Arabidopsis ENOR3 regulates RNAi-mediated antiviral defense

Hua Gao; Mai Yang; Haitao Yang; Yue Qin; Biyun Zhu; Gang Xu; Chengyuan Xie; Dewei Wu; Xiaolin Zhang; Wanxiang Li; Jianbin Yan; Susheng Song; Tiancong Qi; Shou-Wei Ding; Daoxin Xie

doi:10.1016/j.jgg.2017.11.005

Volume 45 Issue 1

Jan. 2018

Turn off MathJax

Article Contents

Article Navigation > Journal of Genetics and Genomics > 2018 > 45(1): 33-40

PDF( 2321 KB)

Arabidopsis ENOR3 regulates RNAi-mediated antiviral defense

doi: 10.1016/j.jgg.2017.11.005

a
Tsinghua-Peking Joint Center for Life Sciences, and MOE Key Laboratory of Bioinformatics, School of Life Sciences, Tsinghua University, Beijing 100084, China
b
Department of Microbiology and Plant Pathology, University of California, Riverside, CA 92521, USA
c
Beijing Key Laboratory of Plant Gene Resources and Biotechnology for Carbon Reduction and Environmental Improvement, College of Life Sciences, Capital Normal University, Beijing 100048, China

More Information

Corresponding author: E-mail address: qitiancong@163.com (Tiancong Qi); E-mail address: shou-wei.ding@ucr.edu (Shou-Wei Ding); E-mail address: daoxinlab@tsinghua.edu.cn (Daoxin Xie)
Received Date: 2017-08-03
Accepted Date: 2017-11-27
Rev Recd Date: 2017-11-23

Available Online: 2017-12-24

Publish Date: 2018-01-20

Abstract

Abstract

Viruses can infect host plants to cause severe diseases and substantial agricultural loss, while plants have evolved RNA interference (RNAi) strategy to defend against viral infection. Despite enormous efforts, only a few host proteins in RNAi pathway were shown to mediate antiviral defense, including RNA-dependent RNA polymerase 1 (RDR1), RDR6, DICER-LIKE 2 (DCL2) and DCL4. In this study, we carried out a genetic screen for antiviral factors of RNAi pathway in Arabidopsis rdr6 background via inoculation with a 2b-deficient Cucumber Mosaic Virus (CMV-Δ2b). We identified a mutant susceptible to CMV-Δ2b, referred to as (enor) 3-1 rdr6, and found that ENOR3 encodes a functionally unknown protein with high homology to the mammalian Non Imprinted in Prader-Willi/Angelman (NIPA) magnesium transporters. ENOR3 inhibits accumulation of CMV-Δ2b and acts additively with RDR1, RDR6, DCL2 and DCL4 in antiviral defense. These results uncover that ENOR3 is a key component in antiviral RNAi pathway, and provide new insights into antiviral immunity.
- Antiviral defense,
- CMV-Δ2b,
- DCL2/4,
- ENOR3,
- RDR1/6,
- RNAi

These authors contributed equally to this work.

FullText(HTML)

References(37)

References

[1]	Akbergenov, R., Si-Ammour, A., Blevins, T. et al. Molecular characterization of geminivirus-derived small RNAs in different plant species Nucleic Acids Res., 34 (2006),pp. 462-471
[2]	Baulcombe, D. RNA silencing in plants Nature, 431 (2004),pp. 356-363
[3]	Bouche, N., Lauressergues, D., Gasciolli, V. et al. EMBO J., 25 (2006),pp. 3347-3356
[4]	Chai, J.H., Locke, D.P., Greally, J.M. et al. Identification of four highly conserved genes between breakpoint hotspots BP1 and BP2 of the Prader-Willi/Angelman syndromes deletion region that have undergone evolutionary transposition mediated by flanking duplicons Am. J. Hum. Genet., 73 (2003),pp. 898-925
[5]	Csorba, T., Burgyán, J.
[6]	Dalmay, T., Hamilton, A., Rudd, S. et al. Cell, 101 (2000),pp. 543-553
[7]	Deleris, A., Gallego-Bartolome, J., Bao, J.S. et al. Hierarchical action and inhibition of plant Dicer-like proteins in antiviral defense Science, 313 (2006),pp. 68-71
[8]	Diaz-Pendon, J.A., Li, F., Li, W.X. et al. Plant Cell, 19 (2007),pp. 2053-2063
[9]	Ding, S.W. RNA-based antiviral immunity Nat. Rev. Immunol., 10 (2010),pp. 632-644
[10]	Ding, S.W., Lu, R. Virus-derived siRNAs and piRNAs in immunity and pathogenesis Curr. Opin. Virol., 1 (2011),pp. 533-544
[11]	Duan, C.G., Fang, Y.Y., Zhou, B.J. et al. Plant Cell, 24 (2012),pp. 259-274
[12]	Fusaro, A.F., Matthew, L., Smith, N.A. et al. RNA interference-inducing hairpin RNAs in plants act through the viral defence pathway EMBO Rep., 7 (2006),pp. 1168-1175
[13]	Garcia-Ruiz, H., Takeda, A., Chapman, E.J. et al. Plant Cell, 22 (2010),pp. 481-496
[14]	Gonzalez, I., Rakitina, D., Semashko, M. et al. RNA binding is more critical to the suppression of silencing function of Cucumber mosaic virus 2b protein than nuclear localization RNA, 18 (2012),pp. 771-782
[15]	Goytain, A., Hines, R.M., El-Husseini, A. et al. J. Biol. Chem., 282 (2007),pp. 8060-8068
[16]	Goytain, A., Hines, R.M., Quamme, G.A. Am. J. Physiol. Cell Physiol., 295 (2008),pp. C944-C953
[17]	Guo, Z.X., Lu, J.F., Wang, X.B. et al. Proc. Natl. Acad. Sci. U. S. A., 114 (2017),pp. 1377-1382
[18]	Harvey, J.J.W., Lewsey, M.G., Patel, K. et al. An antiviral defense role of AGO2 in Plants PLoS One, 6 (2011),p. e14639
[19]	Li, F., Ding, S.W. Virus counterdefense: diverse strategies for evading the RNA-silencing immunity Annu. Rev. Microbiol., 60 (2006),pp. 503-531
[20]	Li, S., Liu, L., Zhuang, X. et al. Cell, 153 (2013),pp. 562-574
[21]	Mourrain, P., Beclin, C., Elmayan, T. et al. Cell, 101 (2000),pp. 533-542
[22]	Neff, M.M., Turk, E., Kalishman, M. Web-based primer design for single nucleotide polymorphism analysis Trends Genet., 18 (2002),pp. 613-615
[23]	Nelson, B.K., Cai, X., Nebenfuhr, A. Plant J., 51 (2007),pp. 1126-1136
[24]	Palukaitis, P., Garcia-Arenal, F. Cucumoviruses Adv. Virus Res., 62 (2003),pp. 241-323
[25]	Qi, T., Song, S., Ren, Q. et al. Plant Cell, 23 (2011),pp. 1795-1814
[26]	Qu, F., Ye, X.H., Morris, T.J. Proc. Natl. Acad. Sci. U. S. A., 105 (2008),pp. 14732-14737
[27]	Rainier, S., Chai, J.H., Tokarz, D. et al. Am. J. Hum. Genet., 73 (2003),pp. 967-971
[28]	Schneeberger, K., Ossowski, S., Lanz, C. et al. SHOREmap: simultaneous mapping and mutation identification by deep sequencing Nat. Med., 6 (2009),pp. 550-551
[29]	Song, S., Qi, T., Fan, M. et al. The bHLH subgroup IIId factors negatively regulate jasmonate-mediated plant defense and development PLoS Genet., 9 (2013),p. e1003653
[30]	Sun, H., Schneeberger, K. SHOREmap v3.0: fast and accurate identification of causal mutations from forward genetic screens Meth. Mol. Biol., 1284 (2015),pp. 381-395
[31]	Tamura, K., Stecher, G., Peterson, D. et al. MEGA6: molecular evolutionary genetics analysis version 6.0 Mol. Biol. Evol., 30 (2013),pp. 2725-2729
[32]	Wang, X.B., Jovel, J., Udomporn, P. et al. Plant Cell, 23 (2011),pp. 1625-1638
[33]	Wang, X.B., Wu, Q.F., Ito, T. et al. Proc. Natl. Acad. Sci. U. S. A., 107 (2010),pp. 484-489
[34]	Xie, H., Zhang, Y.H., Zhang, P.P. et al. PLoS One, 9 (2014),p. e109749
[35]	Yan, L.H., Wei, S.W., Wu, Y.R. et al. Mol. Plant, 8 (2015),pp. 1820-1823
[36]	Zhang, X.R., Yuan, Y.R., Pei, Y. et al. Genes Dev., 20 (2006),pp. 3255-3268
[37]	Zhu, B.Y., Gao, H., Xu, G. et al. Front. Plant Sci., 8 (2017),p. 422