Skip to main content
SpringerLink
Log in

Effect of elevated CO2 on interactions between the host plant Phaseolus vulgaris and the invasive western flower thrips, Frankliniella occidentalis

  • Original Paper
  • Published:
Journal of Pest Science Aims and scope Submit manuscript

Abstract

Elevated CO2 can alter the growth and development of herbivorous insects by changing the host plants, including nutrient quality and defensive chemicals/metabolites. The western flower thrips, Frankliniella occidentalis, is a highly destructive invasive pest in agriculture worldwide. In this study, we investigated the effect of elevated CO2 on the growth, development and reproduction of F. occidentalis by changing its host plant of kidney bean Phaseolus vulgaris and, in particular, the hormonal regulation of the transcription factors in F. occidentalis. Elevated CO2 increased the contents of total amino acids, soluble sugar and soluble protein in P. vulgaris. Besides, elevated CO2 shortened the pre-adult duration (PAD) and longevity of F. occidentalis, lowered their survival rate and increased the weight and fecundity. PAD was positively correlated with the expression levels of br, Krh-1, JHEH and EIP in F. occidentalis larvae. The longevity of F. occidentalis female adults was negatively correlated with JHEH, but positively correlated with ER and EIP. The fecundity of F. occidentalis female adults was negatively correlated with ER and Vg, but positively correlated with JHEH. We have demonstrated that elevated CO2 could enhance the nutrient quality of host plants and, therefore, accelerate the development and reproduction of F. occidentalis, which is regulated by JH, MH and Vg.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

References

  • Abe H, Ohnishi J, Narusaka M, Seo S et al (2008) Function of jasmonate in response and tolerance of Arabidopsis to thrip feeding. Plant Cell Physiol 49:68–80

    CAS  PubMed  Google Scholar 

  • Ainsworth EA, Rogers A (2007) The response of photosynthesis and stomatal conductance to rising CO2: mechanisms and environmental interactions. Plant, Cell Environ 30:258–270

    CAS  Google Scholar 

  • Amiri-Jami AR, Sadeghi H, Shoor M (2012) The performance of Brevicoryne brassicae on ornamental cabbages grown in CO2-enriched atmospheres. J Asia-Pac Entomol 15:249–253

    Google Scholar 

  • Arimura G, Matsui K, Takabayashi J (2009) Chemical and molecular ecology of herbivore-induced plant volatiles: proximate factors and their ultimate functions. Plant Cell Physiol 50:911–923

    CAS  PubMed  Google Scholar 

  • Awmack CS, Harrington R, Leather SR, Lawton JH (1996) The impact of elevated CO2 on aphid-plant interactions. Asp Appl Biol 45:317–322

    Google Scholar 

  • Bede JC, Tobe SS (2000) Activity of insect juvenile hormone III: seed germination and seedling growth studies. Chemoecology 10:89–97

    CAS  Google Scholar 

  • Bloom AJ, Burger M, Asensio JSR, Cousins AB (2010) Carbon dioxide enrichment inhibits nitrate assimilation in wheat and Arabidopsis. Science 328:899–903

    CAS  PubMed  Google Scholar 

  • Boughton AJ, Hoover K, Felton GW (2005) Methyl jasmonate application induces increased densities of glandular trichomes on tomato, Lycopersicon esculentum. J Chem Ecol 31:2211–2216

    CAS  PubMed  Google Scholar 

  • Brooks GL, Whittaker JB (1999) Responses of three generations of a xylem-feeding insect, Neophilaenus lineatus (Homoptera), to elevated CO2. Glob Change Biol 5:395–401

    Google Scholar 

  • Cai F, Watson BS, Meek D, Huhman DT et al (2017) Medicago truncatula oleanolic-derived saponins are correlated with caterpillar deterrence. J Chem Ecol 43:712–724

    CAS  PubMed  Google Scholar 

  • Chen FJ, Ge F, Parajulee MN (2005a) Impact of elevated CO2 on tri-trophic interaction of Gossypium hirsutum, Aphis gossypii, and Leis axyridis. Environ Entomol 34:37–46

    Google Scholar 

  • Chen FJ, Wu G, Ge F, Parajulee MN, Shrestha RB (2005b) Effects of elevated CO2 and transgenic Bt cotton on plant chemistry, performance, and feeding of an insect herbivore, the cotton bollworm. Entomol Exp Appl 115:341–350

    CAS  Google Scholar 

  • Cong C, Zhi J, Xie L, Gao H (2013) Effects of Franklinella occidentalis feeding on the chlorophyll and nutrients in the leaves of Phaseolus vulgaris. Plant Protection 39:20–24

    CAS  Google Scholar 

  • Corona M, Velarde RA, Remolina S, Moran-Lauter A et al (2007) Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. Proc Natl Acad Sci USA 104:7128–7133

    CAS  PubMed  Google Scholar 

  • Coviella CE, Trumble JT (1999) Effects of elevated atmospheric carbon dioxide on insect-plant interactions. Conserv Biol 13:700–712

    Google Scholar 

  • De Vos M, Van Oosten VR, Van Poecke RMP (2005) Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol Plant Microbe Inter 18:923–937

    Google Scholar 

  • Dubrovsky EB (2005) Hormonal cross talk in insect development. Trends Endocrinol Metab 16:6–11

    CAS  PubMed  Google Scholar 

  • Dudareva N, Negre F, Nagegowda DA, Orlova I (2006) Plant volatiles: recent advances and future perspectives. Crit Rev Plant Sci 25:417–440

    CAS  Google Scholar 

  • Ekert Van, Powell CA, Shatters RG, Borovsky D (2014) Control of larval and egg development in Aedes aegypti with RNA interference against juvenile hormone acid methyl transferase. J Insect Physiol 70:143–150

    PubMed  Google Scholar 

  • Flatt T, Amdam GV, Kirkwood TB, Omholt SW (2013) Life-history evolution and the polyphenic regulation of somatic maintenance and survival. Q Rev Biol 88:185–218

    PubMed  Google Scholar 

  • Fromme P, Melkozernov A, Jordan P, Krauss N (2003) Structure and function of photosystem I: interaction with its soluble electron carriers and external antenna systems. FEBS Lett 555:40–44

    CAS  PubMed  Google Scholar 

  • Ge F, Chen FJ, Wu G, Sun YC (2010) Research advance on the response of insects to elevated CO2 in China. J Chin Bull Entomol 47:229–235

    CAS  Google Scholar 

  • Gholami A, De Geyter N, Pollier J, Goormachtic S, Goossens A (2014) Natural product biosynthesis in Medicago species. Nat Prod Rep 31:356–380

    CAS  PubMed  Google Scholar 

  • Gilbert LI, Rybczynski R, Warren JT (2002) Control and biochemical nature of the ecdysteroidogenic pathway. Annu Rev Entomol 47:883–916

    CAS  PubMed  Google Scholar 

  • Guerenstein PG, Hildebrand JG (2008) Roles and effects of environmental carbon dioxide in insect life. Annu Rev Entomol 53:161–178

    CAS  PubMed  Google Scholar 

  • Guo H, Sun Y, Li Y, Tong B et al (2013) Pea aphid promotes amino acid metabolism both in medicago truncatula and bacteriocytes to favor aphid population growth under elevated CO2. Glob Change Biol 19:3210–3223

    Google Scholar 

  • He SQ, Lin Y, Qian L, Li ZH et al (2017) The influence of elevated CO2 concentration on the fitness traits of Frankliniella occidentalis and Frankliniella intonsa (Thysanoptera: Thripidae). Environ Entomol 46:722–728

    CAS  Google Scholar 

  • Heagle AS (2003) Influence of elevated carbon dioxide on interactions between Frankliniella occidentalis and Trifolium repens. Environ Entomol 32:421–424

    Google Scholar 

  • Hughes L, Bazzaz FA (1997) Effect of elevated CO2 on interactions between the western flower thrips, Frankliniella occidentalis (Thysanoptera: Thripidae) and the common milkweed, Asclepias syriaca. Oecologia 109:286–290

    CAS  PubMed  Google Scholar 

  • IPCC (2014) Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. IPCC, Geneva, Switzerland

  • Jackson RB, Cook CW, Pippen JS, Palmer SM (2009) Increased belowground biomass and soil CO2 fluxes after a decade of carbon dioxide enrichment in a warm-temperate forest. Ecology 90:3352–3366

    PubMed  Google Scholar 

  • Jensen SE (2000) Insecticide resistance in the western flower thrips, Frankliniella occidentalis. Integr Pest Manag Rev 5:131–146

    Google Scholar 

  • Jiang S, Liu T, Yu F, Li T et al (2016) Feeding behavioral response of cotton aphid, Aphis gossypii, to elevated CO2: EPG test with leaf microstructure and leaf chemistry. Entomol Exp Appl 160:1–10

    Google Scholar 

  • Jindra M, Palli SR, Riddiford LM (2013) The juvenile hormone signaling pathway in insect development. Annu Rev Entomol 58:181–204

    CAS  PubMed  Google Scholar 

  • Kamimura M (2004) Hormonal control of a metamorphosis-specific transcriptional factor Broad-Complex in silkworm. Comp Biochem Physiol B: Biochem Mol Biol 139:753–761

    Google Scholar 

  • Kawazu K, Mochizuki A, Sato Y, Sugeno W et al (2012) Different expression profiles of jasmonic acid and salicylic acid inducible genes in the tomato plant against herbivores with various feeding modes. Arthropod Plant Interact 6:221–230

    Google Scholar 

  • Keinanen M, Oldham NJ, Baldwin IT (2001) Rapid HPLC screening of jasmonate-induced increases in tobacco alkaloids, phenolics, and diterpene glycosides in Nicotiana attenuata. J Agric Food Chem 49:3553–3558

    CAS  PubMed  Google Scholar 

  • Kessler A, Baldwin IT (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291:2141–2144

    CAS  Google Scholar 

  • Kirk WDJ, Terry LI (2003) The spread of the western flower thrips Frankliniella occidentalis (Pergande). Agr Forest Entomol 5:301–310

    Google Scholar 

  • Konopova B, Jindra M (2008) Broad-Complex acts downstream of Met in juvenile hormone signaling to coordinate primitive holometabolan metamorphosis. Development 135:559–568

    CAS  PubMed  Google Scholar 

  • Konopova B, Smykal V, Jindra M (2011) Common and distinct roles of juvenile hormone signaling genes in metamorphosis of holometabolous and hemimetabolous insects. PLoS ONE 6:e28728

    CAS  PubMed  PubMed Central  Google Scholar 

  • Landosky JM , Karowe DN (2013) Elevated CO2 affects bottom-up and top-down driver impacts in plant-insect interaction. 98th ESA Annual Conven

  • Li L, Li C, Lee GI, Howe GA (2002) Distinct roles for jasmonic acid synthesis and action in the systemic wound response of tomato. Proc Natl Acad Sci USA 99:6416–6421

    CAS  PubMed  Google Scholar 

  • Lim UT, Van Driesche RG, Heinz KM (2001) Biological attributes of the nematode, Thripinema nicklewoodi, a potential biological control agent of western flower thrips. Biol Control 22:300–306

    Google Scholar 

  • Lindroth RL (2010) Impacts of elevated atmospheric CO2 and O3 on forests: phytochemistry, trophic interactions, and ecosystem dynamics. J Chem Ecol 36:2–21

    CAS  PubMed  Google Scholar 

  • Liu JY, Qian L, Jiang XC, He SQ, Li ZY, Gui FR (2014) Effects of elevated CO2 concentration on the activities of detoxifying enzymes and protective enzymes in adults of Frankliniella occidentalis and Frankliniella intonsa (Thysanoptera: Thripidae). Acta Entomologica Sinica 57:754–761

    CAS  Google Scholar 

  • Manners HR, Grimes ST, Sutton PA, Domingo L et al (2013) Magnitude and profile of organic carbon isotope records from the paleocene-eocene thermal maximun: evidence from Northern Spain. Earth Planet Sci Lett 376:220–230

    CAS  Google Scholar 

  • Massad TJ, Dyer LA (2010) A meta-analysis of the effects of global environmental change on plant-herbivore interactions. Arthropod-Plant Inte 4:181–188

    Google Scholar 

  • Minakuchi C, Zhou X, Riddiford LM (2008) Krüppel homolog 1 (Kr-h1) mediates juvenile hormone action during metamorphosis of Drosophila melanogaster. Mech Dev 125:91–105

    CAS  PubMed  Google Scholar 

  • Minakuchi C, Namiki T, Shinoda T (2009) Krüppel homolog 1, an early juvenile hormone-response gene downstream of Methoprene-tolerant, mediates its anti-metamorphic action in the red flour beetle Tribolium castaneum. Dev Biol 325:341–350

    CAS  PubMed  Google Scholar 

  • Minakuchi C, Tanaka M, Miura K, Tanaka T (2011) Developmental profile and hormonal regulation of the transcription factors broad and Krüppel homolog 1 in hemimetabolous thrips. Insect Biochem Molec 41:125–134

    CAS  Google Scholar 

  • Morse JG, Hoddle MS (2006) Invasion biology of thrips. Annu Rev Entomol 51:67–89

    CAS  PubMed  Google Scholar 

  • Mouden S, Sarmiento KF, Klinkhamer PGL, Leiss KA (2017) Integrated pest management in western flower thrips: past, present and future. Pest Manag Sci 73:813–822

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pincebourde S, Van Baaren J, Rasmann S, Rasmont P et al (2017) Plant-insect interactions in a changing world. Adv Bot Res 81:289–332

    Google Scholar 

  • Paudel R, Mahowald NM, Hess PGM, Meng L et al (2016) Attribution of changes in global wetland methane emissions from pre-industrial to present using CLM4.5-BGC. Environ Res Lett 11:3

    Google Scholar 

  • Qian L, Chen FJ, Liu JN, He SQ et al (2017) Effects of elevated CO2 on life-history traits of three successive generations of Frankliniella occidentalis and F. intonsa on kidney bean, Phaseolus vulgaris. Entomol Exp Appl 165:50–61

    CAS  Google Scholar 

  • Radhakrishnan R, Kang SM, Baek IY, Lee IJ (2014) Characterization of plant growth-promoting traits of Penicillium species against the effects of high soil salinity and root disease. J Plan Intera 9:754–762

    CAS  Google Scholar 

  • Reza AMS, Kanamori Y, Shinoda T, Shimura S, Mita K, Nakahara Y, Kiuchi M, Riddiford LM (2008) Juvenile hormone action: a 2007 perspective. J Insect Physiol 54:895–901

    Google Scholar 

  • Riddiford LM (1994) Cellular and molecular actions of juvenile hormone I general considerations and premetamorphic actions. Adv Insect Physiol 24:213–274

    CAS  Google Scholar 

  • Riddiford LM, Hiruma K, Zhou X, Nelson CA (2003) Insights into the molecular basis of the hormonal control of molting and metamorphosis from Manduca sexta and Drosophila melanogaster. Insect Biochem Mol Biol 33:1327–1338

    CAS  PubMed  Google Scholar 

  • Robinson GE, Vargo EL (1997) Juvenile hormone in adult eusocial Hymenoptera: gonadotropin and behavioral pacemaker. Arch Insect Biochem Physiol 35:559–583

    CAS  PubMed  Google Scholar 

  • Robinson EA, Ryan GD, Newman JA (2012) A meta-analytical review of the effects of elevated CO2 on plant–arthropod interactions highlights the importance of interacting environmental and biological variables. New Phytol 194:321–336

    CAS  PubMed  Google Scholar 

  • Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3:1101–1108

    CAS  Google Scholar 

  • Shinya T, Hojo Y, Desaki Y et al (2016) Modulation of plant defense responses to herbivores by simultaneous recognition of different herbivore-associated elicitors in rice. Sci Rep-UK 6:325–337

    Google Scholar 

  • Stiling P, Cornelissen T (2007) How does elevated carbon dioxide (CO2) affect plant-herbivore interactions? A field experiment and meta-analysis of CO2-mediated changes on plant chemistry and herbivore performance. Global Change Biol 13:1823–1842

    Google Scholar 

  • Sun Y (2008) Effects of Bemisia tabaci on the nutrient quality and physiological and biochemical indexes of tomatoes. Yangzhou University, Yangzhou

    Google Scholar 

  • Tufail M, Nagaba Y, Elgendy AM, Takeda M (2014) Regulation of vitellogenin genes in insects. Entomol Sci 17:269–282

    Google Scholar 

  • Uhlirova M, Foy BD, Beaty BJ, Olson KE, Riddiford LM, Jindra M (2003) Use of Sindbis virus-mediated RNA interference to demonstrate a conserved role of Broad-Complex in insect metamorphosis. Proc Natl Acad Sci USA 100:15607–15612

    CAS  PubMed  Google Scholar 

  • Yamanaka N, Rewitz KF, O’Connor MB (2013) Ecdysone control of developmental transitions: lessons from Drosophila research. Annu Rev Entomol 58:497–516

    CAS  PubMed  Google Scholar 

  • Zavala JA, Nabity PD, Delucia EH (2013) An emerging understanding of mechanisms governing insect herbivory under elevated CO2. Annu Rev Entomol 58:79–97

    CAS  PubMed  Google Scholar 

  • Zhai YF, Zhang JQ, Sun ZX, Dong XL et al (2013) Proteomic and transcriptomic analyses of fecundity in the brown planthopper Nilaparvata lugens (Stål). J Proteome Res 12:5199–5212

    CAS  PubMed  Google Scholar 

  • Zhou X, Riddiford LM (2002) Broad specifies pupal development and mediates the ‘status quo’ action of juvenile hormone on the pupal-adult transformation in Drosophila and Manduca. Development 129:2259–2269

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We sincerely appreciate Dr. Jacqueline Bede from Faculty of Agriculture and Environment in McGill University, Montreal, Quebec, Canada, who helped us revise English writing. This research was funded by the National Nature Science Foundations of China (NSFC) (31871963, 31272051 and 31660546), the Fundamental Research Funds for the Central Universities (KYZ201818), the Postgraduate Research and Practice Innovation Program of Jiangsu Province (KYCX180665), the Qing-Lan Project of Jiangsu Province of China and the SAAS Program for Excellent Research Team (i.e., SPERT).

Author information

Authors and Affiliations

  1. Department of Entomology, Nanjing Agricultural University, Nanjing, 210095, China

    Lei Qian, Zujin Huang, Xiaowei Liu, Chunxu Li & Fajun Chen

  2. Institute of Plant Protection, Chinese Academy of Agricultural Science, Beijing, 100193, China

    Yulin Gao

  3. College of Plant Protection, Yunnan Agricultural University, Kunming, 650201, China

    Furong Gui

  4. Shanghai Engineering Research Centre of Low-carbon Agriculture, Eco-Environmental Protection Research Institute, Shanghai Academy of Agricultural Sciences, Shanghai, 201403, China

    Xiaoli Chang

Authors
  1. Lei Qian
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zujin Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xiaowei Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chunxu Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yulin Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Furong Gui
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xiaoli Chang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Fajun Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fajun Chen.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

All applicable international, national and institutional guidelines for the care and use of animals were considered in the present investigation.

Informed consent

All authors of this manuscript accepted that the paper is submitted for publication in the Journal of Pest Science, and reported that this paper has not been published or accepted for publication in another journal, and it is not under consideration at another journal.

Additional information

Communicated by S. Reitz.

Publisher's Note

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

Special Issue on novel management tactics for the Western Flower Thrips.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 447 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Qian, L., Huang, Z., Liu, X. et al. Effect of elevated CO2 on interactions between the host plant Phaseolus vulgaris and the invasive western flower thrips, Frankliniella occidentalis. J Pest Sci 94, 43–54 (2021). https://doi.org/10.1007/s10340-020-01208-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10340-020-01208-8

Keywords

Search

Navigation