Scientia Agricultura Sinica ›› 2023, Vol. 56 ›› Issue (24): 4866-4879.doi: 10.3864/j.issn.0578-1752.2023.24.006

• PLANT PROTECTION • Previous Articles     Next Articles

The Effect of Environmental Stress on Respiratory Rate and Expression Level of Mitochondrial Protein-Coding Genes in Cryptolestes ferrugineus

CHEH ErHu(), YUAN GuoQing, SUN ShengYuan, TANG PeiAn()   

  1. College of Food Science and Engineering/Collaborative Innovation Center for Modern Grain Circulation and Safety of Jiangsu Province/Key Laboratory of Grains and Oils Quality Control and Processing of Jiangsu Province, Nanjing University of Finance and Economics, Nanjing 210023
  • Received:2023-08-14 Accepted:2023-09-09 Online:2023-12-16 Published:2023-12-21
  • Contact: TANG PeiAn

Abstract:

【Background】Mitochondria is an important organelle in the organism, which is the primary site for cellular oxygen consumption and the production of the energy substance adenosine triphosphate (ATP), playing a significant role in the organism’s resistance to adversity. The rusty grain beetle (Cryptolestes ferrugineus) is a type of global stored grain pest, possessing extremely strong environmental adaptability.【Objective】The objective of this study is to analyze the respiratory rate of C. ferrugineus and the response of mitochondrial protein-coding genes to different environmental stresses, and to investigate the stress response of mitochondria in the adversity resistance of C. ferrugineus.【Method】Mitochondrial protein-coding genes were identified based on the mitochondrial genome data of C. ferrugineus, and corresponding real-time fluorescence quantitative PCR (RT-qPCR) primers were designed. The toxicity regression equation and LC30 of C. ferrugineus to fumigants (ethyl formate), botanical insecticides (rotenone), and stored grain protectants (avermectin) were determined by using bioassay methods, and these concentrations were used for subsequent drug stress treatment on the test insects. The spatial and temporal expression patterns (different developmental stages and different tissues of larvae) of mitochondrial protein-coding genes in C. ferrugineus were analyzed by using RT-qPCR technology. Finally, the changes in the respiratory rate of C. ferrugineus under various adversity stresses such as high temperatures (35 and 40 ℃), ethyl formate, rotenone, avermectin, and starvation, as well as the expression patterns of mitochondrial protein-coding genes, were studied by using a CO2 detector and RT-qPCR technology, respectively.【Result】Twelve mitochondrial protein-coding genes (excluding nad6) quantitative primers were designed. RT-qPCR results showed that these mitochondrial protein-coding genes had a higher expression level at the 3rd instar larval stage, and mitochondrial genes were specifically highly expressed in the Malpighian tubules of 3rd instar larvae. Moreover, under high-temperature stress, the respiratory rate of C. ferrugineus significantly increased, and the expression levels of mitochondrial protein-coding genes nad2, cytb, and cox2 increased significantly, while nad4, nad4L, cox3, and atp6 showed a significant downregulation trend. Under ethyl formate fumigation stress, the respiratory rate of C. ferrugineus significantly decreased, and all 12 mitochondrial protein-coding genes were significantly downregulated. Among them, the expression levels of nad4L and nad5 were only 3.48% and 1.91% of the control group, respectively. Under rotenone and avermectin stress, the respiratory rate of C. ferrugineus significantly decreased, and the expression levels of mitochondrial protein-coding genes, except for cox2, were significantly downregulated. Under starvation stress, the respiratory rate of C. ferrugineus significantly decreased, and as the stress duration increased, the downregulation of mitochondrial encoded gene expression levels became more pronounced.【Conclusion】The respiratory metabolism rate and mitochondrial protein-coding gene expressions of C. ferrugineus changed significantly under different environmental stresses, indicating that the mitochondria plays an important role in the adaption to high temperature, pesticides, and starvation stress in C. ferrugineus.

Key words: Cryptolestes ferrugineus, environmental stress, respiratory rate, mitochondrial protein-coding gene

Table 1

Primer sequences used in this study"

引物名称
Primer name
引物序列
Primer sequence (5′ to 3′)
产物长度
Product length (bp)
决定系数
Determination coefficient (R2)
扩增效率
Amplification efficiency (%)
nad1-F TAATGGGTTAGTTCAGCCTT 296 1.000 91.464
nad1-R AAATAGTTTGAGCAACAGCC
nad2-F TAGTATATGGCTAGGACTGGA 92 1.000 88.099
nad2-R TTAAGGCTGATTCTGATGGA
nad3-F TTGACCCTAAATCTACCGCA 219 0.993 102.414
nad3-R TGGCTCAGTTTAAGGCTCCT
nad4-F TGCTTATTCTTCTGTTGCTC 166 0.991 102.742
nad4-R ACTTCGTCTATGAGTTCGTT
nad4L-F TTAACTATAAGTGTATGTGAGGG 63 0.996 91.195
nad4L-R ATAATATAATCATTTCCATGC
nad5-F GCCCTTTCAACTTTAAGTCA 89 0.995 106.110
nad5-R TAAAGCCTTAAAGAGGGCAT
cytb-F GAGGTGCCACAGTTATTAC 109 0.992 102.519
cytb-R CGAGTTAATGTTGCGTTATC
cox1-F TGCTCATGGAGGATCTTCAG 122 0.994 102.676
cox1-R TTATACCTTGGGGCCGTATA
cox2-F CGTTCGTCCAATAATTGTTG 128 0.998 93.275
cox2-R AAGTCCTTCCGATTCCAG
cox3-F CGCCGTTTACTATTGCTGAT 153 0.993 103.234
cox3-R ACCCAAAATGGTGAGTTCTT
atp6-F ATATTAGCCCATTTAGTCCCACA 115 0.998 93.255
atp6-R CAGATAGCCGGACAGCCAAA
atp8-F TTCCTCAAATAGCCCCTTTAAGT 50 0.997 97.458
atp8-R AGTAAAATAGAAGAAAAGAGTTAAT
RPS13-F ATCCGTAAGCATTTGGAACG 162 0.997 91.571
RPS13-R AGCCACTAAGGCTGAAGCTG
EF1α-F CCAGGCATGGTAGTGACCTT 184 0.999 96.033
EF1α-R TTGGAGGGTTGTTTTTGGAG

Table 2

The sensitivity of C. ferrugineus to different insecticides"

杀虫剂Insecticide 回归方程Regression equation (y=) LC30 (95%置信区间95% CI) 决定系数Determination coefficient (R2)
甲酸乙酯Ethyl formate -3.665+3.409x 8.3 μL·L-1 (6.2-10.1) 0.953
鱼藤酮Rotenone -7.903+2.285x 1696.7 mg·L-1 (1176.7-2138.5) 0.986
阿维菌素Avermectin -2.007+3.640x 2.6 mg·L-1 (1.5-3.1) 0.930

Fig. 1

The expression patterns of mitochondrial protein-coding genes at different developmental stages of C. ferrugineus"

Fig. 2

The expression patterns of mitochondrial protein-coding genes in different larval tissues of C. ferrugineus"

Fig. 3

The changes of respiratory rate and expression pattern of mitochondrial protein-coding genes under high temperature stress in C. ferrugineus"

Fig. 4

The changes of respiratory rate and expression pattern of mitochondrial protein-coding genes under ethyl formate stress in C. ferrugineus"

Fig. 5

The changes of respiratory rate and expression pattern of mitochondrial protein-coding genes under rotenone and avermectin stress in C. ferrugineus"

Fig. 6

The changes of respiratory rate and expression pattern of mitochondrial protein-coding genes under starvation stress in C. ferrugineus"

[1]
JIAN F, JAYAS D S, WHITE N D G. Optimal environmental search and scattered orientations during movement of adult rusty grain beetles, Cryptolestes ferrugineus (Stephens), in grain bulks-suggested movement and distribution patterns. Journal of Stored Products Research, 2009, 45(3): 177-183.

doi: 10.1016/j.jspr.2008.11.003
[2]
FLINN P W, HAGSTRUM D W. Distribution of Cryptolestes ferrugineus (Coleoptera: Cucujidae) in response to temperature gradients in stored wheat. Journal of Stored Products Research, 1998, 34(2/3): 107-112.

doi: 10.1016/S0022-474X(98)00002-2
[3]
JARMUSZKIEWICZ W, DOMINIAK K, GALGANSKI L, GALGANSKA H, KICINSKA A, MAJERCZAK J, ZOLADZ J A. Lung mitochondria adaptation to endurance training in rats. Free Radical Biology and Medicine, 2020, 161: 163-174.

doi: 10.1016/j.freeradbiomed.2020.10.011 pmid: 33075501
[4]
YANG Y X, XU S X, XU J X, GUO Y, YANG G. Adaptive evolution of mitochondrial energy metabolism genes associated with increased energy demand in flying insects. PLoS ONE, 2014, 9(6): e99120.

doi: 10.1371/journal.pone.0099120
[5]
ZHANG Q L, YANG X Z, ZHANG L, FENG R Q, ZHU Q H, CHEN J Y, YUAN M L. Adaptive evidence of mitochondrial genomes in Dolycoris baccarum (Hemiptera: Pentatomidae) to divergent altitude environments. Mitochondrial DNA Part A, DNA Mapping Sequencing and Analysis, 2019, 30(1): 9-15.
[6]
LI X D, JIANG G F, YAN L Y, LI R, MU Y, DENG W A. Positive selection drove the adaptation of mitochondrial genes to the demands of flight and high-altitude environments in grasshoppers. Frontiers in Genetics, 2018, 9: 605.

doi: 10.3389/fgene.2018.00605
[7]
MA C S, MA G, PINCEBOURDE S. Survive a warming climate: Insect responses to extreme high temperatures. Annual Review of Entomology, 2021, 66: 163-184.

doi: 10.1146/ento.2021.66.issue-1
[8]
KANG D, SHIM S K. Early heat exposure effect on the heat shock proteins in broilers under acute heat stress. Poultry Science, 2021, 100(3): 100964.

doi: 10.1016/j.psj.2020.12.061
[9]
FU D, LIU J, PAN Y N, ZHU J Y, XIAO F, LIU M, XIAO R. Three heat shock protein genes and antioxidant enzymes protect Pardosa pseudoannulata (Araneae: Lycosidae) from high temperature stress. International Journal of Molecular Sciences, 2022, 23(21): 12821.

doi: 10.3390/ijms232112821
[10]
YANG T, LI T, FENG X C, LI M, LIU S K, LIU N N. Multiple cytochrome P450 genes: Conferring high levels of permethrin resistance in mosquitoes, Culex quinquefasciatus. Scientific Reports, 2021, 11(1): 9041.

doi: 10.1038/s41598-021-88121-x
[11]
ZHANG J Q, MA W, YIN F, PARK Y, ZHU K Y, ZHANG X Y, QIN X M, LI D Q. Evaluations of two glutathione S-transferase epsilon genes for their contributions to metabolism of three selected insecticides in Locusta migratoria. Pesticide Biochemistry and Physiology, 2022, 183: 105084.

doi: 10.1016/j.pestbp.2022.105084
[12]
ZHAO R Z, JIANG S, ZHANG L, YU Z B. Mitochondrial electron transport chain, ROS generation and uncoupling. International Journal of Molecular Medicine, 2019, 44(1): 3-15.
[13]
CAITO S W, ASCHNER M. Mitochondrial redox dysfunction and environmental exposures. Antioxidants and Redox Signaling, 2015, 23(6): 578-595.
[14]
王磊. 桔小实蝇线粒体编码基因转录表达及atp6cox2的抗逆性功能[D]. 重庆: 西南大学, 2022.
WANG L. The expression profiles of mitochondrial genes and the functions of atp6 and cox2 underlying environmental stresses in the oriental fruit fly, Bactrocera dorsalis (Hendel)[D]. Chongqing: Southwest University, 2022. (in Chinese)
[15]
SIGNES A, FERNANDEZ-VIZARRA E. Assembly of mammalian oxidative phosphorylation complexes I-V and super complexes. Essays in Biochemistry, 2018, 62(3): 255-270.

doi: 10.1042/EBC20170098
[16]
高峰, 苏建伟, 戈峰, 吴刚, 刘向辉. 温度对龟纹瓢虫呼吸代谢的影响. 湖北农业科学, 2007, 46(4): 562-564.
GAO F, SU J W, GE F, WU G, LIU X H. Effect of temperature on the respiration and metabolism of ladybeetles, Propylaea japonica, Hubei Agricultural Sciences, 2007, 46(4): 562-564. (in Chinese)
[17]
BOWLER K, KASHMEERY A M S. Effects of in vivo heating of blowflies on the oxidative capacity of flight muscle sarcosomes: A differential effect on glycerol 3-phosphate and pyruvate plus proline respiration. Journal of Thermal Biology, 1981, 6(1): 11-18.

doi: 10.1016/0306-4565(81)90036-X
[18]
SUN J T, DUAN X Z, HOFFMANN A A, LIU Y, GARVIN M R, CHEN L, HU G, ZHOU J C, HUANG H J, XUE X F, HONG X Y. Mitochondrial variation in small brown planthoppers linked to multiple traits and probably reflecting a complex evolutionary trajectory. Molecular Ecology, 2019, 28(14): 3306-3323.

doi: 10.1111/mec.2019.28.issue-14
[19]
郎宁. 辣根素熏蒸处理下三色书虱线粒体相关基因表达研究[D]. 重庆: 西南大学, 2019.
LANG N. Expression of mitochondrial associated genes in Liposcelis tricolor under allyl isothiocyanate fumigation[D]. Chongqing: Southwest University, 2019. (in Chinese)
[20]
BALABAN R S, NEMOTO S, FINKEL T. Mitochondria, oxidants, and aging. Cell, 2005, 120(4): 483-495.

doi: 10.1016/j.cell.2005.02.001 pmid: 15734681
[21]
张同梅. 中国常用农药对蛋白酶体和线粒体的影响[D]. 长沙: 中南大学, 2011.
ZHANG T M. Effects of pesticides commonly used in China on the proteasome and mitochondria[D]. Changsha: Central South University, 2011. (in Chinese)
[22]
BORRERO LANDAZABAL M A, CARRENO OTERO A L, KOUZNETSOV V V, DUQUE LUNA J E, MENDEZ-SANCHEZ S C. Alterations of mitochondrial electron transport chain and oxidative stress induced by alkaloid-like alpha-aminonitriles on Aedes aegypti larvae. Pesticide Biochemistry and Physiology, 2018, 144: 64-70.

doi: 10.1016/j.pestbp.2017.11.006
[23]
ZHANG C, MA Z, ZHANG X, WU H. Transcriptomic alterations in Sitophilus zeamais in response to allyl isothiocyanate fumigation. Pesticide Biochemistry and Physiology, 2017, 137: 62-70.

doi: 10.1016/j.pestbp.2016.10.001
[24]
ZHANG C, WU H, ZHAO Y, MA Z Q, ZHANG X. Comparative studies on mitochondrial electron transport chain complexes of Sitophilus zeamais treated with allyl isothiocyanate and calcium phosphide. Pesticide Biochemistry and Physiology, 2016, 126: 70-75.

doi: 10.1016/j.pestbp.2015.07.009
[25]
LI X C, PERIS D, HITTINGER C T, SIA E A, FAY J C. Mitochondria-encoded genes contribute to evolution of heat and cold tolerance in yeast. Science Advances, 2019, 5(1): eaav1848.
[26]
AW W C, GARVIN M R, MELVIN R G, BALLARD J W O. Sex-specific influences of mtDNA mitotype and diet on mitochondrial functions and physiological traits in Drosophila melanogaster. PLoS ONE, 2017, 12(11): e0187554.

doi: 10.1371/journal.pone.0187554
[27]
LLOPART A, HERRIG D, BRUD E, STECKLEIN Z. Sequential adaptive introgression of the mitochondrial genome in Drosophila yakuba and Drosophila santomea. Molecular Ecology, 2014, 23(5): 1124-1136.

doi: 10.1111/mec.2014.23.issue-5
[28]
TANG P A, DUAN J Y, WU H J, JU X R, YUAN M L. Reference gene selection to determine differences in mitochondrial gene expressions in phosphine-susceptible and phosphine-resistant strains of Cryptolestes ferrugineus, using qRT-PCR. Scientific Reports, 2017, 7: 7047.

doi: 10.1038/s41598-017-07430-2
[29]
LIVAK K J, SCHMITTGEN T D. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods, 2001, 25(4): 402-408.

doi: 10.1006/meth.2001.1262
[30]
ZHAO L, PRIDGEON J W, BECNEL J J, CLARK G G, LINTHICUM K J. Mitochondrial gene cytochrome b developmental and environmental expression in Aedes aegypti (Diptera: Culicidae). Journal of Medical Entomology, 2009, 46(6): 1361-1369.

doi: 10.1603/033.046.0615
[31]
VAFOPOULOU X. Ecdysteroid receptor (EcR) is associated with microtubules and with mitochondria in the cytoplasm of prothoracic gland cells of Rhodnius prolixus (Hemiptera). Archives of Insect Biochemistry and Physiology, 2009, 72(4): 249-262.

doi: 10.1002/arch.v72:4
[32]
FARINA P, BEDINI S, CONTI B. Multiple functions of Malpighian tubules in insects: A review. Insects, 2022, 13(11): 1001.

doi: 10.3390/insects13111001
[33]
郭娜, 高书晶, 王宁, 韩海斌, 徐林波, 董瑞文, 娜仁满都呼, 娜布其亚. 温度对亚洲小车蝗成虫体内呼吸代谢相关酶和抗氧化酶活性的影响. 昆虫学报, 2020, 63(11): 1358-1365.
GUO N, GAO S J, WANG N, HAN H B, XU L B, DONG R W, NARENMANDUHU , NABUQIYA . Effects of temperature on the activities of respiratory metabolism-related and antioxidant enzymes in adults of Oedaleus asiaticus (Orthoptera: Acridoidea). Acta Entomologica Sinica, 2020, 63(11): 1358-1365. (in Chinese)
[34]
陈菊红, 崔娟, 张金平, 毕锐, 高宇, 徐伟, 史树森. 温度胁迫对点蜂缘蝽成虫呼吸代谢关键酶活性的影响. 昆虫学报, 2018, 61(9): 1003-1009.

doi: 10.16380/j.kcxb.2018.09.001
CHEN J H, CUI J, ZHANG J P, BI R, GAO Y, XU W, SHI S S. Effects of temperature on the activities of key enzymes related to respiratory metabolism in Riptortus pedestris (Hemiptera: Coreidae) adults. Acta Entomologica Sinica, 2018, 61(9): 1003-1009. (in Chinese)
[35]
钱雪, 王月莹, 谢欢欢, 窦洁, 李占武, JASHENKO R, 季荣. 温度对西伯利亚蝗呼吸代谢关键酶活性的影响. 昆虫学报, 2017, 60(5): 499-504.

doi: 10.16380/j.kcxb.2017.05.001
QIAN X, WANG Y Y, XIE H H, DOU J, LI Z W, JASHENKO R, JI R. Effects of temperature on the activities of key enzymes related to respiratory metabolism in adults of Gomphocerus sibiricus (Orthoptera: Acrididae). Acta Entomologica Sinica, 2017, 60(5): 499-504. (in Chinese)

doi: 10.16380/j.kcxb.2017.05.001
[36]
WANG H W, ZHANG Y, TAN P P, JIA L S, CHEN Y, ZHOU B H. Mitochondrial respiratory chain dysfunction mediated by ROS is a primary point of fluoride-induced damage in Hepa1-6 cells. Environmental Pollution, 2019, 255(3): 113359.

doi: 10.1016/j.envpol.2019.113359
[37]
NAYAK M K, HOLLOWAY J C, EMERY R N, PAVIC H, BARTLET J, COLLINS P J. Strong resistance to phosphine in the rusty grain beetle, Cryptolestes ferrugineus (Stephens) (Coleoptera: Laemophloeidae): Its characterisation, a rapid assay for diagnosis and its distribution in Australia. Pest Management Science, 2013, 69(1): 48-53.

doi: 10.1002/ps.2013.69.issue-1
[38]
AGRAFIOTI P, ATHANASSIOU C G, NAYAK M K. Detection of phosphine resistance in major stored-product insects in Greece and evaluation of a field resistance test kit. Journal of Stored Products Research, 2019, 82: 40-47.

doi: 10.1016/j.jspr.2019.02.004
[39]
陈二虎, 沈丹蓉, 杜文蔚, 孟宏杰, 唐培安. 表皮蛋白基因参与锈赤扁谷盗磷化氢抗性形成. 中国农业科学, 2023, 56(9): 1696-1707. doi: 10.3864/j.issn.0578-1752.2023.09.007.
CHEN E H, SHEN D R, DU W W, MENG H J, TANG P A. Cuticle protein genes are involved in phosphine resistance of Cryptolestes ferrugineus. Scientia Agricultura Sinica, 2023, 56(9): 1696-1707. doi: 10.3864/j.issn.0578-1752.2023.09.007. (in Chinese)
[40]
陈艳. 基于呼吸速率的锈赤扁谷盗监测模型建立及呼吸调控机理研究[D]. 南京: 南京财经大学, 2022.
CHEN Y. Establishment of a monitoring model for the Cryptolestes ferrugineus based on respiration rate and research on the mechanism of respiration regulation[D]. Nanjing: Nanjing University of Finance and Economics, 2022. (in Chinese)
[41]
段锦艳. 基于线粒体基因的锈赤扁谷盗磷化氢抗性机理研究[D]. 南京: 南京财经大学, 2017.
DUAN J Y. Study on the mechanisms of phosphine resistance in Cryptolestes ferrugineus (Stephens) based on mitochondrial gene[D]. Nanjing: Nanjing University of Finance and Economics, 2017. (in Chinese)
[42]
WANG H, HUO M H, JIN Y Z, WANG Y, WANG X W, YU W H, JIANG X W. Rotenone induces hepatotoxicity in rats by activating the mitochondrial pathway of apoptosis. Toxicology Mechanisms and Methods, 2022, 32(7): 510-517.

doi: 10.1080/15376516.2022.2049940
[43]
HEO G, SUN M H, JIANG W J, LI X H, LEE S H, GUO J, ZHOU D J, CUI X S. Rotenone causes mitochondrial dysfunction and prevents maturation in porcine oocytes. PLoS ONE, 2022, 17(11): e0277477.

doi: 10.1371/journal.pone.0277477
[44]
BAI S H, OGBOURNE S. Eco-toxicological effects of the avermectin family with a focus on abamectin and ivermectin. Chemosphere, 2016, 154: 204-214.

doi: S0045-6535(16)30437-4 pmid: 27058912
[45]
SOUDERS C L, RUSHIN A, SANCHEZ C L, TOTH D, ADAMOVSKY O, MARTYNIUK C J. Mitochondrial and transcriptome responses in rat dopaminergic neuronal cells following exposure to the insecticide fipronil. Neurotoxicology, 2021, 85: 173-185.

doi: 10.1016/j.neuro.2021.05.011
[46]
PEDRA-REZENDE Y, FERNANDES M C, MESQUITA- RODRIGUES C, STIEBLER R, BOMBAÇA A C S, PINHO N, CUERVO P, DE CASTRO S L, MENNA-BARRETO R F S. Starvation and pH stress conditions induced mitochondrial dysfunction, ROS production and autophagy in Trypanosoma cruzi epimastigotes. Biochimica et Biophysica Acta-Molecular Basis of Disease, 2021, 1867(2): 166028.
[47]
HIBSHMAN J D, LEUTHNER T C, SHOBEN C, MELLO D F, SHERWOOD D R, MEYER J N, BAUGH L R. Nonselective autophagy reduces mitochondrial content during starvation in Caenorhabditis elegans. American Journal of Physiology. Cell Physiology, 2018, 315(6): 781-792.
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