice swarming caterpillar, Spodoptera mauritia (Biosduval, 1833) (Lepidoptera: Noctuidae), has been considered a severe pest and has caused the extreme loss of rice paddies in the nursery stages. The massive reproductive efficiency of pests results from balanced endocrine functioning. Insect treatments with exogenous either juvenile hormones (JH) or juvenile hormone analogues (JHAs) during low endogenous JH titers disrupt metamorphosis and ovarian development. Hence, it was thought worthwhile to develop a primary ovarian cell culture of Spodoptera mauritia to study the biological efficiency of JHA, fenoxycarb, at the cellular level. The study envisioned the cell characteristics and growth properties and found that most cells were spherical. Spindle-shaped cells were also present during the initial stage of active cell division. The majority of the cells grew attached to the bottom of the culture plates, and a few grew in suspension. The cell doubling time was 144 ± 14 h. The growth curve exhibited a sigmoid pattern of cell proliferation at first, followed by a declining phase. These properties indicate that the primary ovarian culture is a suitable candidate for developing a novel cell line of S. mauritia. The preliminary study investigated the cytotoxicity of the insect growth regulator fenoxycarb in ovarian, primary cell culture. Incubated cells showed noticeable morphological changes, including cell shrinkage and apoptotic body formation; inhibition of cellular proliferation; and apoptosis-inducing effects in ovarian, primary cell culture of S. mauritia. Evidently, from these results, it is clear that juvenile hormone mimics can react in a meaningful way to control the rice pest S. mauritia by inducing cellular apoptosis in ovarian cells, which may cause adult females to become sterile.
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References
Banu CA, Manogem EM (2022) Anti-proliferative and apoptosis-inducing effects of juvenile hormone analogue, fenoxycarb in the Sf21cell line. Pestic Biochem Physiol 187:105182. https://doi.org/10.1016/j.p00estbp.2022.105182
Banu CA, Praseeja C, Manogem EM (2022) Evaluation of the histopathological and biochemical effects of fenoxycarb in the ovaries of Spodoptera mauritia (Lepidoptera: Noctuidae). Int J Trop Insect Sci 1–12:2143. https://doi.org/10.1007/s42690-022-00769-8
Banu CA, Sathyakala KP, Manogem EM (2019) Efficacy of JHA, fenoxycarb on egg hatchability and postembryonic development of Spodoptera mauritia Boisd. (Lepidoptera: Noctuidae). Int J Adv Res 7(06):80–86. https://doi.org/10.21474/IJAR01/9198
Banu CA, Sathyakala KP, Manogem EM (2019) Evaluation and screening of growth disrupting juvenile hormone analogue, fenoxycarb on the development and metamorphosis of Spodoptera mauritia Boisd.(Lepidoptera: Noctuidae). Crop Res 54(5and6):158–164. https://doi.org/10.31830/2454-1761.2019.027
Bicchi C, D’Amato A, Tonutti I, Cantamessa L (1990) Simultaneous determination of clofentezine, fenoxycarb and hexythiazox by HPLC on apples, pears and their pulps. Pestic Sci 30(1):13–19. https://doi.org/10.1002/ps.2780300103
Bruce DH, Gary BQ (1981) Metabolism and mode of action of juvenile hormone, juvenoids and other insect growth regulators. In: Progress in pesticide biochemistry (eds. D.H. Hutson and T.R. Roberts), John Wiley and Sons Ltd., 1–85
Can H, Soya S, Yıkılmaz MS (2017) Primary culture of lepidopteran adherent and suspension cells from larval testes of Bombyx mori. Hacettepe J Biol Chem 45(2):213–218. https://dergipark.org.tr/en/download/article-file/1728110. Accessed 01.06.2017
Cherbas L, Koehler MMD, Cherbas P (1989) Effects of juvenile hormone on the ecdysone response of Drosophila Kc cells. Dev Genet 10(3):177–188. https://doi.org/10.1002/dvg.1020100307
Garcia JJ, Li G, Wang P, Zhong J, Granados RR (2001) Primary and continuous midgut cell cultures from Pseudaletia unipuncta (lepidoptera: Noctuidae). In Vitro Cell Dev Biol-Anim 37(6):353–359. https://doi.org/10.1007/BF02577570
Gelernter WD, Federici BA (1986) Continuous cell line from Spodoptera exigua (Lepidoptera: Noctuidae) that supports replication of nuclear polyhedrosis viruses from Spodoptera exigua and Autographa californica. J Invertebr Pathol 48(2):199–207. https://doi.org/10.1016/0022-2011(86)90124-2
Goodman CL, El Sayed GN, Mcintosh AH, Grasela JJ, Stiles B (2001) Establishment and characterization of insect cell lines from 10 lepidopteran species. In Vitro Cell Dev Biol-Anim 37(6):367–373. https://doi.org/10.1007/BF02577573.pdf
Govind TR (2014) Research article effect of juvenile hormone analogue (fenoxycarb) on ovarian development of Dysdercus similis. Int J Recent Sci Res 5(9):1714–1716. https://recentscientific.com/effect-juvenile-hormone-analogue-fenoxycarb-ovarian-development-dysdercus-similis. Accessed 2017
Himeno M, Takahashi J, Komano T (1979) Effect of juvenile hormone on macromolecular synthesis of an insect cell line. Agric Biol Chem 43(6):1285–1292. https://doi.org/10.1080/00021369.1979.10863608
Hink WF, Ellis BJ (1971) Establishment and characterization of two new cell lines (CP-1268 and CP-169) from the codling moth, Carpocapsa pomonella (with a review of culture of cells and tissues from Lepidoptera). Arthropod Cell Cult Their App Study Viruses 55:19–28. https://doi.org/10.1007/978-3-642-65224-0_3
Khurad AM, Bahekar RS, Zhang MJ, Tiple AD, Lee JM, Zhang CX, Kusakabe T (2013) Development and characterization of a new Bombyx mori cell line for protein expression. J Asia-Pacific Entomol 16(1):17–22. https://doi.org/10.1016/j.aspen.2012.09.004
Khurad AM, Kanginakudru S, Qureshi SO, Rathod MK, Rai MM, Nagaraju J (2006) A new Bombyx mori larval ovarian cell line highly susceptible to nucleopolyhedrovirus. J Invertebr Pathol 92(2):59–65. https://doi.org/10.1016/j.jip.2006.03.005
Khurad AM, Zhang MJ, Deshmukh CG, Bahekar RS, Tiple AD, Zhang CX (2009) A new continuous cell line from larval ovaries of silkworm, Bombyx mori. In Vitro Cell Dev Biol-Anim 45(8):414–419. https://doi.org/10.1007/s11626-009-9197-2
Knudson DL, Lescott T, Tinsley TW (1980) Establishment of a continuous cell line of Spodoptera littoralis (Lepidoptera; Noctuidae). In Vitro 16(5):369–370 (file:///C:/Users/Dell/Desktop/bf02618358.pdf)
Lezzi M, & Wyss C(1976). The antagonism between juvenile hormone and ecdysone. In The Juvenile Hormones 252 – 269. https://doi.org/10.1007/978-1-4684-7947-8_18
Li J, He F, Yang Y, Xiao Y, Peng R, Yao H, Li X, Peng J, Hong H, Liu K (2015) Establishment and characterization of a novel cell line from midgut tissue of Helicoverpa armigera (Lepidoptera: Noctuidae). In Vitro Cell Dev Biol-Anim 51(6):562–571. https://doi.org/10.1007/s11626-015-9870-6
Li X, Qin Q, Zhang N, Zhu W, Zhang J, Wang H, Miao L, Zhang H (2012) A new insect cell line from pupal ovary of Spodoptera exigua established by stimulation with N-methyl-N′-nitro-N-nitrosoguanidine (MNNG). In Vitro Cell Dev Biol-Anim 48(5):271–275. https://doi.org/10.1007/s11626-012-9511-2
Lynn DE (1996) Development and characterization of insect cell lines.Cytotechnology 20(1–3):3–11. https://link.springer.com/article/10.1007%2FBF00350384. Accessed 2017
Lynn DE (2001) Novel techniques to establish new insect cell lines. In Vitro Cell Dev Biol-Anim 37(6):319–321. https://doi.org/10.1007/BF02577564.pdf
Metwally MM, Landa V (1972) Sterilization of the Khapra beetle, Trogoderma granarium Everts, with juvenile hormone analogues. Z Angew Entomol 72:97–109. https://doi.org/10.1111/j.1439-0418.1972.tb02223.x
Masner P, Angst M, Dorn S (1987) Fenoxycarb, an insect growth regulator with juvenile hormone activity: a candidate for Heliothis virescens (F.) control on cotton. Pestic Sci 18(2):89–94. https://doi.org/10.1002/ps.2780180203
Masner P, Dorn S, Vogel W, Kalin M, Graf O (1981) Types of response of insects to a new IGR and to proven standards. Regulation of insect development and behavior: International Conference, Karpacz, Poland, June 23–28
Michel M, Krause A, Buszewski B (2001) Column switching and liquid chromatographic technique for the rapid determination of fenoxycarb insecticide residues in apples. Polish J Environ Studies 10(4):283–288.
Mitsuhashi J (2002) Invertebrate tissue culture methods. Springer, Tokyo, pp 107–115. https://doi.org/10.1007/978-4-431-67875-5_10
Miyamoto J, Hirano M, Takimoto Y, Hatakoshi M (1993) Insect growth regulators for pest control, with emphasis on juvenile hormone analogs: present status and future prospects. ACS Symp Ser 524:144–168. https://doi.org/10.1021/bk-1993-0524.ch011
Oberlander H, Leach CE, Shaaya E (2000) Juvenile hormone and juvenile hormone mimics inhibit proliferation in a lepidopteran imaginal disc cell line. J Insect Physiol 46(3):259–265. https://doi.org/10.1016/S0022-1910(99)00178-X
Pan MH, Cai XJ, Liu M, Lv J, Tang H, Tan J, Lu C (2010) Establishment and characterization of an ovarian cell line of the silkworm Bombyx mori. Tissue Cell 42(1):42–46. https://doi.org/10.1016/j.tice.2009.07.002
Pant U, Sudeep AB, AthawaleSS,Vipat VC (2002) Baculovirus studies in new, indigenous lepidopteran cell lines. Ind J Exp Biol 40:63 68. http://hdl.handle.net/123456789/17166. Accessed 2017
Peronnet F, Ziarczyk P, Rollet E, Courgeon AM, Becker J, Maisonhaute C, Echalier G, Best-Belpomme M (1989) Drosophila cell lines as a model for studying the mechanisms of ecdysteroid action. In: Koolman J (ed) Ecdysone: from chemistry to mode of action. Georg Thieme-Verlag, Stutgart, pp 378–383
Raikhel A, Brown M, Belles X (2005) 3.9 Hormonal control of reproductive processes. Comprehens Mol Insect Sci 3:433 91. https://www.biologiaevolutiva.org/xbelles/pdfs/2005-Raikhel-Comprehensive.pdf. Accessed 2017
Reall T, Kraus S, Goodman CL, Ringbauer J, Geibel S, Stanley D (2019) Next-generation cell lines established from the fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae). In Vitro Cell Dev Biol-Anim 55(9):686–693. https://doi.org/10.1007/s11626-019-00394-9
Retnakaran A, Granett J, Ennis T (1985) Insect growth regulators. In: Comprehensive insect physiology, biochemistry and pharmacology, Kerkut GA, Gilbert LI (eds) Pergamon Press, New York, 12:529–601. https://d-nb.info/851000223/04. Accessed 2017
Rohdendorf EB, Sehnal F (1972) The induction of ovarian dysfunctions in Thermobia domestica by the Cecropia juvenile hormones. Experientia 28(9):1099–1101. https://doi.org/10.1007/BF01918699
Rohdendorf EB, Sehnal F (1973) Inhibition of reproduction and embryogenesis in the firebrat, Thermobia domestica, by juvenile hormone analogues. J Insect Physiol 19(1):37–56. https://doi.org/10.1016/0022-1910(73)90220-5
Roy S, Saha TT, Zou Z, Raikhel AS (2018) Regulatory pathways controlling female insect reproduction. Annu Rev Entomol 63:489–511. https://doi.org/10.1146/annurev-ento-020117-043258
Shih CJ, Lin RW, Wang CH (1997) Establishment of a cell line from Spodoptera litura (Lepidoptera: Noctuidae) and replication of S. litura nuclear polyhedrosis virus in vitro. J Invertebr Pathol 69(1):1–6. https://doi.org/10.1006/jipa.1996.4625
Smagghe G, Goodman CL, Stanley D (2009) Insect cell culture and applications to research and pest management. In Vitro Cell Dev Biol-Anim 45(3):93–105. https://doi.org/10.1007/s11626-009-9181-x
Soya S, Can H (2019) Characteristics of various cell types in primary insect cell culture from larval ovaries of silkworm (Bombyx mori L.). J Animal Plant Sci 29(1):325–332. https://www.researchgate.net/publication/330909731. Accessed 2017
Spindler KD, Quack S, Spindler-Barth M (1993) Insect cell lines as tools for insecticide screening. Trends Comp Biochem Physiol 1:1045–1056
Sudeep AB, Mourya DT, Shouche YS, Pidiyar V, Pant U (2002) A new cell line from the embryonic tissue of Helicoverpa armigera HBN.(Lepidoptera: Noctuidae). In Vitro Cell Dev Biol-Anim 38(5):262–264
Sullivan J (2000) Environmental fate of fenoxycarb. Environmental Monitoring Fate Reviews, Environmental Monitoring Branch. Department of Pesticide Regulation EPA, California, Sacramento USA. http://piat.org.nz/uploads/PIAT_content/pdfs/Environmental%20fate%20of%20Fenoxycarb.pdf. Accessed 2017
Vaughn JL, Goodwin RH, Tompkins GJ, Mc Cawley PJIV (1977) The establishment of two cell lines from the insect Spodoptera frugiperda (Lepidoptera; Noctuidae). In vitro 13(4):213–217>
Xu M, Tan J, Wang X, Zhong X, Cui H (2015) Establishment and characterization of a new embryonic cell line from the silkworm, Bombyx mori. Invertebr Surv J 12(1):13–18. https://www.isj.unimore.it/index.php/ISJ/article/view/339/254. Accessed 2017
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We gratefully acknowledge DST-SERB, New Delhi, and the special assistance program (SAP) of the Department of Zoology, University of Calicut, for the completion of this work.
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The first author was funded by the University Grant Commission (UGC), New Delhi, with Maulana Azad National Fellowship for 2015–16 F1-17.1/2015–16/MANF-2015–17-KER-51524/(SA-III/Website). Individual research funding was provided to the corresponding author as a major research project from DST-SERB, New Delhi (SB/FT/LS-402/2012).
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Two authors contributed to the study. Dr. C. Ayisha Banu performed material preparation, research work, data analysis, interpretation, and manuscript writing. Dr. E. M. Manogem participated in the experimental design, supervision, suggestions, and critical reviews. Both authors read and approved the final manuscript.
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Banu, C.A., Manogem, E.M. Development and characterization of Spodoptera mauritia ovarian primary cell culture and evaluation of fenoxycarb toxicity. In Vitro Cell.Dev.Biol.-Animal 58, 788–797 (2022). https://doi.org/10.1007/s11626-022-00728-0
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DOI: https://doi.org/10.1007/s11626-022-00728-0