DOI QR코드

DOI QR Code

Comparative Analysis of Cold Tolerance and Overwintering Site of Two Flower Thrips, Frankliniella occidentalis and F. intonsa

꽃노랑총채벌레와 대만총채벌레의 내한성과 월동처 비교 연구

  • Chulyoung, Kim (Department of Plant Medicals, College of Life Sciences, Andong National University) ;
  • Du-yeol, Choi (Department of Plant Medicals, College of Life Sciences, Andong National University) ;
  • Falguni, Khan (Department of Plant Medicals, College of Life Sciences, Andong National University) ;
  • Md Tafim Hossain, Hrithik (Department of Plant Medicals, College of Life Sciences, Andong National University) ;
  • Jooan, Hong (Department of Plant Medicals, College of Life Sciences, Andong National University) ;
  • Yonggyun, Kim (Department of Plant Medicals, College of Life Sciences, Andong National University)
  • Received : 2022.04.27
  • Accepted : 2022.06.13
  • Published : 2022.09.01

Abstract

Two dominant thrips in hot pepper (Capsicum annuum) cultivating in greenhouses are Frankliniella occidentalis and F. intonsa in Korea. This study investigated their overwintering physiology. These two thrips were freeze-susceptible and suppressed the body freezing temperature by lowering supercooling point (SCP) down to -15~-27℃. However, these SCPs varied among species and developmental stages. SCPs of F. occidentalis were -25.7±0.5℃ for adults, -17.2±0.3℃ for pupae, and -15.0±0.4℃ for larvae. SCPs of F. intonsa were -24.0±1.0℃ for adults, -27.0±0.5℃ for pupae, -17.2±0.8℃ for larvae. Cold injuries of both species occurred at low temperature treatments above SCPs. Thrips mortality increased as the treatment temperature decreased and its exposure period increased. F. occidentalis exhibited higher cold tolerance than F. intonsa. In both species, adults were more cold-tolerant than larvae. Two thrips species exhibited a rapid cold hardening because a pre-exposure to 0℃ for 2 h significantly enhanced the cold tolerance to a lethal cold temperature treatment at -10℃ for 2 h. In addition, a sequential exposure of the thrips to decreasing temperatures made them to be acclimated to low temperatures. To investigate the overwintering sites of the two species, winter monitoring of the thrips was performed at the greenhouses. During winter season (November~February), adults of the two species were not captured in outside of the greenhouses. However, F. occidentalis adults were captured to the traps and observed in weeds within the greenhouses. F. occidentalis adults were also emerged from soil samples obtained from the greenhouses during the winter season. F. intonsa adults did not come out from the soil samples at November and December, but emerged from the soil samples obtained after January. To determine the adult emergence due to diapause development, two thrips species were reared under different photoperiods. Adult development occurred in all photoperiod treatments in F. occidentalis, but did not in F. intonsa especially under short periods. Tomato spotted wilt virus, which is transmitted by these two species, was detected in the weeds infested by the thrips during the winter season. These results suggest that F. occidentalis develops on weeds in the greenhouses while F. intonsa undergoes a diapause in the soil during winter.

시설재배지 고추(Capsicum annuum)에 주요 총채벌레는 꽃노랑총채벌레(Frankliniella occidentalis)와 대만총채벌레(F. intonsa)이다. 본 연구는 이들 총채벌레의 월동 생리를 분석하는 데 목적을 두었다. 두 총채벌레는 동결감수성 곤충으로 낮은 저온(-15~-25℃)에서 체내빙결점을 보였다. 그러나 이 체내빙결점은 두 종 사이에 그리고 발육태에 따라 상이하였다. 꽃노랑총채벌레의 경우 성충 -25.7±0.5℃, 번데기 -17.2±0.3℃, 약충 -15.0±0.4℃였고 대만총채벌레는 성충 -24.0±1.0℃, 번데기 -27.0±0.5℃, 약충 -17.2±0.8℃에서 체내빙결점을 기록하였다. 그러나 실제로 두 종의 저온 피해는 체내빙결점보다 높은 온도에서 일어났으며, 처리온도가 내려갈수록 그리고 노출시간이 증가할수록 증가하였다. 대만총채벌레에 비해 꽃노랑총채벌레가 저온에 대해서 높은 내한성을 보였으며 발육태에 따라 약충보다는 성충이 높은 내한성을 나타냈다. 그러나 두 종 모두는 치사 저온조건(-10℃, 2시간)에 노출되기 전에 0℃에서 2시간 미리 노출되면 저온 피해가 현저하게 줄어드는 급속내한성유기를 보였다. 또한 단계적으로 감소하는 저온에 노출되면서 저온순화를 발현하였다. 이들 총채벌레의 월동처를 알아보기 위해 시설재배지 안팎에서 동계모니터링이 진행되었다. 동계기간(11월~2월) 두 종 성충은 야외에서 채집되지 않았지만, 시설재배지 내부에서는 꽃노랑총채벌레가 황색점착트랩과 잡초에서 포획되었다. 동계기간 시설재배지 토양시료에서 꽃노랑총채벌레 성충이 지속적으로 우화되었으나, 대만 총채벌레는 11월과 12월 토양시료에서 나오지 않았지만, 1월 이후 채집된 시료에서 성충 우화가 관찰되었다. 휴면에 따른 우화율 차이인지를 분석하기 위해 상이한 일장을 이들 두 총채벌레 종에 처리하였다. 이 결과 꽃노랑총채벌레는 일장조건과 무관하게 우화한 반면 대만총채벌레는 단일조건에서는 우화하지 않았다. 한편 이들 총채벌레가 전파하는 Tomato spotted wilt virus도 동계기간 총채벌레가 채집된 잡초에서 검출되었다. 이상의 결과는 꽃노랑총채벌레가 겨울기간 시설재배지 내부에서 잡초를 먹이로 발육하는 반면, 대만총채벌레의 경우는 휴면상태로 토양 속에서 월동하는 것으로 추정되었다.

Keywords

Acknowledgement

본 논문은 농촌진흥청 공동연구사업(과제번호: PJ01578901)과 안동대학교 기본연구지원사업에 의해 이루어졌다.

References

  1. Ahn, J., Choi, K., Huang, S.Y., Al Baki, M.A., Ahmed, S., Kim, Y., 2018. Calcium/calmodulin-dependent protein kinase II of the oriental fruit fly, Bactrocera dorsalis, and its association with rapid cold hardiness. J. Asia Pac. Entomol. 21, 1275-1282. https://doi.org/10.1016/j.aspen.2018.09.010
  2. Bale, J.S., Hayward, S.A., 2010. Insect overwintering in a changing climate. J. Exp. Biol. 213, 980-994. https://doi.org/10.1242/jeb.037911
  3. Barbagallo, B., Garrity, P.A., 2015. Temperature sensation in Drosophila. Curr. Opin. Neurobiol. 34, 8-13. https://doi.org/10.1016/j.conb.2015.01.002
  4. Brodsgaard, H.F., 1993. Cold hardiness and tolerance to submergence in water in Frankliniella occidentalis (Thysanoptera: Thripidae). Environ. Entomol. 22, 647-653. https://doi.org/10.1093/ee/22.3.647
  5. Costanzo, J.P., Humphreys, T.L., Lee, Jr., R.E., Moore, J.B., Lee, M.R., Wyman, J.A., 1998. Long-term reduction of cold hardiness following ingestion of ice-nucleating bacteria in the Colorado potato beetle, Leptinotarsa decemlineata. J. Insect Physiol. 44, 1173-1180. https://doi.org/10.1016/S0022-1910(98)00082-1
  6. Ditrich, T., 2018. Supercooling point is an individually fixed metric of cold tolerance in Pyrrhocoris apterus. J. Therm. Biol. 74, 208-213. https://doi.org/10.1016/j.jtherbio.2018.04.004
  7. Dong, W., Cheng, T., Li, C., Xu, C., Long, P., Chen, C., Zhou, S., 2014. Discriminating plants using the DNA barcode rbcLb: an appraisal based on a large data set. Mol. Ecol. Resour. 14, 336-343. https://doi.org/10.1111/1755-0998.12185
  8. Feng, Q., 2014. Temperature sensing by thermal TRP channels: thermodynamic basis and molecular insights. Curr. Top. Membr. 74, 19-50. https://doi.org/10.1016/B978-0-12-800181-3.00002-6
  9. Gallio, M., Ofstad, T.A., Macpherson, L.J., Wang, J.W., Zuker, C.S., 2011. The coding of temperature in the Drosophila brain. Cell 144, 614-624. https://doi.org/10.1016/j.cell.2011.01.028
  10. Hamada, F.N., Rosenzweig, M., Kang, K., Pulver, S.R., Ghezzi, A., Jegla, T.J., Garrity, P.A., 2008. An internal thermal sensor controlling temperature preference in Drosophila. Nature 454, 217-220. https://doi.org/10.1038/nature07001
  11. Hasebe, M., Omori, T., Nakazawa, M., Sano, T., Kato, M., Iwatsuki, K., 1994. rbcL gene sequences provide evidence for the evolutionary lineages of leptosporangiate ferns. Proc. Natl. Acad. Sci. USA 91, 5730-5734. https://doi.org/10.1073/pnas.91.12.5730
  12. Ishida, H., Murai, T., Sonoda, S., Yoshida, H., Izumi, Y., Tsumuki, H., 2003. Effects of temperature and photoperiod on development and oviposition of Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae). Appl. Entomol. Zool. 38, 65-68. https://doi.org/10.1303/aez.2003.65
  13. Jung, J.K., Seo, B.Y., Kim, Y., Lee, S.W., 2016. Can Maruca vitrata (Lepidoptera: Crambidae) over-winter in Suwon area? Korean J. Appl. Entomol. 55, 439-444. https://doi.org/10.5656/KSAE.2016.11.0.060
  14. Kim, Y., Kim, N., 1997. Cold hardiness in Spodoptera exigua (Lepidoptera: Noctuidae). Environ. Entomol. 26, 1117-1123. https://doi.org/10.1093/ee/26.5.1117
  15. Kim, Y., Song, W., 2000. Effect of thermoperiod and photoperiod on cold tolerance of Spodoptera exigua (Lepidoptera: Noctuidae). Environ. Entomol. 29, 868-873. https://doi.org/10.1603/0046-225X-29.5.868
  16. Kim, Y., Lee, D.W., Jung, J.K., 2017. Rapid cold-hardening of a subtropical species, Maruca vitrata (Lepidoptera: Crambidae), accompanies hypertrehalosemia by upregulating trehalose-6-phosphate synthase. Environ. Entomol. 46, 1432-1438. https://doi.org/10.1093/ee/nvx153
  17. Kim, C.Y., Choi, D.Y., Kang, J.H., Ahmed, S., Kil, E.J., Kwon, G.M., Lee, G.S., Kim, Y., 2021. Thrips infesting hot pepper cultured in greenhouses and variation in gene sequences encoded in TSWV. Korean J. Appl. Entomol. 60, 381-401.
  18. Kita, Y., Ito, M., 2000. Nuclear ribosomal ITS sequences and phylogeny in East Asian Aconitum subgenus Aconitum (Ranunculaceae), with special reference to extensive polymorphism in individual plants. Plant Syst. Evol. 225, 1-13. https://doi.org/10.1007/bf00985455
  19. Lee, G.S., Lee, J.H., Kang, S.H., Woo, K.S., 2001. Thrips species (Thysanoptera: Thripidae) in winter season and their vernal activities on Jeju island, Korea. J. Asia Pac. Entomol. 4, 115-122. https://doi.org/10.1016/S1226-8615(08)60112-0
  20. Lee, R.E. Jr., Damodaran, K., Yi, S.X., Lorigan, G.A., 2006. Rapid cold-hardening increases membrane fluidity and cold tolerance of insect cells. Cryobiology 52, 459-463. https://doi.org/10.1016/j.cryobiol.2006.03.003
  21. Li, K., Gong, Z., 2017. Feeling hot and cold: thermal sensation in Drosophila. Neurosci. Bull. 33, 317-322. https://doi.org/10.1007/s12264-016-0087-9
  22. Ni, L., Bronk, P., Chang, E.C., Lowell, A.M., Flam, J.O., Panzano, V.C., Theobald, D.L., Griffith, L.C., Garrity, P.A., 2013. A gustatory receptor paralogue controls rapid warmth avoidance in Drosophila. Nature 500, 580-584. https://doi.org/10.1038/nature12390
  23. Ni, L., Klein, M., Svec, K.V., Budelli, G., Chang, E.C., Ferrer, A.J., Benton, R., Samueal, A.D.T., Garrity, P.A., 2016. The ionotropic receptors IR21a and IR25a mediate cool sensing in Drosophila. Elife 5, e13254. https://doi.org/10.7554/elife.13254
  24. Park, Y., Kim, Y., 2013. RNA interference of glycerol biosynthesis suppresses rapid cold hardening of the beet armyworm, Spodoptera exigua. J. Exp. Biol. 216, 4196-4203. https://doi.org/10.1242/jeb.092031
  25. Park, Y., Kim, K., Kim, Y., 2014. Rapid cold hardening of Thrips palmi (Thysanoptera: Thripidae). Environ. Entomol. 43, 1076-1083. https://doi.org/10.1603/EN13291
  26. SAS Institute, Inc., 1989. SAS/STAT User's Guide. SAS Institute, Inc., Cary, NC.
  27. Sinclair, B.J., 2015. Linking energetics and overwintering in temperate insects. J. Therm. Biol. 54, 5-11. https://doi.org/10.1016/j.jtherbio.2014.07.007
  28. Storey, K.B., 1997. Organic solutes in freezing tolerance. Comp. Biochem. Physiol. 117A, 319-326. https://doi.org/10.1016/S0300-9629(96)00270-8
  29. Storey, K.B., Storey, J.M., 2013. Molecular biology of freezing tolerance. Comp. Physiol. 3, 1283-1308. https://doi.org/10.1002/cphy.c130007
  30. Teets, N.M., Yi, S.X., Lee, R.E. Jr., Denlinger, D.L., 2013. Calcium signaling mediates cold sensing in insect tissues. Proc. Natl. Acad. Sci. USA 110, 9154-9159. https://doi.org/10.1073/pnas.1306705110
  31. Teets, N.M., Gantz, J.D., Kawarasaki, Y., 2020. Rapid cold hardening: ecological relevance, physiological mechanisms and new perspectives. J. Exp. Biol. 223, jeb203448. https://doi.org/10.1242/jeb.203448
  32. Teets, N.M., Denlinger, D.L., 2014. Surviving in a frozen desert: environmental stress physiology of terrestrial Antarctic arthropods. J. Exp. Biol. 217, 84-93. https://doi.org/10.1242/jeb.089490
  33. Toxopeus, J., Sinclair, B.J., 2018. Mechanisms underlying insect freeze tolerance. Biol. Rev. Camb. Philos. Soc. 93, 1891-1914. https://doi.org/10.1111/brv.12425
  34. Tsumuki, H., Ishida, H., Yoshida, H., Sonoda, S., Izumi, Y., Murai, T., 2007. Cold hardiness of adult western flower thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae). Appl. Entomo. Zool. 42, 223-229. https://doi.org/10.1303/aez.2007.223
  35. White, T.J., Bruns, T., Lee, S., Taylor, J., 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics, in: Innis, M.A., Gelfand, D.H., Sninsky, J.J., White, T.J. (Eds), PCR protocols. A guide to methods and applications. Academic Press, SanDiego, CA, USA, pp. 315-322.
  36. Yi, S.X., Lee, R.E. Jr., 2003. Detecting freeze injury and seasonal cold-hardening of cells and tissues in the gall fly larvae, Eurosta solidaginis (Diptera: Tephritidae) using fluorescent vital dyes. J. Insect Physiol. 49, 999-1004. https://doi.org/10.1016/S0022-1910(03)00168-9
  37. Zachariassen, K.E., Kristiansen, E., 2000. Ice nucleation and antinucleation in nature. Cryobiology 41, 257-279. https://doi.org/10.1006/cryo.2000.2289
  38. Zhang, B., Qian, W., Qiao, X., Xi, Y., Wan, F., 2019. Invasion biology, ecology, and management of Frankliniella occidentalis in China. Arch. Insect Biochem. Physiol. 102, e21613. https://doi.org/10.1002/arch.21613