Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-23T14:25:28.318Z Has data issue: false hasContentIssue false
  • English
  • Français

Comparative transcriptome analyses of adzuki bean weevil (Callosobruchus chinensis) response to hypoxia and hypoxia/hypercapnia

Published online by Cambridge University Press:  12 July 2018

S.F. Cui ,
L. Wang ,
L. Ma ,
Y.L. Wang ,
J.P. Qiu ,
Zh.Ch. Liu  and
X.Q. Geng
S.F. Cui
Affiliation:
School of Grain Science and Technology, Jiangsu University of Science and Technology, Zhenjiang 212004, China Department of Resources and Environment, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, China
L. Wang
Affiliation:
Department of Resources and Environment, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, China
L. Ma
Affiliation:
Behavioral & Physiological Ecology (BPE) Group, Groningen Institute for Evolutionary Life Sciences, University of Groningen, Nijenborgh 7, 9747 AG Groningen, Netherlands
Y.L. Wang
Affiliation:
Department of Resources and Environment, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, China
J.P. Qiu
Affiliation:
Department of Resources and Environment, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, China
Zh.Ch. Liu*
Affiliation:
Department of Resources and Environment, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, China
X.Q. Geng*
Affiliation:
Department of Resources and Environment, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, China
*
*Author for correspondence Phone: 86-21-34208239 and 86-021-34208042 Fax: 86-34205877 and 86-21-34206142 E-mail: zhchl@sjtu.edu.cn and xqgeng@sjtu.edu.cn
*Author for correspondence Phone: 86-21-34208239 and 86-021-34208042 Fax: 86-34205877 and 86-21-34206142 E-mail: zhchl@sjtu.edu.cn and xqgeng@sjtu.edu.cn
Get access Rights & Permissions [Opens in a new window]

Abstract

Stored product insects show high adaption to hypoxia and hypercapnia, but the underlying mechanism is still unclear. Herein, a comparative transcriptome on 4th adzuki bean weevil (Callosobruchus chinensis) instar larvae was studied to clarify the response mechanisms to hypoxia (HA) and hypoxia/hypercapnia (HHA) using NextSeq500 RNA-Seq. Transcript profiling showed a significant difference in HA or HHA exposure both quantitatively and qualitatively. Compared with control, 631 and 253 genes were significantly changed in HHA and HA, respectively. Comparing HHA with HA, 1135 differentially expressed genes (DEGs) were identified. The addition of hypercapnia made a complex alteration on the hypoxia response of bean weevil transcriptome, carbohydrate, energy, lipid and amino acid metabolism were the most highly enriched pathways for genes significantly changed. In addition, some biological processes that were not significantly enriched but important were also discussed, such as immune system and signal transduction. Most of the DEGs related to metabolism both in HHA and HA were up-regulated, while the DEGs related to the immune system, stress response or signal transduction were significantly down-regulated or suppressed. This research reveals a comparatively full-scale result in adzuki bean weevil hypoxia and hypoxia/hypercapnia tolerance mechanism at transcription level, which might provide new insights into the genomic research of this species.

Keywords

adzuki bean weevilcomparative transcriptomehypoxiahypercapnia
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 109 , Issue 2 , April 2019 , pp. 266 - 277
Check for updates
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ahn, J.-E., Zhou, X., Dowd, S.E., Chapkin, R.S. & Zhu-Salzman, K. (2013) Insight into hypoxia tolerance in cowpea bruchid: metabolic repression and heat shock protein regulation via hypoxia-inducible factor 1. PLoS ONE 8, e57267.Google Scholar
Altschul, S.F., Gish, W., Miller, W., Myers, E.W. & Lipman, D.J. (1990) Basic local alignment search tool. Journal of Molecular Biology 215, 403–410.Google Scholar
Anders, S. & Huber, W. (2010) Differential expression analysis for sequence count data. Genome Biology 11, R106.Google Scholar
Aprille, J. (1988) Regulation of the mitochondrial adenine nucleotide pool size in liver: mechanism and metabolic role. The FASEB Journal 2, 2547–2556.Google Scholar
Ashburner, M., Ball, C.A., Blake, J.A., Botstein, D., Butler, H., Cherry, J.M., Davis, A.P., Dolinski, K., Dwight, S.S. & Eppig, J.T. (2000) Gene Ontology: tool for the unification of biology. Nature Genetics 25, 25–29.Google Scholar
Azab, M., Darwish, A., Mohamed, R. & Sanad, M. (2013) Comparative efficacy of controlled atmospheres against two stored product insects. Journal of Crop Protection 2, 343–353.Google Scholar
Cheng, W., Lei, J., Ahn, J.-E., Liu, T.-X. & Zhu-Salzman, K. (2012) Effects of decreased O2 and elevated CO2 on survival, development, and gene expression in cowpea bruchids. Journal of Insect Physiology 58, 792–800.Google Scholar
Cheng, W., Lei, J., Ahn, J.-E., Wang, Y., Lei, C. & Zhu-Salzman, K. (2013) CO2 enhances effects of hypoxia on mortality, development, and gene expression in cowpea bruchid, Callosobruchus maculatus. Journal of Insect Physiology 59, 1160–1168.Google Scholar
Cheng, W., Lei, J., Fox, C.W., Johnston, J.S. & Zhu-Salzman, K. (2015) Comparison of life history and genetic properties of cowpea bruchid strains and their response to hypoxia. Journal of Insect Physiology 75, 5–11.Google Scholar
Chi, Y.H., Ahn, J.-E., Yun, D.-J., Lee, S.Y., Liu, T.-X. & Zhu-Salzman, K. (2011) Changes in oxygen and carbon dioxide environment alter gene expression of cowpea bruchids. Journal of Insect Physiology 57, 220–230.Google Scholar
Colinet, H. & Renault, D. (2012) Metabolic effects of CO2 anaesthesia in Drosophila melanogaster. Biology Letters 8, 1050–1054.Google Scholar
Conyers, S. & Bell, C. (2007) A novel use of modified atmospheres: storage insect population control. Journal of Stored Products Research 43, 367–374.Google Scholar
Cui, S., Wang, L., Qiu, J., Liu, Z. & Geng, X. (2017) Comparative metabolomics analysis of Callosobruchus chinensis larvae under hypoxia, hypoxia/hypercapnia and normoxia. Pest Management Science 73, 1267–1276.Google Scholar
Donahaye, E. (1990) The potential for stored-product insects to develop resistance to modified atmospheres. pp. 989–996 in Proceedings of the Proceedings of the Fifth International Working Conference on Stored-Product Protection. 9–14 September 1990, Bordeaux, France.Google Scholar
Donahaye, E. & Navarro, S. (2000) Comparisons of energy reserves among strains of Tribolium castaneum selected for resistance to hypoxia and hypercarbia, and the unselected strain. Journal of Stored Products Research 36, 223–234.Google Scholar
Duan, C., Li, W., Zhu, Z., Li, D., Sun, S. & Wang, X. (2016) Genetic differentiation and diversity of Callosobruchus chinensis collections from China. Bulletin of Entomological Research 106, 124–134.Google Scholar
Duan, C.X., Li, D.D., Sun, S.L., Wang, X.M. & Zhu, Z.D. (2014) Rapid development of microsatellite markers for Callosobruchus chinensis using Illumina paired-end sequencing. PLoS ONE 9, e95458.Google Scholar
Duncan, F.D. & Newton, R.D. (2000) The use of the anaesthetic, enflurane, for determination of metabolic rates and respiratory parameters in insects, using the ant, Camponotus maculatus (Fabricius) as the model. Journal of Insect Physiology 46, 1529–1534.Google Scholar
Dziarski, R. & Gupta, D. (2006) The peptidoglycan recognition proteins (PGRPs). Genome Biology 7, 1–13.Google Scholar
Emekci, M., Navarro, S., Donahaye, E., Rindner, M., Azrieli, A., 2002) Respiration of Tribolium castaneum (Herbst) at reduced oxygen concentrations. Journal of Stored Products Research 38, 413–425.Google Scholar
Förster, T.D. & Hetz, S.K. (2010) Spiracle activity in moth pupae—the role of oxygen and carbon dioxide revisited. Journal of Insect Physiology 56, 492–501.Google Scholar
Feala, J.D., Coquin, L., Zhou, D., Haddad, G.G., Paternostro, G. & McCulloch, A.D. (2009) Metabolism as means for hypoxia adaptation: metabolic profiling and flux balance analysis. BMC Systems Biology 3, 91.Google Scholar
García-Lara, S., Ortiz-Islas, S. & Villers, P. (2013) Portable hermetic storage bag resistant to Prostephanus truncatus, Rhyzopertha dominica, and Callosobruchus maculatus. Journal of Stored Products Research 54, 23–25.Google Scholar
Gersten, M., Zhou, D., Azad, P., Haddad, G.G. & Subramaniam, S. (2014) Wnt pathway activation increases hypoxia tolerance during development. PLoS ONE 9, e103292.Google Scholar
Gleason, J.E., Corrigan, D.J., Cox, J.E., Reddi, A.R., McGinnis, L.A. & Culotta, V.C. (2011) Analysis of hypoxia and hypoxia-like states through metabolite profiling. PLoS ONE 6, e24741.Google Scholar
Guzy, R.D., Hoyos, B., Robin, E., Chen, H., Liu, L., Mansfield, K.D., Simon, M.C., Hammerling, U. & Schumacker, P.T. (2005) Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing. Cell Metabolism 1, 401–408.Google Scholar
Haas, B.J., Papanicolaou, A., Yassour, M., Grabherr, M., Blood, P.D., Bowden, J., Couger, M.B., Eccles, D., Li, B. & Lieber, M. (2013) De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nature Protocols 8, 1494–1512.Google Scholar
Harrison, J.F. (2001) Insect acid-base physiology. Annual Review of Entomology 46, 221–250.Google Scholar
Helenius, I.T., Krupinski, T., Turnbull, D.W., Gruenbaum, Y., Silverman, N., Johnson, E.A., Sporn, P.H., Sznajder, J.I. & Beitel, G.J. (2009) Elevated CO2 suppresses specific Drosophila innate immune responses and resistance to bacterial infection. Proceedings of the National Academy of Sciences 106, 18710–18715.Google Scholar
Huss, J.M., Levy, F.H. & Kelly, D.P. (2001) Hypoxia inhibits the peroxisome proliferator-activated receptor α/retinoid X receptor gene regulatory pathway in cardiac myocytes a mechanism for o2-dependent modulation of mitochondrial fatty acid oxidation. Journal of Biological Chemistry 276, 27605–27612.Google Scholar
Iturralde-García, R.D., Borboa-Flores, J., Cinco-Moroyoqui, F.J., Riudavets, J., Del Toro-Sánchez, C.L., Rueda-Puente, E.O., Martínez-Cruz, O. & Wong-Corral, F.J. (2016) Effect of controlled atmospheres on the insect Callosobruchus maculatus Fab. in stored chickpea. Journal of Stored Products Research 69, 78–85.Google Scholar
Jha, A.R., Zhou, D., Brown, C.D., Kreitman, M., Haddad, G.G. & White, K.P. (2015) Shared genetic signals of hypoxia adaptation in Drosophila and in high-altitude human populations. Molecular Biology and Evolution 33, 501–517.Google Scholar
Kanehisa, M., Goto, S., Kawashima, S., Okuno, Y. & Hattori, M. (2004) The KEGG resource for deciphering the genome. Nucleic Acids Research 32, D277–D280.Google Scholar
Kedia, A., Prakash, B., Mishra, P.K., Singh, P. & Dubey, N.K. (2015) Botanicals as eco friendly biorational alternatives of synthetic pesticides against Callosobruchus spp.(Coleoptera: Bruchidae) – a review. Journal of Food Science and Technology 52, 1239–1257.Google Scholar
Khalimonchuk, O. & Rödel, G. (2005) Biogenesis of cytochrome c oxidase. Mitochondrion 5, 363–388.Google Scholar
Krishnamurthy, T.S., Spratt, E.C. & Bell, C.H. (1986) The toxicity of carbon dioxide to adult beetles in low oxygen atmospheres. Journal of Stored Products Research 22,145 −151.Google Scholar
Langdon, W.B. (2015) Performance of genetic programming optimised Bowtie2 on genome comparison and analytic testing (GCAT) benchmarks. BioData Mining 8, 1.Google Scholar
Lin, T., Cai, Z., Wu, H. & Luo, L. (2016) Changes in midgut gene expression following Bacillus thuringiensis (Bacillales: Bacillaceae) infection in Monochamus alternatus (Coleoptera: Cerambycidae). Florida Entomologist 99, 60–66.Google Scholar
Majmundar, A.J., Wong, W.J. & Simon, M.C. (2010) Hypoxia-inducible factors and the response to hypoxic stress. Molecular Cell 40, 294–309.Google Scholar
Manekar, A., Godshalwar, M., Rewale, M. & Singh, M. (2005) Effect of tyrosine on central nervous system of marine male crab, scylla serrata: a biochemial study. Journal of Cell and Tissue Research 5, 345–348.Google Scholar
Marmaras, V.J. & Lampropoulou, M. (2009) Regulators and signalling in insect haemocyte immunity. Cellular Signalling 21, 186–195.Google Scholar
Maroz, A., Kelso, G.F., Smith, R.A., Ware, D.C. & Anderson, R.F. (2008) Pulse radiolysis investigation on the mechanism of the catalytic action of Mn (II)− pentaazamacrocycle compounds as superoxide dismutase mimetics. The Journal of Physical Chemistry A 112, 4929–4935.Google Scholar
Martin, M. (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. Journal 17, 10–12.Google Scholar
Matthews, P.G. & White, C.R. (2011) Regulation of gas exchange and haemolymph pH in the cockroach Nauphoeta cinerea. Journal of Experimental Biology 214, 3062–3073.Google Scholar
McMullen, D.C. & Storey, K.B. (2008) Mitochondria of cold hardy insects: responses to cold and hypoxia assessed at enzymatic, mRNA and DNA levels. Insect Biochemistry and Molecular Biology 38, 367–373.Google Scholar
Mohapatra, D., Kar, A. & Giri, S.K. (2015) Insect pest management in stored pulses: an overview. Food and Bioprocess Technology 8, 239–265.Google Scholar
Nicolas, G. & Sillans, D. (1989) Immediate and latent effects of carbon dioxide on insects. Annual Review of Entomology 34, 97–116.Google Scholar
O'Reilly, D.R. & Miller, L.K. (1989) A baculovirus blocks insect molting by producing ecdysteroid UDP-glucosyl transferase. Science 245, 1110–1112.Google Scholar
Powell, S., Forslund, K., Szklarczyk, D., Trachana, K., Roth, A., Huerta-Cepas, J., Gabaldón, T., Rattei, T., Creevey, C. & Kuhn, M. (2014) eggNOG v4. 0: nested orthology inference across 3686 organisms. Nucleic Acids Research 42, D231-D239.Google Scholar
Ragland, G.J., Denlinger, D.L. & Hahn, D.A. (2010) Mechanisms of suspended animation are revealed by transcript profiling of diapause in the flesh fly. Proceedings of the National Academy of Sciences 107, 14909–14914.Google Scholar
Ramputh, A.-I. & Bown, A.W. (1996) Rapid [gamma]-aminobutyric acid synthesis and the inhibition of the growth and development of oblique-banded leaf-roller larvae. Plant Physiology 111, 1349–1352.Google Scholar
Rash, L.D. & Hodgson, W.C. (2002) Pharmacology and biochemistry of spider venoms. Toxicon 40, 225–254.Google Scholar
Riudavets, J., Castañé, C., Alomar, O., Pons, M.J. & Gabarra, R. (2009) Modified atmosphere packaging (MAP) as an alternative measure for controlling ten pests that attack processed food products. Journal of Stored Products Research 45, 91–96.Google Scholar
Schmittgen, T.D. & Livak, K.J. (2008) Analyzing real-time PCR data by the comparative CT method. Nature protocols 3, 1101–1108.Google Scholar
Schmitz, A. & Harrison, J.F. (2004) Hypoxic tolerance in air-breathing invertebrates. Respiratory Physiology & Neurobiology 141, 229–242.Google Scholar
Selfridge, A.C., Cavadas, M.A., Scholz, C.C., Campbell, E.L., Welch, L.C., Lecuona, E., Colgan, S.P., Barrett, K.E., Sporn, P.H. & Sznajder, J.I. (2016) Hypercapnia suppresses the HIF-dependent adaptive response to hypoxia. Journal of Biological Chemistry 291, 11800–11808.Google Scholar
Tuda, M., Chou, L.-Y., Niyomdham, C., Buranapanichpan, S. & Tateishi, Y. (2005) Ecological factors associated with pest status in Callosobruchus (Coleoptera: Bruchidae): high host specificity of non-pests to Cajaninae (Fabaceae). Journal of Stored Products Research 41, 31–45.Google Scholar
Vermehren-Schmaedick, A., Ainsley, J.A., Johnson, W.A., Davies, S.-A. & Morton, D.B. (2010) Behavioral responses to hypoxia in Drosophila larvae are mediated by atypical soluble guanylyl cyclases. Genetics 186, 183–196.Google Scholar
Wingrove, J.A. & O'farrell, P.H. (1999) Nitric oxide contributes to behavioral, cellular, and developmental responses to low oxygen in Drosophila. Cell 98, 105–114.Google Scholar
Wong-Corral, F.J., Castañé, C. & Riudavets, J. (2013) Lethal effects of CO2-modified atmospheres for the control of three Bruchidae species. Journal of Stored Products Research 55, 62–67.Google Scholar
Yan, Y., Williams, S.B., Baributsa, D. & Murdock, L.L. (2016) Hypoxia treatment of Callosobruchus maculatus females and Its effects on reproductive output and development of progeny following exposure. Insects 7, 26.Google Scholar
Zhang, Z.-Y., Chen, B., Zhao, D.-J. & Kang, L. (2013) Functional modulation of mitochondrial cytochrome c oxidase underlies adaptation to high-altitude hypoxia in a Tibetan migratory locust. Proceedings of the Royal Society of London B: Biological Sciences, 280:20122758.Google Scholar
Zhou, D., Xue, J., Lai, J.C., Schork, N.J., White, K.P. & Haddad, G.G. (2008 a) Mechanisms underlying hypoxia tolerance in Drosophila melanogaster: hairy as a metabolic switch. PLoS Genetics 4, e1000221.Google Scholar
Zhou, X.R., Horne, I., Damcevski, K., Haritos, V., Green, A. & Singh, S. (2008 b) Isolation and functional characterization of two independently-evolved fatty acid Δ12-desaturase genes from insects. Insect Molecular Biology 17, 667–676.Google Scholar
Supplementary material: PDF

Cui et al. supplementary material

Tables S1-S6

Download Cui et al. supplementary material(PDF)
PDF 895.8 KB