The Secret Life of Insect-associated Microbes and How They Shape Insect-plant Interactions

Overview

Journal FEMS Microbiol Ecol

Publisher Oxford University Press

Specialties Environmental Health
Microbiology

Date 2022 Jul 13

PMID 35830517

Authors

Silvia Coolen

Rogowska-van der-Molen Magda

Cornelia U Welte

Affiliations

Soon will be listed here.

Abstract

Insects are associated with a plethora of different microbes of which we are only starting to understand their role in shaping insect-plant interactions. Besides directly benefitting from symbiotic microbial metabolism, insects obtain and transmit microbes within their environment, making them ideal vectors and potential beneficiaries of plant diseases and microbes that alter plant defenses. To prevent damage, plants elicit stress-specific defenses to ward off insects and their microbiota. However, both insects and microbes harbor a wealth of adaptations that allow them to circumvent effective plant defense activation. In the past decades, it has become apparent that the enormous diversity and metabolic potential of insect-associated microbes may play a far more important role in shaping insect-plant interactions than previously anticipated. The latter may have implications for the development of sustainable pest control strategies. Therefore, this review sheds light on the current knowledge on multitrophic insect-microbe-plant interactions in a rapidly expanding field of research.

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References

Winde I, Wittstock U . Insect herbivore counteradaptations to the plant glucosinolate-myrosinase system. Phytochemistry. 2011; 72(13):1566-75. DOI: 10.1016/j.phytochem.2011.01.016. View

Ramos A, Esteves M, Cortes M, Lopes J . Maize Bushy Stunt Phytoplasma Favors Its Spread by Changing Host Preference of the Insect Vector. Insects. 2020; 11(9). PMC: 7565095. DOI: 10.3390/insects11090600. View

Beran F, Kollner T, Gershenzon J, Tholl D . Chemical convergence between plants and insects: biosynthetic origins and functions of common secondary metabolites. New Phytol. 2019; 223(1):52-67. DOI: 10.1111/nph.15718. View

Ankrah N, Wilkes R, Zhang F, Aristilde L, Douglas A . The Metabolome of Associations between Xylem-Feeding Insects and their Bacterial Symbionts. J Chem Ecol. 2019; 46(8):735-744. DOI: 10.1007/s10886-019-01136-7. View

Perilla-Henao L, Casteel C . Vector-Borne Bacterial Plant Pathogens: Interactions with Hemipteran Insects and Plants. Front Plant Sci. 2016; 7:1163. PMC: 4977473. DOI: 10.3389/fpls.2016.01163. View

Qin F, Shinozaki K, Yamaguchi-Shinozaki K . Achievements and challenges in understanding plant abiotic stress responses and tolerance. Plant Cell Physiol. 2011; 52(9):1569-82. DOI: 10.1093/pcp/pcr106. View

Hannula S, Heinen R, Huberty M, Steinauer K, De Long J, Jongen R . Persistence of plant-mediated microbial soil legacy effects in soil and inside roots. Nat Commun. 2021; 12(1):5686. PMC: 8478921. DOI: 10.1038/s41467-021-25971-z. View

Toyota M, Spencer D, Sawai-Toyota S, Jiaqi W, Zhang T, Koo A . Glutamate triggers long-distance, calcium-based plant defense signaling. Science. 2018; 361(6407):1112-1115. DOI: 10.1126/science.aat7744. View

Li P, Liu C, Deng W, Yao D, Pan L, Li Y . Plant begomoviruses subvert ubiquitination to suppress plant defenses against insect vectors. PLoS Pathog. 2019; 15(2):e1007607. PMC: 6400417. DOI: 10.1371/journal.ppat.1007607. View

10.

Kikuchi Y, Hosokawa T, Fukatsu T . An ancient but promiscuous host-symbiont association between Burkholderia gut symbionts and their heteropteran hosts. ISME J. 2010; 5(3):446-60. PMC: 3105724. DOI: 10.1038/ismej.2010.150. View

11.

Ziebell H, Murphy A, Groen S, Tungadi T, Westwood J, Lewsey M . Cucumber mosaic virus and its 2b RNA silencing suppressor modify plant-aphid interactions in tobacco. Sci Rep. 2012; 1:187. PMC: 3240964. DOI: 10.1038/srep00187. View

12.

Casteel C, Hansen A, Walling L, Paine T . Manipulation of plant defense responses by the tomato psyllid (Bactericerca cockerelli) and its associated endosymbiont Candidatus Liberibacter psyllaurous. PLoS One. 2012; 7(4):e35191. PMC: 3335145. DOI: 10.1371/journal.pone.0035191. View

13.

Thoen M, Davila Olivas N, Kloth K, Coolen S, Huang P, Aarts M . Genetic architecture of plant stress resistance: multi-trait genome-wide association mapping. New Phytol. 2016; 213(3):1346-1362. PMC: 5248600. DOI: 10.1111/nph.14220. View

14.

Boyko A, Blevins T, Yao Y, Golubov A, Bilichak A, Ilnytskyy Y . Transgenerational adaptation of Arabidopsis to stress requires DNA methylation and the function of Dicer-like proteins. PLoS One. 2010; 5(3):e9514. PMC: 2831073. DOI: 10.1371/journal.pone.0009514. View

15.

Robert-Seilaniantz A, Grant M, Jones J . Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu Rev Phytopathol. 2011; 49:317-43. DOI: 10.1146/annurev-phyto-073009-114447. View

16.

Wenig M, Ghirardo A, Sales J, Pabst E, Breitenbach H, Antritter F . Systemic acquired resistance networks amplify airborne defense cues. Nat Commun. 2019; 10(1):3813. PMC: 6707303. DOI: 10.1038/s41467-019-11798-2. View

17.

Shikano I, Rosa C, Tan C, Felton G . Tritrophic Interactions: Microbe-Mediated Plant Effects on Insect Herbivores. Annu Rev Phytopathol. 2017; 55:313-331. DOI: 10.1146/annurev-phyto-080516-035319. View

18.

Mittler R, Blumwald E . Genetic engineering for modern agriculture: challenges and perspectives. Annu Rev Plant Biol. 2010; 61:443-62. DOI: 10.1146/annurev-arplant-042809-112116. View

19.

Comandatore F, Damiani C, Cappelli A, Ribolla P, Gasperi G, Gradoni F . Phylogenomics Reveals that Symbionts from Insects Underwent Convergent Genome Reduction, Preserving an Insecticide-Degrading Gene. mBio. 2021; 12(2). PMC: 8092202. DOI: 10.1128/mBio.00106-21. View

20.

Ammar E, Fulton D, Bai X, Meulia T, Hogenhout S . An attachment tip and pili-like structures in insect- and plant-pathogenic spiroplasmas of the class Mollicutes. Arch Microbiol. 2003; 181(2):97-105. DOI: 10.1007/s00203-003-0630-8. View