Dynamics of rice microbiomes reveal core vertically transmitted seed endophytes
Abstract Background Plants and their associated microbiota constitute an assemblage of species known as holobionts. The plant seed microbiome plays an important role in nutrient uptake and stress attenuation. However, the core vertically transmitted endophytes remain largely unexplored. Results To g...
| Main Authors: | , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2022-12-01
|
| Series: | Microbiome |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s40168-022-01422-9 |
| _version_ | 1811188212298678272 |
|---|---|
| author | Xiaoxia Zhang Yi-Nan Ma Xing Wang Kaiji Liao Shanwen He Xia Zhao Hebao Guo Dongfang Zhao Hai-Lei Wei |
| author_facet | Xiaoxia Zhang Yi-Nan Ma Xing Wang Kaiji Liao Shanwen He Xia Zhao Hebao Guo Dongfang Zhao Hai-Lei Wei |
| author_sort | Xiaoxia Zhang |
| collection | DOAJ |
| description | Abstract Background Plants and their associated microbiota constitute an assemblage of species known as holobionts. The plant seed microbiome plays an important role in nutrient uptake and stress attenuation. However, the core vertically transmitted endophytes remain largely unexplored. Results To gain valuable insights into the vertical transmission of rice seed core endophytes, we conducted a large-scale analysis of the microbiomes of two generations of six different rice varieties from five microhabitats (bulk soil, rhizosphere, root, stem, and seed) from four geographic locations. We showed that the microhabitat rather than the geographic location and rice variety was the primary driver of the rice microbiome assemblage. The diversity and network complexity of the rice-associated microbiome decreased steadily from far to near the roots, rice exterior to interior, and from belowground to aboveground niches. Remarkably, the microbiomes of the roots, stems, and seeds of the rice interior compartments were not greatly influenced by the external environment. The core bacterial endophytes of rice were primarily comprised of 14 amplicon sequence variants (ASVs), 10 of which, especially ASV_2 (Pantoea) and ASV_48 (Xanthomonas), were identified as potentially vertically transmitted taxa because they existed across generations, were rarely present in exterior rice microhabitats, and were frequently isolated from rice seeds. The genome sequences of Pantoea and Xanthomonas isolated from the parental and offspring seeds showed a high degree of average nucleotide and core protein identity, indicating vertical transmission of seed endophytes across generations. In silico prediction indicated that the seed endophytes Pantoea and Xanthomonas possessed streamlined genomes with short lengths, low-complexity metabolism, and various plant growth-promoting traits. We also found that all strains of Pantoea and Xanthomonas exhibited cellulase activity and produced indole-3-acetic acid. However, most strains exhibited insignificant antagonism to the major pathogens of rice, such as Magnaporthe oryzae and X. oryzae pv. oryzae. Conclusion Overall, our study revealed that microhabitats, rather than site-specific environmental factors or host varieties, shape the rice microbiome. We discovered the vertically transmitted profiles and keystone taxa of the rice microbiome, which led to the isolation of culturable seed endophytes and investigation of their potential roles in plant-microbiome interactions. Our results provide insights on vertically transmitted microbiota and suggest new avenues for improving plant fitness via the manipulation of seed-associated microbiomes. Video Abstract |
| first_indexed | 2024-04-11T14:15:51Z |
| format | Article |
| id | doaj.art-6317d65f596a4c2b838b973277f17a27 |
| institution | Directory Open Access Journal |
| issn | 2049-2618 |
| language | English |
| last_indexed | 2024-04-11T14:15:51Z |
| publishDate | 2022-12-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj.art-6317d65f596a4c2b838b973277f17a272022-12-22T04:19:25ZengBMCMicrobiome2049-26182022-12-0110111910.1186/s40168-022-01422-9Dynamics of rice microbiomes reveal core vertically transmitted seed endophytesXiaoxia Zhang0Yi-Nan Ma1Xing Wang2Kaiji Liao3Shanwen He4Xia Zhao5Hebao Guo6Dongfang Zhao7Hai-Lei Wei8Key Laboratory of Microbial Resources Collection and Preservation, Ministry of Agriculture and Rural Affairs, Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural SciencesKey Laboratory of Microbial Resources Collection and Preservation, Ministry of Agriculture and Rural Affairs, Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural SciencesKey Laboratory of Microbial Resources Collection and Preservation, Ministry of Agriculture and Rural Affairs, Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural SciencesKey Laboratory of Microbial Resources Collection and Preservation, Ministry of Agriculture and Rural Affairs, Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural SciencesKey Laboratory of Microbial Resources Collection and Preservation, Ministry of Agriculture and Rural Affairs, Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural SciencesKey Laboratory of Microbial Resources Collection and Preservation, Ministry of Agriculture and Rural Affairs, Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural SciencesKey Laboratory of Microbial Resources Collection and Preservation, Ministry of Agriculture and Rural Affairs, Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural SciencesKey Laboratory of Microbial Resources Collection and Preservation, Ministry of Agriculture and Rural Affairs, Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural SciencesKey Laboratory of Microbial Resources Collection and Preservation, Ministry of Agriculture and Rural Affairs, Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural SciencesAbstract Background Plants and their associated microbiota constitute an assemblage of species known as holobionts. The plant seed microbiome plays an important role in nutrient uptake and stress attenuation. However, the core vertically transmitted endophytes remain largely unexplored. Results To gain valuable insights into the vertical transmission of rice seed core endophytes, we conducted a large-scale analysis of the microbiomes of two generations of six different rice varieties from five microhabitats (bulk soil, rhizosphere, root, stem, and seed) from four geographic locations. We showed that the microhabitat rather than the geographic location and rice variety was the primary driver of the rice microbiome assemblage. The diversity and network complexity of the rice-associated microbiome decreased steadily from far to near the roots, rice exterior to interior, and from belowground to aboveground niches. Remarkably, the microbiomes of the roots, stems, and seeds of the rice interior compartments were not greatly influenced by the external environment. The core bacterial endophytes of rice were primarily comprised of 14 amplicon sequence variants (ASVs), 10 of which, especially ASV_2 (Pantoea) and ASV_48 (Xanthomonas), were identified as potentially vertically transmitted taxa because they existed across generations, were rarely present in exterior rice microhabitats, and were frequently isolated from rice seeds. The genome sequences of Pantoea and Xanthomonas isolated from the parental and offspring seeds showed a high degree of average nucleotide and core protein identity, indicating vertical transmission of seed endophytes across generations. In silico prediction indicated that the seed endophytes Pantoea and Xanthomonas possessed streamlined genomes with short lengths, low-complexity metabolism, and various plant growth-promoting traits. We also found that all strains of Pantoea and Xanthomonas exhibited cellulase activity and produced indole-3-acetic acid. However, most strains exhibited insignificant antagonism to the major pathogens of rice, such as Magnaporthe oryzae and X. oryzae pv. oryzae. Conclusion Overall, our study revealed that microhabitats, rather than site-specific environmental factors or host varieties, shape the rice microbiome. We discovered the vertically transmitted profiles and keystone taxa of the rice microbiome, which led to the isolation of culturable seed endophytes and investigation of their potential roles in plant-microbiome interactions. Our results provide insights on vertically transmitted microbiota and suggest new avenues for improving plant fitness via the manipulation of seed-associated microbiomes. Video Abstracthttps://doi.org/10.1186/s40168-022-01422-9High-throughput sequencingRice microbiomeSeed endophytic microbiotaVertical transmissionPlant growth promotion |
| spellingShingle | Xiaoxia Zhang Yi-Nan Ma Xing Wang Kaiji Liao Shanwen He Xia Zhao Hebao Guo Dongfang Zhao Hai-Lei Wei Dynamics of rice microbiomes reveal core vertically transmitted seed endophytes Microbiome High-throughput sequencing Rice microbiome Seed endophytic microbiota Vertical transmission Plant growth promotion |
| title | Dynamics of rice microbiomes reveal core vertically transmitted seed endophytes |
| title_full | Dynamics of rice microbiomes reveal core vertically transmitted seed endophytes |
| title_fullStr | Dynamics of rice microbiomes reveal core vertically transmitted seed endophytes |
| title_full_unstemmed | Dynamics of rice microbiomes reveal core vertically transmitted seed endophytes |
| title_short | Dynamics of rice microbiomes reveal core vertically transmitted seed endophytes |
| title_sort | dynamics of rice microbiomes reveal core vertically transmitted seed endophytes |
| topic | High-throughput sequencing Rice microbiome Seed endophytic microbiota Vertical transmission Plant growth promotion |
| url | https://doi.org/10.1186/s40168-022-01422-9 |
| work_keys_str_mv | AT xiaoxiazhang dynamicsofricemicrobiomesrevealcoreverticallytransmittedseedendophytes AT yinanma dynamicsofricemicrobiomesrevealcoreverticallytransmittedseedendophytes AT xingwang dynamicsofricemicrobiomesrevealcoreverticallytransmittedseedendophytes AT kaijiliao dynamicsofricemicrobiomesrevealcoreverticallytransmittedseedendophytes AT shanwenhe dynamicsofricemicrobiomesrevealcoreverticallytransmittedseedendophytes AT xiazhao dynamicsofricemicrobiomesrevealcoreverticallytransmittedseedendophytes AT hebaoguo dynamicsofricemicrobiomesrevealcoreverticallytransmittedseedendophytes AT dongfangzhao dynamicsofricemicrobiomesrevealcoreverticallytransmittedseedendophytes AT haileiwei dynamicsofricemicrobiomesrevealcoreverticallytransmittedseedendophytes |