Please wait a minute...
Journal of Integrative Agriculture
Advanced Online Publication | Current Issue | Archive | Adv Search
The TRPA1 channel regulates temperature preference in the green peach aphid Myzus persicae

Lulu Yang1, 2, Tianyu Huang1, Jie Shen2, Bing Wang1#, Guirong Wang1, 3#

1 State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China
2 Department of Entomology and MOA Key Laboratory for Monitory and Green Control of Crop Pest, China Agricultural University, Beijing 100193, China
3 Shenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518120, China

 Highlights 

l Two variants were identified, MperTRPA1(A) and MperTRPA1(B), and they are abundantly expressed in chemosensory tissues.

l MperTRPA1 is activated by increasing temperatures from 20 to 45°C, and MperTRPA1(B) exhibits greater thermosensitivity than MperTRPA1(A).

l MperTRPA1 is involved in the temperature preference of Myzus persicae.

Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
摘要  

瞬时受体电位(transient receptor potentialTRP)通道是一类与昆虫热感应密切相关的离子通道蛋白。它们参与识别环境温度,在昆虫的生存繁衍过程中发挥着重要作用。本研究鉴定并克隆桃蚜Myzus persicae中TRPA亚家族TRPA1基因两个剪切型MperTRPA1(A)MperTRPA1(B),并通过实时荧光定量PCR技术分析了它们在桃蚜不同组织中的表达模式。随后,在爪蟾卵母细胞系统中表达了MperTRPA1基因的两个剪切型,并利用双电极电压钳技术它们的体外功能进行了深入研究。此外,通过RNA干扰技术结合行为选择试验评估桃蚜对温度梯度反应的变化,进一步明确MperTRPA1基因在桃蚜温度适应机制中的作用。研究结果显示MperTRPA1基因在桃蚜成虫多种组织中均有广泛表达。具体而言,MperTRPA1(A)在口器中表达量较高MperTRPA1(B)主要在触角中表达。功能研究进一步揭示MperTRPA1两个剪切型均能被20℃至45℃的温度范围所激活且表现出非脱敏特性。深入研究发现,与MperTRPA1(A)相比,MperTRPA1(B)具有更高的电流值和热敏感性(以Q10系数值衡量)。在行为实验中,与野生型和dsGFP处理的桃蚜相比,MperTRPA1基因表达水平敲低的桃蚜对最适温度区域的偏好明显减弱,倾向于分布在更高的温度区域。综上所述,研究结果阐明了热传导受体MperTRPA1在介导桃蚜适应性温度感知过程中的分子机制。



Abstract  

Transient receptor potential (TRP) channels are a class of ion channel proteins that are closely related to thermosensation in insects. They are involved in detecting the ambient temperature and play vital rolein insect survival and reproduction. In this study, we identified and cloned two variants of the TRPA subfamily gene in Myzus persicae, MperTRPA1(A) and MperTRPA1(B), and analyzed their tissue expression by real-time quantitative PCR. Subsequently, these two variants of MperTRPA1 were expressed in the Xenopus oocyte system, and their functions were investigated using the two-electrode voltage clamp technique. The role of the MperTRPA1 gene in temperature adaptation of M. persicae was further determined by RNA interference and behavioral choice assay to evaluate responses to temperature gradients. The results showed that the MperTRPA1 gene is widely expressed in tissues of M. persicae, with MperTRPA1(A) highly expressed in the mouthparts and MperTRPA1(B) mainly expressed in the antennae. The functional characterization results showed that both variants of MperTRPA1 could be activated and were not desensitizewhen the temperature increased from 20 to 45°C. The current value and thermal sensitivity (coefficient Q10 value) of MperTRPA1(B) were significantly higher than those of MperTRPA1(A). When the MperTRPA1 gene was knocked down, the behavioral preference of M. persicae for the optimal temperature was reduced and tended to be at a higher temperature, showing a shift in the temperature adaptation range compared to both the wild type and dsGFP-treated M. persicae. In summary, our results elucidated the molecular mechanism of adaptive temperature perception in M. persicae mediated by the thermal sensor MperTRPA1.

Keywords:  TRP channel       TRPA1       Myzus persicae       thermosensation       thermal preference  
Online: 24 February 2025  
Fund: 

This study was funded by the Natural Science Foundation of National Natural Science Foundation of China (31872039 and 32472553), Major special projects for green pest control (110202201017(LS-01)), a grant from the Shenzhen Science and Technology Program (KQTD20180411143628272) and the Agricultural Science and Technology Innovation Program. 

About author:  Lulu Yang, E-mail: 82101219117@caas.cn; #Correspondence Bing Wang, E-mail: wangbing02@caas.cn; Guirong Wang, E-mail: wangguirong@caas.cn

Cite this article: 

Lulu Yang, Tianyu Huang, Jie Shen, Bing Wang, Guirong Wang. 2025. The TRPA1 channel regulates temperature preference in the green peach aphid Myzus persicae. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2025.02.046

Ahn J J, Cho J R, Kim J H, Seo B Y. 2020. Thermal effects on the population parameters and growth of Acyrthosiphon pisum (Harris) (Hemiptera: Aphididae). Insects, 11, 481.

Baral S, Thapa R B, Jha R K, Joshi S L, Aryal S. 2022. Effects of temperature on development of Myzus persicae (Sulzer). Indian Journal of Entomology, 84, 761-765.

Bass C, Puinean A M, Zimmer C T, Denholm I, Field L M, Foster S P, Gutbrod O, Nauen R, Slater R, Williamson M S. 2014. The evolution of insecticide resistance in the peach potato aphid, Myzus persicaeInsect Biochemistry and Molecular Biology51, 41-51.

Bayhan E, Ölmez-Bayhan S, Ulusoy M R, Chi H. 2006. Effect of temperature on development, mortality, fecundity, and reproduction of Aphis rumicis L. (Homoptera: Aphididae) on broadleaf dock (Rumex obtusifolius) and Swiss chard (Beta vulgaris vulgaris var. cida). Journal of Pest Science, 79, 57-61.

Blanchard S, Lognay G, Verheggen F, Detrain C. 2019. Today and tomorrow: Impact of climate change on aphid biology and potential consequences on their mutualism with ants. Physiological Entomology, 44, 77-86.

Chen S C, Tang X, Goda T, Umezaki Y, Riley A C, Sekiguchi M, Yoshii T, Hamada F N. 2022. Dorsal clock networks drive temperature preference rhythms in Drosophila. Cell Reports, 39, 110668.

Cordero-Morales J F, Gracheva E O, Julius D. 2011. Cytoplasmic ankyrin repeats of transient receptor potential A1 (TRPA1) dictate sensitivity to thermal and chemical stimuli. Proceedings of the National Academy of Sciences of the United States of America108, E1184-E1191.

Davis J A, Radcliffe E B, Ragsdale D W. 2006. Effects of high and fluctuating temperatures on Myzus persicae (Hemiptera: Aphididae). Environmental Entomology, 35, 1461-1468.

Fu T, Hull J J, Yang T, Wang G. 2016. Identification and functional characterization of four transient receptor potential ankyrin 1 variants in Apolygus lucorum (Meyer-Dür). Insect Molecular Biology25, 370-384.

Fowler M A, Montell C. 2013. Drosophila TRP channels and animal behavior. Life Sciences, 92, 394-403.

Gracheva E O, Ingolia N T, Kelly Y M, Cordero-Morales J F, Hollopeter G, Chesler A T, Sánchez E E, Perez J C, Weissman J S, Julius D. 2010. Molecular basis of infrared detection by snakes. Nature, 464, 1006-1011.

Gu P, Gong J, Shang Y, Wang F, Ruppell K T, Ma Z, Sheehan A E, Freeman M R, Xiang Y. 2019. Polymodal nociception in Drosophila requires alternative splicing of TrpA1. Current Biology29, 3961-3973.

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. Nature454, 217-220.

Huang T, Zhang R, Yang L, Cao S, Francis F, Wang B, Wang G. 2022. Identification and functional characterization of ApisOr23 in pea aphid Acyrthosiphon pisumJournal of Integrative Agriculture, 21, 1414-1423.

Hubhachen Z, Madden R D, Dillwith J W. 2018. Influence of rearing temperature on triacylglycerol storage in the pea aphid, Acyrthosiphon pisum. Archives of Insect Biochemistry and Physiology99, e21495.

Hullé M, d’Acier A C, Bankhead-Dronnet S, Harrington R. 2010. Aphids in the face of global changes. Comptes Rendus Biologies, 333, 497-503.

Jabba S, Goyal R, Sosa-Pagán J, Moldenhauer H, Wu J, Kalmeta B, Bandell M, Latorre R, Patapoutian A, Grandl J. 2014. Directionality of temperature activation in mouse TRPA1 ion channel can be inverted by single-point mutations in ankyrin repeat six. Neuron82, 1017-1031.

Kang K, Panzano V C, Chang E C, Ni L, Dainis A M, Jenkins A M, Regna K, Muskavitch M A, Garrity P A. 2012. Modulation of TRPA1 thermal sensitivity enables sensory discrimination in Drosophila. Nature, 481, 76-80.

Kang K, Pulver S R, Panzano V C, Chang E C, Griffith L C, Theobald D L, Garrity P A. 2010. Analysis of Drosophila TRPA1 reveals an ancient origin for human chemical nociception. Nature, 464, 597-600.

Kim H G, Margolies D, Park Y. 2015. The roles of thermal transient receptor potential channels in thermotactic behavior and in thermal acclimation in the red flour beetle, Tribolium castaneum. Journal of Insect Physiology, 76, 47-55.

Kwon Y, Shim H S, Wang X, Montell C. 2008. Control of thermotactic behavior via coupling of a trp channel to a phospholipase c signaling cascade. Nature Neuroscience, 11, 871-873.

Laursen W J, Anderson E O, Hoffstaetter L J, Bagriantsev S N, Gracheva E O. 2015. Species-specific temperature sensitivity of TRPA1. Temperature, 2, 214-226.

Lee Y, Lee Y, Lee J, Bang S, Hyun S, Kang J, Hong S T, Bae E, Kaang B K, Kim J. 2005. Pyrexia is a new thermal transient receptor potential channel endowing tolerance to high temperatures in Drosophila melanogaster. Nature Genetics37, 305-310.

Letunic I, Khedkar S, Bork P. 2021. SMART: Recent updates, new developments and status in 2020. Nucleic Acids Research, 49, D458-D460.

Liu L, Li Y, Wang R, Yin C, Dong Q, Hing H, Kim C, Welsh M J. 2007. Drosophila hygrosensation requires the TRP channels water witch and nanchung. Nature, 450, 294-298.

Liu J, Wang C, Desneux N, Lu Y. 2021. Impact of temperature on survival rate, fecundity, and feeding behavior of two aphids, Aphis gossypii and Acyrthosiphon gossypii, when reared on cotton. Insects, 12, 565.

Ma G, Bai C M, Wang X J, Majeed M Z, Ma C S. 2018. Behavioural thermoregulation alters microhabitat utilization and demographic rates in ectothermic invertebrates. Animal Behaviour, 142, 49-57.

Ma G, Ma C S. 2012. Climate warming may increase aphids' dropping probabilities in response to high temperatures. Journal of Insect Physiology, 58, 1456-1462.

Ma C S, Hau B, Poehling H M. 2004. The effect of heat stress on the survival of the rose grain aphid, Metopolophium dirhodum (Hemiptera: Aphididae). European Journal of Entomology, 101, 327-331.

Melo N, Capek M, Arenas O M, Afify A, Yilmaz A, Potter C J, Laminette P J, Para A, Gallio M, Stensmyr M C. 2021. The irritant receptor TRPA1 mediates the mosquito repellent effect of catnip. Current Biology, 31, 1988-1994.

Michaud J P, Bain C, Abdel-Wahab A. 2018. Mortality of sugarcane aphid, Melanaphis sacchari (Zehntner, Hemiptera: Aphididae), at low temperatures. Journal of Economic Entomology111, 2496-2498.

Montell C. 2008. TRP channels: It's not the heat, it's the humidity. Current Biology18, R123-R126.

Montell C. 2021. Drosophila sensory receptors-a set of molecular Swiss Army Knives. Genetics, 21, 1-34.

Neely G G, Keene A C, Duchek P, Chang E C, Wang Q P, Aksoy Y A, Rosenzweig M, Costigan M, Woolf C J, Garrity P A, Penninger J M. 2011. TrpA1 regulates thermal nociception in Drosophila. PLoS ONE, 6, e24343.

Rosenzweig M, Kang K, Garrity P A. 2008. Distinct TRP channels are required for warm and cool avoidance in Drosophila melanogaster. Proceedings of the National Academy of Sciences of the United States of America105, 14668-14673.

Pan M Z, Shen R C, Fu Z X, Lu Z Z, Ma B B, Liu T X. 2024. High-temperature responses of Myzus persicae and its parasitoid Aphidius gifuensis in relation to heat level, duration and developmental stage. Pest Management Science, 80, 4628-4636.

Saeidi F, Mikani A, Moharramipour S. 2021. Thermal tolerance variations and physiological adjustments in a winter active and a summer active aphid species. Journal of Thermal Biology, 98, 102950.

Sato A, Sokabe T, Kashio M, Yasukochi Y, Tominaga M, Shiomi K. 2014. Embryonic thermosensitive TRPA1 determines transgenerational diapause phenotype of the silkworm, Bombyx mori. Proceedings of the National Academy of Sciences of the United States of America111, E1249-E1255.

Skendžić S, Zovko M, Ivkovi I P, Lei V, Lemi D. 2021. The impact of climate change on agricultural insect pests. Insects, 12, 440.

Soh B S B, Kekeunou S, Nanga N S, Dongmo M, Hanna R. 2018. Effect of temperature on the biological parameters of the cabbage aphid Brevicoryne brassicae. Ecology and Evolution, 8, 11819-11832.

Sokabe T, Tominaga M. 2009. A temperature-sensitive TRP ion channel, Painless, functions as a noxious heat sensor in fruit flies. Communicative and Integrative Biology2, 170-173.

Sokabe T, Tsujiuchi S, Kadowaki T, Tominaga M. 2008. Drosophila painless is a Ca2+-requiring channel activated by noxious heat. Journal of Neuroscience28, 9929-9938.

Sun J, Tan X, Li Q, Francis F, Chen J. 2022. Effects of different temperatures on the development and reproduction of Sitobion miscanthi from six different regions in China. Frontiers in Ecology and Evolution, 10, 794495.

Szentgyörgyi H, Czekońska K, Tofilski A. 2018. Honey bees are larger and live longer after developing at low temperature. Journal of Thermal Biology78, 219-226.

Tamura K, Stecher G, Kumar S. 2021. MEGA11: Molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution, 38, 3022-3027.

Taylor M, Hayashida R, Hoback W W, Armstrong J S. 2023. Effects of temperature and host plant on hedgehog grain aphid, Sipha maydis demographics. Insects, 14, 862.

Tracey W D, Wilson R I, Laurent G, Benzer S. 2003. Painless, a Drosophila gene essential for nociception. Cell, 113, 261-273.

Wang B, Dong W, Li H, D'Onofrio C, Bai P, Chen R, Yang L, Wu J, Wang X, Wang B. 2022a. Molecular basis of (E)-beta-farnesene-mediated aphid location in the predator Eupeodes corollae. Current Biology, 32, 951-962.

Wang B, Huang T, Yao Y, Francis F, Yan C, Wang G, Wang B. 2022b. A conserved odorant receptor identified from antennal transcriptome of Megoura crassicauda that specifically responds to cis-jasmone. Journal of Integrative Agriculture, 21, 2042-2054.

Wang G, Qiu Y T, Lu T, Kwon H W, Pitts R J, Van Loon J J, Takken W, Zwiebel L J. 2009. Anopheles gambiae TRPA1 is a heat-activated channel expressed in thermosensitive sensilla of female antennae. European Journal of Neuroscience30, 967-974.

Wang X, Li Y, Wei H, Yang Z, Luo R, Gao Y, Zhang W, Liu X, Sun L. 2023. Molecular architecture and gating mechanisms of the Drosophila TRPA1 channel. Cell Discovery, 9, 36.

Wang Y, Yan J, Sun J, Shi W, Harwood J D, Monticelli L S, Chen J. 2021. Effects of field simulated warming on feeding behavior of Sitobion avenae (Fabricius) and host defense systems. Entomologia Generalis, 41, 567–578.

Weber G. 1985. Genetic variability in host plant adaptation of the green peach aphid, Myzus persicae. Entomologia Experimentalis et Applicata, 38, 49-56.

Webster C G, Pichon E, Munster van M, Monsion B, Deshoux M, Gargani D, Calevro F, Jimenez J, Moreno A, Krenz B, Thompson J R, Perry K L, Fereres A, Blanc S, Uzest M, 2018. Identification of plant virus receptor candidates in the stylets of their aphid vectors. Journal of Virology92, e00432-18.

Wei J J, Fu T, Yang T, Liu Y, Wang G R. 2015. A TRPA1 channel that senses thermal stimulus and irritating chemicals in Helicoverpa armigera. Insect Molecular Biology24, 412-421.

Wu Y, Li J, Liu H, Qiao G, Huang X. 2020. Investigating the impact of climate warming on phenology of aphid pests in china using long-term historical data. Insects, 11, 167.

Zhang R, Wang B, Grossi G, Falabella P, Liu Y, Yan S, Lu J, Xi J, Wang G. 2017. Molecular basis of alarm pheromone detection in aphids. Current Biology, 27, 55-61.

Zhang Y, Liu H, Cao S, Li B, Liu Y, Wang G. 2023. Identification of transient receptor potential channel genes and functional characterization of TRPA1 in Spodoptera frugiperda. Journal of Integrative Agriculture23, 1994-2005.

Zheng Y, Hu Y, Yan S, Zhou H, Song D, Yin M, Shen J. 2019. A polymer/detergent formulation improves dsRNA penetration through the body wall and RNAi-induced mortality in the soybean aphid Aphis glycines. Pest Management Science75, 1993-1999.

Zhong L, Bellemer A, Yan H, Ken H, Jessica R, Hwang R Y, Pitt G S, Tracey W D. 2012. Thermosensory and nonthermosensory isoforms of Drosophila melanogaster TRPA1 reveal heat-sensor domains of a thermoTRP Channel. Cell Reports, 1, 43-55.

Zhou X, Harrington R, Woiwod I P, Perry J N, Bale J S, Clark S J. 1995. Effects of temperature on aphid phenology. Global Change Biology, 1, 303-313.

No related articles found!
No Suggested Reading articles found!