Abstract
Main conclusion
For the first time it is reported that members of the nsLTP protein family could promote viral infection by inhibiting virus-induced RNA silencing.
Abstract
Non-specific lipid transfer proteins (nsLTPs) are a class of soluble proteins with low relative molecular weight and widely present in higher plants. The role of nsLTPs in biotic and abiotic stresses has been studied, but no report has shown that nsLTPs play a role in the process of viral infection. We report the function and mechanism of the classical nsLTP protein StLTP6 in viral infection. We found that StLTP6 expression was remarkably upregulated in potato infected with potato virus Y and potato virus S. The infection efficiency and virus content of StLTP6-overexpressed potato and Nicotiana benthamiana were remarkable increased. Further study found that the overexpression of StLTP6 inhibited the expression of multiple genes in the RNA silencing pathway, thereby inhibiting virus-induced RNA silencing. This result indicated that StLTP6 expression was induced during viral infection to inhibit the resistance of virus-induced RNA silencing and promote viral infection. In summary, we reported the role of StLTP6 in viral infection, broadening the biological function range of the nsLTP family and providing valuable information for the study of viral infection mechanism.
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Availability of data and materials
All relevant data and materials that support the findings of this study are available from the corresponding author upon request.
Abbreviations
- nsLTPs:
-
Non-specific lipid transfer proteins
- PVS:
-
Potato virus S
- PVX:
-
Potato virus X
- PVY:
-
Potato virus Y
- StLTP6:
-
Solanum tuberosum L. lipid transfer protein 6
References
Adhikari PB, Han JY, Ahn CH, Choi YE (2019) Lipid transfer proteins (AaLTP3 and AaLTP4) are involved in sesquiterpene lactone secretion from glandular trichomes in Artemisia annua. Plant Cell Physiol 60(12):2826–2836. https://doi.org/10.1093/pcp/pcz171
Agius C, Eamens AL, Millar AA, Watson JM, Wang MB (2012) RNA silencing and antiviral defense in plants. Methods Mol Biol 894:17–38. https://doi.org/10.1007/978-1-61779-882-5_2
Aliyari R, Ding SW (2009) RNA-based viral immunity initiated by the Dicer family of host immune receptors. Immunol Rev 227(1):176–188. https://doi.org/10.1111/j.1600-065X.2008.00722.x
Anandalakshmi R, Pruss GJ, Ge X, Marathe R, Mallory AC, Smith TH, Vance VB (1998) A viral suppressor of gene silencing in plants. Proc Natl Acad Sci USA 95(22):13079–13084. https://doi.org/10.1073/pnas.95.22.13079
Anandalakshmi R, Marathe R, Ge X, Herr JM Jr, Mau C, Mallory A, Pruss G, Bowman L, Vance VB (2000) A calmodulin-related protein that suppresses posttranscriptional gene silencing in plants. Science 290(5489):142–144. https://doi.org/10.1126/science.290.5489.142
Baulcombe D (2002) Viral suppression of systemic silencing. Trends Microbiol 10(7):306–308. https://doi.org/10.1016/s0966-842x(02)02387-9
Baulcombe D (2004) RNA silencing in plants. Nature 431(7006):356–363. https://doi.org/10.1038/nature02874
Ben Hsouna A, Ben Saad R, Dhifi W, Mnif W, Brini F (2021) Novel non-specific lipid-transfer protein (TdLTP4) isolated from durum wheat: Antimicrobial activities and anti-inflammatory properties in lipopolysaccharide (LPS)-stimulated RAW 264.7 macrophages. Microb Pathog 154:104869. https://doi.org/10.1016/j.micpath.2021.104869
Bernhard WR, Thoma S, Botella J, Somerville CR (1991) Isolation of a cDNA clone for spinach lipid transfer protein and evidence that the protein is synthesized by the secretory pathway. Plant Physiol 95(1):164–170. https://doi.org/10.1104/pp.95.1.164
Caarls L, Van der Does D, Hickman R, Jansen W, Van Verk MC, Proietti S, Lorenzo O, Solano R, Pieterse CMJ, Van Wees SCM (2017) Assessing the role of ETHYLENE RESPONSE FACTOR transcriptional repressors in salicylic acid-mediated suppression of jasmonic acid-responsive genes. Plant Cell Physiol 58(2):266–278. https://doi.org/10.1093/pcp/pcw187
Chae K, Kieslich CA, Morikis D, Kim SC, Lord EM (2009) A gain-of-function mutation of Arabidopsis lipid transfer protein 5 disturbs pollen tube tip growth and fertilization. Plant Cell 21(12):3902–3914. https://doi.org/10.1105/tpc.109.070854
Chen P-Y, Wang C-K, Soong S-C, To K-Y (2003) Complete sequence of the binary vector pBI121 and its application in cloning T-DNA insertion from transgenic plants. Mol Breeding 11(4):287–293. https://doi.org/10.1023/A:1023475710642
Cheng D-J, Tian Y-P, Geng C, Guo Y, Jia M-A, Li X-D (2020) Development and application of a full-length infectious clone of potato virus Y isolate belonging to SYR-I strain. Virus Res 276:197827. https://doi.org/10.1016/j.virusres.2019.197827
Cowan GH, Roberts AG, Jones S, Kumar P, Kalyandurg PB, Gil JF, Savenkov EI, Hemsley PA, Torrance L (2018) Potato mop-top virus co-opts the stress sensor HIPP26 for long-distance movement. Plant Physiol 176(3):2052–2070. https://doi.org/10.1104/pp.17.01698
Csorba T, Kontra L, Burgyán J (2015) Viral silencing suppressors: tools forged to fine-tune host–pathogen coexistence. Virology 479–480:85–103. https://doi.org/10.1016/j.virol.2015.02.028
Daròs JA (2017) Viral suppressors: combatting RNA silencing. Nat Plants 3:17098. https://doi.org/10.1038/nplants.2017.98
Devaux A, Goffart JP, Kromann P, Andrade-Piedra J, Polar V, Hareau G (2021) The potato of the future: opportunities and challenges in sustainable agri-food systems. Potato Res. https://doi.org/10.1007/s11540-021-09501-4
Ding SW, Voinnet O (2007) Antiviral immunity directed by small RNAs. Cell 130(3):413–426. https://doi.org/10.1016/j.cell.2007.07.039
Duan CG, Wang CH, Guo HS (2012) Application of RNA silencing to plant disease resistance. Silence 3(1):5. https://doi.org/10.1186/1758-907x-3-5
Finkina EI, Melnikova DN, Bogdanov IV, Ovchinnikova TV (2016) Lipid transfer proteins as components of the plant innate immune system: structure, functions, and applications. Acta Naturae 8(2):47–61
Gao G, Jin LP, Xie KY, Qu DY (2009) The potato StLTPa7 gene displays a complex Ca-associated pattern of expression during the early stage of potato-Ralstonia solanacearum interaction. Mol Plant Pathol 10(1):15–27. https://doi.org/10.1111/j.1364-3703.2008.00508.x
Giangrieco I, Alessandri C, Rafaiani C, Santoro M, Zuzzi S, Tuppo L, Tamburrini M, D’Avino R, Ciardiello MA, Mari A (2015) Structural features, IgE binding and preliminary clinical findings of the 7kDa lipid transfer protein from tomato seeds. Mol Immunol 66(2):154–163. https://doi.org/10.1016/j.molimm.2015.02.025
Godfray HC, Beddington JR, Crute IR, Haddad L, Lawrence D, Muir JF, Pretty J, Robinson S, Thomas SM, Toulmin C (2010) Food security: the challenge of feeding 9 billion people. Science 327(5967):812–818. https://doi.org/10.1126/science.1185383
Guo L, Yang H, Zhang X, Yang S (2013) Lipid transfer protein 3 as a target of MYB96 mediates freezing and drought stress in Arabidopsis. J Exp Bot 64(6):1755–1767. https://doi.org/10.1093/jxb/ert040
Gy I, Gasciolli V, Lauressergues D, Morel JB, Gombert J, Proux F, Proux C, Vaucheret H, Mallory AC (2007) Arabidopsis FIERY1, XRN2, and XRN3 are endogenous RNA silencing suppressors. Plant Cell 19(11):3451–3461. https://doi.org/10.1105/tpc.107.055319
Hellens R, Mullineaux P, Klee H (2000) Technical Focus:a guide to Agrobacterium binary Ti vectors. Trends Plant Sci 5(10):446–451. https://doi.org/10.1016/S1360-1385(00)01740-4
Hentze MW, Castello A, Schwarzl T, Preiss T (2018) A brave new world of RNA-binding proteins. Nat Rev Mol Cell Biol 19(5):327–341. https://doi.org/10.1038/nrm.2017.130
Huang X, Yu R, Li W, Geng L, Jing X, Zhu C, Liu H (2019) Identification and characterisation of a glycine-rich RNA-binding protein as an endogenous suppressor of RNA silencing from Nicotiana glutinosa. Planta 249(6):1811–1822. https://doi.org/10.1007/s00425-019-03122-5
Jacq A, Pernot C, Martinez Y, Domergue F, Payré B, Jamet E, Burlat V, Pacquit VB (2017) The Arabidopsis lipid transfer protein 2 (AtLTP2) is involved in cuticle-cell wall interface integrity and in etiolated hypocotyl permeability. Front Plant Sci 8:263. https://doi.org/10.3389/fpls.2017.00263
Kang H, Park SJ, Kwak KJ (2013) Plant RNA chaperones in stress response. Trends Plant Sci 18(2):100–106. https://doi.org/10.1016/j.tplants.2012.08.004
Krüger DM, Neubacher S, Grossmann TN (2018) Protein–RNA interactions: structural characteristics and hotspot amino acids. RNA 24(11):1457–1465. https://doi.org/10.1261/rna.066464.118
Li C, Xie W, Bai W, Li Z, Zhao Y, Liu H (2008) Calmodulin binds to maize lipid transfer protein and modulates its lipids binding ability. FEBS J 275(21):5298–5308. https://doi.org/10.1111/j.1742-4658.2008.06660.x
Li F, Huang C, Li Z, Zhou X (2014) Suppression of RNA silencing by a plant DNA virus satellite requires a host calmodulin-like protein to repress RDR6 expression. PLoS Pathog 10(2):e1003921. https://doi.org/10.1371/journal.ppat.1003921
Maldonado AM, Doerner P, Dixon RA, Lamb CJ, Cameron RK (2002) A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature 419(6905):399–403. https://doi.org/10.1038/nature00962
McLaughlin JE, Darwish NI, Garcia-Sanchez J, Tyagi N, Trick HN, McCormick S, Dill-Macky R, Tumer NE (2021) A lipid transfer protein has antifungal and antioxidant activity and suppresses Fusarium head blight disease and DON accumulation in transgenic wheat. Phytopathology 111(4):671–683. https://doi.org/10.1094/phyto-04-20-0153-r
Meng C, Yan Y, Liu Z, Chen L, Zhang Y, Li X, Wu L, Zhang G, Wang X, Ma Z (2018) Systematic analysis of cotton non-specific lipid transfer protein family revealed a special group that is involved in fiber elongation. Front Plant Sci 9:1285. https://doi.org/10.3389/fpls.2018.01285
Mitter N, Zhai Y, Bai AX, Chua K, Eid S, Constantin M, Mitchell R, Pappu HR (2016) Evaluation and identification of candidate genes for artificial microRNA-mediated resistance to tomato spotted wilt virus. Virus Res 211:151–158. https://doi.org/10.1016/j.virusres.2015.10.003
Niehl A, Heinlein M (2019) Perception of double-stranded RNA in plant antiviral immunity. Mol Plant Pathol 20(9):1203–1210. https://doi.org/10.1111/mpp.12798
Patkar RN, Chattoo BB (2006) Transgenic indica rice expressing nsLTP-like protein shows enhanced resistance to both fungal and bacterial pathogens. Mol Breed 17(2):159–171. https://doi.org/10.1007/s11032-005-4736-3
Qin Q, Li G, Jin L, Huang Y, Wang Y, Wei C, Xu Z, Yang Z, Wang H, Li Y (2020) Auxin response factors (ARFs) differentially regulate rice antiviral immune response against rice dwarf virus. PLoS Pathog 16(12):e1009118. https://doi.org/10.1371/journal.ppat.1009118
Sarmiento C, Nigul L, Kazantseva J, Buschmann M, Truve E (2006) AtRLI2 is an endogenous suppressor of RNA silencing. Plant Mol Biol 61(1–2):153–163. https://doi.org/10.1007/s11103-005-0001-8
Sarowar S, Kim YJ, Kim KD, Hwang BK, Ok SH, Shin JS (2009) Overexpression of lipid transfer protein (LTP) genes enhances resistance to plant pathogens and LTP functions in long-distance systemic signaling in tobacco. Plant Cell Rep 28(3):419–427. https://doi.org/10.1007/s00299-008-0653-3
Scholthof KB, Adkins S, Czosnek H, Palukaitis P, Jacquot E, Hohn T, Hohn B, Saunders K, Candresse T, Ahlquist P, Hemenway C, Foster GD (2011) Top 10 plant viruses in molecular plant pathology. Mol Plant Pathol 12(9):938–954. https://doi.org/10.1111/j.1364-3703.2011.00752.x
Song S, You J, Shi L, Sheng C, Zhou W, Dossou SSK, Dossa K, Wang L, Zhang X (2021) Genome-Wide analysis of nsLTP gene family and identification of SiLTPs contributing to high oil accumulation in sesame (Sesamum indicum L.). Int J Mol Sci. https://doi.org/10.3390/ijms22105291
Sun D, Nandety RS, Zhang Y, Reid MS, Niu L, Jiang C-Z (2016) A petunia ethylene-responsive element binding factor, PhERF2, plays an important role in antiviral RNA silencing. J Exp Bot 67(11):3353–3365. https://doi.org/10.1093/jxb/erw155
Tilsner J, Linnik O, Wright KM, Bell K, Roberts AG, Lacomme C, Santa Cruz S, Oparka KJ (2012) The TGB1 movement protein of potato virus X reorganizes actin and endomembranes into the X-body, a viral replication factory. Plant Physiol 158(3):1359–1370. https://doi.org/10.1104/pp.111.189605
Tiwari JK, Buckseth T, Zinta R, Bhatia N, Dalamu D, Naik S, Poonia AK, Kardile HB, Challam C, Singh RK, Luthra SK, Kumar V, Kumar M (2022) Germplasm, breeding, and genomics in potato improvement of biotic and abiotic stresses tolerance. Front Plant Sci 13:805671. https://doi.org/10.3389/fpls.2022.805671
Vargason JM, Szittya G, Burgyán J, Hall TM (2003) Size selective recognition of siRNA by an RNA silencing suppressor. Cell 115(7):799–811. https://doi.org/10.1016/s0092-8674(03)00984-x
Voinnet O (2005) Induction and suppression of RNA silencing: insights from viral infections. Nat Rev Genet 6(3):206–220. https://doi.org/10.1038/nrg1555
Wang NJ, Lee CC, Cheng CS, Lo WC, Yang YF, Chen MN, Lyu PC (2012) Construction and analysis of a plant non-specific lipid transfer protein database (nsLTPDB). BMC Genom 13(Suppl 1):S9. https://doi.org/10.1186/1471-2164-13-s1-s9
Wang C, Gao H, Chu Z, Ji C, Xu Y, Cao W, Zhou S, Song Y, Liu H, Zhu C (2021) A nonspecific lipid transfer protein, StLTP10, mediates resistance to Phytophthora infestans in potato. Mol Plant Pathol 22(1):48–63. https://doi.org/10.1111/mpp.13007
Xu Y, Zheng X, Song Y, Zhu L, Yu Z, Gan L, Zhou S, Liu H, Wen F, Zhu C (2018) NtLTP4, a lipid transfer protein that enhances salt and drought stresses tolerance in Nicotiana tabacum. Sci Rep 8(1):8873. https://doi.org/10.1038/s41598-018-27274-8
Xu Y, Shang K, Wang C, Yu Z, Zhao X, Song Y, Meng F, Zhu C (2022) WIPK-NtLTP4 pathway confers resistance to Ralstonia solanacearum in tobacco. Plant Cell Rep 41(1):249–261. https://doi.org/10.1007/s00299-021-02808-z
Yang Z, Li Y (2018) Dissection of RNAi-based antiviral immunity in plants. Curr Opin Virol 32:88–99. https://doi.org/10.1016/j.coviro.2018.08.003
Zhang X, Yuan YR, Pei Y, Lin SS, Tuschl T, Patel DJ, Chua NH (2006) Cucumber mosaic virus-encoded 2b suppressor inhibits Arabidopsis Argonaute1 cleavage activity to counter plant defense. Genes Dev 20(23):3255–3268. https://doi.org/10.1101/gad.1495506
Zhang X, Zhu Z, An F, Hao D, Li P, Song J, Yi C, Guo H (2014) Jasmonate-activated MYC2 represses ETHYLENE INSENSITIVE3 activity to antagonize ethylene-promoted apical hook formation in Arabidopsis. Plant Cell 26(3):1105–1117. https://doi.org/10.1105/tpc.113.122002
Zhang M, Kim Y, Zong J, Lin H, Dievart A, Li H, Zhang D, Liang W (2019) Genome-wide analysis of the barley non-specific lipid transfer protein gene family. Crop J 7(1):65–76. https://doi.org/10.1016/j.cj.2018.07.009
Acknowledgements
This research was funded by [National Natural Science Foundation of China] grant number [31720103912], and [Shandong “Double Tops” Program] grant number [SYL2017XTTD11]. The infectious clone of potato virus Y was given by Professor Xiangdong Li from College of Plant Protection of Shandong Agricultural University.
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425_2022_3948_MOESM1_ESM.tif
Supplementary file1 Supplementary Fig. S1 Relative accumulation levels of StLTP6 mRNA. a Relative accumulation levels of StLTP6 mRNA in N. benthamiana leaves coinfection with PVY. b Relative accumulation levels of StLTP6 mRNA in N. benthamiana leaves coinfection with PVX (TIF 493217 KB)
425_2022_3948_MOESM2_ESM.tif
Supplementary file2 Supplementary Fig. S2 StLTP6 induced by phytohormones. a The induced expression of StLTP6 by ACC. b The induced expression of StLTP6 by SA. c The induced expression of StLTP6 by JA. d The induced expression of StLTP6 by ABA (TIF 484119 KB)
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Supplementary file3 Supplementary Fig. S3 Liquid chromatography-tandem mass spectrometry results. a–e Liquid chromatography-tandem mass spectrometry of RNA-directed RNA polymerase, 11K protein, coat protein, TGB1, and TGB2 of PVS. f–h Liquid chromatography-tandem mass spectrometry of NIb protein, coat protein, and P1 protein of PVY (TIF 487717 KB)
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Shang, K., Xu, Y., Cao, W. et al. Potato (Solanum tuberosum L.) non-specific lipid transfer protein StLTP6 promotes viral infection by inhibiting virus-induced RNA silencing. Planta 256, 54 (2022). https://doi.org/10.1007/s00425-022-03948-6
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DOI: https://doi.org/10.1007/s00425-022-03948-6