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Molecular characterization of rice sphingosine-1-phosphate lyase gene OsSPL1 and functional analysis of its role in disease resistance response

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Abstract

Key message

Our results indicate that overexpression of OsSPL1 in transgenic tobacco plants attenuated disease resistance and facilitated programmed cell death.

Abstract

Long-chain base phosphates including sphingosine-1-phosphate have been shown to act as signaling mediators in regulating programmed cell death (PCD) and stress responses in mammals. In the present study, we characterized a rice gene OsSPL1, encoding a putative sphingosine-1-phosphate lyase that is involved in metabolism of sphingosine-1-phosphate. Expression of OsSPL1 was down-regulated in rice plants after treatments with salicylic acid, benzothiadiazole and 1-amino cyclopropane-1-carboxylic acid, but was induced by infection with a virulent strain of Magnaporthe oryzae, the causal agent of rice blast disease. Transgenic tobacco lines with overexpression of OsSPL1 were generated and analyzed for the possible role of OsSPL1 in disease resistance response and PCD. The OsSPL1-overexpressing tobacco plants displayed increased susceptibility to infection of Pseudomonas syringae pv. tabaci (Pst), the causal agent of wildfire disease, showing severity of disease symptom and bacterial titers in inoculated leaves, and attenuated pathogen-induced expression of PR genes after infection of Pst as compared to the wild-type and vector-transformed plants. Higher level of cell death, as revealed by dead cell staining, leakage of electrolyte and expression of hypersensitive response indicator genes, was observed in the OsSPL1-overexpressing plants after treatment with fumonisin B1, a fungal toxin that induces PCD in plants. Our results suggest that OsSPL1 has different functions in regulating disease resistance response and PCD in plants.

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Abbreviations

ACC:

1-Amino cyclopropane-1-carboxylic acid

At:

Arabidopsis thaliana

BTH:

Benzothiadiazole

DOPA_deC:

Pyridoxal-dependent decarboxylase

FB1:

Fumonisin B1

FITC:

Fluorescein isothiocyanate

HR:

Hypersensitive response

JA:

Jasmonic acid

LCBs:

Sphingolipid long-chain bases

M. oryzae :

Magnaporthe oryzae

MS medium:

Murashige and Skoog medium

ORF:

Open reading frame

Os:

Oryza sativa

PCD:

Programmed cell death

PR:

Pathogenesis-related

Pst :

Pseudomonas syringae pv. tabaci

RT-PCR:

Reverse transcription-PCR

S1P:

Sphingosine-1-phosphate

SA:

Salicylic acid

SPL:

Sphingosine-1-phosphate lyase

SPT:

Serine palmitoyltransferase

WT:

Wild-type

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Acknowledgments

This study was supported by the National Key Project for Research on Transgenic Plant (2011ZX08009-003), the National Natural Science Foundation of China (no. 31272028 and no. 31101397), the High-Tech Research and Development Program of China (No. 2012AA101504) and the Fundamental Research Funds for the Central Universities.

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  1. State Key Laboratory of Rice Biology, Institute of Biotechnology, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, Zhejiang, 310058, People’s Republic of China

    Huijuan Zhang, Xiaoyi Jin, Lei Huang, Yongbo Hong, Yafen Zhang, Zhigang Ouyang, Xiaohui Li, Fengming Song & Dayong Li

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  1. Huijuan Zhang
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  2. Xiaoyi Jin
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Correspondence to Dayong Li.

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Communicated by Qiao Zhao.

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Zhang, H., Jin, X., Huang, L. et al. Molecular characterization of rice sphingosine-1-phosphate lyase gene OsSPL1 and functional analysis of its role in disease resistance response. Plant Cell Rep 33, 1745–1756 (2014). https://doi.org/10.1007/s00299-014-1653-0

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