References
Aidemark,
M., Andersson, C., Rasmusson, A. G., & Widell, S. (2009). Regulation of
callose synthase activity in situ in alamethicin-permeabilizedArabidopsis and tobacco suspension cells. BMC Plant
Biology , 9(1), 27-27.
Burke,
G. R., Fiehn, O., & Moran, N. A. (2010). Effects of facultative
symbionts and heat stress on the metabolome of pea aphids. The
ISME Journal , 4(2), 242-252.
Casteel, C. L., Hansen, A. K.,
Walling, L. L., & Paine, T. D. (2012). Manipulation of plant defense
responses by the tomato psyllid (Bactericerca cockerelli ) and its
associated endosymbiont Candidatus Liberibacter
psyllaurous. PLOS ONE , 7(4).
Chung, S. H., Rosa, C., Hoover,
K., Luthe, D. S., & Felton, G. W. (2013). Colorado potato beetle
manipulates plant defenses in local and systemic leaves. Plant
Signaling & Behavior , 8(12).
Chaudhary, R., Atamian, H. S., Shen, Z., Briggs, S. P., & Kaloshian, I.
(2014). GroEL from the endosymbiont Buchnera aphidicola betrays
the aphid by triggering plant defense. Proceedings of the National
Academy of Sciences of the United States of America , 111(24),
8919-8924.
Chen, D., Montllor, C. B., &
Purcell, A. H. (2000). Fitness effects of two facultative endosymbiotic
bacteria on the pea aphid, Acyrthosiphon pisum , and the blue
alfalfa aphid, A. kondoi . Entomologia Experimentalis Et
Applicata , 95(3), 315-323.
Costopoulos, K., Kovacs, J. L.,
Kamins, A., & Gerardo, N. M. (2014). Aphid facultative symbionts reduce
survival of the predatory lady beetle Hippodamia
convergens . BMC Ecology , 14(1), 5-5.
Cui, N., Lu, H., Wang, T., Zhang,
W., Kang, L., & Cui, F. (2019). Armet, an aphid effector protein,
induces pathogen resistance in plants by promoting the accumulation of
salicylic acid. Philosophical Transactions of the Royal Society
B , 374(1767).
Defalco, T. A., Toyota, M., Phan,
V., Karia, P., Moeder, W., Gilroy, S., & Yoshioka, K. (2017). Using
GCaMP3 to Study Ca2+ Signaling in NicotianaSpecies. Plant and Cell Physiology , 58(7), 1173-1184.
De Vos, M., Van Oosten, V. R., Van Poecke, R. M., Van Pelt, J. A., Pozo,
M. J., Mueller, M. J., … & Pieterse, C. M. (2005). Signal signature
and transcriptome changes of Arabidopsis during pathogen and
insect attack. Molecular Plant-microbe Interactions , 18(9),
923-937.
Douglas, A. E., & Prosser, W. A. (1992). Synthesis of the essential
amino acid tryptophan in the pea aphid (Acyrthosiphon pisum )
symbiosis. Journal of Insect Physiology , 38(8), 565-568.
Douglas, A. E. (1998). Nutritional
Interactions in Insect-Microbial Symbioses: Aphids and Their Symbiotic
Bacteria Buchnera . Annual Review of Entomology , 43(1),
17-37.
Doremus, M. R., & Oliver, K. M.
(2017). Aphid Heritable Symbiont Exploits Defensive Mutualism. Applied
and Environmental Microbiology, 83(8).
Farmer, E. E., Gasperini, D., & Acosta, I. F. (2014). The squeeze cell
hypothesis for the activation of jasmonate synthesis in response to
wounding. New Phytologist, 204(2), 282-288.
Ferrari, J., Darby, A. C.,
Daniell, T. J., Godfray, H. C., & Douglas, A. E. (2004). Linking the
bacterial community in pea aphids with host-plant use and natural enemy
resistance. Ecological Entomology , 29(1), 60-65.
Fukatsu, T., Tsuchida, T., Nikoh,
N., & Koga, R. (2001). Spiroplasma symbiont of the pea aphid,Acyrthosiphon pisum (Insecta : Homoptera). Applied andEnvironmental Microbiology, 67(3), 1284-1291.
Frantz, A., Calcagno, V., Mieuzet, L., Plantegenest, M., & Simon, J.
(2009). Complex trait differentiation between host-populations of the
pea aphid Acyrthosiphon pisum (Harris): implications for the
evolution of ecological specialisation. Biological Journal of The
Linnean Society , 97(4), 718-727.
Gerardo, N. M., Altincicek, B., Anselme, C., Atamian, H. S., Barribeau,
S. M., De Vos, M., … & Vilcinskas, A. (2010). Immunity and other
defenses in pea aphids, Acyrthosiphon pisum . Genome
Biology , 11(2), 1-17.
Henry, L. M., Peccoud, J., Simon, J., Hadfield, J. D., Maiden, M.,
Ferrari, J., & Godfray, H. C. (2013). Horizontally Transmitted
Symbionts and Host Colonization of Ecological Niches. Current
Biology , 23(17), 1713-1717.
Hogenhout, S. A., & Bos, J. I.
(2011). Effector proteins that modulate plant–insect
interactions. Current Opinion in Plant Biology , 14(4), 422-428.
Hopper, K. R., Kuhn, K. L., Lanier, K., Rhoades, J. H., Oliver, K. M.,
White, J. A., … & Heimpel, G. E. (2018). The defensive aphid symbiontHamiltonella defensa affects host quality differently forAphelinus glycinis versus Aphelinus
atriplicis . Biological Control , 116, 3-9.
Jaouannet, M. L., Rodriguez, P. A., Thorpe, P., Lenoir, C. J., Macleod,
R., Escuderomartinez, C., & Bos, J. I. (2014). Plant immunity in
plant–aphid interactions. Frontiers in Plant Science ,, 663-663.
Laitinen, T., Morreel, K., Delhomme, N., Gauthier, A., Schiffthaler, B.,
Nickolov, K., … & Karkonen, A. (2017). A Key Role for Apoplastic
H2O2 in Norway Spruce Phenolic
Metabolism. Plant Physiology , 174(3), 1449-1475.
La Pena, E. D., Vandomme, V., &
Frago, E. (2014). Facultative endosymbionts of aphid populations from
coastal dunes of the North Sea. Belgian Journal of Zoology ,
144(1), 41-50.
Lamelas, A., Gosalbes, M. J., Manzanomarin, A., Pereto, J., Moya, A., &
Latorre, A. (2011). Serratia symbiotica from the AphidCinara cedri : A Missing Link from Facultative to Obligate Insect
Endosymbiont. PLOS Genetics , 7(11).
Leather S.R. & Dixon A.F.G (1984)
Aphid growth and reproductive rates. Entomologia Experimentalis et
Applicata , 35, 137–140.
Lei R, Du Z, Qiu Y, Zhu S. (2016). The detection of hydrogen peroxide
involved in plant virus infection by fluorescence spectroscopy.Luminescence , 31, 1158–1165.
Leonardo, T. E., & Muiru, G. T.
(2003). Facultative symbionts are associated with host plant
specialization in pea aphid populations. PROCEEDING OF THE ROYAL
SOCIETY B , 270, S209–S212.
Li,
Z., Feng, Z., Maeli, M., Jian, Y., Sheng, Y. H. (2017). Jasmonate
signaling and manipulation by pathogens and insects. Journal of
experimental botany , 68(6), 1371-1385.
Li, G., Zhou, J., Jia, H., Gao, Z., Fan, M., Luo, Y., … & Ma, Z.
(2019). Mutation of a histidine-rich calcium-binding-protein gene in
wheat confers resistance to Fusarium head blight. Nature
Genetics , 51(7), 1106-1112.
Łukasik, P., Van Asch, M., Guo, H., Ferrari, J., & Godfray, H. C.
(2013). Unrelated facultative endosymbionts protect aphids against a
fungal pathogen. Ecology Letters , 16(2), 214-218.
Manzanomarin, A., Lamelas, A.,
Moya, A., & Latorre, A. (2012). Comparative Genomics of Serratiaspp.: Two Paths towards Endosymbiotic Life. PLOS ONE , 7(10).
Mewis, I., Tokuhisa, J. G., Schultz, J. C., Appel, H. M., Ulrichs, C.,
& Gershenzon, J. (2006). Gene expression and glucosinolate accumulation
in Arabidopsis thaliana in response to generalist and specialist
herbivores of different feeding guilds and the role of defense signaling
pathways. Phytochemistry , 67(22), 2450-2462.
Mohase, L., & Der Westhuizen, A. J. (2002). Salicylic acid is involved
in resistance responses in the Russian wheat aphid-wheat
interaction. Journal of Plant Physiology , 159(6), 585-590.
Montllor C, Maxmen A, & Purcell
AH. (2002). Facultative bacterial endosymbionts benefit pea aphidsAcyrthosiphon pisum under heat stress. Ecol Entomol , 27:
189–195.
Moran, N. A., Russell, J. A.,
Koga, R., & Fukatsu, T. (2005). Evolutionary Relationships of Three New
Species of Enterobacteriaceae Living as Symbionts of Aphids and Other
Insects. Applied and Environmental Microbiology , 71(6),
3302-3310.
Moran, P. J., & Thompson, G. A. (2001). Molecular Responses to Aphid
Feeding in Arabidopsis in Relation to Plant Defense
Pathways. Plant Physiology , 125(2), 1074-1085.
Moran, P. J., Cheng, Y., Cassell, J. L., & Thompson, G. A. (2002). Gene
Expression Profiling of Arabidopsis thaliana in Compatible
Plant-Aphid Interactions. Archives of Insect Biochemistry and
Physiology , 51(4), 182-203.
Mutti, N. S., Louis, J., Pappan, L. K., Pappan, K. L., Begum, K., Chen,
M., … & Reeck, G. R. (2008). A protein from the salivary glands of
the pea aphid, Acyrthosiphon pisum , is essential in feeding on a
host plant. Proceedings of the National Academy of Sciences of the
United States of America, 105(29), 9965-9969.
Oliver, K. M., Russell, J. A.,
Moran, N. A., & Hunter, M. S. (2003). Facultative bacterial symbionts
in aphids confer resistance to parasitic wasps. Proceedings of the
National Academy of Sciences of the United States of America , 100(4),
1803-1807.
Oliver, K. M., Moran, N. A., &
Hunter, M. S. (2005). Variation in resistance to parasitism in aphids is
due to symbionts not host genotype. Proceedings of the National
Academy of Sciences of the United States of America , 102(36),
12795-12800.
Pegadaraju, V., Knepper, C., Reese, J. C., & Shah, J. (2005). Premature
Leaf Senescence Modulated by the Arabidopsis PHYTOALEXIN
DEFICIENT4 Gene Is Associated with Defense against the Phloem-Feeding
Green Peach Aphid. Plant Physiology , 139(4), 1927-1934.
Polin, S., Simon, J., & Outreman,
Y. (2014). An ecological cost associated with protective symbionts of
aphids. Ecology and Evolution , 4(6), 836-840.
Rodriguez, P. A., Stam, R.,
Warbroek, T., & Bos, J. I. (2014). Mp10 and Mp42 from the aphid speciesMyzus persicae trigger plant defenses in Nicotiana
benthamiana through different activities. Molecular Plant-microbe
Interactions , 27(1), 30-39.
Russell, J. A., & Moran, N. A.
(2006). Costs and benefits of symbiont infection in aphids: variation
among symbionts and across temperatures. Proceedings of the Royal
Society B , 273, 603–610.
Selig, P., Keough, S., Nalam, V. J., & Nachappa, P. (2016).
Jasmonate-dependent plant defenses mediate soybean thrips and soybean
aphid performance on soybean. Arthropod-plant Interactions ,
10(4), 273-282.
Simon,
J. C., Carre, S., Boutin, M., Leterme, N. P., Munoz, B. S., Latorre, A.,
& Bournoville, R. (2003). Host-based divergence in populations of the
pea aphid: insights from nuclear markers and the prevalence of
facultative symbionts. Proceedings of the Royal Society B , 270,
1703–1712.
Sorokan, A. V., Burkhanova, G. F.,
Benkovskaya, G. V., & Maksimov, I. V. (2019). Colorado potato beetle
microsymbiont Enterobacter BC-8 inhibits defense mechanisms of
potato plants using crosstalk between jasmonate- and salicylate-mediated
signaling pathways. Arthropod-plant Interactions ,
https://doi.org/10.1007/s11829-019-09732-w.
Sun, M., Voorrips, R. E., Kaauwen,
M., Visser, R., & Vosman, B. (2020). The ability to manipulate ROS
metabolism in pepper may affect aphid virulence. Horticulture
Research , 7, 6.
Tian, W., Hou, C., Ren, Z., Wang,
C., Zhao, F., Dahlbeck, D., … & Luan, S. (2019). A calmodulin-gated
calcium channel links pathogen patterns to plant
immunity. Nature , 572(7767), 131-135.
Tjallingii, W. F., & Esch, T. H.
(1993) Fine structure of the stylet route in plant tissues by some
aphids. Physiol. Entomol. , 18, 317–328.
Vincent, T. R., Avramova, M.,
Canham, J., Higgins, P., Bilkey, N., Mugford, S.T., … Sanders, D.
(2017). Interplay of Plasma Membrane and Vacuolar Ion Channels, Together
with BAK1, Elicits Rapid Cytosolic Calcium Elevations inArabidopsis during Aphid Feeding. The Plant Cell , 29(6),
1460-1479.
Wang, W., Dai, H., Zhang, Y.,
Chandrasekar, R., Luo, L., Hiromasa, Y., … & Cui, F. (2015). Armet is
an effector protein mediating aphid–plant interactions. The FASEB
Journal , 29(5), 2032-2045.
Fig 1. S. symbiotica facilitated pea
aphids’ feeding on M. truncatula (cv. A17) and its location in
aphid body.
(a-c) EPG results of Serratia -: Serratia -free,Serratia +: Serratia -infected, and Serratia +r:Serratia -rebuilt aphids for 8 h on M. truncatula . (a) Time
spent on salivary secretion into sieve elements (E1 wave) (n=10). (b)
Ingestion time (E2 wave) (n=10). (c) Time to phloem ingestion (n=10).
(d-f) Fluorescence in situ hybridization (FISH) to detect B.
aphidicola and S. symbiotica in aphid abdomen. Aphid DNA was
stained with 4’,6-diamidino-2-phenylindole (blue), B. aphidicolaDNA was hybridized with Cy5-labeled DNA probe (red), S.
symbiotica DNA was hybridized with Cy3-labeled DNA probe (green). (d)B. aphidicola in Serratia -free aphids. (e) B.
aphidicola and S. symbiotica in Serratia -infected aphids.
(f) B. aphidicola and S. symbiotica inSerratia -rebuilt aphids. The data shown are mean ± standard error
(SEM). * indicate significant differences among different treatments at
P < 0.05 (*P < 0.05, **P < 0.01, ***P
< 0.001) one-way ANOVA analysis for EPG data.