The Natural Antisense Transcript DONE40 Derived from the lncRNA ENOD40 Locus Interacts with SET Domain Protein ASHR3 During Inception of Symbiosis in Arachis hypogaea
The long noncoding RNA ENOD40 is required for cortical cell division during root nodule symbiosis (RNS) of legumes, though it is not essential for actinorhizal RNS. Our objective was to understand whether ENOD40 was required for aeschynomenoid nodule formation in Arachis hypogaea. AhENOD40 express f...
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| Format: | Article |
| Language: | English |
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The American Phytopathological Society
2021-09-01
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| Series: | Molecular Plant-Microbe Interactions |
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| Online Access: | https://apsjournals.apsnet.org/doi/10.1094/MPMI-12-20-0357-R |
| _version_ | 1819045905976786944 |
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| author | Pritha Ganguly Dipan Roy Troyee Das Anindya Kundu Fabienne Cartieaux Zhumur Ghosh Maitrayee DasGupta |
| author_facet | Pritha Ganguly Dipan Roy Troyee Das Anindya Kundu Fabienne Cartieaux Zhumur Ghosh Maitrayee DasGupta |
| author_sort | Pritha Ganguly |
| collection | DOAJ |
| description | The long noncoding RNA ENOD40 is required for cortical cell division during root nodule symbiosis (RNS) of legumes, though it is not essential for actinorhizal RNS. Our objective was to understand whether ENOD40 was required for aeschynomenoid nodule formation in Arachis hypogaea. AhENOD40 express from chromosome 5 (chr5) (AhENOD40-1) and chr15 (AhENOD40-2) during symbiosis, and RNA interference of these transcripts drastically affected nodulation, indicating the importance of ENOD40 in A. hypogaea. Furthermore, we demonstrated several distinct characteristics of ENOD40. (i) Natural antisense transcript (NAT) of ENOD40 was detected from the AhENOD40-1 locus (designated as NAT-AhDONE40). (ii) Both AhENOD40-1 and AhENOD40-2 had two exons, whereas NAT-AhDONE40 was monoexonic. Reverse-transcription quantitative PCR analysis indicated both sense and antisense transcripts to be present in both cytoplasm and nucleus, and their expression increased with the progress of symbiosis. (iii) RNA pull-down from whole cell extracts of infected roots at 4 days postinfection indicated NAT-AhDONE40 to interact with the SET (Su(var)3-9, enhancer of Zeste and Trithorax) domain containing absent small homeotic disc (ASH) family protein AhASHR3 and this interaction was further validated using RNA immunoprecipitation and electrophoretic mobility shift assay. (iv) Chromatin immunoprecipitation assays indicate deposition of ASHR3-specific histone marks H3K36me3 and H3K4me3 in both of the ENOD40 loci during the progress of symbiosis. ASHR3 is known for its role in optimizing cell proliferation and reprogramming. Because both ASHR3 and ENOD40 from legumes cluster away from those in actinorhizal plants and other nonlegumes in phylogenetic distance trees, we hypothesize that the interaction of DONE40 with ASHR3 could have evolved for adapting the nodule organogenesis program for legumes.[Graphic: see text] Copyright © 2021 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license. |
| first_indexed | 2024-12-21T10:36:00Z |
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| id | doaj.art-4c13897093004a96a1aac2f2d5ba5f7a |
| institution | Directory Open Access Journal |
| issn | 0894-0282 1943-7706 |
| language | English |
| last_indexed | 2024-12-21T10:36:00Z |
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| publisher | The American Phytopathological Society |
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| series | Molecular Plant-Microbe Interactions |
| spelling | doaj.art-4c13897093004a96a1aac2f2d5ba5f7a2022-12-21T19:07:04ZengThe American Phytopathological SocietyMolecular Plant-Microbe Interactions0894-02821943-77062021-09-013491057107010.1094/MPMI-12-20-0357-RThe Natural Antisense Transcript DONE40 Derived from the lncRNA ENOD40 Locus Interacts with SET Domain Protein ASHR3 During Inception of Symbiosis in Arachis hypogaeaPritha Ganguly0Dipan Roy1Troyee Das2Anindya Kundu3Fabienne Cartieaux4Zhumur Ghosh5Maitrayee DasGupta6Department of Biochemistry, University of Calcutta, Kolkata, West Bengal, 700019, IndiaDepartment of Biochemistry, University of Calcutta, Kolkata, West Bengal, 700019, IndiaDivision of Bioinformatics, Bose Institute, Kolkata, West Bengal, 700054, IndiaDepartment of Biochemistry, University of Calcutta, Kolkata, West Bengal, 700019, IndiaLSTM, Université de Montpellier, CIRAD, INRA, IRD, SupAgro, Montpellier, FranceDivision of Bioinformatics, Bose Institute, Kolkata, West Bengal, 700054, IndiaDepartment of Biochemistry, University of Calcutta, Kolkata, West Bengal, 700019, IndiaThe long noncoding RNA ENOD40 is required for cortical cell division during root nodule symbiosis (RNS) of legumes, though it is not essential for actinorhizal RNS. Our objective was to understand whether ENOD40 was required for aeschynomenoid nodule formation in Arachis hypogaea. AhENOD40 express from chromosome 5 (chr5) (AhENOD40-1) and chr15 (AhENOD40-2) during symbiosis, and RNA interference of these transcripts drastically affected nodulation, indicating the importance of ENOD40 in A. hypogaea. Furthermore, we demonstrated several distinct characteristics of ENOD40. (i) Natural antisense transcript (NAT) of ENOD40 was detected from the AhENOD40-1 locus (designated as NAT-AhDONE40). (ii) Both AhENOD40-1 and AhENOD40-2 had two exons, whereas NAT-AhDONE40 was monoexonic. Reverse-transcription quantitative PCR analysis indicated both sense and antisense transcripts to be present in both cytoplasm and nucleus, and their expression increased with the progress of symbiosis. (iii) RNA pull-down from whole cell extracts of infected roots at 4 days postinfection indicated NAT-AhDONE40 to interact with the SET (Su(var)3-9, enhancer of Zeste and Trithorax) domain containing absent small homeotic disc (ASH) family protein AhASHR3 and this interaction was further validated using RNA immunoprecipitation and electrophoretic mobility shift assay. (iv) Chromatin immunoprecipitation assays indicate deposition of ASHR3-specific histone marks H3K36me3 and H3K4me3 in both of the ENOD40 loci during the progress of symbiosis. ASHR3 is known for its role in optimizing cell proliferation and reprogramming. Because both ASHR3 and ENOD40 from legumes cluster away from those in actinorhizal plants and other nonlegumes in phylogenetic distance trees, we hypothesize that the interaction of DONE40 with ASHR3 could have evolved for adapting the nodule organogenesis program for legumes.[Graphic: see text] Copyright © 2021 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.https://apsjournals.apsnet.org/doi/10.1094/MPMI-12-20-0357-RENOD40DONE40ASHR3long noncoding RNAnatural antisense transcriptroot nodule symbiosis |
| spellingShingle | Pritha Ganguly Dipan Roy Troyee Das Anindya Kundu Fabienne Cartieaux Zhumur Ghosh Maitrayee DasGupta The Natural Antisense Transcript DONE40 Derived from the lncRNA ENOD40 Locus Interacts with SET Domain Protein ASHR3 During Inception of Symbiosis in Arachis hypogaea Molecular Plant-Microbe Interactions ENOD40 DONE40 ASHR3 long noncoding RNA natural antisense transcript root nodule symbiosis |
| title | The Natural Antisense Transcript DONE40 Derived from the lncRNA ENOD40 Locus Interacts with SET Domain Protein ASHR3 During Inception of Symbiosis in Arachis hypogaea |
| title_full | The Natural Antisense Transcript DONE40 Derived from the lncRNA ENOD40 Locus Interacts with SET Domain Protein ASHR3 During Inception of Symbiosis in Arachis hypogaea |
| title_fullStr | The Natural Antisense Transcript DONE40 Derived from the lncRNA ENOD40 Locus Interacts with SET Domain Protein ASHR3 During Inception of Symbiosis in Arachis hypogaea |
| title_full_unstemmed | The Natural Antisense Transcript DONE40 Derived from the lncRNA ENOD40 Locus Interacts with SET Domain Protein ASHR3 During Inception of Symbiosis in Arachis hypogaea |
| title_short | The Natural Antisense Transcript DONE40 Derived from the lncRNA ENOD40 Locus Interacts with SET Domain Protein ASHR3 During Inception of Symbiosis in Arachis hypogaea |
| title_sort | natural antisense transcript done40 derived from the lncrna enod40 locus interacts with set domain protein ashr3 during inception of symbiosis in arachis hypogaea |
| topic | ENOD40 DONE40 ASHR3 long noncoding RNA natural antisense transcript root nodule symbiosis |
| url | https://apsjournals.apsnet.org/doi/10.1094/MPMI-12-20-0357-R |
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