TY - JOUR
T1 - Dicer-like proteins influence Arabidopsis root microbiota independent of RNA-directed DNA methylation
AU - Kaushal, Richa
AU - Peng, Li
AU - Singh, Sunil K.
AU - Zhang, Mengrui
AU - Zhang, Xinlian
AU - Vílchez, Juan I.
AU - Wang, Zhen
AU - He, Danxia
AU - Yang, Yu
AU - Lv, Suhui
AU - Xu, Zhongtian
AU - Morcillo, Rafael J.L.
AU - Wang, Wei
AU - Huang, Weichang
AU - Paré, Paul W.
AU - Song, Chun Peng
AU - Zhu, Jian Kang
AU - Liu, Renyi
AU - Zhong, Wenxuan
AU - Ma, Ping
AU - Zhang, Huiming
N1 - Funding Information:
Research in H.Z. lab is supported by the Chinese Academy of Sciences.
Funding Information:
We thank the Core Facilities of Genomics, Cell Biology, and Plant Proteomics & Metabolomics at Shanghai Center for Plant Stress Biology for sequencing, microscopic analyses, and GC-MS respectively. M.Z., X.Z., Z.W., W.Z. and P.M. acknowledge support from the U.S. National Science Foundation grants DMS-1903226 and DMS-1925066.
Publisher Copyright:
© 2021, The Author(s).
PY - 2021/12
Y1 - 2021/12
N2 - 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. [MediaObject not available: see fulltext.]
AB - 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. [MediaObject not available: see fulltext.]
KW - Cell wall
KW - DCL
KW - Defense
KW - Microbiome
KW - RNA-directed DNA methylation
KW - Root microbiota
KW - Small RNA
UR - http://www.scopus.com/inward/record.url?scp=85101753660&partnerID=8YFLogxK
U2 - 10.1186/s40168-020-00966-y
DO - 10.1186/s40168-020-00966-y
M3 - Article
C2 - 33637135
AN - SCOPUS:85101753660
VL - 9
JO - Microbiome
JF - Microbiome
SN - 2049-2618
IS - 1
M1 - 57
ER -