Changes in Aphid Host Plant Diet Influence the Small-RNA Expression Profiles of Its Obligate Nutritional Symbiont, <italic toggle="yes">Buchnera</italic>

ABSTRACT Plants are a difficult food resource to use, and herbivorous insects have evolved a variety of mechanisms that allow them to fully exploit this poor nutritional resource. One such mechanism is the maintenance of bacterial symbionts that aid in host plant feeding and development. The majorit...

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Autores principales: Margaret W. Thairu, Allison K. Hansen
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Publicado: American Society for Microbiology 2019
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spelling oai:doaj.org-article:55777453cb9a43d1bc809e2747adcac22021-11-15T15:54:46ZChanges in Aphid Host Plant Diet Influence the Small-RNA Expression Profiles of Its Obligate Nutritional Symbiont, <italic toggle="yes">Buchnera</italic>10.1128/mBio.01733-192150-7511https://doaj.org/article/55777453cb9a43d1bc809e2747adcac22019-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01733-19https://doaj.org/toc/2150-7511ABSTRACT Plants are a difficult food resource to use, and herbivorous insects have evolved a variety of mechanisms that allow them to fully exploit this poor nutritional resource. One such mechanism is the maintenance of bacterial symbionts that aid in host plant feeding and development. The majority of these intracellular symbionts have highly eroded genomes that lack many key regulatory genes; consequently, it is unclear if these symbionts can respond to changes in the insect’s diet to facilitate host plant use. There is emerging evidence that symbionts with highly eroded genomes express small RNAs (sRNAs), some of which potentially regulate gene expression. In this study, we sought to determine if the reduced genome of the nutritional symbiont (Buchnera) in the pea aphid responds to changes in the aphid’s host plant diet. Using transcriptome sequencing (RNA-seq), Buchnera sRNA expression profiles were characterized within two Buchnera life stages when pea aphids fed on either alfalfa or fava bean. Overall, this study demonstrates that Buchnera sRNA expression changes not only with life stage but also with changes in aphid host plant diet. Of the 321 sRNAs characterized in this study, 47% were previously identified and 22% showed evidence of conservation in two or more Buchnera taxa. Functionally, 13 differentially expressed sRNAs were predicted to target genes related to pathways involved in essential amino acid biosynthesis. Overall, results from this study reveal that host plant diet influences the expression of conserved and lineage-specific sRNAs in Buchnera and that these sRNAs display distinct host plant-specific expression profiles among biological replicates. IMPORTANCE In general, the genomes of intracellular bacterial symbionts are reduced compared to those of free-living relatives and lack many key regulatory genes. Many of these reduced genomes belong to obligate mutualists of insects that feed on a diet that is deficient in essential nutrients, such as essential amino acids. It is unclear if these symbionts respond with their host to changes in insect diet, because of their reduced regulatory capacity. Emerging evidence suggests that these symbionts express small RNAs (sRNAs) that regulate gene expression at the posttranscriptional level. Therefore, in this study, we sought to determine if the reduced genome of the nutritional symbiont Buchnera in the pea aphid responds to changes in the aphid’s host plant diet. This study demonstrates for the first time that Buchnera sRNAs, some conserved in two or more Buchnera lineages, are differentially expressed when aphids feed on different plant species and potentially target genes within essential amino acid biosynthesis pathways.Margaret W. ThairuAllison K. HansenAmerican Society for MicrobiologyarticlesRNAAcyrthosiphon pisumBuchneraregulationpea aphidreduced genomeMicrobiologyQR1-502ENmBio, Vol 10, Iss 6 (2019)
institution DOAJ
collection DOAJ
language EN
topic sRNA
Acyrthosiphon pisum
Buchnera
regulation
pea aphid
reduced genome
Microbiology
QR1-502
spellingShingle sRNA
Acyrthosiphon pisum
Buchnera
regulation
pea aphid
reduced genome
Microbiology
QR1-502
Margaret W. Thairu
Allison K. Hansen
Changes in Aphid Host Plant Diet Influence the Small-RNA Expression Profiles of Its Obligate Nutritional Symbiont, <italic toggle="yes">Buchnera</italic>
description ABSTRACT Plants are a difficult food resource to use, and herbivorous insects have evolved a variety of mechanisms that allow them to fully exploit this poor nutritional resource. One such mechanism is the maintenance of bacterial symbionts that aid in host plant feeding and development. The majority of these intracellular symbionts have highly eroded genomes that lack many key regulatory genes; consequently, it is unclear if these symbionts can respond to changes in the insect’s diet to facilitate host plant use. There is emerging evidence that symbionts with highly eroded genomes express small RNAs (sRNAs), some of which potentially regulate gene expression. In this study, we sought to determine if the reduced genome of the nutritional symbiont (Buchnera) in the pea aphid responds to changes in the aphid’s host plant diet. Using transcriptome sequencing (RNA-seq), Buchnera sRNA expression profiles were characterized within two Buchnera life stages when pea aphids fed on either alfalfa or fava bean. Overall, this study demonstrates that Buchnera sRNA expression changes not only with life stage but also with changes in aphid host plant diet. Of the 321 sRNAs characterized in this study, 47% were previously identified and 22% showed evidence of conservation in two or more Buchnera taxa. Functionally, 13 differentially expressed sRNAs were predicted to target genes related to pathways involved in essential amino acid biosynthesis. Overall, results from this study reveal that host plant diet influences the expression of conserved and lineage-specific sRNAs in Buchnera and that these sRNAs display distinct host plant-specific expression profiles among biological replicates. IMPORTANCE In general, the genomes of intracellular bacterial symbionts are reduced compared to those of free-living relatives and lack many key regulatory genes. Many of these reduced genomes belong to obligate mutualists of insects that feed on a diet that is deficient in essential nutrients, such as essential amino acids. It is unclear if these symbionts respond with their host to changes in insect diet, because of their reduced regulatory capacity. Emerging evidence suggests that these symbionts express small RNAs (sRNAs) that regulate gene expression at the posttranscriptional level. Therefore, in this study, we sought to determine if the reduced genome of the nutritional symbiont Buchnera in the pea aphid responds to changes in the aphid’s host plant diet. This study demonstrates for the first time that Buchnera sRNAs, some conserved in two or more Buchnera lineages, are differentially expressed when aphids feed on different plant species and potentially target genes within essential amino acid biosynthesis pathways.
format article
author Margaret W. Thairu
Allison K. Hansen
author_facet Margaret W. Thairu
Allison K. Hansen
author_sort Margaret W. Thairu
title Changes in Aphid Host Plant Diet Influence the Small-RNA Expression Profiles of Its Obligate Nutritional Symbiont, <italic toggle="yes">Buchnera</italic>
title_short Changes in Aphid Host Plant Diet Influence the Small-RNA Expression Profiles of Its Obligate Nutritional Symbiont, <italic toggle="yes">Buchnera</italic>
title_full Changes in Aphid Host Plant Diet Influence the Small-RNA Expression Profiles of Its Obligate Nutritional Symbiont, <italic toggle="yes">Buchnera</italic>
title_fullStr Changes in Aphid Host Plant Diet Influence the Small-RNA Expression Profiles of Its Obligate Nutritional Symbiont, <italic toggle="yes">Buchnera</italic>
title_full_unstemmed Changes in Aphid Host Plant Diet Influence the Small-RNA Expression Profiles of Its Obligate Nutritional Symbiont, <italic toggle="yes">Buchnera</italic>
title_sort changes in aphid host plant diet influence the small-rna expression profiles of its obligate nutritional symbiont, <italic toggle="yes">buchnera</italic>
publisher American Society for Microbiology
publishDate 2019
url https://doaj.org/article/55777453cb9a43d1bc809e2747adcac2
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