Age- and morph-dependent activation of the lysosomal system and Buchnera degradation in aphid endosymbiosis

Nishikori, Kenji; Morioka, Kazuyuki; Kubo, Takeo; Morioka, Mizue

doi:10.1016/j.jinsphys.2009.01.001

Cited by 83 publications

(91 citation statements)

References 32 publications

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“…2D). The mechanism of the symbiont segregation is unknown, but, although speculative, bacteriocyte-specific lysozyme/lysosomal activities might be involved in the symbiont sorting (19,20).…”

Section: Resultsmentioning

confidence: 99%

Cellular mechanism for selective vertical transmission of an obligate insect symbiont at the bacteriocyte–embryo interface

Koga

Meng

Tsuchida

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

236

268

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Many insects are associated with obligate symbiotic bacteria, which are localized in specialized cells called bacteriocytes, vertically transmitted through host generations via ovarial passage, and essential for growth and reproduction of their hosts. Although vertical transmission is pivotal for maintenance of such intimate host–symbiont associations, molecular and cellular mechanisms underlying the process are largely unknown. Here we report a cellular mechanism for vertical transmission of the obligate symbiont Buchnera in the pea aphid Acyrthosiphon pisum . In the aphid body, Buchnera cells are transmitted from maternal bacteriocytes to adjacent blastulae at the ovariole tips in a highly coordinated manner. By making use of symbiont-manipulated strains of A. pisum , we demonstrated that the facultative symbiont Serratia is, unlike Buchnera , not transmitted from maternal bacteriocytes to blastulae, suggesting a specific mechanism for Buchnera transmission. EM observations revealed a series of exo-/endocytotic processes operating at the bacteriocyte–blastula interface: Buchnera cells are exocytosed from the maternal bacteriocyte, temporarily released to the extracellular space, and endocytosed by the posterior syncytial cytoplasm of the blastula. These results suggest that the selective Buchnera transmission is likely attributable to Buchnera -specific exocytosis by the maternal bacteriocyte, whereas both Buchnera and Serratia are nonselectively incorporated by the endocytotic activity of the posterior region of the blastula. The sophisticated cellular mechanism for vertical transmission of Buchnera must have evolved to ensure the obligate host–symbiont association, whereas facultative symbionts like Serratia may coopt the endocytotic component of the mechanism for their entry into the host embryos.

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Section: Resultsmentioning

confidence: 99%

Cellular mechanism for selective vertical transmission of an obligate insect symbiont at the bacteriocyte–embryo interface

Koga

Meng

Tsuchida

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

236

268

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“…Because Buchnera are housed within bacteriocytes, the discovery of Buchnera proteins in the aphid saliva suggests that these proteins are present in the hemolymph and are likely released into the salivary duct by salivary gland cells. This release is likely to occur during bacteriocyte turnover and/or degeneration in the postreproductive aphid stage (22,23). Because bacteriocytes contain a full set of eukaryotic organelles (24), it is likely that proteins of aphid origin in the saliva, not predicted for secretions, originate from these cells too.…”

Section: Significancementioning

confidence: 99%

GroEL from the endosymbiont Buchnera aphidicola betrays the aphid by triggering plant defense

Chaudhary

Atamian

Shen

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

185

220

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Significance Aphids are sap-feeding plant pests of great agricultural importance. Aphid saliva is known to modulate plant immune responses, but limited information exists about the composition of aphid saliva. By means of mass spectrometry, we identified 105 proteins in the saliva of the potato aphid Macrosiphum euphorbiae . Among these proteins were some originating from the proteobacterium Buchnera aphidicola , which lives endosymbiotically within bacteriocytes in the hemocoel of the aphid. We demonstrate that one of these endosymbiont-derived proteins, the chaperonin GroEL, is recognized by the plant immune surveillance system and activates pattern-triggered immunity. Our findings indicate that the outcome of plant–aphid interactions critically depends on a third element, the aphid endosymbiotic prokaryotic component, which induces plant immunity.

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“…The data indicate that plant secondary metabolites might influence endosymbiont dynamics in herbivorous insects. The host plant might influence Buchnera dynamics directly or indirectly through the aphid host, for example, by effects on the expression of aphid carboxypeptidase vitellogenic-like protein or by affecting bacteriocyte development and lysozyme production (48,49). The second hypothesis is that the host may manipulate its endosymbiont titer to compensate for specific deficiencies in the nutrient profile of its host plant (8,50,51).…”

Section: Host Plant Affects Endosymbiont Population Density In Aphidsmentioning

confidence: 99%

Host Plant Determines the Population Size of an Obligate Symbiont (Buchnera aphidicola) in Aphids

Zhang

Cao

Zhong

et al. 2016

Appl Environ Microbiol

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bBuchnera aphidicola is an obligate endosymbiont that provides aphids with several essential nutrients. Though much is known about aphid-Buchnera interactions, the effect of the host plant on Buchnera population size remains unclear. Here we used quantitative PCR (qPCR) techniques to explore the effects of the host plant on Buchnera densities in the cotton-melon aphid, Aphis gossypii. Buchnera titers were significantly higher in populations that had been reared on cucumber for over 10 years than in populations maintained on cotton for a similar length of time. Aphids collected in the wild from hibiscus and zucchini harbored more Buchnera symbionts than those collected from cucumber and cotton. The effect of aphid genotype on the population size of Buchnera depended on the host plant upon which they fed. When aphids from populations maintained on cucumber or cotton were transferred to novel host plants, host survival and Buchnera population size fluctuated markedly for the first two generations before becoming relatively stable in the third and later generations. Host plant extracts from cucumber, pumpkin, zucchini, and cowpea added to artificial diets led to a significant increase in Buchnera titers in the aphids from the population reared on cotton, while plant extracts from cotton and zucchini led to a decrease in Buchnera titers in the aphids reared on cucumber. Gossypol, a secondary metabolite from cotton, suppressed Buchnera populations in populations from both cotton and cucumber, while cucurbitacin from cucurbit plants led to higher densities. Together, the results suggest that host plants influence Buchnera population processes and that this may provide phenotypic plasticity in host plant use for clonal aphids.A phids harbor two types of bacterial endosymbionts: the obligate symbiont Buchnera aphidicola, which occurs in almost all aphids, and facultative bacteria belonging to a variety of taxa that are not essential for aphid survival and typically are found in some but not all individuals of a population (1-3). The association between Buchnera and aphids was established 80 to 150 million years ago (4), and because transmission is strictly maternal, bacteria and host phylogenies are perfectly congruent. Buchnera is essential for the aphid, and if the symbiont is experimentally removed, the host grows very slowly and cannot reproduce (5-7). Buchnera synthesizes essential amino acids and other substances that are absent in the aphid's phloem diet (1,(8)(9)(10)(11)(12)(13) and is active in purine metabolism (14, 15). The symbiont's activities can be disrupted by heat shock, and it has been shown that variation in the promoter of a Buchnera heat shock gene impacts aphid thermal tolerance (16,17). The genome of Buchnera is much smaller than those of its free-living relatives (18, 19) and in many ways it now resembles an organelle, highly integrated within the physiology of its host.Densities of Buchnera (as measured by quantitative PCR [qPCR] relative to the host) are affected by host age and genotype and by ...

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Age- and morph-dependent activation of the lysosomal system and Buchnera degradation in aphid endosymbiosis

Cited by 83 publications

References 32 publications

Cellular mechanism for selective vertical transmission of an obligate insect symbiont at the bacteriocyte–embryo interface

Cellular mechanism for selective vertical transmission of an obligate insect symbiont at the bacteriocyte–embryo interface

GroEL from the endosymbiont Buchnera aphidicola betrays the aphid by triggering plant defense

Host Plant Determines the Population Size of an Obligate Symbiont (Buchnera aphidicola) in Aphids

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