Development responses of symbiotic and aposymbiotic weevils Sitophilus oryzae L. (Coleoptera, curculionidae) to a diet supplemented with aromatic amino acids

Wicker, Claude; Nardon, P.

doi:10.1016/0022-1910(82)90008-7

Cited by 37 publications

(25 citation statements)

References 13 publications

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“…Pellets were made following a method previously described (Wicker & Nardon, 1982). Normal wheat pellets were obtained by mixing 200 g of wholemeal wheat flour with 160 ml of distilled water, making long rolls (0.5 cm in diameter) with this pastry, and cutting little pieces after drying.…”

Section: Methodsmentioning

confidence: 99%

The role of symbiotes in flight activity of Sitophilus weevils

Grenier

Nardon

1994

Entomologia Exp Applicata

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The flight activity (take-off) of various strains of Sitophilus oryzae L. and S. zeamais Mots. (Coleoptera, Curculionidae) have been compared on wheat. It was shown that males are more active than females and that S. zeamais, is more active than S. oryzae. Furthermore, in the two species, when reared on wheat kernels, only symbiotic weevils were able to fly, while aposymbiotic insects did not. By supplementation of the diet with vitamins (pantothenic acid, riboflavin) and amino acids (phenylalanine and proline), this activity could be restored in part. The influence of symbiosis on the flight ability of Sitophilus weevil is discussed in relation to the energy metabolism (coenzymes, proline), the role played by symbiosis in this behaviour and its possible effect on the dissemination of the species.

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Section: Methodsmentioning

confidence: 99%

The role of symbiotes in flight activity of Sitophilus weevils

Grenier

Nardon

1994

Entomologia Exp Applicata

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“…Notably, a set of metabolic genes is conspicuously retained in the Nardonella genomes, namely synthesis pathway genes for a specific amino acid, tyrosine. Weevils are armored with hard cuticle, tyrosine is the principal precursor needed for cuticle formation, and the Nardonella genome has been streamlined for a single biological function, tyrosine provisioning, for sustaining the weevil's highly sclerotized exoskeleton, which elucidates the general importance of endosymbiontprovisioned tyrosine for cuticle formation in weevils (36,37), and potentially also in other beetles. Furthermore, we demonstrate that, reflecting the absence of transcriptional regulators in the tiny symbiont genome, Nardonella's tyrosine provisioning is controlled by host's final step regulation of the synthesis pathway.…”

Section: Significancementioning

confidence: 99%

“…The weevil-associated Sodalis genome was determined as 4.5 Mb in size, which was much larger than the Nardonella genome and retaining many metabolic pathways intact; however, the Sodalis genome was full of amplified IS elements and pseudogenes (50,51), representing an early stage of the degenerative genome evolution after replacing the original Nardonella symbiont. A number of classic and recent studies have documented a variety of biological roles of the Sodalis symbiont for the grain weevils: at phenotypic levels, enhanced growth, survival, and fecundity (37,52,53), improved flight activity (52,54) and facilitated cuticular tanning and hardening (36,37,52); and at biochemical and metabolic levels, provisioning of B vitamins such as pantothenic acid, biotin, and riboflavin (55), supply of aromatic amino acids phenylalanine and tyrosine (36,37), metabolism of methionine and sarcosine (56,57), and involvement in mitochondrial energy metabolism (58,59). Our results strongly suggest that the tyrosine provisioning, which underpins the cuticle hardening and the fitness improvement, is the original essential role of the weevilbacterium endosymbiosis, and the other biological functions are likely acquired following the symbiont replacement from Nardonella to Sodalis in an ancestor of the grain weevils.…”

Section: Insights Into Symbiont Replacements and Diversification In Ementioning

confidence: 99%

Small genome symbiont underlies cuticle hardness in beetles

Anbutsu

Moriyama

Nikoh

et al. 2017

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

128

157

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Beetles, representing the majority of the insect species diversity, are characterized by thick and hard cuticle, which plays important roles for their environmental adaptation and underpins their inordinate diversity and prosperity. Here, we report a bacterial endosymbiont extremely specialized for sustaining beetle’s cuticle formation. Many weevils are associated with a γ-proteobacterial endosymbiont lineage Nardonella, whose evolutionary origin is estimated as older than 100 million years, but its functional aspect has been elusive. Sequencing of Nardonella genomes from diverse weevils unveiled drastic size reduction to 0.2 Mb, in which minimal complete gene sets for bacterial replication, transcription, and translation were present but almost all of the other metabolic pathway genes were missing. Notably, the only metabolic pathway retained in the Nardonella genomes was the tyrosine synthesis pathway, identifying tyrosine provisioning as Nardonella’s sole biological role. Weevils are armored with hard cuticle, tyrosine is the principal precursor for cuticle formation, and experimental suppression of Nardonella resulted in emergence of reddish and soft weevils with low tyrosine titer, confirming the importance of Nardonella-mediated tyrosine production for host’s cuticle formation and hardening. Notably, Nardonella’s tyrosine synthesis pathway was incomplete, lacking the final step transaminase gene. RNA sequencing identified host’s aminotransferase genes up-regulated in the bacteriome. RNA interference targeting the aminotransferase genes induced reddish and soft weevils with low tyrosine titer, verifying host’s final step regulation of the tyrosine synthesis pathway. Our finding highlights an impressively intimate and focused aspect of the host–symbiont metabolic integrity via streamlined evolution for a single biological function of ecological relevance.

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“…On one hand, they are clearly obligate mutualists, provisioning nutrients to their hosts (24,25), living exclusively within specialized host cells (bacteriocytes) and ovaries, and undergoing strict vertical transmission from mother to offspring (6). On the other hand, they lack many of the genomic hallmarks of very-long-term intimate endosymbionts (23), including a very small genome size (2), extreme AϩT richness (7), and an absence of IS elements (3).…”

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confidence: 99%