Richa Kaushal1, Li Peng1, Sunil K Singh1, Mengrui Zhang2, Xinlian Zhang2, Juan I Vílchez1, Zhen Wang2, Danxia He1,3, Yu Yang1, Suhui Lv1,3, Zhongtian Xu1,4, Rafael J L Morcillo1,5, Wei Wang6, Weichang Huang6, Paul W Paré7, Chun-Peng Song8, Jian-Kang Zhu1,9, Renyi Liu1,4, Wenxuan Zhong2, Ping Ma2, Huiming Zhang10,11. 1. Shanghai Center for Plant Stress Biology, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai, 201602, China. 2. Department of Statistics, University of Georgia, Athens, GA, 30602, USA. 3. University of Chinese Academy of Sciences, Beijing, 100049, China. 4. Current address: Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, 350002, China. 5. Current address: Institute for Water Research and Department of Microbiology, University of Granada, Granada, Spain. 6. Shanghai Chenshan Botanical Garden, Shanghai, 201602, China. 7. Department of Chemistry & Biochemistry, Texas Tech University, Lubbock, TX, 79409, USA. 8. State Key Laboratory of Crop Stress Adaptation and Improvement, Henan University, Kaifeng, 475004, China. 9. Department of Horticulture & Landscape Architecture, Purdue University, West Lafayette, IN, 47906, USA. 10. Shanghai Center for Plant Stress Biology, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai, 201602, China. hmzhang@psc.ac.cn. 11. State Key Laboratory of Crop Stress Adaptation and Improvement, Henan University, Kaifeng, 475004, China. hmzhang@psc.ac.cn.
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.
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.
Entities:
Keywords:
Cell wall; DCL; Defense; Microbiome; RNA-directed DNA methylation; Root microbiota; Small RNA
Authors: Omri M Finkel; Gabriel Castrillo; Sur Herrera Paredes; Isai Salas González; Jeffery L Dangl Journal: Curr Opin Plant Biol Date: 2017-06-13 Impact factor: 7.834
Authors: Danxia He; Sunil K Singh; Li Peng; Richa Kaushal; Juan I Vílchez; Chuyang Shao; Xiaoxuan Wu; Shuai Zheng; Rafael J L Morcillo; Paul W Paré; Huiming Zhang Journal: ISME J Date: 2022-07-16 Impact factor: 11.217