Geographically isolated Colorado potato beetle mediating distinct defense responses in potato is associated with the alteration of gut microbiota

Abstract

Colorado potato beetle (CPB; Leptinotarsa decemlineata) has been detected in Xinjiang, China, since 1993 and has caused serious damage to potato production during its eastward expansion to new geographic ranges. Symbiotic bacteria often play an essential role for insects to exploit novel food sources and expand into otherwise inaccessible ecological niches. An important yet unresolved question is whether herbivore populations from different geographic ranges have distinct or equal abilities to adapt to plant-induced defenses. We examined whether two geographic CPB populations collected from Urumqi and Ili varied in triggering induced defenses in potato plants, and the results demonstrated that plants damaged by Ili CPB larvae showed higher levels/activities of the defensive protein polyphenol oxidase (PPO) than those damaged by Urumqi CPB larvae. Intriguingly, application of oral secretions (OS) from Ili CPB larvae triggered higher PPO activity in potato compared with the treatments by OS collected from Urumqi larvae. Moreover, higher counts of bacterial colonies were observed in Urumqi CPB larvae by traditional culturing and quantitative PCR. Comparing the gut bacterial composition of CPB individuals by 16S rRNA amplicon sequencing also revealed higher abundance and diversity of gut-associated bacteria in the Urumqi population than that in the Ili population. These results indicate that the gut bacteria of CPB larvae were geographically shaped during the process of invasion, which played an important role in mediating plant–insect interactions and possesses a great potential to drive further invasion.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Acevedo FE, Rivera-Vega LJ, Chung SH, Ray S, Felton GW (2015) Cues from chewing insects - the intersection of DAMPs, HAMPs, MAMPs and effectors. Curr Opin Plant Biol 26:80–86

    CAS  PubMed  Google Scholar 

  2. Adams AS, Adams SM, Currie CR, Gillette NE, Raffa KF (2010) Geographic variation in bacterial communities associated with the red turpentine beetle (Coleoptera: Curculionidae). Environ Entomol 39:406–414

    PubMed  Google Scholar 

  3. Alyokhin A (2009) Colorado potato beetle management on potatoes: current challenges and future prospects. Fruit Veg Cereal Sci Biotechnol 3:10–19

    Google Scholar 

  4. Anderson PK, Cunningham AA, Patel NG, Morales FJ, Epstein PR, Daszak P (2004) Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers. Trends Ecol Evol 19:535–544

    PubMed  Google Scholar 

  5. Bosch M, Berger S, Schaller A, Stintzi A (2014) Jasmonate-dependent induction of polyphenol oxidase activity in tomato foliage is important for defense against Spodoptera exigua but not against Manduca sexta. BMC Plant Biol 14:257

    PubMed  PubMed Central  Google Scholar 

  6. Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Caporaso JG, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high- throughput community sequencing data Intensity normalization improves color calling in SOLiD sequencing. Nat Publ Gr 7:335–336

    CAS  Google Scholar 

  8. Carini P, Marsden PJ, Leff JW, Morgan EE, Strickland MS, Fierer N (2016) Relic DNA is abundant in soil and obscures estimates of soil microbial diversity. Nat Microbiol 2:16242

    PubMed  Google Scholar 

  9. Chandler JA, Lang J, Bhatnagar S, Eisen JA, Kopp A (2011) Bacterial communities of diverse drosophila species: ecological context of a host-microbe model system. PLoS Genet 7(9):e1002272

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Chu CC, Spencer JL, Curzi MJ, Zavala JA, Seufferheld M (2013) Gut bacteria facilitate adaptation to crop rotation in the western corn rootworm. Proc Natl Acad Sci U S A 110:11917–11922

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Chung SH, Rosa C, Scully ED, Peiffer M, Tooker JF, Hoover K, Luthe DS, Felton GW (2013) Herbivore exploits orally secreted bacteria to suppress plant defenses. Proc Natl Acad Sci U S A 110:15728–15733

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Chung SH, Scully ED, Peiffer M, Geib SM, Rosa C, Hoover K, Felton GW (2017) Host plant species determines symbiotic bacterial community mediating suppression of plant defenses. Sci Rep 7:39690

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Clark TB, Whitcomb RF, Tully JG (1982) Spiroplasmas from coleopterous insects: new ecological dimensions. Microb Ecol 8:401–409

    CAS  PubMed  Google Scholar 

  14. Constabel C, Bergey D, Ryan C (1995) Systemin activates synthesis of wound-inducible tomato leaf polyphenol oxidase via the octadecanoid defense signaling pathway. Proc Natl Acad Sci U S A 92:407–411

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998

    CAS  PubMed  Google Scholar 

  17. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Felton GW, Donato K, Del Vecchio RJ, Duffey SS (1989) Activation of plant foliar oxidases by insect feeding reduces nutritive quality of foliage for noctuid herbivores. J Chem Ecol 15:2667–2694

    CAS  PubMed  Google Scholar 

  19. Felton GW, Donato KK, Broadway RM, Duffey SS (1992) Impact of oxidized plant phenolics on the nutritional quality of dietar protein to a noctuid herbivore, Spodoptera exigua. J Insect Physiol 38(4):277–285

    CAS  Google Scholar 

  20. Guillemaud T, Ciosi M, Lombaert É, Estoup A (2011) Biological invasions in agricultural settings: insights from evolutionary biology and population genetics. C R Biol 334:237–246

    PubMed  Google Scholar 

  21. Haas BJ, Gevers D, Earl AM et al (2011) Chimeric 16S rRNA sequence formation and detection in sanger and 454-pyrosequenced PCR amplicons. Genome Res 21:494–504

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Hamady M, Lozupone C, Knight R (2010) Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J 4:17–27

    CAS  PubMed  Google Scholar 

  23. Hammer TJ, Janzen DH, Hallwachs W, Jaffe SP, Fierer N (2017) Caterpillars lack a resident gut microbiome. Proc Natl Acad Sci U S A 114:9641–9646

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Hansen AK, Moran NA (2014) The impact of microbial symbionts on host plant utilization by herbivorous insects. Mol Ecol 23:1473–1496

    PubMed  Google Scholar 

  25. Himler AG, Adachi-Hagimori T, Bergen JE et al (2011) Rapid spread of a bacterial symbiont in an invasive whitefly is driven by fitness benefits and female bias. Science 332:254–256

    CAS  PubMed  Google Scholar 

  26. Hosokawa T, Kikuchi Y, Shimada M, Fukatsu T (2007) Obligate symbiont involved in pest status of host insect. Proc R Soc Lond B 274:1979–1984

    CAS  Google Scholar 

  27. Hsiao T (1978) Host plant adaptations among geographic populations of the colorado potato beetle. Entomol Exp Appl 24:237–247

    Google Scholar 

  28. Izzo VM, Mercer N, Armstrong J, Chen YH (2004) Variation in host usage among geographic populations of Leptinotarsa decemlineata, the Colorado potato beetle. J Pest Sci 87:597–608

    Google Scholar 

  29. Jacques RL (1988) The potato beetles: the genus Leptinotarsa in North America (Coleoptera, Chrysomelidae). In: Mockford EL (ed) Flora and fauna hand-book, no. 3. Brill, New York

    Google Scholar 

  30. Kaiser W, Huguet E, Casas J, Commin C, Giron D (2010) Plant green-island phenotype induced by leaf-miners is mediated by bacterial symbionts. Proc R Soc Lond B 277:2311–2319

    CAS  Google Scholar 

  31. Lavergne S, Molofsky J (2007) Increased genetic variation and evolutionary potential drive the success of an invasive grass. Proc Natl Acad Sci U S A 104:3883–3888

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391

    Google Scholar 

  33. Liu N, Li Y, Zhang R (2012) Invasion of Colorado potato beetle, Leptinotarsa decemlineata, in China: dispersal, occurrence, and economic impact. Entomol Exp Appl 143:207–217

    Google Scholar 

  34. Liu Y, Fu KY, Tuerxun A, Jiang H, Guo WC, Zhou J (2016) Analysis on genetic diversity of different geographical population of the Leptinotarsa decemlineata using RAPD and SSR markers. Xinjiang Agric Sci 53:1608–1617 (in Chinese)

    Google Scholar 

  35. Logarzo GA, Casalinuovo MA, Piccinali RV, Braun K, Hasson E (2011) Geographic host use variability and host range evolutionary dynamics in the phytophagous insect Apagomerella versicolor (Cerambycidae). Oecologia 165:387–402

    PubMed  Google Scholar 

  36. Lu M, Wingfield MJ, Gillette N, Sun JH (2011) Do novel genotypes drive the success of an invasive bark beetle-fungus complex? Implications for potential reinvasion. Ecology 92:2013–2019

    PubMed  Google Scholar 

  37. Lu F, Kang X, Lorenz G, Espino L, Jiang MX, Way MO (2014) Culture-independent analysis of bacterial communities in the gut of rice water weevil (Coleoptera: Curculionidae). Ann Entomol Soc Am 107:592–600

    CAS  Google Scholar 

  38. Lu M, Hulcr J, Sun J (2016) The role of symbiotic microbes in insect invasions. Annu Rev Ecol Evol Syst 47:487–505

    Google Scholar 

  39. Mack NR, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz F (2000) Biotic invasions, causes, epidemiology, global consequences and control. Ecol Appl 10:689–710

    Google Scholar 

  40. Mason CJ, Raffa KF (2014) Acquisition and structuring of midgut bacterial communities in gypsy moth (Lepidoptera: Erebidae) larvae. Environ Entomol 43:595–604

    PubMed  Google Scholar 

  41. Ministry of Agriculture of the People’s Republic of China, General Administration of Quality Supervision & Inspection and Quarantine ofthe People’s Republic of China (2007) Catalogue of quarantine pests for import plants to the People’s Republic of China. Ministry of Agriculture, Beijing (in Chinese)

    Google Scholar 

  42. Moody ME, Mack RN (2006) Controlling the spread of plant invasions: the importance of nascent foci. J Appl Ecol 25:1009

    Google Scholar 

  43. Pan Q, Shikano I, Hoover K, Liu TX, Felton GW (2019) Pathogen-mediated tritrophic interactions: baculovirus-challenged caterpillars induce higher plant defenses than healthy caterpillars. J Chem Ecol. https://doi.org/10.1007/s10886-019-01077-1

    Article  PubMed  Google Scholar 

  44. Priya NG, Ojha A, Kajla MK, Raj A, Rajagopal R (2012) Host plant induced variation in gut bacteria of Helicoverpa armigera. PLoS ONE 7:e30768

    PubMed  Google Scholar 

  45. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:590–596

    Google Scholar 

  46. Sakai AK, Allendorf FW, Holt JS et al (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332

    Google Scholar 

  47. Shikano I, Rosa C, Tan C, Felton GW (2017) Tritrophic interactions: microbe-mediated plant effects on insect herbivores. Annu Rev Phytopathol 55:13:1–13:19

    Google Scholar 

  48. Simberloff D (2009) The role of propagule pressure in biological invasions. Ann Rev Ecol Evol Syst 40:81–102

    Google Scholar 

  49. Su Q, Oliver KM, Xie W, Wu Q, Wang S, Zhang Y (2015) The whitefly-associated facultative symbiont Hamiltonella defensa suppresses induced plant defences in tomato. Funct Ecol 29:1007–1018

    Google Scholar 

  50. Sudakaran S, Salem H, Kost C, Kaltenpoth M (2012) Geographical and ecological stability of the symbiotic mid-gut microbiota in European firebugs, Pyrrhocoris apterus (Hemiptera, Pyrrhocoridae). Mol Ecol 21:6134–6151

    CAS  PubMed  Google Scholar 

  51. Thaler JS, Humphrey PT, Whiteman NK (2012) Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci 17:260–270

    CAS  PubMed  Google Scholar 

  52. Toju H, Fukatsu T (2011) Diversity and infection prevalence of endosymbionts in natural populations of the chestnut weevil: relevance of local climate and host plants. Mol Ecol 20:853–868

    PubMed  Google Scholar 

  53. Traveset A, Richardson DM (2014) Mutualistic interactions and biological invasions. Annu Rev Ecol Evol Syst 45:89–113

    Google Scholar 

  54. Vilcinskas A, Stoecker K, Schmidtberg H, Rőhrich CR, Vogel H (2013) Invasive harlequin ladybird carries biological weapons against native competitors. Science 340:862–863

    CAS  PubMed  Google Scholar 

  55. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Wang J, Chung SH, Peiffer M, Rosa C, Hoover K, Zeng RS, Felton GW (2016) Herbivore oral secreted bacteria trigger distinct defense responses in preferred and non-preferred host plants. J Chem Ecol 42:463–474

    CAS  PubMed  Google Scholar 

  57. Wang J, Peiffer M, Rosa C, Zeng RS, Felton GW (2017) Helicoverpa zea gut-associated bacteria indirectly induce defenses in tomato through mediating salivary elicitor(s). New Phytol 214(3):1294–1306

    CAS  PubMed  Google Scholar 

  58. Weber DC, Drummond FA, Ferro DN (1995) Recruitment of colorado potato beetles (Coleoptera, Chrysomelidae) to solanaceous hosts in the field. Environ Entomol 24:608–622

    Google Scholar 

  59. Whitcomb RF (1981) The biology of spiroplasmas. Annu Rev Entomol 26:397–425

    Google Scholar 

  60. Xu LT, Lu M, Sun JH (2016) Invasive bark beetle-associated microbes degrade a host defensive monoterpene. Insect Sci 23:183–190

    CAS  PubMed  Google Scholar 

  61. Yin JH, Xu YY (2007) Analysis of climate change characteristics in Yili Valley. Desert Oasis Meteorol 6:20–23 (in Chinese)

    Google Scholar 

  62. Yu Y, Lee C, Kim J, Hwang S (2005) Group-specific primer and probe sets to detect methanogenic communities using quantitative real-time polymerase chain reaction. Biotechnol Bioeng 89:670–679

    CAS  PubMed  Google Scholar 

  63. Zhang JJ, Yang J, Li YC et al (2013) Genetic relationships of introduced colorado potato beetle Leptinotarsa decemlineata populations in Xinjiang, China. Insect Sci 20:643–654

    PubMed  Google Scholar 

  64. Zhu F, Poelman EH, Dicke M (2014) Insect herbivore-associated organisms affect plant responses to herbivory. New Phytol 204:315–321

    Google Scholar 

Download references

Acknowledgements

This project was supported by the National Natural Science Foundation of China (31701855), Natural Science Foundation of Fujian province (2018J017012), State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops (SKL2018009), Research Project of Department of Education of Fujian for Young and Middle-age teachers (JAT170155), Talent Programs of Fujian Agriculture and Forestry University (KXJQ17013), and China Postdoctoral Science Foundation (2019M652237).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Rensen Zeng.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Communicated by S.T. Jaronski.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLS 58 kb)

Supplementary material 2 (DOCX 1371 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Wang, J., Gao, Z., Yang, M. et al. Geographically isolated Colorado potato beetle mediating distinct defense responses in potato is associated with the alteration of gut microbiota. J Pest Sci 93, 379–390 (2020). https://doi.org/10.1007/s10340-019-01173-x

Download citation

Keywords

  • Gut microbiota
  • Leptinotarsa decemlineata
  • Invasive insects
  • Induced defense
  • Polyphenol oxidase
  • Solanum tuberosum