Transcriptome profilling analysis characterized the gene expression patterns responded to combined drought and heat stresses in soybean

doi:10.1016/j.compbiolchem.2018.09.012

Computational Biology and Chemistry

Volume 77, December 2018, Pages 413-429

https://doi.org/10.1016/j.compbiolchem.2018.09.012 Get rights and content

Highlights

•
Combining dynamic changing SOD, MDA, soluble sugar and proline contents and the degree of leaf damage under stress, samples of 8 h and 24 h after heat, drought and combined stress treatments were selected for RNA-seq.
•
The RNA sequencing analysis demonstrated that many genes involved in the defense response, photosynthesis, metabolic process, etc. are differentially expressed in response to drought and heat. However, 1468 and 1220 upregulated and 1146 and 686 downregulated genes were confirmed as overlapping differentially expressed genes at 8 h and 24 h after treatment, and these genes are mainly involved in transport, binding and defense responses.
•
Comparison of single and combined stress suggests the combined stress did not result in a simple additive response, and that there may be a synergistic response to the combination of drought and heat in soybean.
•
TFs in the single and combination stress were identified from DEGs, which classified into 9 clusters according to expression levels of six treatment and one control groups, revealed dynamic changing TF expression profiles and molecular mechanisms in response to single and combination stress.

Abstract

Heat and drought are the two major abiotic stress limiting soybean growth and output worldwide. Knowledge of the molecular mechanisms underlying the responses to heat, drought, and combined stress is essential for soybean molecular breeding. In this study, RNA-sequencing was used to determine the transcriptional responses of soybean to heat, drought and combined stress. RNA-sequencing analysis demonstrated that many genes involved in the defense response, photosynthesis, metabolic process, etc. are differentially expressed in response to drought and heat. However, 1468 and 1220 up-regulated and 1146 and 686 down-regulated genes were confirmed as overlapping differentially expressed genes at 8 h and 24 h after treatment, and these genes are mainly involved in transport, binding and defense response. Furthermore, we compared the heat, drought and the combined stress-responsive genes and identified potential new targets for enhancing stress tolerance of soybean. Comparison of single and combined stress suggests the combined stress did not result in a simple additive response, and that there may be a synergistic response to the combination of drought and heat in soybean.

Graphical abstract

Section snippets

Plant materials and stress treatment

The drought-resistant soybean cultivar ‘Heinong44′ was grown in pots with a dimension of 13 × 10 × 10 cm (top diameter × bottom diameter × height), each filled with 1 kg sand. Seeds of ‘Heinong44′ were surface-sterilized in 1% sodium hypochlorite for 10 min, rinsed in distilled water three times, and then sown and grown in a growth chamber at 25°/20 °C (day/night), 14 h/10 h (light/dark), and 60%-80% humidity. Before the V1 stage of development, the seedling was irrigated with 100 mL distilled

Physiological analyses of soybean under drought and heat stress

We studied the physiological response of soybean under heat, drought and combined stress from 0 to 32 h at the V3 stage of development. The SOD activity initially showed a decreasing trend and then increased over time under the heat (H) and combined heat and drought (DH) treatments, and the SOD activity at 8 h was the lowest under both treatment conditions. However, the SOD activity under the drought (D) treatment initially increased and then decreased as the stress time increased, and the

Discussion

Extreme temperature and drought are two major abiotic stresses that often result in significant losses of the yields of crops such as soybean (Tran and Mochida, 2010). Transcriptomic analysis of plant response to stresses is an effective method of discovering key resistance genes, processes and pathways for stress response. The effect of individual drought stress on soybean has been investigated previously by RNA-seq (Chen et al., 2016; Le et al., 2012), while to our knowledge, no report has

Conclusions

Our results showed that many genes are differentially expressed in response to drought and heat, but only a small number of these genes were identified as overlapping DEGs. These overlapping DEGs may play key roles in modulating physiological function in response to stress. Furthermore, comparison of individual and combined heat and drought stress suggests combined stress is not a simple additive mechanism but may involve a complicated gene regulatory network in response to the combination of

Acknowledgments

This work was supported by the National Key Technology Research and Development Program of the Ministry of Science and Technology of China (grant numbers 2014BAD11B01) and the Collaborative Innovation Program of Heilongjiang Soybean Industrial Technology R&D System.

References (83)

R.A. Candeia et al.
Influence of soybean biodiesel content on basic properties of biodiesel–diesel blends
Fuel
(2009)
V. Cavallaro et al.
Evaluation of variability to drought and saline stress through the germination of different ecotypes of carob (Ceratonia siliqua L.) using a hydrotime model
Ecol. Eng.
(2016)
A. Chaoui et al.
Cadmium and zinc induction of lipid peroxidation and effects on antioxidant enzyme activities in bean (Phaseolus vulgaris L.)
Plant Sci.
(1997)
F.P. Gomes et al.
Osmotic adjustment, proline accumulation and cell membrane stability in leaves of Cocos nucifera submitted to drought stress
Sci. Hortic.
(2010)
B. He et al.
Physiological responses of Scaevola aemula seedlings under high temperature stress
South Afr. J. Bot.
(2017)
F. Hosseini et al.
Effect of the fungus Piriformospora indica on physiological characteristics and root morphology of wheat under combined drought and mechanical stresses
Plant Physiol. Biochem. Ppb
(2017)
L. Li et al.
Physiological response and resistance of three cultivars of Acer rubrum L. To continuous drought stress
Acta Ecol. Sin.
(2015)
R.C. Lin et al.
Role of Arabidopsis RAP2.4 in regulating light- and ethylene-mediated developmental processes and drought stress tolerance
Mol. Plant
(2008)
H. Liu et al.
Alginate oligosaccharides enhanced Triticum aestivum L. Tolerance to drought stress
Plant Physiol. Biochem.
(2013)
Z. Liu et al.
Temporal transcriptome profiling reveals expression partitioning of homeologous genes contributing to heat and drought acclimation in wheat (Triticum aestivum L.)
BMC Plant Biol.
(2015)

R. Mahalingam

Phenotypic, physiological and malt quality analyses of US barley varieties subjected to short periods of heat and drought stress

J. Cereal Sci.

(2017)

Y. Maruyama et al.

The Arabidopsis transcriptional repressor ERF9 participates in resistance against necrotrophic fungi

Plant Sci.

(2013)

S. Meng et al.

Nitrogen uptake and metabolism of Populus simonii in response to PEG-induced drought stress

Environ. Exp. Bot.

(2016)

R. Mittler

Abiotic stress, the field environment and stress combination

Trends Plant Sci.

(2006)

O. Ozkur et al.

Physiochemical and antioxidant responses of the perennial xerophyte Capparis ovata Desf. To drought

Environ. Exp. Bot.

(2009)

G. Shi et al.

PEG-simulated drought stress decreases cadmium accumulation in castor bean by altering root morphology

Environ. Exp. Bot.

(2015)

D.H. Shin et al.

HY5 regulates anthocyanin biosynthesis by inducing the transcriptional activation of the MYB75/PAP1 transcription factor in Arabidopsis

FEBS Lett.

(2013)

S. Weber

Light-driven enzymatic catalysis of DNA repair: a review of recent biophysical studies on photolyase

Biochim. Biophys. Acta

(2005)

K. Yamada et al.

Cytosolic HSP90 regulates the heat shock response that is responsible for heat acclimation in Arabidopsis thaliana

J. Biol. Chem.

(2007)

Y. Zheng et al.

Potassium nitrate application alleviates sodium chloride stress in winter wheat cultivars differing in salt tolerance

J. Plant Physiol.

(2008)

V.Y. Alvarado et al.

A cis regulatory element in the TAPNAC promoter directs tapetal gene expression

Plant Mol. Biol.

(2011)

M. Ashburner et al.

Gene ontology: tool for the unification of biology. The gene ontology consortium

Nat. Genet.

(2000)

K. Boutilier et al.

Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth

Plant Cell Online

(2002)

W. Chen et al.

Identification and comparative analysis of differential gene expression in soybean leaf tissue under drought and flooding stress revealed by RNA-Seq

Front. Plant Sci.

(2016)

E.K. Cho et al.

ATP-independent thermoprotective activity of Nicotiana tabacum heat shock protein 70 in Escherichia coli

J. Biochem. Mol. Biol.

(2007)

X. Chu et al.

The cotton WRKY gene GhWRKY41 positively regulates salt and drought stress tolerance in transgenic Nicotiana benthamiana

PLoS One

(2015)

L. Cui et al.

Genome-wide identification, phylogeny and expression analysis of AP2/ERF transcription factors family in Brachypodium distachyon

BMC Genomics

(2016)

J.W. Cutcliffe et al.

CRFs form protein-protein interactions with each other and with members of the cytokinin signalling pathway in Arabidopsis via the CRF domain

J. Exp. Bot.

(2011)

A. Damerum et al.

Elucidating the genetic basis of antioxidant status in lettuce (Lactuca sativa)

Hortic. Res.

(2015)

A. Das et al.

Leaf proteome analysis reveals prospective drought and heat stress response mechanisms in soybean

Biomed Res. Int.

(2016)

R.S. Dhindsa et al.

Leaf senescence : correlation with increased levels of membrane permeability and lipid peroxidation and increased levels of superoxide dismutase and catalase

J. Exp. Bot.

(1981)

W.E. Emmerich et al.

Polyethylene glycol solution contact effects on seed germination

Agron. J.

(1990)

FAO

Global Agriculture Towards 2050

(2009)

P.H. Graham et al.

Legumes: importance and constraints to greater use

Plant Physiol.

(2003)

N. Haga et al.

R1R2R3-Myb proteins positively regulate cytokinesis through activation ofKNOLLE transcription in Arabidopsis thaliana

Development

(2007)

N. Haga et al.

Mutations in MYB3R1 and MYB3R4 cause pleiotropic developmental defects and preferential down-regulation of multiple G2/M-specific genes in Arabidopsis

Plant Physiol.

(2011)

D.R. Hoagland et al.

The water-culture method for growing plants without soil

Calif. Agric. Exp. Station Circ.

(1950)

D.W. Hopper et al.

Transcriptomic network analyses of leaf dehydration responses identify highly connected ABA and ethylene signaling hubs in three grapevine species differing in drought tolerance

BMC Plant Biol.

(2016)

E.J. Hsieh et al.

Functional characterization of an abiotic stress-inducible transcription factor AtERF53 in Arabidopsis thaliana

Plant Mol. Biol.

(2013)

X. Huang et al.

OsSLI1, a homeodomain containing transcription activator, involves abscisic acid related stress response in rice (Oryza sativa L.)

Sci. World J.

(2014)

S.Y. Hwang et al.

Reduced susceptibility to waterlogging together with high-light stress is related to increases in superoxide dismutase and catalase activities in sweet potato

Plant Growth Regul.

(1999)

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Transcriptome profilling analysis characterized the gene expression patterns responded to combined drought and heat stresses in soybean

Highlights

Abstract

Graphical abstract

Section snippets

Plant materials and stress treatment

Physiological analyses of soybean under drought and heat stress

Discussion

Conclusions

Acknowledgments

Fuel

Ecol. Eng.

Plant Sci.

Sci. Hortic.

South Afr. J. Bot.

Plant Physiol. Biochem. Ppb

Acta Ecol. Sin.

Mol. Plant

Plant Physiol. Biochem.

BMC Plant Biol.

J. Cereal Sci.

Plant Sci.

Environ. Exp. Bot.

Trends Plant Sci.

Environ. Exp. Bot.

Environ. Exp. Bot.

FEBS Lett.

Biochim. Biophys. Acta

J. Biol. Chem.

J. Plant Physiol.

A cis regulatory element in the TAPNAC promoter directs tapetal gene expression

Plant Mol. Biol.

Gene ontology: tool for the unification of biology. The gene ontology consortium

Nat. Genet.

Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth

Plant Cell Online

Identification and comparative analysis of differential gene expression in soybean leaf tissue under drought and flooding stress revealed by RNA-Seq

Front. Plant Sci.

ATP-independent thermoprotective activity of Nicotiana tabacum heat shock protein 70 in Escherichia coli

J. Biochem. Mol. Biol.

The cotton WRKY gene GhWRKY41 positively regulates salt and drought stress tolerance in transgenic Nicotiana benthamiana

PLoS One

Genome-wide identification, phylogeny and expression analysis of AP2/ERF transcription factors family in Brachypodium distachyon

BMC Genomics

CRFs form protein-protein interactions with each other and with members of the cytokinin signalling pathway in Arabidopsis via the CRF domain

J. Exp. Bot.

Elucidating the genetic basis of antioxidant status in lettuce (Lactuca sativa)

Hortic. Res.

Leaf proteome analysis reveals prospective drought and heat stress response mechanisms in soybean

Biomed Res. Int.

Leaf senescence : correlation with increased levels of membrane permeability and lipid peroxidation and increased levels of superoxide dismutase and catalase

J. Exp. Bot.

Polyethylene glycol solution contact effects on seed germination

Agron. J.

Global Agriculture Towards 2050

Legumes: importance and constraints to greater use

Plant Physiol.

R1R2R3-Myb proteins positively regulate cytokinesis through activation ofKNOLLE transcription in Arabidopsis thaliana

Development

Mutations in MYB3R1 and MYB3R4 cause pleiotropic developmental defects and preferential down-regulation of multiple G2/M-specific genes in Arabidopsis

Plant Physiol.

The water-culture method for growing plants without soil

Calif. Agric. Exp. Station Circ.

Transcriptomic network analyses of leaf dehydration responses identify highly connected ABA and ethylene signaling hubs in three grapevine species differing in drought tolerance

BMC Plant Biol.

Functional characterization of an abiotic stress-inducible transcription factor AtERF53 in Arabidopsis thaliana

Plant Mol. Biol.

OsSLI1, a homeodomain containing transcription activator, involves abscisic acid related stress response in rice (Oryza sativa L.)

Sci. World J.

Reduced susceptibility to waterlogging together with high-light stress is related to increases in superoxide dismutase and catalase activities in sweet potato

Plant Growth Regul.