Scientia Agricultura Sinica ›› 2021, Vol. 54 ›› Issue (13): 2781-2788.doi: 10.3864/j.issn.0578-1752.2021.13.008

• PLANT PROTECTION • Previous Articles     Next Articles

Response of Liriomyza trifolii to Cold Acclimation and Differences of Cold Tolerance Among Different Populations

ZHANG QiKai1(),XING ZhenLong2,WU ShengYong1,XU RuiRui1,LEI ZhongRen1()   

  1. 1State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193
    2State Key Laboratory of Crop Stress Adaptation and Improvement, School of Life Sciences, Henan University, Kaifeng 475004, Henan
  • Received:2020-10-16 Revised:2020-12-14 Online:2021-07-01 Published:2021-07-12
  • Contact: ZhongRen LEI E-mail:18810521205@163.com;leizhr@sina.com

RichHTML

29

PDF

537

Abstract:

【Objective】The response of the major invasive pest Liriomyza trifolii to cold acclimation and the cold tolerance of three geographical populations (Wuhan City, Hubei Province; Haikou City, Hainan Province; Anqing City, Anhui Province) were studied to provide references for the potential colonization of L. trifolii in high latitudes of China.【Method】The pupae and adults of L. trifolii population in Hainan were exposed to low temperatures of -12, -14, -16, -18, -20, -22 and -24℃ for 30 min, and the temperature with a survival rate of 15%-30% was selected as the recognition temperature. The L. trifolii pupae and adults were put at 5℃ for 1-6 h or 12℃ for 1-6 d, and then put at the recognition temperature for 30 min to detect the survival rate. The undomesticated pupae and adults were also placed at the recognition temperature for 30 min as a control, and the difference in low-temperature survival rate after cold acclimation was compared. Besides, five target temperatures were set at 0, -5, -10, -15, and -20℃, respectively, and the pupae of three geographical populations were exposed to the target temperatures for 2 h, the difference of survival rate was studied. Finally, the supercooling point (SCP) of pupae of three geographical populations was measured by supercooling point tester.【Result】When theL. trifolii pupae and adults were exposed to -20℃ for 30 min, the survival rates were 15.0%, 19.6%, and 21.0%, respectively. Therefore, -20℃ was determined as the cold acclimation recognition temperature of L. trifolii. The cold tolerance ofL. trifolii pupae and adults was improved after rapid cold acclimation at 5℃, and the adults responded more positively to rapid cold acclimation. The effect of cold acclimation for 1 h and 2 h was the best, and the effect of rapid cold acclimation decreased gradually until disappeared with the extension of exposure time. Within 6 days, the cold tolerance ofL. trifolii pupae and adults was improved by low-temperature exposure at 12℃ for different periods, and there was little difference in cold tolerance after cold acclimation for different periods. Besides, under the low-temperature exposure of 5, 0 and -5℃, there was no significant difference in the survival rate of pupae between the Hainan population and Anhui, Hubei populations, but under the low-temperature exposure of -10, -15 and -20℃, the pupa survival rate of Hainan population was significantly lower than that of Anhui and Hubei populations. The SCP of pupae in the Anhui and Hubei populations was significantly lower than that in the Hainan population.【Conclusion】The cold tolerance of L. trifolii can be enhanced by cold acclimation, which may be one of the reasons why L. trifolii gradually spread to high latitudes in China. The cold tolerance of the Hubei and Anhui populations is stronger than that of the Hainan population. The results are helpful to predict the overwintering distribution area of L. trifolii in China and guide its monitoring, early warning, and prevention and control.

Key words: Liriomyza trifolii, cold acclimation, supercooling point, cold tolerance

Fig. 1

Survival rate of the Hainan L. trifolii pupae and adults exposed to different temperatures for 30 min "

Fig. 2

Effects of rapid cold acclimation on the low-temperature survival rate of the Hainan L. trifolii at different insect stages Different lowercases on the bars indicate significant differences (one-way ANOVA, Tukey’s HSD,P<0.05). The same asFig. 3, Fig. 5 "

Fig. 3

Effects of long-term cold acclimation on the low-temperature survival rate of the HainanL. trifolii at different insect stages "

Fig. 4

The low-temperature survival rate of L. trifolii pupae of different geographical populations under different temperatures Different lowercases on the bars indicate significant differences (two-way ANOVA, Tukey’s HSD,P<0.05) "

Fig. 5

Supercooling points of L. trifolii pupae of different geographical populations "

[1] 雷仲仁, 姚君明, 朱灿建, 王海鸿. 三叶斑潜蝇在中国的适生区预测. 植物保护, 2007, 33(5):100-103.
LEI Z R, YAO J M, ZHU C J, WANG H H. Prediction of suitable areas for Liriomyza trifolii (Burgess) in China . Plant Protection, 2007, 33(5):100-103. (in Chinese)
[2] JOHNSON M W, WELTER S C, TOSCANO N C, TING I P, TRUMBLE J T. Reduction of tomato leaflet photosynthesis rates by mining activity ofLiriomyza sativae(Diptera: Agromyzidae). Journal of Economic Entomology, 1983, 76(5):1061-1063.
doi: 10.1093/jee/76.5.1061
[3] PARRELLA M P, JONES V P, YOUNGMAN R R, LEBECK L M. Effect of leaf mining and leaf stippling ofLiriomyzaspp.on photosynthetic rates ofChrysanthemum. Annals of the Entomological Society of America, 1985, 78(1):90-93.
doi: 10.1093/aesa/78.1.90
[4] REITZ S R, TRUMBLE J T. Interspecific and intraspecific differences in twoLiriomyza leafminer species in California. Entomologia Experimentalis et Applicata, 2002, 102(2):101-113.
doi: 10.1046/j.1570-7458.2002.00930.x
[5] 王宪辉, 齐宪磊, 康乐. 昆虫的快速冷驯化现象及其生态适应意义. 自然科学进展, 2003, 13(11):1128-1133.
WANG X H, QI X L, KANG L. The phenomenon of rapid cold acclimation of insects and its significance of ecological adaptation. Progress in Natural Science, 2003, 13(11):1128-1133. (in Chinese)
[6] KIM Y, KIM N. Cold hardiness inSpodoptera exigua(Lepidoptera: Noctuidae). Environmental Entomology, 1997, 26(5):1117-1123.
doi: 10.1093/ee/26.5.1117
[7] OVERGAARD J, MALMENDAL A, SØRENSEN J G, BUNDY J G, LOESCHCKE V, NIELSEN N C, HOLMSTRUP M. Metabolomic profiling of rapid cold hardening and cold shock in Drosophila melanogaster. Journal of Insect Physiology, 2007, 53(12):1218-1232.
doi: 10.1016/j.jinsphys.2007.06.012
[8] WANG X H, KANG L. Rapid cold hardening in young hoppers of the migratory locustLocusta migratoriaL. (Orthoptera: Acridiidae). Cryo Letters, 2003, 24(5):331-340.
[9] SINCLAIR B J, CHOWN S L. Rapid cold-hardening in a Karoo beetle,Afrinussp. Physiological Entomology, 2006, 31(1):98-101.
doi: 10.1111/pen.2006.31.issue-1
[10] KANG L, CHEN B, WEI J N, LIU T X. Roles of thermal adaptation and chemical ecology in Liriomyza distribution and control. Annual Review of Entomology, 2009, 54:127-145.
doi: 10.1146/annurev.ento.54.110807.090507
[11] SHINTANI Y, ISHIKAWA Y. Relationship between rapid cold- hardening and cold acclimation in the eggs of the yellow-spotted longicorn beetle, Psacothea hilaris. Journal of Insect Physiology, 2007, 53(10):1055-1062.
doi: 10.1016/j.jinsphys.2007.05.012
[12] 孔璐, 郭建英, 周忠实, 万方浩. 昆虫冷驯化机制研究进展. 应用昆虫学报, 2012, 49(6):1664-1669.
KONG L, GUO J Y, ZHOU Z S, WAN F H. Progress in research on cold hardening in insects. Chinese Journal of Applied Entomology, 2012, 49(6):1664-1669. (in Chinese)
[13] TURNOCK W J, BOIVIN G, RING R A. Interpopulation differences in the coldhardiness of Delia radicum (Diptera: Anthomyiidae). The Canadian Entomologist, 1998, 130(2):119-129.
doi: 10.4039/Ent130119-2
[14] SHINTANI Y, ISHIKAWA Y. Geographic variation in cold hardiness of eggs and neonate larvae of the yellow-spotted longicorn beetle Psacothea hilaris. Physiological Entomology, 1999, 24(2):158-164.
doi: 10.1046/j.1365-3032.1999.00126.x
[15] TANAKA K. Cold tolerance in the house spider,Achaearanea tepidariorum (Araneae: Theridiidae). Entomological Science, 1999, 2(4):597-604.
[16] JING X H, KANG L. Geographical variation in egg cold hardiness: A study on the adaptation strategies of the migratory locust Locusta migratoriaL. Ecological Entomology, 2003, 28(2):151-158.
doi: 10.1046/j.1365-2311.2003.00497.x
[17] OVERGAARD J, HOFFMANN A A, KRISTENSEN T N. Assessing population and environmental effects on thermal resistance in Drosophila melanogaster using ecologically relevant assays. Journal of Thermal Biology, 2011, 36(7):409-416.
doi: 10.1016/j.jtherbio.2011.07.005
[18] CHEN B, KANG L. Variation in cold hardiness of Liriomyza huidobrensis (Diptera: Agromyzidae) along latitudinal gradients. Environmental Entomology, 2004, 33(2):155-164.
doi: 10.1603/0046-225X-33.2.155
[19] CHEN B, KANG L. Can greenhouses eliminate the development of cold resistance of the leafminers? Oecologia, 2005, 144(2):187-195.
doi: 10.1007/s00442-005-0051-2
[20] 相君成, 雷仲仁, 王海鸿, 高玉林. 三种外来入侵斑潜蝇种间竞争研究进展. 生态学报, 2012, 32(5):1616-1622.
XIANG J C, LEI Z R, WANG H H, GAO Y L. Interspecific competition among three invasiveLiriomyzaspecies . Acta Ecologica Sinica, 2012, 32(5):1616-1622. (in Chinese)
[21] WAN F H, YANG N W. Invasion and management of agricultural alien insects in China. Annual Review of Entomology, 2016, 61:77-98.
doi: 10.1146/annurev-ento-010715-023916
[22] PARRELLA M P. Biology of Liriomyza. Annual Review of Entomology, 1987, 32:201-224.
doi: 10.1146/annurev.en.32.010187.001221
[23] XING Z L, LIU Y Q, CAI W Z, HUANG X Z, WU S Y, LEI Z R. Efficiency of trichome-based plant defense in Phaseolus vulgaris depends on insect behavior, plant ontogeny, and structure. Frontiers in Plant Science, 2017, 8:2006.
doi: 10.3389/fpls.2017.02006
[24] ZHAO Y X, KANG L. Cold tolerance of the leafminerLiriomyza sativae (Dipt., Agromyzidae). Journal of Applied Entomology, 2000, 124(3/4):185-189.
doi: 10.1046/j.1439-0418.2000.00463.x
[25] WANG H H, LEI Z R, LI X, OETTING R D. Rapid cold hardening and expression of heat shock protein genes in the B-biotypeBemisia tabaci. Environmental Entomology, 2011, 40(1):132-139.
doi: 10.1603/EN09357
[26] 张智, 郑乔, 张云慧, 刘杰, 殷新田, 汤清波, 李静, 袁源, 李祥瑞, 朱勋. 草地贪夜蛾室内种群抗寒能力测定. 植物保护, 2019, 45(6):43-49.
ZHANG Z, ZHENG Q, ZHANG Y H, LIU J, YIN X T, TANG Q B, LI J, YUAN Y, LI X R, ZHU X. Cold hardiness of laboratory populations of Spodoptera frugiperda. Plant Protection, 2019, 45(6):43-49. (in Chinese)
[27] CHEN C P, DENLINGER D L, LEE JR R E. Cold-shock injury and rapid cold hardening in the flesh fly Sarcophaga crassipalpis. Physiological Zoology, 1987, 60(3):297-304.
doi: 10.1086/physzool.60.3.30162282
[28] DANKS H V. The wider integration of studies on insect cold- hardiness. European Journal of Entomology, 1996, 93:383-404.
[29] RAKO L, HOFFMANN A A. Complexity of the cold acclimation response in Drosophila melanogaster. Journal of Insect Physiology, 2006, 52(1):94-104.
doi: 10.1016/j.jinsphys.2005.09.007
[30] JENSEN D, OVERGAARD J, SØRENSEN J G. The influence of developmental stage on cold shock resistance and ability to cold-harden in Drosophila melanogaster. Journal of Insect Physiology, 2007, 53(2):179-186.
doi: 10.1016/j.jinsphys.2006.11.008
[31] WANG X H, KANG L. Differences in egg thermotolerance between tropical and temperate populations of the migratory locust Locusta migratoria (Orthoptera: Acridiidae). Journal of Insect Physiology, 2005, 51(11):1277-1285.
doi: 10.1016/j.jinsphys.2005.07.010
[32] 邢振龙. 三叶斑潜蝇在我国的入侵扩散及其与美洲斑潜蝇的竞争取代[D]. 北京: 中国农业大学, 2018.
XING Z L. Range expansion of Liriomyza trifolii (Burgess) and competitive displacement with its’ congener species,L. sativae Blanchard, in China [D]. Beijing: China Agricultural University, 2018. (in Chinese)
[33] CHEN B, KANG L. Implication of pupal cold tolerance for the northern over-wintering range limit of the leafminer Liriomyza sativae (Diptera: Agromyzidae) in China. Applied Entomology and Zoology, 2005, 40(3):437-446.
doi: 10.1303/aez.2005.437
[34] MASAKI S. Geographical variation of life cycle in crickets (Ensifera: Grylloidea). European Journal of Entomology, 1996, 93:281-302.
[35] KIMURA M T. Cold and heat tolerance of drosophilid flies with reference to their latitudinal distributions. Oecologia, 2004, 140(3):442-449.
doi: 10.1007/s00442-004-1605-4
[36] MORGAN D J W, REITZ S R, ATKINSON P W, TRUMBLE J T. The resolution of Californian populations of Liriomyza huidobrensis and Liriomyza trifolii (Diptera: Agromyzidae) using PCR. Heredity, 2000, 85(1):53-61.
doi: 10.1046/j.1365-2540.2000.00731.x
[37] FULLER S J, CHAVIGNY P, LAPCHIN L, VANLERBERGHE- MASUTTI F. Variation in clonal diversity in glasshouse infestations of the aphid,Aphis gossypiiGlover in southern France. Molecular Ecology, 1999, 8(11):1867-1877.
doi: 10.1046/j.1365-294x.1999.00782.x
[38] HOFFMANN A A, HERCUS M J. Environmental stress as an evolutionary force. Bioscience, 2000, 50(3):217-226.
doi: 10.1641/0006-3568(2000)050[0217:ESAAEF]2.3.CO;2
[1] WANG JunJuan,LU XuKe,WANG YanQin,WANG Shuai,YIN ZuJun,FU XiaoQiong,WANG DeLong,CHEN XiuGui,GUO LiXue,CHEN Chao,ZHAO LanJie,HAN YingChun,SUN LiangQing,HAN MingGe,ZHANG YueXin,FAN YaPeng,YE WuWei. Characteristics and Cold Tolerance of Upland Cotton Genetic Standard Line TM-1 [J]. Scientia Agricultura Sinica, 2022, 55(8): 1503-1517.
[2] SHEN Qian,ZHANG SiPing,LIU RuiHua,LIU ShaoDong,CHEN Jing,GE ChangWei,MA HuiJuan,ZHAO XinHua,YANG GuoZheng,SONG MeiZhen,PANG ChaoYou. Construction of A Comprehensive Evaluation System and Screening of Cold Tolerance Indicators for Cold Tolerance of Cotton at Seedling Emergence Stage [J]. Scientia Agricultura Sinica, 2022, 55(22): 4342-4355.
[3] PANG HongBo, CHENG Lu, YU MingLan, CHEN Qiang, LI YueYing, WU LongKun, WANG Ze, PAN XiaoWu, ZHENG XiaoMing. Genome-Wide Association Study of Cold Tolerance at the Germination Stage of Rice [J]. Scientia Agricultura Sinica, 2022, 55(21): 4091-4103.
[4] AN JunXia,ZHAO Yu,ZHANG ZhengKun,SHI HaiPeng,JI DongMing,CAO HongYi,DU Qian,LI QiYun. Induction of Cold Tolerance in Rice at the Breeding Stage by Gongzhulingmycin [J]. Scientia Agricultura Sinica, 2020, 53(11): 2195-2206.
[5] PU YuanYuan,ZHAO YuHong,WU JunYan,LIU LiJun,BAI Jing,MA Li,NIU ZaoXia,JIN JiaoJiao,FANG Yan,LI XueCai,SUN WanCang. Comprehensive Assessment on Cold Tolerance of the Strong Winter Brassica napus L. Cultivated in Northern China [J]. Scientia Agricultura Sinica, 2019, 52(19): 3291-3308.
[6] RU JingNa, YU TaiFei, CHEN Jun, CHEN Ming, ZHOU YongBin, MA YouZhi, XU ZhaoShi, MIN DongHong. Response of Wheat Zinc-Finger Transcription Factor TaDi19A to Cold and Its Screening of Interacting Proteins [J]. Scientia Agricultura Sinica, 2017, 50(13): 2411-2422.
[7] LI Na, ZHOU Xiao-rong, PANG Bao-ping. Relationship Between Supercooling Capacity and Low Molecular Sugars and Polyols, and Amino Acids in Eggs of Oedaleus asiaticus [J]. Scientia Agricultura Sinica, 2014, 47(24): 4830-4839.
[8] LIU Hui, LI De-jun, DENG Zhi. Advances in Research of Transcriptional Regulatory Network in Response to Cold Stress in Plants [J]. Scientia Agricultura Sinica, 2014, 47(18): 3523-3533.
[9] ZHU Wen-Ying, LIU Xin-Chun, FANG Wei-Min, GUAN Zhi-Yong, CHEN Su-Mei, JIANG Jia-Fu, CHEN Fa-Di. Genetic Presentation of BC1 Between ‘Zhongshanjingui’ and ‘Zhongshanjingui’ × Ajania przewalskii [J]. Scientia Agricultura Sinica, 2012, 45(18): 3812-3819.
[10] XIA Rui-xiang,XIAO Ning,HONG Yi-huan,ZHANG Chao,SU Yan,ZHANG Xiao-meng,CHEN Jian-min
. QTLs Mapping for Cold Tolerance at Seedling Stage in Dongxiang Wild Rice (Oryza rufipogon Griff.)
 [J]. Scientia Agricultura Sinica, 2010, 43(3): 443-451 .
[11] . Analysis of Cold-Tolerance and Determination of Cold-Tolerance Evaluation Indicators in Chrysanthemum
 [J]. Scientia Agricultura Sinica, 2009, 42(3): 974-981 .
[12] . Study on the Supercooling point and Freezing point of Apricot Flower at different stage [J]. Scientia Agricultura Sinica, 2008, 41(4): 1128-1133 .
[13] ,,,. Cytochemical Localization and Changes in Activity of Plasma Membrane Ca2+-ATPase in Young Grape (Vitis vinifera L. cv. Jingxiu) Plants During Cross Adaptation to Temperature Stresses [J]. Scientia Agricultura Sinica, 2006, 39(8): 1617-1625 .
[14] ,. Molecular Mapping of QTLs for Cold Tolerance at the [J]. Scientia Agricultura Sinica, 2005, 38(02): 217-221 .
Viewed
Full text


Abstract

Cited
  Shared   
  Discussed   
No Suggested Reading articles found!
京ICP备09089781号-30
Copyright 2018 © Editorial office of Scientia Agricultura Sinica
Tel: 86-010-82106279    E-mail: zgnykx@mail.caas.net.cn
Supported by Beijing Magtech Co.Ltd