in

Potato leafroll virus reduces Buchnera aphidocola titer and alters vector transcriptome responses

  • 1.

    Remaudiere, G., & Remaudiere, M. Catalogue of the World’s Aphididae: Homoptera Aphidoidea. 473–1275. (Institut National de la Recherche Agronomique (INRA), 1997).

  • 2.

    Fereres, A., Irwin, M.E., & Kamppeier, G.E. Aphid movement: Process and consequences. in (van Emden H.F.R.H. ed.) Aphids as Crop Pests. 2nd edn. 196–200. (CABI, 2017).

  • 3.

    Ng, J. C. K. & Perry, K. L. Transmission of plant viruses by aphid vectors. Mol. Plant Pathol. 5(5), 505–511. https://doi.org/10.1111/j.1364-3703.2004.00240.x (2004).

    Article 
    PubMed 

    Google Scholar 

  • 4.

    Whitfield, A. E., Falk, B. W. & Rotenberg, D. Insect vector-mediated transmission of plant viruses. Virology 479–480, 278–289. https://doi.org/10.1016/j.virol.2015.03.026 (2015).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 5.

    Elena, S. F., Bernet, G. P. & Carrasco, J. L. The games plant viruses play. Curr. Opin. Virol. 8, 62–67. https://doi.org/10.1016/j.coviro.2014.07.003 (2014).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 6.

    Casteel, C.L., & Falk, B.W. Plant virus-vector interactions: More than just for virus transmission. in (Wang, A., & Zhou, X. eds.) Current Research Topics in Plant Virology. 2016. 217–240. https://doi.org/10.1007/978-3-319-32919-2_9 (2016).

  • 7.

    Eigenbrode, S. D., Bosque-Pérez, N. A. & Davis, T. S. Insect-borne plant pathogens and their vectors: Ecology, evolution, and complex interactions. Annu. Rev. Entomol. 63, 169–191. https://doi.org/10.1146/annurev-ento-020117-043119 (2018).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 8.

    Blanc, S. & Michalakis, Y. Manipulation of hosts and vectors by plant viruses and impact of the environment. Curr. Opin. Insect Sci. 16, 36–43. https://doi.org/10.1016/j.cois.2016.05.007 (2016).

    Article 
    PubMed 

    Google Scholar 

  • 9.

    Ingwell, L. L., Eigenbrode, S. D. & Bosque-Pérez, N. A. Plant viruses alter insect behavior to enhance their spread. Sci. Rep. 2(1), 578. https://doi.org/10.1038/srep00578 (2012).

    ADS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 10.

    Stafford, C. A., Yang, L. H., Mcmunn, M. S. & Ullman, D. E. Virus infection alters the predatory behavior of an omnivorous vector. Oikos 123, 1384–1390. https://doi.org/10.1111/oik.01148 (2014).

    Article 

    Google Scholar 

  • 11.

    Wang, Q. et al. Rice dwarf virus infection alters green rice leafhopper host preference and feeding behavior. PLoS ONE 13(9), 1–16. https://doi.org/10.1371/journal.pone.0203364 (2018).

    CAS 
    Article 

    Google Scholar 

  • 12.

    Stafford, C. A., Walker, G. P. & Ullman, D. E. Infection with a plant virus modifies vector feeding behavior. Proc. Natl. Acad. Sci. 108(23), 9350–9355. https://doi.org/10.1073/pnas.1100773108 (2011).

    ADS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 13.

    Zhang, Y. C., Cao, W. J., Zhong, L. R., Godfray, H. C. J. & Liu, X. D. Host plant determines the population size of an obligate symbiont (Buchnera aphidicola) in aphids. Appl. Environ. Microbiol. 82(8), 2336–2346. https://doi.org/10.1128/AEM.04131-15 (2016).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 14.

    Hansen, A. K. & Moran, N. A. Aphid genome expression reveals host-symbiont cooperation in the production of amino acids. Proc. Natl. Acad. Sci. 108(7), 2849–2854. https://doi.org/10.1073/pnas.1013465108 (2011).

    ADS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 15.

    Nakabachi, A. et al. Transcriptome analysis of the aphid bacteriocyte, the symbiotic host cell that harbors an endocellular mutualistic bacterium, Buchnera. Proc. Natl. Acad. Sci. 102(15), 5477–5482. https://doi.org/10.1073/pnas.1013465108 (2005).

    ADS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 16.

    Wernegreen, J. J. Strategies of genomic integration within insect-bacterial mutualisms. Biol Bull. 223(1), 112–122. https://doi.org/10.1086/BBLv223n1p112 (2012).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 17.

    Zhang, Y. et al. Genetic structure of the bacterial endosymbiont, Buchnera aphidicola, from its host aphid, Schlechtendalia chinensis, and evolutionary implications. Curr. Microbiol. 75(3), 309–315. https://doi.org/10.1007/s00284-017-1381-0 (2018).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 18.

    Zhang, F. et al. Bacterial symbionts, Buchnera, and starvation on wing dimorphism in English grain aphid, Sitobion avenae (F) (Homoptera: Aphididae). Front. Physiol. 6, 155. https://doi.org/10.3389/fphys.2015.00155 (2015).

    ADS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 19.

    Machado-Assefh, C. R., Lopez-Isasmendi, G., Tjallingii, W. F., Jander, G. & Alvarez, A. E. Disrupting Buchnera aphidicola, the endosymbiotic bacteria of Myzus persicae, delays host plant acceptance. Arthropod. Plant Interact. 9(5), 529–541. https://doi.org/10.1007/s11829-015-9394-8 (2015).

    Article 

    Google Scholar 

  • 20.

    Douglas, A. E. Nutritional interactions in insect-microbial symbioses: Aphids and their symbiotic bacteria Buchnera. Annu. Rev. Entomol. 43(1), 17–37. https://doi.org/10.1146/annurev.ento.43.1.17 (1998).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 21.

    Tamas, I. et al. 50 million years of genomic stasis in endosymbiotic bacteria. Science 296(5577), 2376–2379. https://doi.org/10.1126/science.1071278 (2002).

    ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 22.

    Van Ham, R. C. H. J. et al. Reductive genome evolution in Buchnera aphidicola. Proc. Natl. Acad. Sci. 100(2), 581–586. https://doi.org/10.1073/pnas.0235981100 (2003).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 23.

    Bouvaine, S., Boonham, N. & Douglas, A. E. Interactions between a Luteovirus and the GroEL chaperonin protein of the symbiotic bacterium Buchnera aphidicola of aphids. J. Gen. Virol. 92(6), 1467–1474. https://doi.org/10.1099/vir.0.029355-0 (2011).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 24.

    Rana, V. S., Singh, S. T., Priya, N. G., Kumar, J. & Rajagopal, R. Arsenophonus GroEL interacts with CLCuV and is localized in midgut and salivary gland of whitefly B. tabaci. PLoS ONE 7(8), e42168. https://doi.org/10.1371/journal.pone.0042168 (2012).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 25.

    Kliot, A. & Ghanim, M. The role of bacterial chaperones in the circulative transmission of plant viruses by insect vectors. Viruses 5(6), 1516–1535. https://doi.org/10.3390/v5061516 (2013).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 26.

    Filichkin, S. A., Brumfield, S., Filichkin, T. P. & Young, M. J. In vitro interactions of the aphid endosymbiotic SymL chaperonin with Barley yellow dwarf virus. J. Virol. 71(1), 569–577. https://doi.org/10.1128/JVI.71.1.569-577.1997 (1997).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 27.

    van den Heuvel, J. F., Verbeek, M. & van der Wilk, F. Endosymbiotic bacteria associated with circulative transmission of Potato leafroll virus by Myzus persicae. J. Gen. Virol. 75(Pt 10), 2559–2565. https://doi.org/10.1099/0022-1317-75-10-2559 (1994).

    Article 
    PubMed 

    Google Scholar 

  • 28.

    Gray, S. M. & Gildow, F. E. Luteovirus-aphid interactions. Annu. Rev. Phytopathol. 41(1), 539–566. https://doi.org/10.1146/annurev.phyto.41.012203.105815 (2003).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 29.

    Li, C., Cox-Foster, D., Gray, S. M. & Gildow, F. Vector specificity of Barley yellow dwarf virus (BYDV) transmission: Identification of potential cellular receptors binding BYDV-MAV in the aphid, Sitobion avenae. Virology 286(1), 125–133. https://doi.org/10.1006/viro.2001.0929 (2001).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 30.

    Dombrovsky, A., Gollop, N., Chen, S., Chejanovsky, N. & Raccah, B. In vitro association between the helper component-proteinase of Zucchini yellow mosaic virus and cuticle proteins of Myzus persicae. J. Gen. Virol. 88(5), 1602–1610. https://doi.org/10.1099/vir.0.82769-0 (2007).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 31.

    van den Heuvel, J. F. et al. The N-terminal region of the luteovirus readthrough domain determines virus binding to Buchnera GroEL and is essential for virus persistence in the aphid. J. Virol. 71(10), 7258–7265. https://doi.org/10.1128/JVI.71.10.7258-7265.1997 (1997).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 32.

    Morin, S. et al. A GroEL homologue from endosymbiotic bacteria of the whitefly Bemisia tabaci is implicated in the circulative transmission of Tomato yellow leaf curl virus. Virology 256(1), 75–84. https://doi.org/10.1006/viro.1999.9631 (1999).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 33.

    Chaudhary, R., Atamian, H. S., Shen, Z., Briggs, S. P. & Kaloshian, I. GroEL from the endosymbiont Buchnera aphidicola betrays the aphid by triggering plant defense. Proc. Natl. Acad. Sci. 111(24), 8919–8924. https://doi.org/10.1073/pnas.1407687111 (2014).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 34.

    Vandermoten, S. et al. Comparative analyses of salivary proteins from three aphid species. Insect Mol. Biol. 23(1), 67–77. https://doi.org/10.1111/imb.12061 (2014).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 35.

    Gray, S. M., Cilia, M. & Ghanim, M. Circulative, “nonpropagative” virus transmission: An orchestra of virus-, insect-, and plant-derived instruments. Adv. Virus Res. 2014, 89. https://doi.org/10.1016/B978-0-12-800172-1.00004-5 (2014).

    Article 

    Google Scholar 

  • 36.

    Eigenbrode, S. D., Ding, H., Shiel, P. & Berger, P. H. Volatiles from potato plants infected with Potato leafroll virus attract and arrest the virus vector, Myzus persicae (Homoptera: Aphididae). Proc. Biol. Sci. 269(1490), 455–460. https://doi.org/10.1098/rspb.2001.1909 (2002).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 37.

    Rajabaskar, D., Wu, Y., Bosque-Pérez, N. A. & Eigenbrode, S. D. Dynamics of Myzus persicae arrestment by volatiles from Potato leafroll virus-infected potato plants during disease progression. Entomol. Exp. Appl. 148(2), 2. https://doi.org/10.1111/eea.12087 (2013).

    Article 

    Google Scholar 

  • 38.

    Patton, M. F., Bak, A., Sayre, J. M., Heck, M. L. & Casteel, C. L. A polerovirus, Potato leafroll virus, alters plant–vector interactions using three viral proteins. Plant Cell Environ. 43(2), 387–399. https://doi.org/10.1111/pce.13684 (2020).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 39.

    Sadowy, E., Juszczuk, M., David, C., Gronenborn, B. & Danuta Hulanicka, M. D. Mutational analysis of the proteinase function of Potato leafroll virus. J. Gen. Virol. 82(Pt 6), 1517–1527. https://doi.org/10.1099/0022-1317-82-6-1517 (2001).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 40.

    DeBlasio, S. L. et al. Insights into the polerovirus– plant interactome revealed by coimmunoprecipitation and mass spectrometry. Mol. Plant-Microbe Interact. 28(4), 467–481. https://doi.org/10.1094/MPMI-11-14-0363-R (2015).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 41.

    Zhong, S. et al. High-throughput illumina strand-specific RNA sequencing library preparation. Cold Spring Harb. Protoc. 2011(8), 940–949. https://doi.org/10.1101/pdb.prot5652 (2011).

    Article 

    Google Scholar 

  • 42.

    Anders, S. et al. Count-based differential expression analysis of RNA sequencing data using R and bioconductor. Nat. Protoc. 8(9), 1765–1786. https://doi.org/10.1038/nprot.2013.099 (2013).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 43.

    Morgan, M. et al. ShortRead: A bioconductor package for input, quality assessment and exploration of high-throughput sequence data. Bioinformatics 25(19), 2607–2608. https://doi.org/10.1093/bioinformatics/btp450 (2009).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 44.

    Andrews, S. FastQC: A Quality Control Tool for High Throughput Sequence Data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/. (2010).

  • 45.

    Gauthier, J. P., Legeai, F., Zasadzinski, A., Rispe, C. & Tagu, D. AphidBase: A database for aphid genomic resources. Bioinformatics 23(6), 783–784. https://doi.org/10.1093/bioinformatics/btl682 (2007).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 46.

    Kim, D. et al. TopHat2: Accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, R36. https://doi.org/10.1186/gb-2013-14-4-r36 (2013).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 47.

    Anders, S., Pyl, P. T. & Huber, W. HTSeq-A Python framework to work with high-throughput sequencing data. Bioinformatics 31(2), 166–169. https://doi.org/10.1093/bioinformatics/btu638 (2015).

    CAS 
    Article 

    Google Scholar 

  • 48.

    Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15(12), 550. https://doi.org/10.1186/s13059-014-0550-8 (2014).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 49.

    Conesa, A. et al. Blast2GO: A universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21(18), 3674–3676. https://doi.org/10.1093/bioinformatics/bti610 (2005).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 50.

    Patton, M. F., Arena, G. D., Salminen, J. P., Steinbauer, M. J. & Casteel, C. L. Transcriptome and defence response in Eucalyptus camaldulensis leaves to feeding by Glycaspis brimblecombei Moore (Hemiptera: Aphalaridae): A stealthy psyllid does not go unnoticed. Austral. Entomol. 57(2), 247–254. https://doi.org/10.1111/aen.12319 (2017).

    Article 

    Google Scholar 

  • 51.

    Casteel, C. L. et al. Disruption of ethylene responses by Turnip mosaic virus mediates suppression of plant defense against the green peach aphid vector. Plant Physiol. 169(1), 209–218. https://doi.org/10.1104/pp.15.00332 (2015).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 52.

    Nikoh, N. et al. Bacterial genes in the aphid genome: Absence of functional gene transfer from Buchnera to its host. PLoS Genet. 6(2), e1000827. https://doi.org/10.1371/journal.pgen.1000827 (2010).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 53.

    Hansen, A. K. & Degnan, P. H. Widespread expression of conserved small RNAs in small symbiont genomes. ISME J. 8(12), 2490–2502. https://doi.org/10.1038/ismej.2014.121 (2014).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 54.

    Hogenhout, S. A., van der Wilk, F., Verbeek, M., Goldbach, R. W. & van den Heuvel, J. F. Potato leafroll virus binds to the equatorial domain of the aphid endosymbiotic GroEL homolog. J. Virol. 72(1), 358–365. https://doi.org/10.1128/JVI.72.1.358-365.1998 (1998).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 55.

    Camberg, J.L., Doyle, S.M., Johnston, D.M., & Wickner, S. Molecular Chaperones. in Brenner’s Encyclopedia of Genetics. 2nd Edn. 456–60. (Elsevier, 2013). https://doi.org/10.1016/B978-0-12-809633-8.06723-6.

  • 56.

    Segal, G. & Ron, E. Z. Regulation and organization of the groE and dnaK operons in Eubacteria. FEMS Microbiol. Lett. 138(1), 1–10. https://doi.org/10.1111/j.1574-6968.1996.tb08126.x (1996).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 57.

    Zhang, L., Pelech, S. & Uitto, V. J. Bacterial GroEL-like heat shock protein 60 protects epithelial cells from stress-induced death through activation of ERK and inhibition of caspase 3. Exp. Cell Res. 292(1), 231–240. https://doi.org/10.1016/j.yexcr.2003.08.012 (2004).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 58.

    Shigenobu, S., Watanabe, H., Hattori, M., Sakaki, Y. & Ishikawa, H. Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS Nat. 407(6800), 81–86. https://doi.org/10.1038/35024074 (2000).

    CAS 
    Article 

    Google Scholar 

  • 59.

    Dombrovsky, A., Sobolev, I., Chejanovsky, N. & Raccah, B. Characterization of RR-1 and RR-2 cuticular proteins from Myzus persicae. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 146(2), 256–264. https://doi.org/10.1016/j.cbpb.2006.11.013 (2007).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 60.

    Dombrovsky, A., Huet, H., Zhang, H., Chejanovsky, N. & Raccah, B. Comparison of newly isolated cuticular protein genes from six aphid species. Insect Biochem. Mol. Biol. 33(7), 709–715. https://doi.org/10.1016/s0965-1748(03)00065-1 (2003).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 61.

    Liang, Y. & Gao, X. W. The cuticle protein gene MPCP4 of Myzus persicae (Homoptera: Aphididae) plays a critical role in cucumber mosaic virus acquisition. J. Econ. Entomol. 110(3), 848–853. https://doi.org/10.1093/jee/tox025 (2017).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 62.

    Silva, A. X., Jander, G., Samaniego, H., Ramsey, J. S. & Figueroa, C. C. Insecticide resistance mechanisms in the green peach aphid Myzus persicae (Hemiptera: Aphididae) I: A transcriptomic survey. PLoS ONE 7(6), e36366. https://doi.org/10.1371/journal.pone.0036366 (2012).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 63.

    Deshoux, M., Monsion, B. & Uzest, M. Insect cuticular proteins and their role in transmission of phytoviruses. Curr. Opin. Virol. 33, 137–143. https://doi.org/10.1016/j.coviro.2018.07.015 (2018).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 64.

    Gallot, A. et al. Cuticular proteins and seasonal photoperiodism in aphids. Insect Biochem. Mol. Biol. 40(3), 235–240. https://doi.org/10.1016/j.ibmb.2009.12.001 (2010).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 65.

    Cilia, M. et al. Genetics coupled to quantitative intact proteomics links heritable aphid and endosymbiont protein expression to circulative polerovirus transmission. J. Virol. 85(5), 2148–2166. https://doi.org/10.1128/JVI.01504-10 (2011).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 66.

    Wang, H., Wu, K., Liu, Y., Wu, Y. & Wang, X. Integrative proteomics to understand the transmission mechanism of Barley yellow dwarf virus-GPV by its insect vector Rhopalosiphum padi. Sci. Rep. 5, 10971. https://doi.org/10.1038/srep10971 (2015).

    ADS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 67.

    Seddas, P. et al. Rack-1, GAPDH3, and actin: proteins of Myzus persicae potentially involved in the transcytosis of Beet western yellows virus particles in the aphid. Virology 325(2), 399–412. https://doi.org/10.1016/j.virol.2004.05.014 (2004).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 68.

    Yang, Z., Zhang, F., Zhu, L. & He, G. Identification of differentially expressed genes in brown planthopper Nilaparvata lugens (Hemiptera: Delphacidae) responding to host plant resistance. Bull. Entomol. Res. 96(1), 53–59. https://doi.org/10.1079/ber2005400 (2006).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 69.

    Bass, C. et al. Gene amplification and microsatellite polymorphism underlie a recent insect host shift. Proc. Natl. Acad. Sci. 110(48), 19460–19465. https://doi.org/10.1073/pnas.1314122110 (2013).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 70.

    Ramsey, J. S. et al. Adaptation to nicotine feeding in Myzus persicae. J. Chem. Ecol. 40(8), 869–877. https://doi.org/10.1007/s10886-014-0482-5 (2014).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 71.

    Casteel, C. L. & Jander, G. New synthesis: Investigating mutualisms in virus-vector interactions. J. Chem. Ecol. 39(7), 809. https://doi.org/10.1007/s10886-013-0305-0 (2013).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 72.

    Götz, M. et al. Implication of Bemisia tabaci HEAT SHOCK PROTEIN 70 in Begomovirus-whitefly interactions. J. Virol. 86(24), 13241–13252. https://doi.org/10.1128/JVI.00880-12 (2012).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 73.

    Porras, M. F. et al. Enhanced heat tolerance of viral-infected aphids leads to niche expansion and reduced interspecific competition. Nat. Commun. 11(1), 1184. https://doi.org/10.1038/s41467-020-14953-2 (2020).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 74.

    Syller, J. The influence of temperature on transmission of potato leaf roll virus by Myzus persicae Sulz. Potato Res. 30(1), 47–58. https://doi.org/10.1007/BF02357683 (1987).

    Article 

    Google Scholar 

  • 75.

    Syller, J. The effects of temperature on the susceptibility of potato plants to infection and accumulation of Potato Leafroll Virus. J. Phytopathol. 133(3), 216–224. https://doi.org/10.1111/j.1439-0434.1991.tb00156.x (1991).

    Article 

    Google Scholar 

  • 76.

    Chung, B. N. et al. The effects of high temperature on infection by Potato virus Y, Potato virus A, and Potato leafroll virus. Plant Pathol. J. 32(4), 321–328. https://doi.org/10.5423/PPJ.OA.12.2015.0259 (2016).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 77.

    Hansen, A. K. & Moran, N. A. The impact of microbial symbionts on host plant utilization by herbivorous insects. Mol. Ecol. 23(6), 1473–96 (2014).

    Article 

    Google Scholar 

  • 78.

    Jiang, Z. et al. Comparative analysis of genome sequences from four strains of the Buchnera aphidicola Mp endosymbion of the green peach aphid, Myzus persicae. BMC Genom. 14(1), 917. https://doi.org/10.1186/1471-2164-14-917 (2013).

    CAS 
    Article 

    Google Scholar 

  • 79.

    Enders, L. S. et al. Abiotic and biotic stressors causing equivalent mortality induce highly variable transcriptional responses in the soybean aphid. G3 (Bethesda) 5(2), 261–270. https://doi.org/10.1534/g3.114.015149 (2014).

    Article 

    Google Scholar 

  • 80.

    Wilcox, J. L., Dunbar, H. E., Wolfinger, R. D. & Moran, N. A. Consequences of reductive evolution for gene expression in an obligate endosymbiont. Mol. Microbiol. 48(6), 1491–1500. https://doi.org/10.1046/j.1365-2958.2003.03522.x (2003).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 81.

    Karp, P. D. et al. The BioCyc collection of microbial genomes and metabolic pathways. Brief Bioinform. 20(4), 1085–1093. https://doi.org/10.1093/bib/bbx085 (2019).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 82.

    Zhang, B., Leonard, S. P., Li, Y. & Moran, N. A. Obligate bacterial endosymbionts limit thermal tolerance of insect host species. Proc. Natl. Acad. Sci. 116(49), 24712–24718. https://doi.org/10.1073/pnas.1915307116 (2019).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 83.

    Chong, R. A. & Moran, N. A. Intraspecific genetic variation in hosts affects regulation of obligate heritable symbionts. PNAS 113(46),13114–13119. https://doi.org/10.1073/pnas.1610749113 (2016).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 84.

    Pers, D. & Hansen, A. K. The boom and bust of the aphid’s essential amino acid metabolism across nymphal development. G3 (Bethesda). 11(9), jkab115. https://doi.org/10.1093/g3journal/jkab115 (2021).

    Article 

    Google Scholar 

  • 85.

    Dunbar, H. E., Wilson, A. C. C., Ferguson, N. R. & Moran, N. A. Aphid thermal tolerance is governed by a point mutation in bacterial symbionts. PLoS Biol. 5(5), e96. https://doi.org/10.1371/journal.pbio.0050096 (2007).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 86.

    Moran, N. A. & Yun, Y. Experimental replacement of an obligate insect symbiont. Proc. Natl. Acad. Sci. 112(7), 2093–2096. https://doi.org/10.1073/pnas.1420037112 (2015).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 87.

    Fares, M. A., Barrio, E., Sabater-Muñoz, B. & Moya, A. The evolution of the heat-shock protein GroEL from Buchnera, the primary endosymbiont of aphids, is governed by positive selection. Mol. Biol. Evol. 19(7), 1162–1170. https://doi.org/10.1093/oxfordjournals.molbev.a004174 (2002).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 88.

    Kliot, A., Cilia, M., Czosnek, H., & Ghanim, M. Implication of the bacterial endosymbiont Rickettsia spp. in interactions of the whitefly Bemisia tabaci with Tomato yellow leaf curl virus. J. Virol. 88(10), 5652–5660. https://doi.org/10.1128/JVI.00071-14 (2014).

  • 89.

    Dheilly, N. M. et al. Who is the puppet master? Replication of a parasitic wasp-associated virus correlates with host behaviour manipulation. Proc. R. Soc. B Biol. Sci. 2015(282), 20142773 (1803).

    Google Scholar 

  • 90.

    Mohan, P. & Sinu, P. A. Does the solitary parasitoid Microplitis pennatulae use a combinatorial approach to manipulate its host?. Entomol. Exp. Appl. 168(4), 295–303 (2020).

    CAS 
    Article 

    Google Scholar 

  • 91.

    Smith, T. E. & Moran, N. A. Coordination of host and symbiont gene expression reveals a metabolic tug-of-war between aphids and Buchnera. Proc. Natl. Acad. Sci. 117(4), 2113–2121. https://doi.org/10.1073/pnas.1916748117 (2020).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 


  • Source: Ecology - nature.com

    Q&A: Can the world change course on climate?

    The global loss of floristic uniqueness