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Title: Drought delays development of the sorghum root microbiome and enriches for monoderm bacteria

Here, drought stress is a major obstacle to crop productivity, and the severity and frequency of drought are expected to increase in the coming century. Certain root-associated bacteria have been shown to mitigate the negative effects of drought stress on plant growth, and manipulation of the crop microbiome is an emerging strategy for overcoming drought stress in agricultural systems, yet the effect of drought on the development of the root microbiome is poorly understood. Through 16S rRNA amplicon and metatranscriptome sequencing, as well as root metabolomics, we demonstrate that drought delays the development of the early sorghum root microbiome and causes increased abundance and activity of monoderm bacteria, which lack an outer cell membrane and contain thick cell walls. Our data suggest that altered plant metabolism and increased activity of bacterial ATP-binding cassette (ABC) transporter genes are correlated with these shifts in community composition. Finally, inoculation experiments with monoderm isolates indicate that increased colonization of the root during drought can positively impact plant growth. Collectively, these results demonstrate the role that drought plays in restructuring the root microbiome and highlight the importance of temporal sampling when studying plant-associated microbiomes.
Authors:
 [1] ;  [1] ; ORCiD logo [1] ;  [1] ;  [1] ;  [2] ; ORCiD logo [2] ;  [2] ;  [2] ;  [1] ; ORCiD logo [3] ;  [3] ;  [3] ;  [4] ;  [4] ;  [5] ;  [6] ;  [7] ;  [4] ; ORCiD logo [2] more »;  [3] ;  [3] ;  [1] « less
  1. Univ. of California, Berkeley, CA (United States); US Dept. of Agriculture-Agricultural Research Service, Albany, CA (United States)
  2. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  3. Univ. of California, Berkeley, CA (United States)
  4. Kearney Agricultural Research & Extension Center, Parlier, CA (United States)
  5. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  6. Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  7. Univ. of California, Davis, Five Points, CA (United States)
Publication Date:
Report Number(s):
PNNL-SA-131119
Journal ID: ISSN 0027-8424
Grant/Contract Number:
DOA-0001207; CRIS-203021430-008-00D; AC05-76RL01830; AC02-05CH11231
Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 115; Journal Issue: 18; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Research Org:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; sorghum; root; microbiome; drought; metatranscriptome
OSTI Identifier:
1433401
Alternate Identifier(s):
OSTI ID: 1437150; OSTI ID: 1457007

Xu, Ling, Naylor, Dan, Dong, Zhaobin, Simmons, Tuesday, Pierroz, Grady, Hixson, Kim K., Kim, Young -Mo, Zink, Erika M., Engbrecht, Kristin M., Wang, Yi, Gao, Cheng, DeGraaf, Stephanie, Madera, Mary A., Sievert, Julie A., Hollingsworth, Joy, Birdseye, Devon, Scheller, Henrik V., Hutmacher, Robert, Dahlberg, Jeffery, Jansson, Christer, Taylor, John W., Lemaux, Peggy G., and Coleman-Derr, Devin. Drought delays development of the sorghum root microbiome and enriches for monoderm bacteria. United States: N. p., Web. doi:10.1073/pnas.1717308115.
Xu, Ling, Naylor, Dan, Dong, Zhaobin, Simmons, Tuesday, Pierroz, Grady, Hixson, Kim K., Kim, Young -Mo, Zink, Erika M., Engbrecht, Kristin M., Wang, Yi, Gao, Cheng, DeGraaf, Stephanie, Madera, Mary A., Sievert, Julie A., Hollingsworth, Joy, Birdseye, Devon, Scheller, Henrik V., Hutmacher, Robert, Dahlberg, Jeffery, Jansson, Christer, Taylor, John W., Lemaux, Peggy G., & Coleman-Derr, Devin. Drought delays development of the sorghum root microbiome and enriches for monoderm bacteria. United States. doi:10.1073/pnas.1717308115.
Xu, Ling, Naylor, Dan, Dong, Zhaobin, Simmons, Tuesday, Pierroz, Grady, Hixson, Kim K., Kim, Young -Mo, Zink, Erika M., Engbrecht, Kristin M., Wang, Yi, Gao, Cheng, DeGraaf, Stephanie, Madera, Mary A., Sievert, Julie A., Hollingsworth, Joy, Birdseye, Devon, Scheller, Henrik V., Hutmacher, Robert, Dahlberg, Jeffery, Jansson, Christer, Taylor, John W., Lemaux, Peggy G., and Coleman-Derr, Devin. 2018. "Drought delays development of the sorghum root microbiome and enriches for monoderm bacteria". United States. doi:10.1073/pnas.1717308115.
@article{osti_1433401,
title = {Drought delays development of the sorghum root microbiome and enriches for monoderm bacteria},
author = {Xu, Ling and Naylor, Dan and Dong, Zhaobin and Simmons, Tuesday and Pierroz, Grady and Hixson, Kim K. and Kim, Young -Mo and Zink, Erika M. and Engbrecht, Kristin M. and Wang, Yi and Gao, Cheng and DeGraaf, Stephanie and Madera, Mary A. and Sievert, Julie A. and Hollingsworth, Joy and Birdseye, Devon and Scheller, Henrik V. and Hutmacher, Robert and Dahlberg, Jeffery and Jansson, Christer and Taylor, John W. and Lemaux, Peggy G. and Coleman-Derr, Devin},
abstractNote = {Here, drought stress is a major obstacle to crop productivity, and the severity and frequency of drought are expected to increase in the coming century. Certain root-associated bacteria have been shown to mitigate the negative effects of drought stress on plant growth, and manipulation of the crop microbiome is an emerging strategy for overcoming drought stress in agricultural systems, yet the effect of drought on the development of the root microbiome is poorly understood. Through 16S rRNA amplicon and metatranscriptome sequencing, as well as root metabolomics, we demonstrate that drought delays the development of the early sorghum root microbiome and causes increased abundance and activity of monoderm bacteria, which lack an outer cell membrane and contain thick cell walls. Our data suggest that altered plant metabolism and increased activity of bacterial ATP-binding cassette (ABC) transporter genes are correlated with these shifts in community composition. Finally, inoculation experiments with monoderm isolates indicate that increased colonization of the root during drought can positively impact plant growth. Collectively, these results demonstrate the role that drought plays in restructuring the root microbiome and highlight the importance of temporal sampling when studying plant-associated microbiomes.},
doi = {10.1073/pnas.1717308115},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 18,
volume = 115,
place = {United States},
year = {2018},
month = {4}
}