Microbiome responses during virulence adaptation by a phloem‐feeding insect to resistant near‐isogenic rice lines

Abstract The microbiomes of phloem‐feeding insects include functional bacteria and yeasts essential for herbivore survival and development. Changes in microbiome composition are implicated in virulence adaptation by herbivores to host plant species or host populations (including crop varieties). We...

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Main Authors: Finbarr G. Horgan, Thanga Suja Srinivasan, Eduardo Crisol‐Martínez, Maria Liberty P. Almazan, Angelee Fame Ramal, Ricardo Oliva, Ian L. Quibod, Carmencita C. Bernal
Format: Article
Language:English
Published: Wiley 2019-10-01
Series:Ecology and Evolution
Subjects:
Online Access:https://doi.org/10.1002/ece3.5699
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spelling doaj-b49d272535dd48af9752234ad23f00fa2021-03-02T07:45:09ZengWileyEcology and Evolution2045-77582019-10-01920119111192910.1002/ece3.5699Microbiome responses during virulence adaptation by a phloem‐feeding insect to resistant near‐isogenic rice linesFinbarr G. Horgan0Thanga Suja Srinivasan1Eduardo Crisol‐Martínez2Maria Liberty P. Almazan3Angelee Fame Ramal4Ricardo Oliva5Ian L. Quibod6Carmencita C. Bernal7EcoLaVerna Integral Restoration Ecology Kildinan IrelandCentre for Plant Molecular Biology and Biotechnology Tamil Nadu Agricultural University Coimbatore IndiaEcoLaVerna Integral Restoration Ecology Kildinan IrelandInternational Rice Research Institute Metro Manila PhilippinesSchool of Environmental Science and Management University of the Philippines Los Baños PhilippinesInternational Rice Research Institute Metro Manila PhilippinesInternational Rice Research Institute Metro Manila PhilippinesInternational Rice Research Institute Metro Manila PhilippinesAbstract The microbiomes of phloem‐feeding insects include functional bacteria and yeasts essential for herbivore survival and development. Changes in microbiome composition are implicated in virulence adaptation by herbivores to host plant species or host populations (including crop varieties). We examined patterns in adaptation by the green leafhopper, Nephotettix virescens, to near‐isogenic rice lines (NILs) with one or two resistance genes and the recurrent parent T65, without resistance genes. Only the line with two resistance genes was effective in reducing leafhopper fitness. After 20 generations on the resistant line, selected leafhoppers attained similar survival, weight gain, and egg laying to leafhoppers that were continually reared on the susceptible recurrent parent, indicating that they had adapted to the resistant host. By sequencing the 16s rRNA gene, we described the microbiome of leafhoppers from colonies associated with five collection sites, and continually reared or switched between NILs. The microbiomes included 69–119 OTUs of which 44 occurred in ≥90% of samples. Of these, 14 OTUs were assigned to the obligate symbiont Candidatus sulcia clade. After 20 generations of selection, collection site had a greater effect than host plant on microbiome composition. Six bacteria genera, including C. sulcia, were associated with leafhopper virulence. However, there was significant within‐treatment, site‐related variability in the prevalence of these taxa such that the mechanisms underlying their association with virulence remain to be determined. Our results imply that these taxa are associated with leafhopper nutrition. Ours is the first study to describe microbiome diversity and composition in rice leafhoppers. We discuss our results in light of the multiple functions of herbivore microbiomes during virulence adaptation in insect herbivores.https://doi.org/10.1002/ece3.5699detoxificationhost plant resistancemutualismNilaparvata lugensvirulence adaptationyeast‐like symbionts
collection DOAJ
language English
format Article
sources DOAJ
author Finbarr G. Horgan
Thanga Suja Srinivasan
Eduardo Crisol‐Martínez
Maria Liberty P. Almazan
Angelee Fame Ramal
Ricardo Oliva
Ian L. Quibod
Carmencita C. Bernal
spellingShingle Finbarr G. Horgan
Thanga Suja Srinivasan
Eduardo Crisol‐Martínez
Maria Liberty P. Almazan
Angelee Fame Ramal
Ricardo Oliva
Ian L. Quibod
Carmencita C. Bernal
Microbiome responses during virulence adaptation by a phloem‐feeding insect to resistant near‐isogenic rice lines
Ecology and Evolution
detoxification
host plant resistance
mutualism
Nilaparvata lugens
virulence adaptation
yeast‐like symbionts
author_facet Finbarr G. Horgan
Thanga Suja Srinivasan
Eduardo Crisol‐Martínez
Maria Liberty P. Almazan
Angelee Fame Ramal
Ricardo Oliva
Ian L. Quibod
Carmencita C. Bernal
author_sort Finbarr G. Horgan
title Microbiome responses during virulence adaptation by a phloem‐feeding insect to resistant near‐isogenic rice lines
title_short Microbiome responses during virulence adaptation by a phloem‐feeding insect to resistant near‐isogenic rice lines
title_full Microbiome responses during virulence adaptation by a phloem‐feeding insect to resistant near‐isogenic rice lines
title_fullStr Microbiome responses during virulence adaptation by a phloem‐feeding insect to resistant near‐isogenic rice lines
title_full_unstemmed Microbiome responses during virulence adaptation by a phloem‐feeding insect to resistant near‐isogenic rice lines
title_sort microbiome responses during virulence adaptation by a phloem‐feeding insect to resistant near‐isogenic rice lines
publisher Wiley
series Ecology and Evolution
issn 2045-7758
publishDate 2019-10-01
description Abstract The microbiomes of phloem‐feeding insects include functional bacteria and yeasts essential for herbivore survival and development. Changes in microbiome composition are implicated in virulence adaptation by herbivores to host plant species or host populations (including crop varieties). We examined patterns in adaptation by the green leafhopper, Nephotettix virescens, to near‐isogenic rice lines (NILs) with one or two resistance genes and the recurrent parent T65, without resistance genes. Only the line with two resistance genes was effective in reducing leafhopper fitness. After 20 generations on the resistant line, selected leafhoppers attained similar survival, weight gain, and egg laying to leafhoppers that were continually reared on the susceptible recurrent parent, indicating that they had adapted to the resistant host. By sequencing the 16s rRNA gene, we described the microbiome of leafhoppers from colonies associated with five collection sites, and continually reared or switched between NILs. The microbiomes included 69–119 OTUs of which 44 occurred in ≥90% of samples. Of these, 14 OTUs were assigned to the obligate symbiont Candidatus sulcia clade. After 20 generations of selection, collection site had a greater effect than host plant on microbiome composition. Six bacteria genera, including C. sulcia, were associated with leafhopper virulence. However, there was significant within‐treatment, site‐related variability in the prevalence of these taxa such that the mechanisms underlying their association with virulence remain to be determined. Our results imply that these taxa are associated with leafhopper nutrition. Ours is the first study to describe microbiome diversity and composition in rice leafhoppers. We discuss our results in light of the multiple functions of herbivore microbiomes during virulence adaptation in insect herbivores.
topic detoxification
host plant resistance
mutualism
Nilaparvata lugens
virulence adaptation
yeast‐like symbionts
url https://doi.org/10.1002/ece3.5699
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