Volume 44 Issue 1
Jan.  2023
Turn off MathJax
Article Contents
Zhi-Ming Yang, Yang-Yang Yan, Yong Wu, Na Yu, Ze-Wen Liu. EcR/USP-1-mediated ecdysteroid signaling regulates wolf spider (Pardosa pseudoannulata) development and reproduction. Zoological Research, 2023, 44(1): 43-52. doi: 10.24272/j.issn.2095-8137.2022.282
Citation: Zhi-Ming Yang, Yang-Yang Yan, Yong Wu, Na Yu, Ze-Wen Liu. EcR/USP-1-mediated ecdysteroid signaling regulates wolf spider (Pardosa pseudoannulata) development and reproduction. Zoological Research, 2023, 44(1): 43-52. doi: 10.24272/j.issn.2095-8137.2022.282

EcR/USP-1-mediated ecdysteroid signaling regulates wolf spider (Pardosa pseudoannulata) development and reproduction

doi: 10.24272/j.issn.2095-8137.2022.282
Supplementary data to this article can be found online.
The authors declare that they have no competing interests.
Z.M.Y. and Z.W.L. designed and supervised the study. Z.M.Y., Y.Y.Y., and Y.W. performed the experiments. Z.M.Y. analyzed the data and wrote the manuscript. N.Y. and Z.W.L. revised the manuscript. All authors read and approved the final version of the manuscript.
Funds:  This work was supported by the National Natural Science Foundation of China (31972296, 32172482)
More Information
  • Corresponding author: E-mail: liuzewen@njau.edu.cn
  • Received Date: 2022-08-23
  • Accepted Date: 2022-10-18
  • Published Online: 2022-10-19
  • Publish Date: 2023-01-18
  • Lycosidae females demonstrate meticulous maternal care of offspring by carrying egg sacs and juvenile spiderlings during the reproductive stage. Nuclear receptors (NRs), especially the ecdysone receptor (EcR) and ultraspiracle (USP), have attracted considerable attention in the regulation of arthropod development and reproduction due to their pivotal roles in ecdysteroid signaling cascades. In the present study, 23 NRs, including one EcR and two USPs, were identified in the genome of the predatory wolf spider Pardosa pseudoannulata. RNA interference (RNAi) targeting EcR and USP-1 inhibited spiderling development and resulted in non-viable eggs in the egg sacs. EcR and USP-1 responded to changes in ecdysteroid levels, and interference in ecdysteroid biosynthesis led to similar phenotypes as dsEcR and dsUSP-1 treatments. These findings suggest that EcR/USP-1-mediated ecdysteroid signaling regulates P. pseudoannulata development and reproduction. The P. pseudoannulata females with suppressed ecdysteroid signaling proactively consumed their non-viable egg sacs, resulting in a 7.19 d shorter first reproductive cycle than the controls. Termination of the failed reproductive cycle enabled the spiders to produce a new egg sac more rapidly. This reproductive strategy may partially rescue the reduction in population growth due to non-viable eggs and compensate for the physiological expenditure of wasted maternal care, which would be beneficial for the conservation of P. pseudoannulata populations and their natural control of insect pests.
  • Supplementary data to this article can be found online.
    The authors declare that they have no competing interests.
    Z.M.Y. and Z.W.L. designed and supervised the study. Z.M.Y., Y.Y.Y., and Y.W. performed the experiments. Z.M.Y. analyzed the data and wrote the manuscript. N.Y. and Z.W.L. revised the manuscript. All authors read and approved the final version of the manuscript.
  • loading
  • [1]
    Adams MD, Celniker SE, Holt RA, Evans CA, Gocayne JD, Amanatides PG, et al. 2000. The genome sequence of Drosophila melanogaster. Science, 287(5461): 2185–2195.
    [2]
    Bednarek AW, Sawadro MK, Nicewicz Ł, Babczyńska AI. 2019. Vitellogenins in the spider Parasteatoda tepidariorum – expression profile and putative hormonal regulation of vitellogenesis. BMC Developmental Biology, 19(1): 4. doi: 10.1186/s12861-019-0184-x
    [3]
    Bertrand S, Brunet FG, Escriva H, Parmentier G, Laudet V, Robinson-Rechavi M. 2004. Evolutionary genomics of nuclear receptors: from twenty-five ancestral genes to derived endocrine systems. Molecular Biology and Evolution, 21(10): 1923−1937. doi: 10.1093/molbev/msh200
    [4]
    Bonneton F, Chaumot A, Laudet V. 2008. Annotation of Tribolium nuclear receptors reveals an increase in evolutionary rate of a network controlling the ecdysone cascade. Insect Biochemistry and Molecular Biology, 38(4): 416−429. doi: 10.1016/j.ibmb.2007.10.006
    [5]
    Borchert DM, Walgenbach JF, Kennedy GG. 2005. Assessment of sublethal effects of methoxyfenozide on oriental fruit moth (Lepidoptera: Tortricidae). Journal of Economic Entomology, 98(3): 765−771. doi: 10.1603/0022-0493-98.3.765
    [6]
    Cheng DJ, Xia QY, Duan J, Wei L, Huang C, Li ZQ, et al. 2008. Nuclear receptors in Bombyx mori: insights into genomic structure and developmental expression. Insect Biochemistry and Molecular Biology, 38(12): 1130−1137. doi: 10.1016/j.ibmb.2008.09.013
    [7]
    Christiaens O, Iga M, Velarde RA, Rougé P, Smagghe G. 2010. Halloween genes and nuclear receptors in ecdysteroid biosynthesis and signalling in the pea aphid. Insect Molecular Biology, 19(S2): 187−200.
    [8]
    Cruz J, Sieglaff DH, Arensburger P, Atkinson PW, Raikhel AS. 2009. Nuclear receptors in the mosquito Aedes aegypti: annotation, hormonal regulation and expression profiling. The FEBS Journal, 276(5): 1233−1254. doi: 10.1111/j.1742-4658.2008.06860.x
    [9]
    Fahrbach SE, Smagghe G, Velarde RA. 2012. Insect nuclear receptors. Annual Review of Entomology, 57: 83−106. doi: 10.1146/annurev-ento-120710-100607
    [10]
    Grbić M, Van Leeuwen T, Clark RM, Rombauts S, Rouzé P, Grbić V, et al. 2011. The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature, 479(7374): 487−492. doi: 10.1038/nature10640
    [11]
    Guo XP, Harmon MA, Laudet V, Mangelsdorf DJ, Palmer MJ. 1997. Isolation of a functional ecdysteroid receptor homologue from the ixodid tick Amblyomma americanum (L. ). Insect Biochemistry and Molecular Biology, 27(11): 945−962. doi: 10.1016/S0965-1748(97)00075-1
    [12]
    Guo XP, Xu Q, Harmon MA, Jin XJ, Laudet V, Mangelsdorf DJ, et al. 1998. Isolation of two functional retinoid X receptor subtypes from the ixodid tick, Amblyomma americanum (L. ). Molecular and Cellular Endocrinology, 139(1–2): 45–60.
    [13]
    Honda Y, Ishiguro W, Ogihara MH, Kataoka H, Taylor D. 2017. Identification and expression of nuclear receptor genes and ecdysteroid titers during nymphal development in the spider Agelena silvatica. General and Comparative Endocrinology, 247: 183–198.
    [14]
    Horigane M, Ogihara K, Nakajima Y, Shinoda T, Taylor D. 2007. Cloning and expression of the ecdysteroid receptor during ecdysis and reproduction in females of the soft tick, Ornithodoros moubata (Acari: Argasidae). Insect Molecular Biology, 16(5): 601−612. doi: 10.1111/j.1365-2583.2007.00754.x
    [15]
    Horigane M, Ogihara K, Nakajima Y, Taylor D. 2008. Isolation and expression of the retinoid X receptor from last instar nymphs and adult females of the soft tick Ornithodoros moubata (Acari: Argasidae). General and Comparative Endocrinology, 156(2): 298−311. doi: 10.1016/j.ygcen.2008.01.021
    [16]
    Iida H, Fujisaki K. 2005. Adaptive significance of the gregarious phase in nymphs of a wolf spider, Pardosa pseudoannulata (Araneae: Lycosidae). Applied Entomology and Zoology, 40(4): 649−657. doi: 10.1303/aez.2005.649
    [17]
    King-Jones K, Thummel CS. 2005. Nuclear receptors – a perspective from Drosophila. Nature Reviews Genetics, 6(4): 311–323.
    [18]
    Kumar S, Stecher G, Li M, Knyaz C, Tamura K. 2018. MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35(6): 1547−1549. doi: 10.1093/molbev/msy096
    [19]
    Li G, Liu XY, Han X, Niu JZ, Wang JJ. 2020. RNAi of the nuclear receptor HR3 suggests a role in the molting process of the spider mite Panonychus citri. Experimental and Applied Acarology, 81(1): 75–83.
    [20]
    Li G, Liu XY, Smagghe G, Niu JZ, Wang JJ. 2022. Molting process revealed by the detailed expression profiles of RXR1/RXR2 and mining the associated genes in a spider mite. Panonychus citri. Insect Science, 29(2): 430−442. doi: 10.1111/1744-7917.12931
    [21]
    Li G, Niu JZ, Zotti M, Sun QZ, Zhu L, Zhang J, et al. 2017. Characterization and expression patterns of key ecdysteroid biosynthesis and signaling genes in a spider mite (Panonychus citri). Insect Biochemistry and Molecular Biology, 87: 136−146. doi: 10.1016/j.ibmb.2017.06.009
    [22]
    Liu WZ, Xie YB, Ma JY, Luo XT, Nie P, Zuo ZX, et al. 2015. IBS: an illustrator for the presentation and visualization of biological sequences. Bioinformatics, 31(20): 3359−3361. doi: 10.1093/bioinformatics/btv362
    [23]
    Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the $2^{-\Delta\Delta C_T}$ method. Methods, 25(4): 402−408. doi: 10.1006/meth.2001.1262
    [24]
    Lu SN, Wang JY, Chitsaz F, Derbyshire MK, Geer RC, Gonzales NR, et al. 2020. CDD/SPARCLE: the conserved domain database in 2020. Nucleic Acids Research, 48(D1): D265−D268. doi: 10.1093/nar/gkz991
    [25]
    Meng XK, Li CR, Bao HB, Fang JC, Liu ZW, Zhang YX. 2015. Validating the importance of two acetylcholinesterases in insecticide sensitivities by RNAi in Pardosa pseudoannulata, an important predatory enemy against several insect pests. Pesticide Biochemistry and Physiology, 125: 26−30. doi: 10.1016/j.pestbp.2015.06.006
    [26]
    Nakagawa Y, Sakai A, Magata F, Ogura T, Miyashita M, Miyagawa H. 2007. Molecular cloning of the ecdysone receptor and the retinoid X receptor from the scorpion Liocheles australasiae. The FEBS Journal, 274(23): 6191–6203.
    [27]
    Nicewicz AW, Sawadro MK, Nicewicz Ł, Babczyńska AI. 2021. Juvenile hormone in spiders. Is this the solution to a mystery?. General and Comparative Endocrinology, 308: 113781. doi: 10.1016/j.ygcen.2021.113781
    [28]
    Palmer MJ, Warren JT, Jin XJ, Guo XP, Gilbert LI. 2002. Developmental profiles of ecdysteroids, ecdysteroid receptor mRNAs and DNA binding properties of ecdysteroid receptors in the ixodid tick Amblyomma americanum (L. ). Insect Biochemistry and Molecular Biology, 32(4): 465−476. doi: 10.1016/S0965-1748(01)00124-2
    [29]
    Ruhland F, Chiara V, Trabalon M. 2016a. Age and egg-sac loss determine maternal behaviour and locomotor activity of wolf spiders (Araneae, Lycosidae). Behavioural Processes, 132: 57−65. doi: 10.1016/j.beproc.2016.09.011
    [30]
    Ruhland F, Pétillon J, Trabalon M. 2016b. Physiological costs during the first maternal care in the wolf spider Pardosa saltans (Araneae, Lycosidae). Journal of Insect Physiology, 95: 42−50. doi: 10.1016/j.jinsphys.2016.09.007
    [31]
    Ruhland F, Schulz S, Hervé MR, Trabalon M. 2019. Do wolf spiders’ egg-sacs emit tactochemical signals perceived by mothers?. Behavioral Ecology, 30(2): 570−581. doi: 10.1093/beheco/ary197
    [32]
    Shen GM, Chen W, Li CZ, Ou SY, He L. 2019. RNAi targeting ecdysone receptor blocks the larva to adult development of Tetranychus cinnabarinus. Pesticide Biochemistry and Physiology, 159: 85–90.
    [33]
    Swift ML. 1997. GraphPad prism, data analysis, and scientific graphing. Journal of Chemical Information and Computer Sciences, 37(2): 411−412. doi: 10.1021/ci960402j
    [34]
    Tan AJ, Palli SR. 2008. Identification and characterization of nuclear receptors from the red flour beetle. Tribolium castaneum. Insect Biochemistry and Molecular Biology, 38(4): 430−439. doi: 10.1016/j.ibmb.2007.09.012
    [35]
    Thomas HE, Stunnenberg HG, Stewart AF. 1993. Heterodimerization of the Drosophila ecdysone receptor with retinoid X receptor and ultraspiracle. Nature, 362(6419): 471–475.
    [36]
    Trabalon M, Pourié G, Hartmann N. 1998. Relationships among cannibalism, contact signals, ovarian development and ecdysteroid levels in Tegenaria atrica (Araneae, Agelenidae). Insect Biochemistry and Molecular Biology, 28(10): 751−758. doi: 10.1016/S0965-1748(98)00066-6
    [37]
    Vancassel M, Foraste M, Strambi A, Strambi C. 1984. Normal and experimentally induced changes in hormonal hemolymph titers during parental behavior of the earwig Labidura riparia. General and Comparative Endocrinology, 56(3): 444–456.
    [38]
    Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, et al. 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology, 3(7): research0034. doi: 10.1186/gb-2002-3-7-reports0034
    [39]
    Velarde RA, Robinson GE, Fahrbach SE. 2006. Nuclear receptors of the honey bee: annotation and expression in the adult brain. Insect Molecular Biology, 15(5): 583−595. doi: 10.1111/j.1365-2583.2006.00679.x
    [40]
    Vieira C, Romero GQ. 2008. Maternal care in a neotropical jumping spider (Salticidae). Journal of Zoology, 276(3): 237−241. doi: 10.1111/j.1469-7998.2008.00480.x
    [41]
    Viera C, Ghione S, Costa FG. 2007. Mechanisms underlying egg-sac opening in the subsocial spider Anelosimus cf. studiosus (Araneae Theridiidae). Ethology Ecology & Evolution, 19(1): 61−67.
    [42]
    Xu L, Zhao CQ, Xu DJ, Xu GC, Xu XL, Han ZJ, et al. 2017. RNAi suppression of nuclear receptor genes results in increased susceptibility to sulfoxaflor in brown planthopper. Nilaparvata lugens. Journal of Asia-Pacific Entomology, 20(2): 645−653. doi: 10.1016/j.aspen.2017.03.022
    [43]
    Yang HL, Peng YD, Tian JX, Wang J, Wei BY, Xie CL, et al. 2018. Rice field spiders in China: a review of the literature. Journal of Economic Entomology, 111(1): 53−64. doi: 10.1093/jee/tox319
    [44]
    Yang PJ, Chen EH, Song ZH, He W, Liu SH, Dou W, et al. 2020. Molecular characterization and expression profiling of nuclear receptor gene families in oriental fruit fly, Bactrocera dorsalis (Hendel). Insects, 11(2): 126. doi: 10.3390/insects11020126
    [45]
    Yang ZM, Lu TY, Wu Y, Yu N, Xu GM, Han QQ, et al. 2022. The importance of vitellogenin receptors in the oviposition of the pond wolf spider. Pardosa pseudoannulata. Insect Science, 29(2): 443−452. doi: 10.1111/1744-7917.12933
    [46]
    Yang ZM, Yu N, Wang SJ, Korai SK, Liu ZW. 2021. Characterization of ecdysteroid biosynthesis in the pond wolf spider. Pardosa pseudoannulata. Insect Molecular Biology, 30(1): 71−80. doi: 10.1111/imb.12678
    [47]
    Yao TP, Forman BM, Jiang ZY, Cherbas L, Chen JD, McKeown M, et al. 1993. Functional ecdysone receptor is the product of EcR and ultraspiracle genes. Nature, 366(6454): 476–479.
    [48]
    Yip EC, Rayor LS. 2014. Maternal care and subsocial behaviour in spiders. Biological Reviews, 89(2): 427−449. doi: 10.1111/brv.12060
    [49]
    Yu N, Chen YR, Xu GM, Yang ZM, Wang SJ, Lu TY, et al. 2022. Cuticular compounds inhibit cannibalism of early-instar spiderlings by pulli-carrying Pardosa pseudoannulata females. Insect Science, 29(5): 1461−1469. doi: 10.1111/1744-7917.13006
    [50]
    Zhang WN, Ma L, Liu XY, Peng YC, Liang GM, Xiao HJ. 2021. Dissecting the roles of FTZ-F1 in larval molting and pupation, and the sublethal effects of methoxyfenozide on Helicoverpa armigera. Pest Management Science, 77(3): 1328–1338.
  • ZR-2022-282-Supplementary Materials.pdf
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures(6)  / Tables(1)

    Article Metrics

    Article views (1651) PDF downloads(350) Cited by()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return