Rickettsia increases its infection and spread in whitefly populations by manipulating the defense patterns of the host plant
Abstract
ABSTRACT The whitefly Bemisia tabaci is a destructive agricultural pest that frequently harbors various species of secondary symbionts including Rickettsia. Previous studies have revealed that the infection of Rickettsia can improve whitefly performance on food plants; however, to date, no evidence has shown, if, and how, Rickettsia manipulates the plant-insect interactions. In the current study, the effects of Rickettsia persistence on the induced plant defenses and the consequent performance of whitefly B. tabaci were investigated. Results revealed that Rickettsia can be transmitted into plants via whitefly feeding and remain alive within the cotton plants for at least 2 weeks. The different expression genes of cotton plants were mostly concentrated in the phytohormone signaling pathways, the marker genes of jasmonic-acid signaling pathway (AOC, AOS, LOX, MYC2) were significantly downregulated, while the marker genes of the salicylic-acid signaling pathway (WRKY70, PR-1) were upregulated. Biological experiments revealed that the fecundity of Rickettsia negative B. tabaci significantly increased when they fed on Rickettsia-persistent cotton plants. Taken together, we provide experimental evidence that the persistence of Rickettsia and its induced defense responses in cotton plants can increase the fitness of whitefly and, by this, Rickettsia may increase its infection and spread within its whitefly host.
- Authors:
-
- College of Coastal Agricultural Sciences, Guangdong Ocean University, Zhanjiang 524088, Guangdong Province, China, Key Laboratory of Bio-Pesticide Innovation and Application, Guangzhou 510640, Guangdong Province, China
- Key Laboratory of Bio-Pesticide Innovation and Application, Guangzhou 510640, Guangdong Province, China, Engineering Research Center of Biocontrol, Ministry of Education, Guangzhou 510640, Guangdong Province, China
- College of Forestry and Landscape Architecture, South China Agricultural University, Guangzhou 510640, Guangdong Province, China
- Key Laboratory of Bio-Pesticide Innovation and Application, Guangzhou 510640, Guangdong Province, China, Engineering Research Center of Biocontrol, Ministry of Education, Guangzhou 510640, Guangdong Province, China, Guangdong Laboratory for Lingnan Modern Agriculture, Guangzhou 510640, Guangdong Province, China, Department of Entomology, South China Agricultural University, Guangzhou 510640, Guangdong Province, China
- Publication Date:
- Sponsoring Org.:
- USDOE Office of Electricity (OE), Advanced Grid Research & Development. Power Systems Engineering Research
- OSTI Identifier:
- 1773545
- Grant/Contract Number:
- 2018B020205003
- Resource Type:
- Published Article
- Journal Name:
- FEMS Microbiology Ecology
- Additional Journal Information:
- Journal Name: FEMS Microbiology Ecology Journal Volume: 97 Journal Issue: 4; Journal ID: ISSN 0168-6496
- Publisher:
- Oxford University Press
- Country of Publication:
- Netherlands
- Language:
- English
Citation Formats
Shi, Pei-Qiong, Chen, Xin-Yi, Chen, Xiao-Sheng, Lv, Ning, Liu, Yuan, and Qiu, Bao-Li. Rickettsia increases its infection and spread in whitefly populations by manipulating the defense patterns of the host plant. Netherlands: N. p., 2021.
Web. doi:10.1093/femsec/fiab032.
Shi, Pei-Qiong, Chen, Xin-Yi, Chen, Xiao-Sheng, Lv, Ning, Liu, Yuan, & Qiu, Bao-Li. Rickettsia increases its infection and spread in whitefly populations by manipulating the defense patterns of the host plant. Netherlands. https://doi.org/10.1093/femsec/fiab032
Shi, Pei-Qiong, Chen, Xin-Yi, Chen, Xiao-Sheng, Lv, Ning, Liu, Yuan, and Qiu, Bao-Li. Fri .
"Rickettsia increases its infection and spread in whitefly populations by manipulating the defense patterns of the host plant". Netherlands. https://doi.org/10.1093/femsec/fiab032.
@article{osti_1773545,
title = {Rickettsia increases its infection and spread in whitefly populations by manipulating the defense patterns of the host plant},
author = {Shi, Pei-Qiong and Chen, Xin-Yi and Chen, Xiao-Sheng and Lv, Ning and Liu, Yuan and Qiu, Bao-Li},
abstractNote = {ABSTRACT The whitefly Bemisia tabaci is a destructive agricultural pest that frequently harbors various species of secondary symbionts including Rickettsia. Previous studies have revealed that the infection of Rickettsia can improve whitefly performance on food plants; however, to date, no evidence has shown, if, and how, Rickettsia manipulates the plant-insect interactions. In the current study, the effects of Rickettsia persistence on the induced plant defenses and the consequent performance of whitefly B. tabaci were investigated. Results revealed that Rickettsia can be transmitted into plants via whitefly feeding and remain alive within the cotton plants for at least 2 weeks. The different expression genes of cotton plants were mostly concentrated in the phytohormone signaling pathways, the marker genes of jasmonic-acid signaling pathway (AOC, AOS, LOX, MYC2) were significantly downregulated, while the marker genes of the salicylic-acid signaling pathway (WRKY70, PR-1) were upregulated. Biological experiments revealed that the fecundity of Rickettsia negative B. tabaci significantly increased when they fed on Rickettsia-persistent cotton plants. Taken together, we provide experimental evidence that the persistence of Rickettsia and its induced defense responses in cotton plants can increase the fitness of whitefly and, by this, Rickettsia may increase its infection and spread within its whitefly host.},
doi = {10.1093/femsec/fiab032},
journal = {FEMS Microbiology Ecology},
number = 4,
volume = 97,
place = {Netherlands},
year = {Fri Feb 19 00:00:00 EST 2021},
month = {Fri Feb 19 00:00:00 EST 2021}
}
https://doi.org/10.1093/femsec/fiab032
Works referenced in this record:
Herbivore exploits orally secreted bacteria to suppress plant defenses
journal, September 2013
- Chung, S. H.; Rosa, C.; Scully, E. D.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 39
Parasitic wasp responses to symbiont-based defense in aphids
journal, February 2012
- Oliver, Kerry M.; Noge, Koji; Huang, Emma M.
- BMC Biology, Vol. 10, Issue 1
Evolution of jasmonate and salicylate signal crosstalk
journal, May 2012
- Thaler, Jennifer S.; Humphrey, Parris T.; Whiteman, Noah K.
- Trends in Plant Science, Vol. 17, Issue 5
Transcription Factor WRKY70 Displays Important but No Indispensable Roles in Jasmonate and Salicylic Acid Signaling
journal, May 2008
- Ren, Chun-Mei; Zhu, Qi; Gao, Bi-Da
- Journal of Integrative Plant Biology, Vol. 50, Issue 5
A herbivore that manipulates plant defence: A herbivore that manipulates plant defence
journal, February 2011
- Sarmento, Renato Almeida; Lemos, Felipe; Bleeker, Petra M.
- Ecology Letters, Vol. 14, Issue 3
Assessments of Fitness Effects by the Facultative Symbiont Rickettsia in the Sweetpotato Whitefly (Hemiptera: Aleyrodidae)
journal, May 2009
- Chiel, Elad; Inbar, Moshe; Mozes-Daube, Netta
- Annals of the Entomological Society of America, Vol. 102, Issue 3
Relative Amount of Symbionts in Insect Hosts Changes with Host-Plant Adaptation and Insecticide Resistance
journal, February 2013
- Pan, Hui Peng; Chu, Dong; Liu, Bai Ming
- Environmental Entomology, Vol. 42, Issue 1
Infection dynamics of endosymbionts reveal three novel localization patterns of Rickettsia during the development of whitefly Bemisia tabaci
journal, August 2018
- Shi, Pei-Qiong; Wang, Lei; Liu, Yuan
- FEMS Microbiology Ecology, Vol. 94, Issue 11
Inherited intracellular ecosystem: symbiotic bacteria share bacteriocytes in whiteflies
journal, February 2008
- Gottlieb, Yuval; Ghanim, Murad; Gueguen, Gwenaelle
- The FASEB Journal, Vol. 22, Issue 7
Comparison of biological parameters between the invasive B biotype and a new defined Cv biotype of Bemisia tabaci (Hemiptera: Aleyradidae) in China
journal, July 2011
- Qiu, Bao-Li; Dang, Fang; Li, Shao-Jian
- Journal of Pest Science, Vol. 84, Issue 4
The Intracellular Bacterium Wolbachia Uses Parasitoid Wasps as Phoretic Vectors for Efficient Horizontal Transmission
journal, February 2015
- Ahmed, Muhammad Z.; Li, Shao-Jian; Xue, Xia
- PLOS Pathogens, Vol. 11, Issue 2
The WRKY70 Transcription Factor: A Node of Convergence for Jasmonate-Mediated and Salicylate-Mediated Signals in Plant Defense
journal, January 2004
- Li, Jing; Brader, Günter; Palva, E. Tapio
- The Plant Cell, Vol. 16, Issue 2
Suitable internal control genes for qRT-PCR normalization in cotton fiber development and somatic embryogenesis
journal, November 2007
- Tu, LiLi; Zhang, XianLong; Liu, DiQiu
- Chinese Science Bulletin, Vol. 52, Issue 22
MYC2 Orchestrates a Hierarchical Transcriptional Cascade That Regulates Jasmonate-Mediated Plant Immunity in Tomato
journal, July 2017
- Du, Minmin; Zhao, Jiuhai; Tzeng, David T. W.
- The Plant Cell, Vol. 29, Issue 8
Arabidopsis Transcriptome Changes in Response to Phloem-Feeding Silverleaf Whitefly Nymphs. Similarities and Distinctions in Responses to Aphids
journal, December 2006
- Kempema, Louisa A.; Cui, Xinping; Holzer, Frances M.
- Plant Physiology, Vol. 143, Issue 2
The Myriad Plant Responses to Herbivores
journal, June 2000
- Walling, Linda L.
- Journal of Plant Growth Regulation, Vol. 19, Issue 2
Facultative bacterial symbionts in aphids confer resistance to parasitic wasps
journal, January 2003
- Oliver, K. M.; Russell, J. A.; Moran, N. A.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 4
The whitefly‐associated facultative symbiont Hamiltonella defensa suppresses induced plant defences in tomato
journal, February 2015
- Su, Qi; Oliver, Kerry M.; Xie, Wen
- Functional Ecology, Vol. 29, Issue 8
Feeding by Whiteflies Suppresses Downstream Jasmonic Acid Signaling by Eliciting Salicylic Acid Signaling
journal, April 2013
- Zhang, Peng-Jun; Li, Wei-Di; Huang, Fang
- Journal of Chemical Ecology, Vol. 39, Issue 5
Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress: Aphid symbionts and heat stress
journal, April 2002
- Montllor, Clytia B.; Maxmen, Amy; Purcell, Alexander H.
- Ecological Entomology, Vol. 27, Issue 2
Facultative 'secondary' bacterial symbionts and the nutrition of the pea aphid, Acyrthosiphon pisum
journal, September 2006
- Douglas, A. E.; Francois, C. L. M. J.; Minto, L. B.
- Physiological Entomology, Vol. 31, Issue 3
Cross talk between signaling pathways in pathogen defense
journal, August 2002
- Kunkel, Barbara N.; Brooks, David M.
- Current Opinion in Plant Biology, Vol. 5, Issue 4
The presence of Rickettsia is associated with increased susceptibility of Bemisia tabaci (Homoptera: Aleyrodidae) to insecticides
journal, August 2008
- Kontsedalov, Svetlana; Zchori‐Fein, Einat; Chiel, Elad
- Pest Management Science, Vol. 64, Issue 8
Closely Related Wolbachia Strains within the Pumpkin Arthropod Community and the Potential for Horizontal Transmission via the Plant
journal, April 2006
- Sintupachee, S.; Milne, J. R.; Poonchaisri, S.
- Microbial Ecology, Vol. 51, Issue 3
Host Plant Specialization Governed by Facultative Symbiont
journal, March 2004
- Tsuchida, T.
- Science, Vol. 303, Issue 5666
Aphid Protected from Pathogen by Endosymbiont
journal, December 2005
- Scarborough, C. L.
- Science, Vol. 310, Issue 5755
Wolbachia infections in natural Anopheles populations affect egg laying and negatively correlate with Plasmodium development
journal, May 2016
- Shaw, W. Robert; Marcenac, Perrine; Childs, Lauren M.
- Nature Communications, Vol. 7, Issue 1
Manipulation of Plant Defense Responses by the Tomato Psyllid (Bactericerca cockerelli) and Its Associated Endosymbiont Candidatus Liberibacter Psyllaurous
journal, April 2012
- Casteel, Clare L.; Hansen, Allison K.; Walling, Linda L.
- PLoS ONE, Vol. 7, Issue 4
Early nuclear events in plant defence signalling: rapid gene activation by WRKY transcription factors
journal, September 1999
- Eulgem, T.
- The EMBO Journal, Vol. 18, Issue 17
Targets of AtWRKY6 regulation during plant senescence and pathogen defense
journal, May 2002
- Robatzek, S.
- Genes & Development, Vol. 16, Issue 9
Horizontal transmission of the insect symbiont Rickettsia is plant-mediated
journal, November 2011
- Caspi-Fluger, Ayelet; Inbar, Moshe; Mozes-Daube, Netta
- Proceedings of the Royal Society B: Biological Sciences, Vol. 279, Issue 1734
Role of plant hormones in plant defence responses
journal, December 2008
- Bari, Rajendra; Jones, Jonathan D. G.
- Plant Molecular Biology, Vol. 69, Issue 4
Horizontal Transmission of Intracellular Insect Symbionts via Plants
journal, November 2017
- Chrostek, Ewa; Pelz-Stelinski, Kirsten; Hurst, Gregory D. D.
- Frontiers in Microbiology, Vol. 8
Cytoplasmic incompatibility and host population structure
journal, May 2009
- Engelstädter, J.; Telschow, A.
- Heredity, Vol. 103, Issue 3
JASMONATE-INSENSITIVE1 Encodes a MYC Transcription Factor Essential to Discriminate between Different Jasmonate-Regulated Defense Responses in Arabidopsis
journal, June 2004
- Lorenzo, Oscar; Chico, Jose M.; Sánchez-Serrano, Jose J.
- The Plant Cell, Vol. 16, Issue 7
Plant-mediated horizontal transmission of Rickettsia endosymbiont between different whitefly species
journal, October 2017
- Li, Yi-Han; Ahmed, Muhammad Z.; Li, Shao-Jian
- FEMS Microbiology Ecology, Vol. 93, Issue 12
The Role of WRKY Transcription Factors in Plant Immunity: Figure 1.
journal, May 2009
- Pandey, Shree P.; Somssich, Imre E.
- Plant Physiology, Vol. 150, Issue 4
Phylogenetic analysis of Bemisia tabaci (Hemiptera: Aleyrodidae) populations from cotton plants in Pakistan, China, and Egypt
journal, October 2009
- Ahmed, Muhammad Z.; Ren, Shun-Xiang; Mandour, Nasser S.
- Journal of Pest Science, Vol. 83, Issue 2
Virulence Factors of Geminivirus Interact with MYC2 to Subvert Plant Resistance and Promote Vector Performance
journal, December 2014
- Li, Ran; Weldegergis, Berhane T.; Li, Jie
- The Plant Cell, Vol. 26, Issue 12
Almost There: Transmission Routes of Bacterial Symbionts between Trophic Levels
journal, March 2009
- Chiel, Elad; Zchori-Fein, Einat; Inbar, Moshe
- PLoS ONE, Vol. 4, Issue 3
Fast gapped-read alignment with Bowtie 2
journal, March 2012
- Langmead, Ben; Salzberg, Steven L.
- Nature Methods, Vol. 9, Issue 4
MYC2 Differentially Modulates Diverse Jasmonate-Dependent Functions in Arabidopsis
journal, July 2007
- Dombrecht, Bruno; Xue, Gang Ping; Sprague, Susan J.
- The Plant Cell, Vol. 19, Issue 7
Variation in resistance to parasitism in aphids is due to symbionts not host genotype
journal, August 2005
- Oliver, K. M.; Moran, N. A.; Hunter, M. S.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 36
Unique clade of alphaproteobacterial endosymbionts induces complete cytoplasmic incompatibility in the coconut beetle
journal, May 2017
- Takano, Shun-ichiro; Tuda, Midori; Takasu, Keiji
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 23
Endosymbiotic bacteria as a source of carotenoids in whiteflies
journal, September 2012
- Sloan, Daniel B.; Moran, Nancy A.
- Biology Letters, Vol. 8, Issue 6
Rickettsia influences thermotolerance in the whitefly Bemisia tabaci B biotype: Rickettsia influence on thermotolerance
journal, January 2011
- Brumin, Marina; Kontsedalov, Svetlana; Ghanim, Murad
- Insect Science, Vol. 18, Issue 1
Plantmediated horizontal transmission of Wolbachia between whiteflies
journal, December 2016
- Li, Shao-Jian; Ahmed, Muhammad Z.; Lv, Ning
- The ISME Journal, Vol. 11, Issue 4
A single-pair method to screen Rickettsia-infected and uninfected whitefly Bemisia tabaci populations
journal, January 2020
- Liu, Yuan; Fan, Ze-Yun; An, Xuan
- Journal of Microbiological Methods, Vol. 168
agriGO: a GO analysis toolkit for the agricultural community
journal, April 2010
- Du, Zhou; Zhou, Xin; Ling, Yi
- Nucleic Acids Research, Vol. 38, Issue suppl_2
Silverleaf Whitefly Induces Salicylic Acid Defenses and Suppresses Effectual Jasmonic Acid Defenses
journal, December 2006
- Zarate, Sonia I.; Kempema, Louisa A.; Walling, Linda L.
- Plant Physiology, Vol. 143, Issue 2
Plant defense responses induced by Bemisia tabaci Middle East-Asia Minor 1 salivary components
journal, May 2016
- Yan, Ying; Zhang, HaiJing; Yang, YiTing
- Entomologia Experimentalis et Applicata, Vol. 159, Issue 3
Facultative Symbiont Hamiltonella Confers Benefits to Bemisia tabaci (Hemiptera: Aleyrodidae), an Invasive Agricultural Pest Worldwide
journal, December 2013
- Su, Qi; Oliver, Kerry M.; Pan, Huipeng
- Environmental Entomology, Vol. 42, Issue 6
Plant-mediated interspecific horizontal transmission of an intracellular symbiont in insects
journal, November 2015
- Gonella, Elena; Pajoro, Massimo; Marzorati, Massimo
- Scientific Reports, Vol. 5, Issue 1
Battle for survival: plants and their allies and enemies
journal, August 2009
- Dong, Xinnian; Kahmann, Regine
- Current Opinion in Plant Biology, Vol. 12, Issue 4
HISAT: a fast spliced aligner with low memory requirements
journal, March 2015
- Kim, Daehwan; Langmead, Ben; Salzberg, Steven L.
- Nature Methods, Vol. 12, Issue 4