Dicer-like proteins influence Arabidopsis root microbiota independent of RNA-directed DNA methylation
Abstract Background Plants are naturally associated with root microbiota, which are microbial communities influential to host fitness. Thus, it is important to understand how plants control root microbiota. Epigenetic factors regulate the readouts of genetic information and consequently many essenti...
| Main Authors: | , , , , , , , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2021-02-01
|
| Series: | Microbiome |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s40168-020-00966-y |
| _version_ | 1818336866923970560 |
|---|---|
| author | Richa Kaushal Li Peng Sunil K. Singh Mengrui Zhang Xinlian Zhang Juan I. Vílchez Zhen Wang Danxia He Yu Yang Suhui Lv Zhongtian Xu Rafael J. L. Morcillo Wei Wang Weichang Huang Paul W. Paré Chun-Peng Song Jian-Kang Zhu Renyi Liu Wenxuan Zhong Ping Ma Huiming Zhang |
| author_facet | Richa Kaushal Li Peng Sunil K. Singh Mengrui Zhang Xinlian Zhang Juan I. Vílchez Zhen Wang Danxia He Yu Yang Suhui Lv Zhongtian Xu Rafael J. L. Morcillo Wei Wang Weichang Huang Paul W. Paré Chun-Peng Song Jian-Kang Zhu Renyi Liu Wenxuan Zhong Ping Ma Huiming Zhang |
| author_sort | Richa Kaushal |
| collection | DOAJ |
| description | Abstract Background Plants are naturally associated with root microbiota, which are microbial communities influential to host fitness. Thus, it is important to understand how plants control root microbiota. Epigenetic factors regulate the readouts of genetic information and consequently many essential biological processes. However, it has been elusive whether RNA-directed DNA methylation (RdDM) affects root microbiota assembly. Results By applying 16S rRNA gene sequencing, we investigated root microbiota of Arabidopsis mutants defective in the canonical RdDM pathway, including dcl234 that harbors triple mutation in the Dicer-like proteins DCL3, DCL2, and DCL4, which produce small RNAs for RdDM. Alpha diversity analysis showed reductions in microbe richness from the soil to roots, reflecting the selectivity of plants on root-associated bacteria. The dcl234 triple mutation significantly decreases the levels of Aeromonadaceae and Pseudomonadaceae, while it increases the abundance of many other bacteria families in the root microbiota. However, mutants of the other examined key players in the canonical RdDM pathway showed similar microbiota as Col-0, indicating that the DCL proteins affect root microbiota in an RdDM-independent manner. Subsequently gene analysis by shotgun sequencing of root microbiome indicated a selective pressure on microbial resistance to plant defense in the dcl234 mutant. Consistent with the altered plant-microbe interactions, dcl234 displayed altered characters, including the mRNA and sRNA transcriptomes that jointly highlighted altered cell wall organization and up-regulated defense, the decreased cellulose and callose deposition in root xylem, and the restructured profile of root exudates that supported the alterations in gene expression and cell wall modifications. Conclusion Our findings demonstrate an important role of the DCL proteins in influencing root microbiota through integrated regulation of plant defense, cell wall compositions, and root exudates. Our results also demonstrate that the canonical RdDM is dispensable for Arabidopsis root microbiota. These findings not only establish a connection between root microbiota and plant epigenetic factors but also highlight the complexity of plant regulation of root microbiota. Video abstract |
| first_indexed | 2024-12-13T14:46:08Z |
| format | Article |
| id | doaj.art-b9d8b53972764a3b8393de53fc12cabe |
| institution | Directory Open Access Journal |
| issn | 2049-2618 |
| language | English |
| last_indexed | 2024-12-13T14:46:08Z |
| publishDate | 2021-02-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj.art-b9d8b53972764a3b8393de53fc12cabe2022-12-21T23:41:28ZengBMCMicrobiome2049-26182021-02-019112010.1186/s40168-020-00966-yDicer-like proteins influence Arabidopsis root microbiota independent of RNA-directed DNA methylationRicha Kaushal0Li Peng1Sunil K. Singh2Mengrui Zhang3Xinlian Zhang4Juan I. Vílchez5Zhen Wang6Danxia He7Yu Yang8Suhui Lv9Zhongtian Xu10Rafael J. L. Morcillo11Wei Wang12Weichang Huang13Paul W. Paré14Chun-Peng Song15Jian-Kang Zhu16Renyi Liu17Wenxuan Zhong18Ping Ma19Huiming Zhang20Shanghai Center for Plant Stress Biology, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of SciencesShanghai Center for Plant Stress Biology, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of SciencesShanghai Center for Plant Stress Biology, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of SciencesDepartment of Statistics, University of GeorgiaDepartment of Statistics, University of GeorgiaShanghai Center for Plant Stress Biology, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of SciencesDepartment of Statistics, University of GeorgiaShanghai Center for Plant Stress Biology, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of SciencesShanghai Center for Plant Stress Biology, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of SciencesShanghai Center for Plant Stress Biology, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of SciencesShanghai Center for Plant Stress Biology, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of SciencesShanghai Center for Plant Stress Biology, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of SciencesShanghai Chenshan Botanical GardenShanghai Chenshan Botanical GardenDepartment of Chemistry & Biochemistry, Texas Tech UniversityState Key Laboratory of Crop Stress Adaptation and Improvement, Henan UniversityShanghai Center for Plant Stress Biology, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of SciencesShanghai Center for Plant Stress Biology, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of SciencesDepartment of Statistics, University of GeorgiaDepartment of Statistics, University of GeorgiaShanghai Center for Plant Stress Biology, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of SciencesAbstract Background Plants are naturally associated with root microbiota, which are microbial communities influential to host fitness. Thus, it is important to understand how plants control root microbiota. Epigenetic factors regulate the readouts of genetic information and consequently many essential biological processes. However, it has been elusive whether RNA-directed DNA methylation (RdDM) affects root microbiota assembly. Results By applying 16S rRNA gene sequencing, we investigated root microbiota of Arabidopsis mutants defective in the canonical RdDM pathway, including dcl234 that harbors triple mutation in the Dicer-like proteins DCL3, DCL2, and DCL4, which produce small RNAs for RdDM. Alpha diversity analysis showed reductions in microbe richness from the soil to roots, reflecting the selectivity of plants on root-associated bacteria. The dcl234 triple mutation significantly decreases the levels of Aeromonadaceae and Pseudomonadaceae, while it increases the abundance of many other bacteria families in the root microbiota. However, mutants of the other examined key players in the canonical RdDM pathway showed similar microbiota as Col-0, indicating that the DCL proteins affect root microbiota in an RdDM-independent manner. Subsequently gene analysis by shotgun sequencing of root microbiome indicated a selective pressure on microbial resistance to plant defense in the dcl234 mutant. Consistent with the altered plant-microbe interactions, dcl234 displayed altered characters, including the mRNA and sRNA transcriptomes that jointly highlighted altered cell wall organization and up-regulated defense, the decreased cellulose and callose deposition in root xylem, and the restructured profile of root exudates that supported the alterations in gene expression and cell wall modifications. Conclusion Our findings demonstrate an important role of the DCL proteins in influencing root microbiota through integrated regulation of plant defense, cell wall compositions, and root exudates. Our results also demonstrate that the canonical RdDM is dispensable for Arabidopsis root microbiota. These findings not only establish a connection between root microbiota and plant epigenetic factors but also highlight the complexity of plant regulation of root microbiota. Video abstracthttps://doi.org/10.1186/s40168-020-00966-yRoot microbiotaMicrobiomeRNA-directed DNA methylationDCLSmall RNADefense |
| spellingShingle | Richa Kaushal Li Peng Sunil K. Singh Mengrui Zhang Xinlian Zhang Juan I. Vílchez Zhen Wang Danxia He Yu Yang Suhui Lv Zhongtian Xu Rafael J. L. Morcillo Wei Wang Weichang Huang Paul W. Paré Chun-Peng Song Jian-Kang Zhu Renyi Liu Wenxuan Zhong Ping Ma Huiming Zhang Dicer-like proteins influence Arabidopsis root microbiota independent of RNA-directed DNA methylation Microbiome Root microbiota Microbiome RNA-directed DNA methylation DCL Small RNA Defense |
| title | Dicer-like proteins influence Arabidopsis root microbiota independent of RNA-directed DNA methylation |
| title_full | Dicer-like proteins influence Arabidopsis root microbiota independent of RNA-directed DNA methylation |
| title_fullStr | Dicer-like proteins influence Arabidopsis root microbiota independent of RNA-directed DNA methylation |
| title_full_unstemmed | Dicer-like proteins influence Arabidopsis root microbiota independent of RNA-directed DNA methylation |
| title_short | Dicer-like proteins influence Arabidopsis root microbiota independent of RNA-directed DNA methylation |
| title_sort | dicer like proteins influence arabidopsis root microbiota independent of rna directed dna methylation |
| topic | Root microbiota Microbiome RNA-directed DNA methylation DCL Small RNA Defense |
| url | https://doi.org/10.1186/s40168-020-00966-y |
| work_keys_str_mv | AT richakaushal dicerlikeproteinsinfluencearabidopsisrootmicrobiotaindependentofrnadirecteddnamethylation AT lipeng dicerlikeproteinsinfluencearabidopsisrootmicrobiotaindependentofrnadirecteddnamethylation AT sunilksingh dicerlikeproteinsinfluencearabidopsisrootmicrobiotaindependentofrnadirecteddnamethylation AT mengruizhang dicerlikeproteinsinfluencearabidopsisrootmicrobiotaindependentofrnadirecteddnamethylation AT xinlianzhang dicerlikeproteinsinfluencearabidopsisrootmicrobiotaindependentofrnadirecteddnamethylation AT juanivilchez dicerlikeproteinsinfluencearabidopsisrootmicrobiotaindependentofrnadirecteddnamethylation AT zhenwang dicerlikeproteinsinfluencearabidopsisrootmicrobiotaindependentofrnadirecteddnamethylation AT danxiahe dicerlikeproteinsinfluencearabidopsisrootmicrobiotaindependentofrnadirecteddnamethylation AT yuyang dicerlikeproteinsinfluencearabidopsisrootmicrobiotaindependentofrnadirecteddnamethylation AT suhuilv dicerlikeproteinsinfluencearabidopsisrootmicrobiotaindependentofrnadirecteddnamethylation AT zhongtianxu dicerlikeproteinsinfluencearabidopsisrootmicrobiotaindependentofrnadirecteddnamethylation AT rafaeljlmorcillo dicerlikeproteinsinfluencearabidopsisrootmicrobiotaindependentofrnadirecteddnamethylation AT weiwang dicerlikeproteinsinfluencearabidopsisrootmicrobiotaindependentofrnadirecteddnamethylation AT weichanghuang dicerlikeproteinsinfluencearabidopsisrootmicrobiotaindependentofrnadirecteddnamethylation AT paulwpare dicerlikeproteinsinfluencearabidopsisrootmicrobiotaindependentofrnadirecteddnamethylation AT chunpengsong dicerlikeproteinsinfluencearabidopsisrootmicrobiotaindependentofrnadirecteddnamethylation AT jiankangzhu dicerlikeproteinsinfluencearabidopsisrootmicrobiotaindependentofrnadirecteddnamethylation AT renyiliu dicerlikeproteinsinfluencearabidopsisrootmicrobiotaindependentofrnadirecteddnamethylation AT wenxuanzhong dicerlikeproteinsinfluencearabidopsisrootmicrobiotaindependentofrnadirecteddnamethylation AT pingma dicerlikeproteinsinfluencearabidopsisrootmicrobiotaindependentofrnadirecteddnamethylation AT huimingzhang dicerlikeproteinsinfluencearabidopsisrootmicrobiotaindependentofrnadirecteddnamethylation |