Transcriptomic analysis of field-droughted sorghum from seedling to maturity reveals biotic and metabolic responses
Abstract
Drought is the most important environmental stress limiting crop yields. The C4 cereal sorghum [ Sorghum bicolor (L.) Moench] is a critical food, forage, and emerging bioenergy crop that is notably drought-tolerant. We conducted a large-scale field experiment, imposing preflowering and postflowering drought stress on 2 genotypes of sorghum across a tightly resolved time series, from plant emergence to postanthesis, resulting in a dataset of nearly 400 transcriptomes. We observed a fast and global transcriptomic response in leaf and root tissues with clear temporal patterns, including modulation of well-known drought pathways. We also identified genotypic differences in core photosynthesis and reactive oxygen species scavenging pathways, highlighting possible mechanisms of drought tolerance and of the delayed senescence, characteristic of the stay-green phenotype. Finally, we discovered a large-scale depletion in the expression of genes critical to arbuscular mycorrhizal (AM) symbiosis, with a corresponding drop in AM fungal mass in the plants’ roots.
- Authors:
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[1];
[1];
[1];
[2];
[7];
[8]
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- Univ. of California, Berkeley, CA (United States)
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Univ. of California, Berkeley, CA (United States); US Department of Agriculture–Agricultural Research Service, Albany, CA (United States)
- Univ. of California Agriculture and Natural Resources, Parlier, CA (United States)
- Boyce Thompson Inst., Ithaca, NY (United States)
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Merced, CA (United States)
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
- Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Univ. of California, Five Points, CA (United States); Univ. of California, Davis, CA (United States)
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States)
- Publication Date:
- Research Org.:
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
- OSTI Identifier:
- 1577228
- Alternate Identifier(s):
- OSTI ID: 1582406
- Report Number(s):
- PNNL-SA-140530
Journal ID: ISSN 0027-8424
- Grant/Contract Number:
- AC05-76RL01830; SC0012460; SC0014081; AC02-05CH11231
- Resource Type:
- Published Article
- Journal Name:
- Proceedings of the National Academy of Sciences of the United States of America
- Additional Journal Information:
- Journal Volume: 116; Journal Issue: 52; Journal ID: ISSN 0027-8424
- Publisher:
- National Academy of Sciences
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; drought; RNA-Seq; S. bicolorarbuscular mycorrhizal fungi
Citation Formats
Varoquaux, Nelle, Cole, Benjamin, Gao, Cheng, Pierroz, Grady, Baker, Christopher R., Patel, Dhruv, Madera, Mary, Jeffers, Tim, Hollingsworth, Joy, Sievert, Julie, Yoshinaga, Yuko, Owiti, Judith A., Singan, Vasanth R., DeGraaf, Stephanie, Xu, Ling, Blow, Matthew J., Harrison, Maria J., Visel, Axel, Jansson, Christer, Niyogi, Krishna K., Hutmacher, Robert, Coleman-Derr, Devin, O’Malley, Ronan C., Taylor, John W., Dahlberg, Jeffery, Vogel, John P., Lemaux, Peggy G., and Purdom, Elizabeth. Transcriptomic analysis of field-droughted sorghum from seedling to maturity reveals biotic and metabolic responses. United States: N. p., 2019.
Web. doi:10.1073/pnas.1907500116.
Varoquaux, Nelle, Cole, Benjamin, Gao, Cheng, Pierroz, Grady, Baker, Christopher R., Patel, Dhruv, Madera, Mary, Jeffers, Tim, Hollingsworth, Joy, Sievert, Julie, Yoshinaga, Yuko, Owiti, Judith A., Singan, Vasanth R., DeGraaf, Stephanie, Xu, Ling, Blow, Matthew J., Harrison, Maria J., Visel, Axel, Jansson, Christer, Niyogi, Krishna K., Hutmacher, Robert, Coleman-Derr, Devin, O’Malley, Ronan C., Taylor, John W., Dahlberg, Jeffery, Vogel, John P., Lemaux, Peggy G., & Purdom, Elizabeth. Transcriptomic analysis of field-droughted sorghum from seedling to maturity reveals biotic and metabolic responses. United States. doi:10.1073/pnas.1907500116.
Varoquaux, Nelle, Cole, Benjamin, Gao, Cheng, Pierroz, Grady, Baker, Christopher R., Patel, Dhruv, Madera, Mary, Jeffers, Tim, Hollingsworth, Joy, Sievert, Julie, Yoshinaga, Yuko, Owiti, Judith A., Singan, Vasanth R., DeGraaf, Stephanie, Xu, Ling, Blow, Matthew J., Harrison, Maria J., Visel, Axel, Jansson, Christer, Niyogi, Krishna K., Hutmacher, Robert, Coleman-Derr, Devin, O’Malley, Ronan C., Taylor, John W., Dahlberg, Jeffery, Vogel, John P., Lemaux, Peggy G., and Purdom, Elizabeth. Thu .
"Transcriptomic analysis of field-droughted sorghum from seedling to maturity reveals biotic and metabolic responses". United States. doi:10.1073/pnas.1907500116.
@article{osti_1577228,
title = {Transcriptomic analysis of field-droughted sorghum from seedling to maturity reveals biotic and metabolic responses},
author = {Varoquaux, Nelle and Cole, Benjamin and Gao, Cheng and Pierroz, Grady and Baker, Christopher R. and Patel, Dhruv and Madera, Mary and Jeffers, Tim and Hollingsworth, Joy and Sievert, Julie and Yoshinaga, Yuko and Owiti, Judith A. and Singan, Vasanth R. and DeGraaf, Stephanie and Xu, Ling and Blow, Matthew J. and Harrison, Maria J. and Visel, Axel and Jansson, Christer and Niyogi, Krishna K. and Hutmacher, Robert and Coleman-Derr, Devin and O’Malley, Ronan C. and Taylor, John W. and Dahlberg, Jeffery and Vogel, John P. and Lemaux, Peggy G. and Purdom, Elizabeth},
abstractNote = {Drought is the most important environmental stress limiting crop yields. The C4 cereal sorghum [ Sorghum bicolor (L.) Moench] is a critical food, forage, and emerging bioenergy crop that is notably drought-tolerant. We conducted a large-scale field experiment, imposing preflowering and postflowering drought stress on 2 genotypes of sorghum across a tightly resolved time series, from plant emergence to postanthesis, resulting in a dataset of nearly 400 transcriptomes. We observed a fast and global transcriptomic response in leaf and root tissues with clear temporal patterns, including modulation of well-known drought pathways. We also identified genotypic differences in core photosynthesis and reactive oxygen species scavenging pathways, highlighting possible mechanisms of drought tolerance and of the delayed senescence, characteristic of the stay-green phenotype. Finally, we discovered a large-scale depletion in the expression of genes critical to arbuscular mycorrhizal (AM) symbiosis, with a corresponding drop in AM fungal mass in the plants’ roots.},
doi = {10.1073/pnas.1907500116},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 52,
volume = 116,
place = {United States},
year = {2019},
month = {12}
}
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DOI: 10.1073/pnas.1907500116
DOI: 10.1073/pnas.1907500116
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Works referenced in this record:
Regulatory Shifts in Plastid Transcription Play a Key Role in Morphological Conversions of Plastids during Plant Development
journal, January 2017
- Liebers, Monique; Grübler, Björn; Chevalier, Fabien
- Frontiers in Plant Science, Vol. 8
Influence of extreme weather disasters on global crop production
journal, January 2016
- Lesk, Corey; Rowhani, Pedram; Ramankutty, Navin
- Nature, Vol. 529, Issue 7584
Whole-genome sequencing reveals untapped genetic potential in Africa’s indigenous cereal crop sorghum
journal, August 2013
- Mace, Emma S.; Tai, Shuaishuai; Gilding, Edward K.
- Nature Communications, Vol. 4, Issue 1
Stay green trait in grain sorghum: relationship between visual rating and leaf chlorophyll concentration
journal, August 2000
- Xu, W.; Rosenow, D. T.; Nguyen, H. T.
- Plant Breeding, Vol. 119, Issue 4
Stay-green plants: what do they tell us about the molecular mechanism of leaf senescence
journal, June 2013
- Kusaba, Makoto; Tanaka, Ayumi; Tanaka, Ryouichi
- Photosynthesis Research, Vol. 117, Issue 1-3
Stay-green alleles individually enhance grain yield in sorghum under drought by modifying canopy development and water uptake patterns
journal, June 2014
- Borrell, Andrew K.; van Oosterom, Erik J.; Mullet, John E.
- New Phytologist, Vol. 203, Issue 3
The Sorghum bicolor genome and the diversification of grasses
journal, January 2009
- Paterson, Andrew H.; Bowers, John E.; Bruggmann, Rémy
- Nature, Vol. 457, Issue 7229
The Sorghum bicolor reference genome: improved assembly, gene annotations, a transcriptome atlas, and signatures of genome organization
journal, December 2017
- McCormick, Ryan F.; Truong, Sandra K.; Sreedasyam, Avinash
- The Plant Journal, Vol. 93, Issue 2
Sorghum bicolor’s Transcriptome Response to Dehydration, High Salinity and ABA
journal, July 2005
- Buchanan, Christina D.; Lim, Sanghyun; Salzman, Ron A.
- Plant Molecular Biology, Vol. 58, Issue 5
Functional annotation of the transcriptome of Sorghum bicolor in response to osmotic stress and abscisic acid
journal, October 2011
- Dugas, Diana V.; Monaco, Marcela K.; Olson, Andrew
- BMC Genomics, Vol. 12, Issue 1
Transcriptomic analysis of Sorghum bicolor responding to combined heat and drought stress
journal, January 2014
- Johnson, Stephanie M.; Lim, Fei-Ling; Finkler, Aliza
- BMC Genomics, Vol. 15, Issue 1
Transcriptomic analysis comparing stay-green and senescent Sorghum bicolor lines identifies a role for proline biosynthesis in the stay-green trait
journal, August 2015
- Johnson, Stephanie M.; Cummins, Ian; Lim, Fei Ling
- Journal of Experimental Botany, Vol. 66, Issue 22
Simultaneous Transcriptome Analysis of Sorghum and Bipolaris sorghicola by Using RNA-seq in Combination with De Novo Transcriptome Assembly
journal, April 2013
- Yazawa, Takayuki; Kawahigashi, Hiroyuki; Matsumoto, Takashi
- PLoS ONE, Vol. 8, Issue 4
Drought stress tolerance strategies revealed by RNA-Seq in two sorghum genotypes with contrasting WUE
journal, May 2016
- Fracasso, Alessandra; Trindade, Luisa M.; Amaducci, Stefano
- BMC Plant Biology, Vol. 16, Issue 1
The Pivotal Role of Ethylene in Plant Growth
journal, April 2018
- Dubois, Marieke; Van den Broeck, Lisa; Inzé, Dirk
- Trends in Plant Science, Vol. 23, Issue 4
Drought delays development of the sorghum root microbiome and enriches for monoderm bacteria
journal, April 2018
- Xu, Ling; Naylor, Dan; Dong, Zhaobin
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 18
Strong succession in arbuscular mycorrhizal fungal communities
journal, August 2018
- Gao, Cheng; Montoya, Liliam; Xu, Ling
- The ISME Journal, Vol. 13, Issue 1
Screening for drought tolerance in Sorghum using cell culture
journal, October 1985
- Smith, R. H.; Bhaskaran, S.; Miller, F. R.
- In Vitro Cellular amp; Developmental Biology, Vol. 21, Issue 10
Five ways to stay green
journal, February 2000
- Thomas, Howard; Howarth, Catherine J.
- Journal of Experimental Botany, Vol. 51, Issue suppl_1
Selection System for the Stay-Green Drought Tolerance Trait in Sorghum Germplasm
journal, January 2010
- Burke, J. J.; Franks, C. D.; Burow, G.
- Agronomy Journal, Vol. 102, Issue 4
Leaf Photoassimilation and Partitioning in Stress-Tolerant Sorghum
journal, January 1997
- Sowder, C. Matt; Tarpley, Lee; Vietor, Donald M.
- Crop Science, Vol. 37, Issue 3
Sorghum stay-green QTL individually reduce post-flowering drought-induced leaf senescence
journal, November 2006
- Harris, K.; Subudhi, P.; Borrell, A.
- Journal of Experimental Botany, Vol. 58, Issue 2
The Role of WRKY Transcription Factors in Plant Immunity: Figure 1.
journal, May 2009
- Pandey, Shree P.; Somssich, Imre E.
- Plant Physiology, Vol. 150, Issue 4
Predisposition in Plant Disease: Exploiting the Nexus in Abiotic and Biotic Stress Perception and Response
journal, August 2014
- Bostock, Richard M.; Pye, Matthew F.; Roubtsova, Tatiana V.
- Annual Review of Phytopathology, Vol. 52, Issue 1
Impact of drought on photosynthesis: Molecular perspective
journal, September 2017
- Zargar, Sajad Majeed; Gupta, Nancy; Nazir, Muslima
- Plant Gene, Vol. 11
ROS and redox signalling in the response of plants to abiotic stress: ROS and redox signalling in plants
journal, June 2011
- Suzuki, Nobuhiro; Koussevitzky, Shai; Mittler, Ron
- Plant, Cell & Environment, Vol. 35, Issue 2
Identification and analysis of glutathione S-transferase gene family in sweet potato reveal divergent GST-mediated networks in aboveground and underground tissues in response to abiotic stresses
journal, November 2017
- Ding, Na; Wang, Aimin; Zhang, Xiaojun
- BMC Plant Biology, Vol. 17, Issue 1
Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants
journal, December 2014
- Das, Kaushik; Roychoudhury, Aryadeep
- Frontiers in Environmental Science, Vol. 2
Overexpression of Ferredoxin, PETF, Enhances Tolerance to Heat Stress in Chlamydomonas reinhardtii
journal, October 2013
- Lin, Yi-Hsien; Pan, Kui-You; Hung, Ching-Hui
- International Journal of Molecular Sciences, Vol. 14, Issue 10
The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells
journal, July 1999
- Maxwell, D. P.; Wang, Y.; McIntosh, L.
- Proceedings of the National Academy of Sciences, Vol. 96, Issue 14
Alternative oxidase respiration maintains both mitochondrial and chloroplast function during drought
journal, August 2016
- Dahal, Keshav; Vanlerberghe, Greg C.
- New Phytologist, Vol. 213, Issue 2
Colonisation with the arbuscular mycorrhizal fungus Glomus mosseae (Nicol. & Gerd.) enhanced phosphorus uptake from dry soil in Sorghum bicolor (L.)
journal, April 2004
- Neumann, Elke; George, Eckhard
- Plant and Soil, Vol. 261, Issue 1/2
Mycorrhizal Fungi
journal, January 1974
- Smith, S. E.
- CRC Critical Reviews in Microbiology, Vol. 3, Issue 3
Plant Signaling and Metabolic Pathways Enabling Arbuscular Mycorrhizal Symbiosis
journal, August 2017
- MacLean, Allyson M.; Bravo, Armando; Harrison, Maria J.
- The Plant Cell, Vol. 29, Issue 10
Arbuscular mycorrhizal symbiosis alters stomatal conductance of host plants more under drought than under amply watered conditions: a meta-analysis
journal, May 2014
- Augé, Robert M.; Toler, Heather D.; Saxton, Arnold M.
- Mycorrhiza, Vol. 25, Issue 1
Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis
journal, May 2001
- Augé, Robert M.
- Mycorrhiza, Vol. 11, Issue 1
Diverse Sorghum bicolor accessions show marked variation in growth and transcriptional responses to arbuscular mycorrhizal fungi
journal, January 2019
- Watts‐Williams, Stephanie J.; Emmett, Bryan D.; Levesque‐Tremblay, Veronique
- Plant, Cell & Environment, Vol. 42, Issue 5
Increased precipitation, rather than warming, exerts a strong influence on arbuscular mycorrhizal fungal community in a semiarid steppe ecosystem
journal, June 2016
- Gao, Cheng; Kim, Yong-Chan; Zheng, Yong
- Botany, Vol. 94, Issue 6
Revisiting the Non-Animal Peroxidase Superfamily
journal, December 2015
- Lazzarotto, Fernanda; Turchetto-Zolet, Andreia Carina; Margis-Pinheiro, Márcia
- Trends in Plant Science, Vol. 20, Issue 12
Two Transcription Factors, DREB1 and DREB2, with an EREBP/AP2 DNA Binding Domain Separate Two Cellular Signal Transduction Pathways in Drought- and Low-Temperature-Responsive Gene Expression, Respectively, in Arabidopsis
journal, August 1998
- Liu, Qiang; Kasuga, Mie; Sakuma, Yoh
- The Plant Cell, Vol. 10, Issue 8
Over-represented promoter motifs in abiotic stress-induced DREB genes of rice and sorghum and their probable role in regulation of gene expression
journal, July 2010
- Srivasta, Amrita; Mehta, Sameet; Lindlof, Angelica
- Plant Signaling & Behavior, Vol. 5, Issue 7
Overexpression of OsWRKY72 gene interferes in the abscisic acid signal and auxin transport pathway of Arabidopsis
journal, July 2010
- Song, Yu; Chen, Ligang; Zhang, Liping
- Journal of Biosciences, Vol. 35, Issue 3
Exploring genetic and expression differences between physiologically extreme ecotypes: comparative genomic hybridization and gene expression studies of Kas-1 and Tsu-1 accessions of Arabidopsis thaliana: Genomic studies of Arabidopsis accessions
journal, March 2010
- Juenger, Thomas E.; Sen, Saunak; Bray, Elizabeth
- Plant, Cell & Environment, Vol. 33, Issue 8
Natural variation and genetic constraints on drought tolerance
journal, June 2013
- Juenger, Thomas E.
- Current Opinion in Plant Biology, Vol. 16, Issue 3