Argonaute5 and its associated small RNAs modulate the transcriptional response during the rhizobia-Phaseolus vulgaris symbiosis
Both plant- and rhizobia-derived small RNAs play an essential role in regulating the root nodule symbiosis in legumes. Small RNAs, in association with Argonaute proteins, tune the expression of genes participating in nodule development and rhizobial infection. However, the role of Argonaute proteins...
| Main Authors: | , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2022-11-01
|
| Series: | Frontiers in Plant Science |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fpls.2022.1034419/full |
| _version_ | 1811307357673619456 |
|---|---|
| author | María del Socorro Sánchez-Correa Mariel C. Isidra-Arellano Eithan A. Pozas-Rodríguez María del Rocío Reyero-Saavedra Alfredo Morales-Salazar Sarah Melissa Lugo-Caro del Castillo Alejandro Sanchez-Flores Verónica Jiménez-Jacinto Jose L. Reyes Damien Formey Oswaldo Valdés-López |
| author_facet | María del Socorro Sánchez-Correa Mariel C. Isidra-Arellano Eithan A. Pozas-Rodríguez María del Rocío Reyero-Saavedra Alfredo Morales-Salazar Sarah Melissa Lugo-Caro del Castillo Alejandro Sanchez-Flores Verónica Jiménez-Jacinto Jose L. Reyes Damien Formey Oswaldo Valdés-López |
| author_sort | María del Socorro Sánchez-Correa |
| collection | DOAJ |
| description | Both plant- and rhizobia-derived small RNAs play an essential role in regulating the root nodule symbiosis in legumes. Small RNAs, in association with Argonaute proteins, tune the expression of genes participating in nodule development and rhizobial infection. However, the role of Argonaute proteins in this symbiosis has been overlooked. In this study, we provide transcriptional evidence showing that Argonaute5 (AGO5) is a determinant genetic component in the root nodule symbiosis in Phaseolus vulgaris. A spatio-temporal transcriptional analysis revealed that the promoter of PvAGO5 is active in lateral root primordia, root hairs from rhizobia-inoculated roots, nodule primordia, and mature nodules. Transcriptional analysis by RNA sequencing revealed that gene silencing of PvAGO5 affected the expression of genes involved in the biosynthesis of the cell wall and phytohormones participating in the rhizobial infection process and nodule development. PvAGO5 immunoprecipitation coupled to small RNA sequencing revealed the small RNAs bound to PvAGO5 during the root nodule symbiosis. Identification of small RNAs associated to PvAGO5 revealed miRNAs previously known to participate in this symbiotic process, further supporting a role for AGO5 in this process. Overall, the data presented shed light on the roles that PvAGO5 plays during the root nodule symbiosis in P. vulgaris. |
| first_indexed | 2024-04-13T09:02:59Z |
| format | Article |
| id | doaj.art-258ced150a604f09b0779f7102c8e7b9 |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-04-13T09:02:59Z |
| publishDate | 2022-11-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-258ced150a604f09b0779f7102c8e7b92022-12-22T02:53:03ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-11-011310.3389/fpls.2022.10344191034419Argonaute5 and its associated small RNAs modulate the transcriptional response during the rhizobia-Phaseolus vulgaris symbiosisMaría del Socorro Sánchez-Correa0Mariel C. Isidra-Arellano1Eithan A. Pozas-Rodríguez2María del Rocío Reyero-Saavedra3Alfredo Morales-Salazar4Sarah Melissa Lugo-Caro del Castillo5Alejandro Sanchez-Flores6Verónica Jiménez-Jacinto7Jose L. Reyes8Damien Formey9Oswaldo Valdés-López10Laboratorio de Genómica Funcional de Leguminosas, Facultad de Estudios Superiores Iztacala, Universidad Nacional Autónoma de México, Tlalnepantla, Estado de México, MexicoLaboratorio de Genómica Funcional de Leguminosas, Facultad de Estudios Superiores Iztacala, Universidad Nacional Autónoma de México, Tlalnepantla, Estado de México, MexicoLaboratorio de Genómica Funcional de Leguminosas, Facultad de Estudios Superiores Iztacala, Universidad Nacional Autónoma de México, Tlalnepantla, Estado de México, MexicoLaboratorio de Genómica Funcional de Leguminosas, Facultad de Estudios Superiores Iztacala, Universidad Nacional Autónoma de México, Tlalnepantla, Estado de México, MexicoLaboratorio de Genómica Funcional de Leguminosas, Facultad de Estudios Superiores Iztacala, Universidad Nacional Autónoma de México, Tlalnepantla, Estado de México, MexicoCentro de Ciencias Genómicas, Universidad Nacional Autónoma de México, Cuernavaca, Morelos, MexicoUnidad Universitaria de Secuenciación Masiva y Bioinformática, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca, Morelos, MexicoUnidad Universitaria de Secuenciación Masiva y Bioinformática, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca, Morelos, MexicoDepartamento de Biología Molecular de Plantas, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca, Morelos, MexicoCentro de Ciencias Genómicas, Universidad Nacional Autónoma de México, Cuernavaca, Morelos, MexicoLaboratorio de Genómica Funcional de Leguminosas, Facultad de Estudios Superiores Iztacala, Universidad Nacional Autónoma de México, Tlalnepantla, Estado de México, MexicoBoth plant- and rhizobia-derived small RNAs play an essential role in regulating the root nodule symbiosis in legumes. Small RNAs, in association with Argonaute proteins, tune the expression of genes participating in nodule development and rhizobial infection. However, the role of Argonaute proteins in this symbiosis has been overlooked. In this study, we provide transcriptional evidence showing that Argonaute5 (AGO5) is a determinant genetic component in the root nodule symbiosis in Phaseolus vulgaris. A spatio-temporal transcriptional analysis revealed that the promoter of PvAGO5 is active in lateral root primordia, root hairs from rhizobia-inoculated roots, nodule primordia, and mature nodules. Transcriptional analysis by RNA sequencing revealed that gene silencing of PvAGO5 affected the expression of genes involved in the biosynthesis of the cell wall and phytohormones participating in the rhizobial infection process and nodule development. PvAGO5 immunoprecipitation coupled to small RNA sequencing revealed the small RNAs bound to PvAGO5 during the root nodule symbiosis. Identification of small RNAs associated to PvAGO5 revealed miRNAs previously known to participate in this symbiotic process, further supporting a role for AGO5 in this process. Overall, the data presented shed light on the roles that PvAGO5 plays during the root nodule symbiosis in P. vulgaris.https://www.frontiersin.org/articles/10.3389/fpls.2022.1034419/fullargonaute proteinsmicroRNAsrhizobial tRNA-derived sRNA fragmentsroot nodule symbiosislegumes |
| spellingShingle | María del Socorro Sánchez-Correa Mariel C. Isidra-Arellano Eithan A. Pozas-Rodríguez María del Rocío Reyero-Saavedra Alfredo Morales-Salazar Sarah Melissa Lugo-Caro del Castillo Alejandro Sanchez-Flores Verónica Jiménez-Jacinto Jose L. Reyes Damien Formey Oswaldo Valdés-López Argonaute5 and its associated small RNAs modulate the transcriptional response during the rhizobia-Phaseolus vulgaris symbiosis Frontiers in Plant Science argonaute proteins microRNAs rhizobial tRNA-derived sRNA fragments root nodule symbiosis legumes |
| title | Argonaute5 and its associated small RNAs modulate the transcriptional response during the rhizobia-Phaseolus vulgaris symbiosis |
| title_full | Argonaute5 and its associated small RNAs modulate the transcriptional response during the rhizobia-Phaseolus vulgaris symbiosis |
| title_fullStr | Argonaute5 and its associated small RNAs modulate the transcriptional response during the rhizobia-Phaseolus vulgaris symbiosis |
| title_full_unstemmed | Argonaute5 and its associated small RNAs modulate the transcriptional response during the rhizobia-Phaseolus vulgaris symbiosis |
| title_short | Argonaute5 and its associated small RNAs modulate the transcriptional response during the rhizobia-Phaseolus vulgaris symbiosis |
| title_sort | argonaute5 and its associated small rnas modulate the transcriptional response during the rhizobia phaseolus vulgaris symbiosis |
| topic | argonaute proteins microRNAs rhizobial tRNA-derived sRNA fragments root nodule symbiosis legumes |
| url | https://www.frontiersin.org/articles/10.3389/fpls.2022.1034419/full |
| work_keys_str_mv | AT mariadelsocorrosanchezcorrea argonaute5anditsassociatedsmallrnasmodulatethetranscriptionalresponseduringtherhizobiaphaseolusvulgarissymbiosis AT marielcisidraarellano argonaute5anditsassociatedsmallrnasmodulatethetranscriptionalresponseduringtherhizobiaphaseolusvulgarissymbiosis AT eithanapozasrodriguez argonaute5anditsassociatedsmallrnasmodulatethetranscriptionalresponseduringtherhizobiaphaseolusvulgarissymbiosis AT mariadelrocioreyerosaavedra argonaute5anditsassociatedsmallrnasmodulatethetranscriptionalresponseduringtherhizobiaphaseolusvulgarissymbiosis AT alfredomoralessalazar argonaute5anditsassociatedsmallrnasmodulatethetranscriptionalresponseduringtherhizobiaphaseolusvulgarissymbiosis AT sarahmelissalugocarodelcastillo argonaute5anditsassociatedsmallrnasmodulatethetranscriptionalresponseduringtherhizobiaphaseolusvulgarissymbiosis AT alejandrosanchezflores argonaute5anditsassociatedsmallrnasmodulatethetranscriptionalresponseduringtherhizobiaphaseolusvulgarissymbiosis AT veronicajimenezjacinto argonaute5anditsassociatedsmallrnasmodulatethetranscriptionalresponseduringtherhizobiaphaseolusvulgarissymbiosis AT joselreyes argonaute5anditsassociatedsmallrnasmodulatethetranscriptionalresponseduringtherhizobiaphaseolusvulgarissymbiosis AT damienformey argonaute5anditsassociatedsmallrnasmodulatethetranscriptionalresponseduringtherhizobiaphaseolusvulgarissymbiosis AT oswaldovaldeslopez argonaute5anditsassociatedsmallrnasmodulatethetranscriptionalresponseduringtherhizobiaphaseolusvulgarissymbiosis |