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Transcriptomic changes and signalling pathways induced by arsenic stress in rice roots

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Abstract

Arsenic (As) is considered the most common toxic metalloid, but its molecular mode of action is not well understood. We investigated whether arsenate [As(V)] can induce intracellular reactive oxygen species production and calcium oscillation in rice roots. To better understand the molecular basis of plant cell responses to As, we performed a large-scale analysis of the rice transcriptome during As(V) stress. As(V) induced genes involved in abiotic stress, detoxification pathways and secondary metabolic process. Genes involved in secondary cell wall biogenesis, cell cycle and oligopeptide transport were mainly downregulated. Genes encoding signalling components such as receptor-like cytoplasmic kinases protein kinase, APETALA2/ethylene response factor, heat shock factor, MYB and zinc-finger protein expressed in inflorescence meristem transcription factors were increased in expression. The expression of GARP-G2-like and C3H transcription factors was specifically modulated by As(V) stress. The predominant families of As(V)-regulated transporters belonged to the ATP-binding cassette superfamily and telurite-resistance/dicarboxylate transporters. Several factors involved in signaling, such as mitogen-activated protein kinase (MAPK), MAPK kinase kinase and calcium-dependent protein kinase (CDPK), were also upregulated. Moreover, As(V) markedly increased the activity of MAPKs and CDPK-like kinases, and CDPK and NADPH oxidases were involved in As-induced MAPK activation. Further characterization of these As(V)-responsive genes and signalling pathways may help better understand the mechanisms of metalloid uptake, tolerance and detoxification in plants.

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Abbreviations

ABA:

Abscissic acid

ABC superfamily:

ATP-binding cassette superfamily

AOX:

Alterative oxidase

AP2/ERF:

APETALA2/ethylene response factor

As:

Arsenic

As(III):

Arsenite

As(V):

Arsenate

BGAL:

Beta-galactosidases

Ca2+ :

Calcium

CDK:

Cyclin-dependent kinase

CDPK:

Ca2+-dependent protein kinase

CK:

Cytokinin

CM-H2DCF-DA:

5-(and-6)-Chloromethyl-2′,7′-dichlorodihydrofluorescein diacetate, acetyl ester

CSL:

Beta-mannan synthase-like

DHAR:

Dehydroascorbate reductase

DPI:

Diphenylene iodonium

EF1G:

Elongation factor 1 gamma

FDR:

False discovery rate

GA:

Gibberellin

GH9:

Glycoside hydrolases 9

GH28:

Polygalacturonases

GO:

Gene ontology

GR:

Glutathione reductase

GT8:

Glycosyl transferases (pectin bios.)

Grx:

Glutaredoxin

GST:

Glutathione S-transferase

HSF:

Heat shock factor

ICP-AES:

Inductively coupled plasma-atmoic emission spectrometry

JA:

Jasmonic acid

MAPK:

Mitogen-activated protein kinase

MAPKKK:

MAPK kinase kinase

MBP:

Myelin basic protein

MC family transporter:

Mitochondrial carrier family transporter

MVA pathway:

Mevalonic acid pathway

PCs:

Phytochelatins

POT-family:

Proton-dependent oligopeptide transporter family

Prx:

Class III peroxidase

qRT-PCR:

Quantitative RT-PCR

RLCK subfamily:

Receptor-like cytoplasmic kinases subfamily

RLK family:

Receptor-like kinase family

ROS:

Reactive oxygen species

TCHQD:

Tetrachlorohydroquinone dehalogenase

TDT:

Telurite-resistance/dicarboxylate

TFs:

Transcription factors

Trx:

Thioredoxin

XGT:

Xyloglucan galactosyltransferases

XTH:

Xyloglucan endotransglycosylases/hydrolases

XXT:

Xyloglucan xylosyltransferases and galactomannan galactosyltransferases

ZIM transcription factor:

Zinc-finger protein expressed in inflorescence meristem transcription factor

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Acknowledgments

This work was supported by research grants from NSC and Ministry of Eudcation. Microarray assays were performed by the DNA Microarray Core Laboratory at the Institute of Plant and Microbial Biology, Academia Sinica. Data mining performed at the Bioinformatics Core for Genomic Medicine and Biotechnology Development at NCKU, supported by NSC (97-3112-B-006-011). Furthermore, we thank Ms. Laura Smales (Canada) for English editing.

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Authors and Affiliations

  1. Department of Life Sciences, National Cheng Kung University, No. 1 University Road, 701, Tainan City, Taiwan

    Tsai-Lien Huang, Quynh Thi Thuy Nguyen, Chung-Yi Lin, Ying-Chih Chen & Hao-Jen Huang

  2. Department of Biology, National Changhua University of Education, No. 1, Jin-De Road, 500, Changhua City, Taiwan

    Shih-Feng Fu

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  1. Tsai-Lien Huang
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  2. Quynh Thi Thuy Nguyen
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  3. Shih-Feng Fu
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Correspondence to Hao-Jen Huang.

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Tsai-Lien Huang, Quynh Thi Thuy Nguyen contributed equally to this article.

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Huang, TL., Nguyen, Q.T.T., Fu, SF. et al. Transcriptomic changes and signalling pathways induced by arsenic stress in rice roots. Plant Mol Biol 80, 587–608 (2012). https://doi.org/10.1007/s11103-012-9969-z

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