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The Chilli Veinal Mottle Virus Regulates Expression of the Tobacco Mosaic Virus Resistance Gene N and Jasmonic Acid/Ethylene Signaling Is Essential for Systemic Resistance Against Chilli Veinal Mottle Virus in Tobacco

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Abstract

Genetic, physiological, and molecular analyses have revealed that the stress-related phytohormones salicylic acid (SA), jasmonic acid (JA), and ethylene (ET) are known to participate in defense responses to mitigate biotic stress in plants. Recent evidence suggests that N-gene (a typical resistance gene) transcription is upregulated by Tobacco mosaic virus (TMV) infection, which is specifically a TMV-related phenomenon. In this study, we investigated N-gene transcription in tobaccoNN infected with Chilli veinal mottle virus (ChiVMV). Furthermore, we used a virus-induced gene-silencing-based genetics approach to investigate the function of SA, JA, and ET biosynthesis or signaling genes in systemic resistance to ChiVMV. Northern blot and qRT-PCR analysis indicate that N-gene transcription is stimulated by ChiVMV. Hormone measurements demonstrate that JA and ET increase rapidly during the early stages of ChiVMV infection, whereas SA increases slightly at later stages. JA and ET biosynthetic, signaling, and marker genes are significantly activated after ChiVMV inoculation, whereas SA biosynthetic, signaling, and marker genes are increased slightly. Silencing of JA, ET biosynthetic and signaling genes strongly increase the plants’ susceptibility to ChiVMV, whereas silencing of SA biosynthetic and signaling genes only partly compromise systemic resistance. Extensive ROS accumulate in JA, ET biosynthetic and signaling gene-silenced plants after ChiVMV infection, whereas only slight ROS produce in SA biosynthetic and signaling gene-silenced plants. Taken together, our results indicate that N-gene transcription is upregulated by ChiVMV infection, and the JA/ET pathways play an important role in plant systemic resistance against ChiVMV, whereas the SA pathway is only minorly involved.

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Abbreviations

ChiVMV:

Chilli veinal mottle virus

DAB:

3,3′-Diaminobenzidine

ET:

Ethylene

JA:

Jasmonic acid

NBS:

Nucleotide-binding site

NBT:

Nitro blue tetrazolium

PCD:

Programmed cell death

ROS:

Reactive oxygen species

SA:

Salicylic acid

TMV:

Tobacco mosaic virus

VIGS:

Virus-induced gene-silencing

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Acknowledgments

We thank Jian-Zhong Liu (Zhejiang Normal University, Jinhua, China) for providing the Nicotiana tabacum (tobacco) cv. Samsun NN (tobaccoNN) and the N. tabacum cv. Petite Havana SR1, termed SR1 nn (tobacconn) seeds. This work was supported by the National Nature Science Foundation of China (91017004, 31070210, 31171835, and 31270290), Doctoral Foundation of the Ministry of Education (20110181110059 and 20120181130008), Sichuan and Chengdu Nature Science Foundation (2010JQ0080, 11DXYB097JH-027, and 2012JY0078) and Fundamental Research Funds for the Central Universities (2011SCU04B34).

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Authors and Affiliations

  1. Ministry of Education Key Laboratory for Bio-Resource and Eco-Environment, College of Life Science, Sichuan University, Chengdu, 610064, China

    Feng Zhu, De-Hui Xi, Xing-Guang Deng, Xing-Ji Peng, He Tang, Ying-Juan Chen, Wei Jian & Hong-Hui Lin

  2. State Key Laboratory of Hydraulics and Mountain River Engineering, Sichuan University, Chengdu, 610065, China

    Hong-Hui Lin

  3. Chengdu Normal College, Chengdu, 611130, China

    Hong Feng

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  1. Feng Zhu
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  2. De-Hui Xi
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Correspondence to Hong-Hui Lin.

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F. Zhu and D.-H. Xi contributed equally to this work.

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Zhu, F., Xi, DH., Deng, XG. et al. The Chilli Veinal Mottle Virus Regulates Expression of the Tobacco Mosaic Virus Resistance Gene N and Jasmonic Acid/Ethylene Signaling Is Essential for Systemic Resistance Against Chilli Veinal Mottle Virus in Tobacco. Plant Mol Biol Rep 32, 382–394 (2014). https://doi.org/10.1007/s11105-013-0654-4

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