Cargando…

Feeding on resistant rice leads to enhanced expression of defender against apoptotic cell death (OoDAD1) in the Asian rice gall midge

BACKGROUND: The Asian rice gall midge (Orseolia oryzae) is a destructive insect pest of rice. Gall midge infestation in rice triggers either compatible or incompatible interactions leading to survival or mortality of the feeding maggots, respectively. In incompatible interactions, generation of plan...

Descripción completa

Detalles Bibliográficos
Autores principales: Sinha, Deepak K., Atray, Isha, Bentur, JS, Nair, Suresh
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4591563/
https://www.ncbi.nlm.nih.gov/pubmed/26428861
http://dx.doi.org/10.1186/s12870-015-0618-y
_version_ 1782393093551554560
author Sinha, Deepak K.
Atray, Isha
Bentur, JS
Nair, Suresh
author_facet Sinha, Deepak K.
Atray, Isha
Bentur, JS
Nair, Suresh
author_sort Sinha, Deepak K.
collection PubMed
description BACKGROUND: The Asian rice gall midge (Orseolia oryzae) is a destructive insect pest of rice. Gall midge infestation in rice triggers either compatible or incompatible interactions leading to survival or mortality of the feeding maggots, respectively. In incompatible interactions, generation of plant allelochemicals/defense molecules and/or inability of the maggots to continue feeding on the host initiate(s) apoptosis within the maggots. Unraveling these molecular events, triggered within the maggots as a response to feeding on resistant hosts, will enable us to obtain a better understanding of host resistance. The present study points towards the likely involvement of a defender against apoptotic cell death gene (DAD1) in the insect in response to the host defense. RESULTS: The cDNA coding for the DAD1 orthologue in the rice gall midge (OoDAD1) consisted of 339 nucleotides with one intron of 85 bp and two exons of 208 and 131 nucleotides. The deduced amino acid sequence of OoDAD1 showed a high degree of homology (94.6 %) with DAD1 orthologue from the Hessian fly (Mayetiola destructor) —a major dipteran pest of wheat. Southern hybridization analysis indicated that OoDAD1 was present as a single copy in the genomes of the Asian rice gall midge biotypes (GMB) 1, 4 and 4 M. In the interactions involving GMB4 with Jaya (susceptible rice host) the expression level of OoDAD1 in feeding maggots gradually increased to 3-fold at 96hai (hours after infestation) and peaked to 3.5-fold at 96hai when compared to that at 24 hai. In contrast, expression in maggots feeding on RP2068 (resistant host) showed a steep increase of more than 8-fold at 24hai and this level was sustained at 48, 72 and 96hai when compared with the level in maggots feeding on Jaya at 24hai. Recombinant OoDAD1, expressed in E. coli cells, when injected into rice seedlings induced a hypersensitive response (HR) in the resistant rice host, RP2068, but not in the susceptible rice variety, Jaya. CONCLUSIONS: The results indicate that the expression of OoDAD1 is triggered in the feeding maggots probably due to the host resistance response and therefore, is likely an important molecule in the initial stages of the interaction between the midge and its rice host. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-015-0618-y) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-4591563
institution National Center for Biotechnology Information
language English
publishDate 2015
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-45915632015-10-03 Feeding on resistant rice leads to enhanced expression of defender against apoptotic cell death (OoDAD1) in the Asian rice gall midge Sinha, Deepak K. Atray, Isha Bentur, JS Nair, Suresh BMC Plant Biol Research Article BACKGROUND: The Asian rice gall midge (Orseolia oryzae) is a destructive insect pest of rice. Gall midge infestation in rice triggers either compatible or incompatible interactions leading to survival or mortality of the feeding maggots, respectively. In incompatible interactions, generation of plant allelochemicals/defense molecules and/or inability of the maggots to continue feeding on the host initiate(s) apoptosis within the maggots. Unraveling these molecular events, triggered within the maggots as a response to feeding on resistant hosts, will enable us to obtain a better understanding of host resistance. The present study points towards the likely involvement of a defender against apoptotic cell death gene (DAD1) in the insect in response to the host defense. RESULTS: The cDNA coding for the DAD1 orthologue in the rice gall midge (OoDAD1) consisted of 339 nucleotides with one intron of 85 bp and two exons of 208 and 131 nucleotides. The deduced amino acid sequence of OoDAD1 showed a high degree of homology (94.6 %) with DAD1 orthologue from the Hessian fly (Mayetiola destructor) —a major dipteran pest of wheat. Southern hybridization analysis indicated that OoDAD1 was present as a single copy in the genomes of the Asian rice gall midge biotypes (GMB) 1, 4 and 4 M. In the interactions involving GMB4 with Jaya (susceptible rice host) the expression level of OoDAD1 in feeding maggots gradually increased to 3-fold at 96hai (hours after infestation) and peaked to 3.5-fold at 96hai when compared to that at 24 hai. In contrast, expression in maggots feeding on RP2068 (resistant host) showed a steep increase of more than 8-fold at 24hai and this level was sustained at 48, 72 and 96hai when compared with the level in maggots feeding on Jaya at 24hai. Recombinant OoDAD1, expressed in E. coli cells, when injected into rice seedlings induced a hypersensitive response (HR) in the resistant rice host, RP2068, but not in the susceptible rice variety, Jaya. CONCLUSIONS: The results indicate that the expression of OoDAD1 is triggered in the feeding maggots probably due to the host resistance response and therefore, is likely an important molecule in the initial stages of the interaction between the midge and its rice host. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-015-0618-y) contains supplementary material, which is available to authorized users. BioMed Central 2015-10-01 /pmc/articles/PMC4591563/ /pubmed/26428861 http://dx.doi.org/10.1186/s12870-015-0618-y Text en © Sinha et al. 2015 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Sinha, Deepak K.
Atray, Isha
Bentur, JS
Nair, Suresh
Feeding on resistant rice leads to enhanced expression of defender against apoptotic cell death (OoDAD1) in the Asian rice gall midge
title Feeding on resistant rice leads to enhanced expression of defender against apoptotic cell death (OoDAD1) in the Asian rice gall midge
title_full Feeding on resistant rice leads to enhanced expression of defender against apoptotic cell death (OoDAD1) in the Asian rice gall midge
title_fullStr Feeding on resistant rice leads to enhanced expression of defender against apoptotic cell death (OoDAD1) in the Asian rice gall midge
title_full_unstemmed Feeding on resistant rice leads to enhanced expression of defender against apoptotic cell death (OoDAD1) in the Asian rice gall midge
title_short Feeding on resistant rice leads to enhanced expression of defender against apoptotic cell death (OoDAD1) in the Asian rice gall midge
title_sort feeding on resistant rice leads to enhanced expression of defender against apoptotic cell death (oodad1) in the asian rice gall midge
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4591563/
https://www.ncbi.nlm.nih.gov/pubmed/26428861
http://dx.doi.org/10.1186/s12870-015-0618-y
work_keys_str_mv AT sinhadeepakk feedingonresistantriceleadstoenhancedexpressionofdefenderagainstapoptoticcelldeathoodad1intheasianricegallmidge
AT atrayisha feedingonresistantriceleadstoenhancedexpressionofdefenderagainstapoptoticcelldeathoodad1intheasianricegallmidge
AT benturjs feedingonresistantriceleadstoenhancedexpressionofdefenderagainstapoptoticcelldeathoodad1intheasianricegallmidge
AT nairsuresh feedingonresistantriceleadstoenhancedexpressionofdefenderagainstapoptoticcelldeathoodad1intheasianricegallmidge