Coat protein of rice stripe virus enhances autophagy activity through interaction with cytosolic glyceraldehyde-3-phosphate dehydrogenases, a negative regulator of plant autophagy

Wanying Zhao, Li Wang, Lipeng Li, Tong Zhou, Fei Yan, Heng Zhang, Ying Zhu, Ida Bagus Andika, Liying Sun

Stress Biology ›› 2023, Vol. 3 ›› Issue (1) : 3. DOI: 10.1007/s44154-023-00084-3
Original Paper

Coat protein of rice stripe virus enhances autophagy activity through interaction with cytosolic glyceraldehyde-3-phosphate dehydrogenases, a negative regulator of plant autophagy

Author information +
History +

Abstract

Viral infection commonly induces autophagy, leading to antiviral responses or conversely, promoting viral infection or replication. In this study, using the experimental plant Nicotiana benthamiana, we demonstrated that the rice stripe virus (RSV) coat protein (CP) enhanced autophagic activity through interaction with cytosolic glyceraldehyde-3-phosphate dehydrogenase 2 (GAPC2), a negative regulator of plant autophagy that binds to an autophagy key factor, autophagy-related protein 3 (ATG3). Competitive pull-down and co-immunoprecipitation (Co-IP)assays showed that RSV CP activated autophagy by disrupting the interaction between GAPC2 and ATG3. An RSV CP mutant that was unable to bind GAPC2 failed to disrupt the interaction between GAPC2 and ATG3 and therefore lost its ability to induce autophagy. RSV CP enhanced the autophagic degradation of a viral movement protein (MP) encoded by a heterologous virus, citrus leaf blotch virus (CLBV). However, the autophagic degradation of RSV-encoded MP and RNA-silencing suppressor (NS3) proteins was inhibited in the presence of CP, suggesting that RSV CP can protect MP and NS3 against autophagic degradation. Moreover, in the presence of MP, RSV CP could induce the autophagic degradation of a remorin protein (NbREM1), which negatively regulates RSV infection through the inhibition of viral cell-to-cell movement. Overall, our results suggest that RSV CP induces a selective autophagy to suppress the antiviral factors while protecting RSV-encoded viral proteins against autophagic degradation through an as-yet-unknown mechanism. This study showed that RSV CP plays dual roles in the autophagy-related interaction between plants and viruses.

Keywords

RSV / Coat protein / Autophagy / GAPC / ATG3

Cite this article

Download citation ▾
Wanying Zhao, Li Wang, Lipeng Li, Tong Zhou, Fei Yan, Heng Zhang, Ying Zhu, Ida Bagus Andika, Liying Sun. Coat protein of rice stripe virus enhances autophagy activity through interaction with cytosolic glyceraldehyde-3-phosphate dehydrogenases, a negative regulator of plant autophagy. Stress Biology, 2023, 3(1): 3 https://doi.org/10.1007/s44154-023-00084-3

References

[1]
AdachiA, KoizumiM, OhsumiY. Autophagy induction under carbon starvation conditions is negatively regulated by carbon catabolite repression. J Biol Chem, 2017, 292(48):19905-19918
CrossRef Google scholar
[2]
Avin-WittenbergT. Autophagy and its role in plant abiotic stress management. Plant Cell Environ., 2019, 42(3):1045-1053
CrossRef Google scholar
[3]
BarbierP, TakahashiM, NakamuraI, ToriyamaS, IshihamaA. Solubilization and promoter analysis of RNA polymerase from rice stripe virus. J Virol., 1992, 66(10):6171
CrossRef Google scholar
[4]
Cerff R (1978) Glyceraldehyde-3-phosphate dehydrogenase (NADP) from Sinapis alba: Steady state kinetics. Phytochemistry 17(12):2061–2067. https://doi.org/10.1016/S0031-9422(00)89281-X
[5]
Chen H, Dong J, Wang T (2021) Autophagy in Plant Abiotic Stress Management. Int J Mol Sci. 22 (8). https://doi.org/10.3390/ijms22084075
[6]
Choi AMK, Ryter SW, Levine B (2013) Autophagy in human health and disease. New Engl J Med 368(7):651–662. https://doi.org/10.1056/NEJMra1205406.
[7]
FalkBW, TsaiJH. Biology and molecular biology of viruses in the genus Tenuivirus. Annu Rev Phytopathol., 1998, 36: 139-163
CrossRef Google scholar
[8]
FuS, XuY, LiC, LiY, WuJ, ZhouX. Rice stripe virus interferes with S-acylation of remorin and induces its autophagic degradation to facilitate virus infection. Mol Plant., 2018, 11(2):269-287
CrossRef Google scholar
[9]
GallegosJ. Autophagy: Both Friend and Foe in Pseudomonas syringae Infection. Plant Cell., 2018, 30(3):522-523
CrossRef Google scholar
[10]
Guan B, Jiang YT, Lin DL, Lin WH, Xue HW (2022) Phosphatidic acid suppresses autophagy through competitive inhibition by binding GAPC (glyceraldehyde-3-phosphate dehydrogenase) and PGK (phosphoglycerate kinase) proteins. Autophagy:1–15. https://doi.org/10.1080/15548627.2022.2046449
[11]
Guo L, Ma F, Wei F, Fanella B, Allen DK, Wang X (2014) Cytosolic phosphorylating glyceraldehyde-3-Phosphate dehydrogenases affect arabidopsis cellular metabolism and promote seed oil accumulation. Plant Cell. 26(7):3023–3035. https://doi.org/10.1105/tpc.114.126946
[12]
HafrénA, MaciaJ-L, LoveAJ, MilnerJJ, DruckerM, HofiusD. Selective autophagy limits cauliflower mosaic virus infection by NBR1-mediated targeting of viral capsid protein and particles. Proc Natl Acad Sci., 2017, 114(10):E2026-E2035
CrossRef Google scholar
[13]
HanK, HuangH, ZhengH, JiM, YuanQ, CuiW, ZhangH, PengJ, LuY, RaoS, WuG, LinL, SongX, SunZ, LiJ, ZhangC, LouY, ChenJ, YanF. Rice stripe virus coat protein induces the accumulation of jasmonic acid, activating plant defence against the virus while also attracting its vector to feed. Mol Plant Pathol., 2020, 21(12):1647-1653
CrossRef Google scholar
[14]
HanS, WangY, ZhengX, JiaQ, ZhaoJ, BaiF, HongY, LiuY. Cytoplastic glyceraldehyde-3-phosphate dehydrogenases interact with ATG3 to negatively regulate autophagy and immunity in nicotiana benthamiana. Plant Cell., 2015, 27(4):1316-1331
CrossRef Google scholar
[15]
Haxim Y, Ismayil A, Qi J, Yan W, Liu Y (2017) Autophagy functions as an antiviral mechanism against geminiviruses in plants. eLife. 6:e23897. https://doi.org/10.7554/eLife.23897
[16]
HeydarnejadJ, BarclayWS, IzadpanahK, HunterFR, GoodingMJ. Molecular characterization of Iranian wheat stripe virus shows its taxonomic position as a distinct species in the genus tenuivirus. Adv Virol., 2006, 151(2):217-227
CrossRef Google scholar
[17]
HongYG, PeiMY, WangXF, BoT, LiL, ChenSX. The study of molecular biology of rice stripe virus (I) (eng). Chin Sci Bull., 1991, 36(7):602-605
[18]
HuangTS, NagyPD. Direct inhibition of tombusvirus plus-strand RNA synthesis by a dominant negative mutant of a host metabolic enzyme, glyceraldehyde-3-phosphate dehydrogenase, in yeast and plants. J Virol., 2011, 85(17):9090-9102
CrossRef Google scholar
[19]
Huo Y, Liu W, Zhang F, Chen X, Li L, Liu Q, Zhou Y, Wei T, Fang R, Wang X (2014) Transovarial transmission of a plant virus is mediated by vitellogenin of its insect vector. PLoS Pathogens. 10(3):e1003949. https://doi.org/10.1371/journal.ppat.1003949
[20]
ImanA, MelanieS, ThomasG, DieterW, Weiergräber OH,. The Atg8 family of proteins—modulating shape and functionality of autophagic membranes. Front Genet., 2017, 8: 109
CrossRef Google scholar
[21]
IsmayilA, YangM, HaximY, WangY, LiJ, HanL, WangY, ZhengX, WeiX, NagalakshmiU, HongY, Hanley-BowdoinL, LiuY. Cotton leaf curl Multan virus βC1 protein induces autophagy by disrupting the interaction of autophagy-related protein 3 with glyceraldehyde-3-phosphate dehydrogenases. Plant Cell., 2020, 32(4):1124-1135
CrossRef Google scholar
[22]
Jeon EJ, Tadamura AK, Murakami AT, Inaba JI, Kim ABM (2017) rgs-CaM detects and counteracts viral RNA silencing suppressors in plant immune priming. J Virol. 91(19):JVI.00761–00717. https://doi.org/10.1128/JVI.00761-17
[23]
JiangL, LuY, ZhengX, YangX, ChenY, ZhangT, ZhaoX, WangS, ZhaoX, SongX, ZhangX, PengJ, ZhengH, LinL, MacFarlaneS, LiuY, ChenJ, YanF. The plant protein NbP3IP directs degradation of Rice stripe virus p3 silencing suppressor protein to limit virus infection through interaction with the autophagy-related protein NbATG8. New Phytol., 2021, 229(2):1036-1051
CrossRef Google scholar
[24]
KabeyaY, MizushimaN, UenoT, YamamotoA, KirisakoT, NodaT, KominamiE, OhsumiY, YoshimoriT. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J., 2000, 19(21):5720-5728
CrossRef Google scholar
[25]
Kakutani T, Hayano Y, Hayashi T, Minobe Y (1990) Ambisense segment 4 of rice stripe virus: possible evolutionary relationship with phleboviruses and uukuviruses (Bunyaviridae). J Gen Virol. 71( Pt 7):1427. https://doi.org/10.1099/0022-1317-71-7-1427
[26]
KimS-C, ShuaibingY, QunZ, XueminW. Phospholipase Dδ and phosphatidic acid mediate heat-induced nuclear localization of glyceraldehyde-3-phosphate dehydrogenase in Arabidopsis. Plant J., 2022, 112(3):786-799
CrossRef Google scholar
[27]
KimS-M, Kook-HyungC, WonK, LianS, Yeonhwa,. Interaction study of rice stripe virus proteins reveals a region of the nucleocapsid protein (NP) required for NP self-interaction and nuclear localization. Virus Res., 2014, 183: 6-14
CrossRef Google scholar
[28]
KimH, ChoWK, LianS, KimKH. Identification of residues or motif(s) of the rice stripe virus NS3 protein required for self-interaction and for silencing suppressor activity. Virus Res., 2017, 235: 14-23
CrossRef Google scholar
[29]
KongL, WuJ, LuL, XuY, ZhouX. Interaction between Rice stripe virus disease-specific protein and host PsbP enhances virus symptoms. Mol Plant., 2014, 7(4):691-708
CrossRef Google scholar
[30]
Kormelink R, Verchot J, Tao X, Desbiez C (2021) The Bunyavirales: the plant-infecting counterparts. Viruses 13 (5). https://doi.org/10.3390/v13050842
[31]
KyongW, ChoS, LianS-M, KimS-H, ParkK-H. Current insights into research on rice stripe virus. Plant Pathol J., 2013
CrossRef Google scholar
[32]
Lan HH (2016) Research of Fonctuonal Region Involved in the Self-interaction of Rice Stripe Virus Coat Protein. Fujian J Agric Sci. http://en.cnki.com.cn/Article_en/CJFDTOTAL-FJNX201609011.htm
[33]
LearyAY, SanguankiattichaiN, DugganC, TumtasY, PandeyP, SegretinME, Salguero LinaresJ, SavageZD, YowRJ, BozkurtTO. Modulation of plant autophagy during pathogen attack. J Exp Bot., 2018, 69(6):1325-1333
CrossRef Google scholar
[34]
Li C, Xu Y, Fu S, Liu Y, Li Z, Zhang T, Wu J, Zhou X (2021) The unfolded protein response plays dual roles in rice stripe virus infection through fine-tuning the movement protein accumulation. PLoS Pathogens. 17 (3):e1009370. https://doi.org/10.1371/journal.ppat.1009370
[35]
LiF, VierstraRD. Autophagy: a multifaceted intracellular system for bulk and selective recycling. Trends Plant Sci., 2012, 17(9):526-537
CrossRef Google scholar
[36]
LiF, ZhangC, LiY, WuG, HouX, ZhouX, WangA. Beclin1 restricts RNA virus infection in plants through suppression and degradation of the viral polymerase. Nat Commun., 2018, 9(1):1268
CrossRef Google scholar
[37]
LiF, ZhangM, ZhangC, ZhouX. Nuclear autophagy degrades a geminivirus nuclear protein to restrict viral infection in solanaceous plants. New Phytol., 2020, 225(4):1746-1761
CrossRef Google scholar
[38]
LiJ, ZhaoW, WangW, ZhangL, CuiF. Evaluation of Rice stripe virus transmission efficiency by quantification of viral load in the saliva of insect vector. Pest Manag Sci., 2019, 75(7):1979-1985
CrossRef Google scholar
[39]
LianS, ChoWK, JoY, KimSM, KimKH. Interaction study of rice stripe virus proteins reveals a region of the nucleocapsid protein (NP) required for NP self-interaction and nuclear localization. Virus Res., 2014, 183: 6-14
CrossRef Google scholar
[40]
Liu X, Jin J, Qiu P, Gao F, Lin W, Xie G, He S, Liu S, Du Z, Wu Z (2018) Rice Stripe Tenuivirus Has a Greater Tendency To Use the Prime-and-Realign Mechanism in Transcription of Genomic than in Transcription of Antigenomic Template RNAs. J Virol. 92 (1). https://doi.org/10.1128/JVI.01414-17
[41]
Liu X, Liu X, Bai J, Gao Y, Song Z, Nauwynck H, Wang X, Yang Y, Jiang P (2021) Glyceraldehyde-3-phosphate dehydrogenase restricted in cytoplasmic location by viral GP5 facilitates porcine reproductive and respiratory syndrome virus replication via Its glycolytic activity. J Virol. 95 (18):e0021021. https://doi.org/10.1128/JVI.00210-21
[42]
LiuY, SchiffM, CzymmekK, TallóczyZ, LevineB, Dinesh-KumarSP. Autophagy regulates programmed cell death during the plant innate immune response. Cell., 2005, 121(4):567-577
CrossRef Google scholar
[43]
Masclaux-DaubresseC, ChenQ, HavéM. Regulation of nutrient recycling via autophagy. Curr Opin Plant Biol., 2017, 39: 8-17
CrossRef Google scholar
[44]
MizushimaN, YoshimoriT, OhsumiY. The role of Atg proteins in autophagosome formation. Annu Rev Cell Dev Biol., 2011, 27(1):107-132
CrossRef Google scholar
[45]
Nagy PD, Lin W (2020) Taking over cellular energy-metabolism for TBSV replication: The high ATP requirement of an RNA virus within the viral replication organelle. Viruses. (1). https://doi.org/10.3390/v12010056
[46]
NakaharaKS, MasutaC, YamadaS, ShimuraH, KashiharaY, WadaTS, MeguroA, GotoK, TadamuraK, SuedaK, SekiguchiT, ShaoJ, ItchodaN, MatsumuraT, IgarashiM, ItoK, CarthewRW, UyedaI. Tobacco calmodulin-like protein provides secondary defense by binding to and directing degradation of virus RNA silencing suppressors. Proc Natl Acad Sci USA., 2012, 109(25):10113-10118
CrossRef Google scholar
[47]
Niu E, Liu H, Zhou H, Luo L, Wu Y, Andika IB, Sun L (2021) Autophagy inhibits intercellular transport of citrus leaf blotch virus by Targeting viral movement protein. Viruses. 13 (11). https://doi.org/10.3390/v13112189
[48]
NiuE, YeC, ZhaoW, KondoH, WuY, ChenJ, AndikaIB, SunL. Coat protein of Chinese wheat mosaic virus upregulates and interacts with cytosolic glyceraldehyde-3-phosphate dehydrogenase, a negative regulator of plant autophagy, to promote virus infection. J Integr Plant Biol., 2022, 64(8):1631-1645
CrossRef Google scholar
[49]
PlaxtonWC. The organization and regulation of plant glycolysis. Annu Rev Plant Physiol Plant Mol Biol., 1996, 47(47):185-214
CrossRef Google scholar
[50]
PrasanthKR, HuangYW, LiouMR, WangYL, HuCC, TsaiCH, MengM, LinNS, HsuYH. Glyceraldehyde 3-Phosphate dehydrogenase negatively regulates the replication of bamboo mosaic virus and its associated satellite RNA. J Virol., 2011, 85(17):8829-8840
CrossRef Google scholar
[51]
RubinszteinD, ShpilkaT, ElazarZ. Mechanisms of Autophagosome Biogenesis. Curr Biol., 2012, 22(1):R29-R34
CrossRef Google scholar
[52]
SchwenderJ, OhlroggeJB, Shachar-HillY. A flux model of glycolysis and the oxidative pentosephosphate pathway in developing brassica napus embryos*. J Biol Chem., 2003, 278(32):29442-29453
CrossRef Google scholar
[53]
Shukla A, Hoffmann G, Hofius D, Hafrén A (2021) Turnip crinkle virus targets host ATG8 proteins to attenuate antiviral autophagy. https://doi.org/10.1101/2021.03.28.437395
[54]
ShuoX, ZhouY. Ribosomal protein L18 is an essential factor that promote rice stripe virus accumulation in small brown planthopper. Virus Res., 2018, 247: 15-20
CrossRef Google scholar
[55]
SlobodkinMR, ElazarZ. The Atg8 family: Multifunctional ubiquitin-like key regulators of autophagy. Essays Biochem., 2013, 55(1):51-64
CrossRef Google scholar
[56]
SunL, AndikaIB, KondoH, ChenJ. Identification of the amino acid residues and domains in the cysteine-rich protein of Chinese wheat mosaic virus that are important for RNA silencing suppression and subcellular localization. Mol Plant Pathol., 2013, 14(3):265-278
CrossRef Google scholar
[58]
SunL, NussDL, SuzukiN. Synergism between a mycoreovirus and a hypovirus mediated by the papain-like protease p29 of the prototypic hypovirus CHV1-EP713. J Gen Virol., 2006, 87(Pt 12):3703-3714
CrossRef Google scholar
[59]
WangA. Dissecting the molecular network of virus-plant interactions: the complex roles of host factors. Annu Rev Phytopathol., 2015, 53: 45-66
CrossRef Google scholar
[60]
WangYL, NagyPD. Tomato bushy stunt virus Co-Opts the RNA-Binding Function of a Host Metabolic Enzyme for Viral Genomic RNA Synthesis. Cell Host Microbe., 2008, 3(3):178-187
CrossRef Google scholar
[61]
Wu W, Zheng L, Chen H, Jia D, Li F, Wei T (2014) Nonstructural protein NS4 of Rice Stripe Virus plays a critical role in viral spread in the body of vector insects. PLoS One. 9 (2):e88636. https://doi.org/10.1371/journal.pone.0088636
[62]
XiongR, WuJ, ZhouY, ZhouX. Identification of a movement protein of the tenuivirus rice stripe virus. J Virol., 2008, 82(24):12304
CrossRef Google scholar
[63]
YangM, IsmayilA, LiuY. Autophagy in plant-virus interactions. Ann Rev Virol., 2020, 7(1):403-419
CrossRef Google scholar
[64]
YangM, LiuY. Autophagy in plant viral infection. FEBS Lett., 2022, 596(17):2152-2162
CrossRef Google scholar
[65]
YangM, ZhangY, XieX, YueN, LiD. Barley stripe mosaic virus γb protein subverts autophagy to promote viral infection by disrupting the ATG7-ATG8 interaction. Plant Cell., 2018, 16(7):146
CrossRef Google scholar
[66]
YuL, ChenY, ToozeSA. Autophagy pathway: Cellular and molecular mechanisms. Autophagy., 2018, 14(2):207-215
CrossRef Google scholar
[67]
Zhang KY, Xiong RY, Jian-Xiang WU, Zhou XP, Zhou YJ (2008) Detection of the proteins encoded by rice stripe virus in laodelphax striatellus fallén and interactions in vitro between CP and the four proteins. Scientia Agricultura Sinica. http://en.cnki.com.cn/Article_en/CJFDTOTAL-ZNYK200812017.htm
[68]
ZhenguoDU, XiaoD, JianguoWU, JiaD, YuanZ, LiuY, LiuyangHU, HanZ, WeiT, LinQ. p2 of Rice stripe virus (RSV) interacts with OsSGS3 and is a silencing suppressor. Mol Plant Pathol., 2011, 12(8):808-814
CrossRef Google scholar
Funding
National Natural Science Foundation of China(32170163)

Accesses

Citations

Detail

Sections
Recommended

/