Identification of Sugarcane Host Factors Interacting with the 6K2 Protein of the Sugarcane Mosaic Virus
Abstract
:1. Introduction
2. Results
2.1. Cloning and Subcellular Localization of SCMV-6K2
2.2. Construction and Evaluation of the pBT3-6K2 Bait Vector
2.3. Screening of the Sugarcane cDNA Library and Gene Cloning
2.3.1. Stress and Defense Proteins
2.3.2. Transport-Related Proteins
2.3.3. Photosynthesis-Related Proteins
2.4. Verification of the Interaction between the Screened Proteins and SCMV-6K2
3. Discussion
4. Materials and Methods
4.1. Materials and Plant Culture
4.2. RNA Isolation and Gene Cloning
4.3. Bioinformatic Analysis
4.4. Plasmid Construction
4.5. Transient Protein Expression and Confocal Microscopy
4.6. Evaluation of the SCMV-6K2 Bait Plasmid
4.7. Screening of the cDNA Library and Positive Colony Sequencing
4.8. Verification of Protein Interaction by Y2H Assays
Supplementary Materials
Author Contributions
Funding
Conflicts of Interest
References
- Koonin, E.; Wolf, Y.; Nagasaki, K.; Dolja, V. The Big Bang of picorna-like virus evolution antedates the radiation of eukaryotic supergroups. Nat. Rev. Microbiol. 2008, 6, 925–939. [Google Scholar] [CrossRef] [PubMed]
- Urcuqui-Inchima, S.; Haenni, A.L.; Bernardi, F. Potyvirus proteins: A wealth of functions. Virus Res. 2001, 74, 157–175. [Google Scholar] [CrossRef]
- Olspert, A.; Carr, J.P.; Firth, A.E. Mutational analysis of the Potyviridae transcriptional slippage site utilized for expression of the P3N-PIPO and P1N-PISPO proteins. Nucleic Acids Res. 2016, 44, 7618–7629. [Google Scholar] [CrossRef] [PubMed]
- Olspert, A.; Chung, B.Y.; Atkins, J.F.; Carr, J.P.; Firth, A.E. Transcriptional slippage in the positive-sense RNA virus family Potyviridae. EMBO Rep. 2015, 16, 995–1004. [Google Scholar] [CrossRef] [PubMed]
- Cheng, G.; Dong, M.; Xu, Q.; Peng, L.; Yang, Z.; Wei, T.; Xu, J. Dissecting the Molecular Mechanism of the Subcellular Localization and Cell-to-cell Movement of the Sugarcane mosaic virus P3N-PIPO. Sci. Rep. 2017, 7, 9868. [Google Scholar] [CrossRef]
- Riechmann, J.L.; Laín, S.; García, J.A. Highlights and prospects of potyvirus molecular biology. J. Gen. Virol. 1992, 73, 1–16. [Google Scholar] [CrossRef]
- Chung, B.Y.; Miller, W.A.; Atkins, J.F.; Firth, A.E. An overlapping essential gene in the Potyviridae. Proc. Natl. Acad. Sci. USA 2008, 105, 5897–5902. [Google Scholar] [CrossRef] [Green Version]
- Wang, A. Dissecting the Molecular Network of Virus-Plant Interactions: The Complex Roles of Host Factors. Annu. Rev. Phytopathol. 2015, 53, 45–66. [Google Scholar] [CrossRef]
- Wei, T.; Wang, A. Biogenesis of cytoplasmic membranous vesicles for plant potyvirus replication occurs at endoplasmic reticulum exit sites in a COPI- and COPII-dependent manner. J. Virol. 2008, 82, 12252–12264. [Google Scholar] [CrossRef]
- Jiang, J.; Patarroyo, C.; Garcia Cabanillas, D.; Zheng, H.; Laliberte, J.F. The Vesicle-Forming 6K2 Protein of Turnip Mosaic Virus Interacts with the COPII Coatomer Sec24a for Viral Systemic Infection. J. Virol. 2015, 89, 6695–6710. [Google Scholar] [CrossRef]
- Cotton, S.; Grangeon, R.; Thivierge, K.; Mathieu, I.; Ide, C.; Wei, T.; Wang, A.; Laliberté, J.-F. Turnip mosaic virus RNA replication complex vesicles are mobile, align with microfilaments, and are each derived from a single viral genome. J. Virol. 2009, 83, 10460–10471. [Google Scholar] [CrossRef] [PubMed]
- Wei, T.; Zhang, C.; Hou, X.; Sanfacon, H.; Wang, A. The SNARE protein Syp71 is essential for turnip mosaic virus infection by mediating fusion of virus-induced vesicles with chloroplasts. PLoS Pathog. 2013, 9, e1003378. [Google Scholar] [CrossRef] [PubMed]
- Grangeon, R.; Jiang, J.; Wan, J.; Agbeci, M.; Zheng, H.; Laliberté, J.F. 6K2-induced vesicles can move cell to cell during turnip mosaic virus infection. Front. Microbiol. 2013, 4, 351. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Movahed, N.; Patarroyo, C.; Sun, J.; Vali, H.; Laliberté, J.F.; Zheng, H. Cylindrical Inclusion Protein of Turnip Mosaic Virus Serves as a Docking Point for the Intercellular Movement of Viral Replication Vesicles. Plant Physiol. 2017, 175, 1732–1744. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Movahed, N.; Sun, J.; Vali, H.; Laliberté, J.F.; Zheng, H. A Host ER Fusogen Is Recruited by Turnip Mosaic Virus for Maturation of Viral Replication Vesicles. Plant Physiol. 2019, 179, 507–518. [Google Scholar] [CrossRef] [PubMed]
- Wei, T.; Zhang, C.; Hong, J.; Xiong, R.; Kasschau, K.D.; Zhou, X.; Carrington, J.C.; Wang, A. Formation of complexes at plasmodesmata for potyvirus intercellular movement is mediated by the viral protein P3N-PIPO. PLoS Pathog. 2010, 6, e1000962. [Google Scholar] [CrossRef] [PubMed]
- Ping, D.; Wu, Z.; Wang, A. The multifunctional protein CI of potyviruses plays interlinked and distinct roles in viral genome replication and intercellular movement. Virol. J. 2015, 12, 1–11. [Google Scholar] [Green Version]
- Nakahara, K.S.; Chikara, M.; Syouta, Y.; Hanako, S.; Yukiko, K.; Wada, T.S.; Ayano, M.; Kazunori, G.; Kazuki, T.; Kae, S. 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, 10113–10118. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hafrén, A.; Üstün, S.; Hochmuth, A.; Svenning, S.; Johansen, T.; Hofius, D. Turnip mosaic virus counteracts selective autophagy of the viral silencing suppressor HCpro. Plant Physiol. 2018, 176, 649–662. [Google Scholar] [CrossRef]
- Cabanillas, D.G.; Jiang, J.; Movahed, N.; Germain, H.; Yamaji, Y.; Zheng, H.; Laliberte, J. Turnip Mosaic Virus Uses the SNARE Protein VTI11 in an Unconventional Route for Replication Vesicle Trafficking. Plant Cell 2018, 30, 2594–2615. [Google Scholar] [CrossRef] [Green Version]
- Biterge, B.; Schneider, R. Histone variants: Key players of chromatin. Cell Tissue Res. 2014, 356, 457–466. [Google Scholar] [CrossRef] [PubMed]
- Macintosh, G.C.; Hillwig, M.S.; Alexander, M.; Flagel, L. RNase T2 genes from rice and the evolution of secretory ribonucleases in plants. Mol. Genet. Genom. 2010, 283, 381–396. [Google Scholar] [CrossRef] [PubMed]
- Kurata, N.; Kariu, T.; Kawano, S.; Kimura, M. Molecular cloning of cDNAs encoding ribonuclease-related proteins in Nicotiana glutinosa leaves, as induced in response to wounding or to TMV-infection. J. Agric. Chem. Soc. Jpn. 2002, 66, 391–397. [Google Scholar]
- Wilkinson, C.R.; Dittmar, G.A.; Ohi, M.D.; Uetz, P.; Jones, N.; Finley, D. Ubiquitin-like Protein Hub1 Is Required for Pre-mRNA Splicing and Localization of an Essential Splicing Factor in Fission Yeast. Curr. Biol. 2006, 16, 2488. [Google Scholar] [CrossRef]
- Feng, H.; Wang, Q.L.; Zhao, X.Q.; Han, L.N.; Wang, X.J.; Kang, Z.S. TaULP5 contributes to the compatible interaction of adult plant resistance wheat seedlings-stripe rust pathogen. Physiol. Mol. Plant Pathol. 2016, 96, 29–35. [Google Scholar] [CrossRef]
- Zhu, X.F.; Liu, Y.; Gai, X.T.; Zhou, Y.; Xia, Z.Y.; Chen, L.; Duan, Y.X.; Xuan, Y.H. SNARE proteins SYP22 and VAMP727 negatively regulate plant defense. Plant Signal. Behav. 2019, 14, 1610300. [Google Scholar] [CrossRef] [PubMed]
- Usami, Y.; Wu, Y.; Göttlinger, H.G. SERINC3 and SERINC5 restrict HIV-1 infectivity and are counteracted by Nef. Nature 2015, 526, 218–223. [Google Scholar] [CrossRef]
- Pause, B.; Saffrich, R.; Hunziker, A.; Ansorge, W.; Just, W.W. Targeting of the 22 kDa integral peroxisomal membrane protein. FEBS Lett. 2000, 471, 23–28. [Google Scholar] [CrossRef] [Green Version]
- Yang, M.; Li, Z.; Zhang, K.; Zhang, X.; Zhang, Y.; Wang, X.; Han, C.; Yu, J.; Xu, K.; Li, D. Barley Stripe Mosaic Virus γb Interacts with Glycolate Oxidase and Inhibits Peroxisomal ROS Production to Facilitate Virus Infection. Mol. Plant 2017, 11, 338–341. [Google Scholar] [CrossRef]
- Muthusamy, S.K.; Dalal, M.; Chinnusamy, V.; Bansal, K.C. Genome-wide identification and analysis of biotic and abiotic stress regulation of small heat shock protein (HSP20) family genes in bread wheat. J. Plant Physiol. 2017, 211, 100–113. [Google Scholar] [CrossRef]
- Gomes, D.; Agasse, A.; Thiébaud, P.; Delrot, S.; Gerós, H.; Chaumont, F. Aquaporins are multifunctional water and solute transporters highly divergent in living organisms. BBA-Biomembr. 2009, 1788, 1213–1228. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chaumont, F.; Barrieu, F.; Wojcik, E.; Chrispeels, M.J.; Jung, R. Aquaporins constitute a large and highly divergent protein family in maize. Plant Physiol. 2001, 125, 1206–1215. [Google Scholar] [CrossRef] [PubMed]
- Ishibashi, K.; Morishita, Y.; Tanaka, Y. The Evolutionary Aspects of Aquaporin Family. Adv. Exp. Med. Biol. 2017, 969, 35–50. [Google Scholar] [PubMed]
- Haydon, M.J.; Cobbett, C.S. A novel major facilitator superfamily protein at the tonoplast influences zinc tolerance and accumulation in Arabidopsis. Plant Physiol. 2007, 143, 1705–1719. [Google Scholar] [CrossRef] [PubMed]
- Ricachenevsky, F.K.; Sperotto, R.A.; Menguer, P.K.; Sperb, E.R.; Lopes, K.L.; Fett, J.P. ZINC-INDUCED FACILITATOR-LIKE family in plants: Lineage-specific expansion in monocotyledons and conserved genomic and expression features among rice (Oryza sativa) paralogs. BMC Plant Biol. 2011, 11, 20. [Google Scholar] [CrossRef] [PubMed]
- Singh, A.K.; Kumar, R.; Tripathi, A.K.; Gupta, B.K.; Pareek, A.; Singla-Pareek, S.L. Genome-wide investigation and expression analysis of Sodium/Calcium exchanger gene family in rice and Arabidopsis. Rice 2015, 8, 54. [Google Scholar] [CrossRef] [PubMed]
- Zhou, A.; Bu, Y.; Takano, T.; Zhang, X.; Liu, S. Conserved V-ATPase c subunit plays a role in plant growth by influencing V-ATPase-dependent endosomal trafficking. Plant Biotechnol. J. 2016, 14, 271–283. [Google Scholar] [CrossRef]
- Chen, Z.; Zhao, P.X.; Miao, Z.Q.; Qi, G.; Wang, Z.; Yuan, Y.; Ahmad, N.; Cao, M.J.; Hell, R.; Wirtz, M.; et al. SULTR3s Function in Chloroplast Sulfate Uptake and Affect ABA Biosynthesis and the Stress Response. Plant Physiol. 2019, 180, 593–604. [Google Scholar] [CrossRef]
- Handford, M.G.; Sicilia, F.; Brandizzi, F.; Chung, J.H.; Dupree, P. Arabidopsis thaliana expresses multiple Golgi-localised nucleotide-sugar transporters related to GONST1. Mol. Genet. Genom. 2004, 272, 397–410. [Google Scholar] [CrossRef]
- Fischer, K.; Kammerer, B.; Gutensohn, M.; Arbinger, B.; Weber, A.; Häusler, R.E.; Flügge, U.I. A new class of plastidic phosphate translocators: A putative link between primary and secondary metabolism by the phosphoenolpyruvate/phosphate antiporter. Plant Cell 1997, 9, 453–462. [Google Scholar]
- Lee, Y.; Nishizawa, T.; Takemoto, M.; Kumazaki, K.; Yamashita, K.; Hirata, K.; Minoda, A.; Nagatoishi, S.; Tsumoto, K.; Ishitani, R.; et al. Structure of the triose-phosphate/phosphate translocator reveals the basis of substrate specificity. Nat. Plants 2017, 3, 825–832. [Google Scholar] [CrossRef]
- Takemoto, M.; Lee, Y.; Ishitani, R.; Nureki, O. Free Energy Landscape for the Entire Transport Cycle of Triose-Phosphate/Phosphate Translocator. Structure 2018, 26, 1284–1296. [Google Scholar] [CrossRef] [PubMed]
- Luang, S.; Cho, J.I.; Mahong, B.; Opassiri, R.; Akiyama, T.; Phasai, K.; Komvongsa, J.; Sasaki, N.; Hua, Y.L.; Matsuba, Y.; et al. Rice Os9BGlu31 is a transglucosidase with the capacity to equilibrate phenylpropanoid, flavonoid, and phytohormone glycoconjugates. J. Biol. Chem. 2013, 288, 10111–10123. [Google Scholar] [CrossRef] [PubMed]
- Zhao, Y.; Hu, J.; Miao, G.; Qu, L.; Wang, Z.; Li, G.; Lv, P.; Ma, D.; Chen, Y. Transmembrane protein 208: A novel ER-localized protein that regulates autophagy and ER stress. PLoS ONE 2013, 8, e64228. [Google Scholar] [CrossRef] [PubMed]
- Correa-Galvis, V.; Poschmann, G.; Melzer, M.; Stühler, K.; Jahns, P. PsbS interactions involved in the activation of energy dissipation in Arabidopsis. Nat. Plants 2016, 2, 15225. [Google Scholar] [CrossRef] [PubMed]
- Daskalakis, V.; Papadatos, S. The Photosystem II Subunit S under Stress. Biophys. J. 2017, 113, 2364–2372. [Google Scholar] [CrossRef] [Green Version]
- Allahverdiyeva, Y.; Mamedov, F.; Suorsa, M.; Styring, S.; Vass, I.; Aro, E.M. Insights into the function of PsbR protein in Arabidopsis thaliana. Biochim. Biophys. Acta 2007, 1767, 677–685. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Allahverdiyeva, Y.; Suorsa, M.; Rossi, F.; Pavesi, A.; Kater, M.; Antonacci, A.; Tadini, L.; Pribil, M.; Schneider, A.; Wanner, G.; et al. Arabidopsis plants lacking PsbQ and PsbR subunits of the oxygen-evolving complex show altered PSII super-complex organization and short-term adaptive mechanisms. Plant J. 2013, 75, 671–684. [Google Scholar] [CrossRef] [PubMed]
- Motohashi, R.; Ito, T.; Kobayashi, M.; Taji, T.; Nagata, N.; Asami, T.; Yoshida, S.; Yamaguchishinozaki, K.; Shinozaki, K. Functional analysis of the 37 kDa inner envelope membrane polypeptide in chloroplast biogenesis using a Ds-tagged Arabidopsis pale-green mutant. Plant J. 2003, 34, 719–731. [Google Scholar] [CrossRef]
- Horn, R.; Grundmann, G.; Paulsen, H. Consecutive Binding of Chlorophylls a and b During the Assembly in Vitro of Light-harvesting Chlorophyll- a/b Protein (LHCIIb). J. Mol. Biol. 2007, 366, 1045–1054. [Google Scholar] [CrossRef]
- Yi, H.; Sardesai, N.; Fujinuma, T.; Chan, C.W.; Gelvin, S.B. Constitutive expression exposes functional redundancy between the Arabidopsis histone H2A gene HTA1 and other H2A gene family members. Plant Cell 2006, 18, 1575–1589. [Google Scholar] [CrossRef] [PubMed]
- Sura, W.; Kabza, M.; Karlowski, W.M.; Bieluszewski, T.; Kuś-Slowinska, M.; Pawełoszek, Ł.; Sadowski, J.; Ziolkowski, P.A. Dual role of the histone variant H2A.Z in transcriptional regulation of stress-response genes. Plant Cell 2017, 29, 791–807. [Google Scholar] [CrossRef] [PubMed]
- Luhtala, N.; Parker, R. T2 Family ribonucleases: Ancient enzymes with diverse roles. Trends Biochem. Sci. 2010, 35, 253–259. [Google Scholar] [CrossRef] [PubMed]
- Megel, C.; Hummel, G.; Lalande, S.; Ubrig, E.; Cognat, V.; Morelle, G.; Salinasgiege, T.; Duchene, A.; Marechaldrouard, L. Plant RNases T2, but not Dicer-like proteins, are major players of tRNA-derived fragments biogenesis. Nucleic Acids Res. 2019, 47, 941–952. [Google Scholar] [CrossRef] [PubMed]
- Hugot, K.; Ponchet, M.; Marais, A.; Ricci, P.; Galiana, E. A tobacco S-like RNase inhibits hyphal elongation of plant pathogens. Mol. Plant-Microbe Interact. 2002, 15, 243–250. [Google Scholar] [CrossRef]
- Mishra, S.K.; Ammon, T.; Popowicz, G.M.; Krajewski, M.; Nagel, R.J.; Ares, M.; Holak, T.A.; Jentsch, S. Role of the ubiquitin-like protein Hub1 in splice-site usage and alternative splicing. Nature 2011, 474, 173–178. [Google Scholar] [CrossRef] [Green Version]
- van der Veen, A.G.; Ploegh, H.L. Ubiquitin-like proteins. Annu. Rev. Biochem. 2012, 81, 323–357. [Google Scholar] [CrossRef]
- Ammon, T.; Mishra, S.K.; Kowalska, K.; Popowicz, G.M.; Holak, T.A.; Jentsch, S. The conserved ubiquitin-like protein Hub1 plays a critical role in splicing in human cells. J. Mol. Cell Biol. 2014, 6, 312–323. [Google Scholar] [CrossRef] [Green Version]
- Sundaramoorthy, S.; Vázquez-Novelle, M.D.; Lekomtsev, S.; Howell, M.; Petronczki, M. Functional genomics identifies a requirement of pre-mRNA splicing factors for sister chromatid cohesion. EMBO J. 2015, 33, 2623–2642. [Google Scholar] [CrossRef]
- Zhang, L.; Liu, Y.; Zhu, X.F.; Jung, J.H.; Sun, Q.; Li, T.Y.; Chen, L.; Duan, Y.X.; Xuan, Y.H. SYP22 and VAMP727 regulate BRI1 plasma membrane targeting to control plant growth in Arabidopsis. New Phytol. 2019, 223, 1059–1065. [Google Scholar] [CrossRef] [Green Version]
- Inuzuka, M.; Hayakawa, M.; Ingi, T. Serinc, an activity-regulated protein family, incorporates serine into membrane lipid synthesis. J. Biol. Chem. 2005, 280, 35776–35783. [Google Scholar] [CrossRef] [PubMed]
- Murphy, M.A.; Phillipson, B.A.; Baker, A.; Mullen, R.T. Characterization of the targeting signal of the Arabidopsis 22-kD integral peroxisomal membrane protein. Plant Physiol. 2003, 133, 813–828. [Google Scholar] [CrossRef] [PubMed]
- Laliberté, J.F.; Sanfaçon, H. Cellular remodeling during plant virus infection. Annu. Rev. Phytopathol. 2010, 48, 69–91. [Google Scholar] [CrossRef] [PubMed]
- Lazarow, P.B. Viruses exploiting peroxisomes. Curr. Opin. Microbiol. 2011, 14, 458–469. [Google Scholar] [CrossRef] [PubMed]
- Rochon, D.; Singh, B.; Reade, R.; Theilmann, J.; Ghoshal, K.; Alam, S.B.; Maghodia, A. The p33 auxiliary replicase protein of Cucumber necrosis virus targets peroxisomes and infection induces de novo peroxisome formation from the endoplasmic reticulum. Virology 2014, 452–453, 133–142. [Google Scholar] [CrossRef] [PubMed]
- Boavida, L.C.; Qin, P.; Broz, M.; Becker, J.D.; Mccormick, S. Arabidopsis tetraspanins are confined to discrete expression domains and cell types in reproductive tissues and form homo- and heterodimers when expressed in yeast. Plant Physiol. 2013, 163, 696–712. [Google Scholar] [CrossRef] [PubMed]
- Mani, B.; Agarwal, M.; Katiyar-Agarwal, S. Comprehensive Expression Profiling of Rice Tetraspanin Genes Reveals Diverse Roles During Development and Abiotic Stress. Front. Plant Sci. 2015, 6, 1088. [Google Scholar] [CrossRef]
- Reimann, R.; Kost, B.; Dettmer, J. TETRASPANINs in Plants. Front. Plant Sci. 2018, 8, 545. [Google Scholar] [CrossRef] [PubMed]
- Ding, G.; Chen, P.; Zhang, H.; Huang, X.; Zang, Y.; Li, J.; Li, J.; Wong, J. Regulation of Ubiquitin-like with PHD and RING Finger Domain 1 (UHRF1) Protein Stability by Heat Shock Protein 90 Chaperone Machinery. J. Biol. Chem. 2016, 291, 20125. [Google Scholar] [CrossRef] [PubMed]
- Maurel, C.; Boursiac, Y.; Luu, D.T.; Santoni, V.; Shahzad, Z.; Verdoucq, L. Aquaporins in Plants. Physiol. Rev. 2015, 95, 1321–1358. [Google Scholar] [CrossRef]
- Bienert, G.P.; Bienert, M.D.; Jahn, T.P.; Boutry, M.; Chaumont, F. Solanaceae XIPs are plasma membrane aquaporins that facilitate the transport of many uncharged substrates. Plant J. 2011, 66, 306–317. [Google Scholar] [CrossRef] [PubMed]
- Kammerloher, W.; Fischer, U.; Piechottka, G.P.; Schäffner, A.R. Water channels in the plant plasma membrane cloned by immunoselection from a mammalian expression system. Plant J. 1994, 6, 187–199. [Google Scholar] [CrossRef] [PubMed]
- Hachez, C.; Veselov, D.; Ye, Q.; Reinhardt, H.; Knipfer, T.; Fricke, W.; Chaumont, F. Short-term control of maize cell and root water permeability through plasma membrane aquaporin isoforms. Plant Cell Environ. 2011, 35, 185–198. [Google Scholar] [CrossRef] [PubMed]
- Pawłowicz, I.; Rapacz, M.; Perlikowski, D.; Gondek, K.; Kosmala, A. Abiotic stresses influence the transcript abundance of PIP and TIP aquaporins in Festuca species. J. Appl. Genet. 2017, 58, 421–435. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hachez, C.; Laloux, T.; Reinhardt, H.; Cavez, D.; Degand, H.; Grefen, C.; DeRycke, R.; Inze, D.; Blatt, M.R.; Russinova, E.; et al. Arabidopsis SNAREs SYP61 and SYP121 coordinate the trafficking of plasma membrane aquaporin PIP2;7 to modulate the cell membrane water permeability. Plant Cell 2014, 26, 3132–3147. [Google Scholar] [CrossRef] [PubMed]
- Heckwolf, M.; Pater, D.; Hanson, D.T.; Kaldenhoff, R. The Arabidopsis thaliana aquaporin AtPIP1;2 is a physiologically relevant CO? transport facilitator. Plant J. 2011, 67, 795–804. [Google Scholar] [CrossRef] [PubMed]
- Kaldenhoff, R. Mechanisms underlying CO2 diffusion in leaves. Curr. Opin. Plant Biol. 2012, 15, 276–281. [Google Scholar] [CrossRef] [PubMed]
- Kaldenhoff, R.; Kai, L.; Uehlein, N. Aquaporins and membrane diffusion of CO2 in living organisms. Biochim. Biophys. Acta 2014, 1840, 1592–1595. [Google Scholar] [CrossRef] [PubMed]
- Remy, E.; Cabrito, T.R.; Baster, P.; Batista, R.A.; Teixeira, M.C.; Friml, J.; Sá-Correia, I.; Duque, P. A major facilitator superfamily transporter plays a dual role in polar auxin transport and drought stress tolerance in Arabidopsis. Plant Cell 2013, 25, 901–926. [Google Scholar] [CrossRef] [PubMed]
- Giladi, M.; Shor, R.; Lisnyansky, M.; Khananshvili, D. Structure-Functional Basis of Ion Transport in Sodium-Calcium Exchanger (NCX) Proteins. Int. J. Mol. Sci. 2016, 17, 1949. [Google Scholar] [CrossRef] [PubMed]
- Zhou, A.; Takano, T.; Liu, S. The role of endomembrane-localized VHA-c in plant growth. Plant Signal. Behav. 2017, 13, e1382796. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Leustek, T.; Martin, M.N.; Bick, J.A.; Davies, J.P. Pathways and regulation of sulfur metabolism revealed through molecular and genetic studies. Annu. Rev. Plant Physiol. Plant Mol. Biol. 2000, 51, 141–165. [Google Scholar] [CrossRef] [PubMed]
- Leustek, T.; Saito, K. Sulfate Transport and Assimilation in Plants. Plant Physiol. 1999, 120, 637–643. [Google Scholar] [CrossRef] [PubMed]
- Vatansever, R.; Koc, I.; Ozyigit, I.I.; Sen, U.; Uras, M.E.; Anjum, N.A.; Pereira, E.; Filiz, E. Genome-wide identification and expression analysis of sulfate transporter (SULTR) genes in potato (Solanum tuberosum L.). Planta 2016, 244, 1167–1183. [Google Scholar] [CrossRef] [PubMed]
- Parker, J.L.; Newstead, S. Structural basis of nucleotide sugar transport across the Golgi membrane. Nature 2017, 551, 521–524. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Akiko, N.; Poster, J.B.; Yoshifumi, J.; Neta, D. Molecular and phenotypic analysis of CaVRG4, encoding an essential Golgi apparatus GDP-mannose transporter. J. Bacteriol. 2002, 184, 29. [Google Scholar]
- Hilgers, E.J.A.; Staehr, P.; Flügge, U.I.; Häusler, R.E. The Xylulose 5-Phosphate/Phosphate Translocator Supports Triose Phosphate, but Not Phosphoenolpyruvate Transport Across the Inner Envelope Membrane of Plastids in Arabidopsis thaliana Mutant Plants. Front. Plant Sci. 2018, 9, 1461. [Google Scholar] [CrossRef] [Green Version]
- Walters, R.G.; Freya, S.; Rogers, J.J.M.; Rolfe, S.A.; Horton, P. Identification of mutants of Arabidopsis defective in acclimation of photosynthesis to the light environment. Plant Physiol. 2003, 131, 472–481. [Google Scholar] [CrossRef] [PubMed]
- Aviram, N.; Ast, T.; Costa, E.A.; Arakel, E.C.; Chuartzman, S.G.; Jan, C.H.; Hassdenteufel, S.; Dudek, J.; Jung, M.; Schorr, S.; et al. The SND proteins constitute an alternative targeting route to the endoplasmic reticulum. Nature 2016, 540, 134–138. [Google Scholar] [CrossRef]
- Kiss, A.Z.; Ruban, A.V.; Peter, H. The PsbS protein controls the organization of the photosystem II antenna in higher plant thylakoid membranes. J. Biol. Chem. 2008, 283, 3972–3978. [Google Scholar] [CrossRef]
- Li, X.P.; Björkman, O.; Shih, C.; Grossman, A.R.; Rosenquist, M.; Jansson, S.; Niyogi, K.K. A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 2000, 403, 391–395. [Google Scholar] [CrossRef] [PubMed]
- Shi, L.X.; Schröder, W.P. The low molecular mass subunits of the photosynthetic supracomplex, photosystem II. Biochim. Biophys. Acta 2004, 1608, 75–96. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Suorsa, M.; Sirpiö, S.; Allahverdiyeva, Y.; Paakkarinen, V.; Mamedov, F.; Styring, S.; Aro, E.M. PsbR, a missing link in the assembly of the oxygen-evolving complex of plant photosystem II. J. Biol. Chem. 2006, 281, 145–150. [Google Scholar] [CrossRef] [PubMed]
- Liu, H.; Frankel, L.K.; Bricker, T.M. Characterization and complementation of a psbR mutant in Arabidopsis thaliana. Arch. Biochem. Biophys. 2009, 489, 34–40. [Google Scholar] [CrossRef] [PubMed]
- Xue, H.; Tokutsu, R.; Bergner, S.V.; Scholz, M.; Minagawa, J.; Hippler, M. PHOTOSYSTEM II SUBUNIT R is required for efficient binding of LIGHT-HARVESTING COMPLEX STRESS-RELATED PROTEIN3 to photosystem II-light-harvesting supercomplexes in Chlamydomonas reinhardtii. Plant Physiol. 2015, 167, 1566–1578. [Google Scholar] [CrossRef]
- Li, L.; Ye, T.; Gao, X.; Chen, R.; Xu, J.; Xie, C.; Zhu, J.; Deng, X.; Wang, P.; Xu, Z. Molecular characterization and functional analysis of the OsPsbR gene family in rice. Mol. Genet. Genom. 2017, 292, 1–11. [Google Scholar] [CrossRef] [PubMed]
- Cheng, Z.; Sattler, S.; Maeda, H.; Sakuragi, Y.; Bryant, D.A.; DellaPenna, D. Highly divergent methyltransferases catalyze a conserved reaction in tocopherol and plastoquinone synthesis in cyanobacteria and photosynthetic eukaryotes. Plant Cell 2003, 15, 2343–2356. [Google Scholar] [CrossRef]
- Laliberté, J.F.; Zheng, H. Viral Manipulation of Plant Host Membranes. Annu. Rev. Virol. 2014, 1, 237–259. [Google Scholar] [CrossRef]
- Zhang, D.W.; Deng, X.G.; Fu, F.Q.; Lin, H.H. Induction of plant virus defense response by brassinosteroids and brassinosteroid signaling in Arabidopsis thaliana. Planta 2015, 241, 875–885. [Google Scholar] [CrossRef]
- Cacas, J.L.; Buré, C.; Grosjean, K.; Gerbeaupissot, P.; Lherminier, J.; Rombouts, Y.; Maes, E.; Bossard, C.; Gronnier, J.; Furt, F.; et al. Revisiting Plant Plasma Membrane Lipids in Tobacco: A Focus on Sphingolipids. Plant Physiol. 2016, 170, 367–384. [Google Scholar] [CrossRef]
- Thomas, O. Membrane nanodomains and microdomains in plant-microbe interactions Curr. Opin. Plant Biol. 2017, 40, 82–88. [Google Scholar]
- Tzin, V.; Galili, G. New Insights into the Shikimate and Aromatic Amino Acids Biosynthesis Pathways in Plants. Mol. Plant 2010, 3, 956–972. [Google Scholar] [CrossRef] [PubMed]
- Dong, M.; Cheng, G.; Peng, L.; Xu, Q.; Yang, Y.; Xu, J. Transcriptome Analysis of Sugarcane Response to the Infection by Sugarcane Steak Mosaic Virus (SCSMV). Trop. Plant Biol. 2017, 10, 45–55. [Google Scholar] [CrossRef]
- Li, Z.R.; Wakao, S.; Fischer, B.B.; Niyogi, K.K. Sensing and responding to excess light. Annu. Rev. Plant Biol. 2009, 60, 239–260. [Google Scholar] [CrossRef]
- Xu, J.S.; Deng, Y.Q.; Cheng, G.Y.; Zhai, Y.-S.; Peng, L.; Dong, M.; Xu, Q.; Yang, Y.Q. Sugarcane mosaic virus infection of model plants Brachypodium distachyon and Nicotiana benthamiana. J. Integr. Agric. 2019. [Google Scholar] [CrossRef]
- Krogh, A.; Larsson, B.; von Heijne, G.; Sonnhammer, E.L. Predicting transmembrane protein topology with a hidden Markov model: Application to complete genomes. J. Mol. Biol. 2001, 305, 567–580. [Google Scholar] [CrossRef] [PubMed]
- Song, P.; Chen, X.; Wu, B.; Gao, L.; Zhi, H.; Cui, X. Identification for soybean host factors interacting with P3N-PIPO protein of Soybean mosaic virus. Acta Physiol. Plant 2016, 38, 131. [Google Scholar] [CrossRef]
Protein Name (Coding Protein) | Accession Number | Specie and Accession Number of Homologue | Functional Description | Homology (%) | Clone Number | Subcellular Location | Reference |
---|---|---|---|---|---|---|---|
Stress and Defense Response | |||||||
ScHTA2 (Histone H2A.2) | MN16790 | Sorghum bicolor XM_002460779.2 | Involved in DNA repair, transcriptional activity, recombination | 96.81 | 1 | N | [21] |
ScRNS4 (Ribonuclease T2) | MN167902 | Sorghum bicolor XM_002462696.2 | Biogenesis of tRNAs derived RNA fragments and viral reverse transcription | 94.36 | 1 | N | [22] |
ScULP5 (Ubiquitin-like protein 5) | MN167908 | Setaria italica XM_004977457.2 | Involved in mRNA splicing and cellular protein modification | 99.10 | 1 | Cyto, N | [23,24] |
ScVAMP727 (Vesicle-associated membrane protein 727) | MN167893 | Sorghum bicolor XM_021465361.1 | Involved in the vacuolar protein deposition and brassinosteroids receptor BRI1 PM targeting | 96.83 | 2 | V | [25] |
ScSERINC3 (Serine incorporator 3) | MN167907 | Sorghum bicolor XM_002454643.2 | Synthesis of phosphatidylserine and sphingolipid | 98.15 | 1 | PM, ER | [26] |
ScPMP22 (Peroxisomal membrane 22 kDa protein) | ScPMP22 | Sorghum bicolor XM_002466831.2 | Import of peroxisomal matrix proteins and the transport of metabolites across the membrane | 96.54 | 3 | P | [27,28] |
ScTSPAN18 (Tetraspanin 18) | MN167910 | Sorghum bicolor XM_002437610.2 | Involved in the development, reproduction, and stress responses in plants | 96.16 | 1 | PM | [29] |
ScHSP82 (Heat shock protein 82) | MN167911 | Sorghum bicolor XM_002447368.2 | Involved in cellular response to heat, protein folding, and protein stabilization | 95.22 | 1 | Cyto | [30] |
Transport-Related Proteins | |||||||
ScPIP1; 2 (Aquaporin PIP1-2) | MN167891 | Sorghum bicolor XM_002454463.2 | Maintenance of cellular water homeostasis | 99.08 | 1 | PM | [31,32,33] |
ScPIP2; 7 (Aquaporin PIP2-7) | MN167895 | Sorghum bicolor XM_021453930.1 | Maintenance of cellular water homeostasis | 93.11 | 4 | PM | [31,32,33] |
ScTIP1; 2 (Aquaporin TIP1-2) | MN167901 | Sorghum bicolor XM_002459138.2 | Maintenance of cellular water homeostasis | 94.79 | 1 | V | [31,32,33] |
ScZIFL1 (Zinc-induced facilitator-like 1) | MN167900 | Sorghum bicolor XM_002457622.2 | Maintenance of Zn homeostasis. Transport of [34] H+-coupled K+ and the polar transport of auxin | 96.08 | 1 | V, PM | [35] |
ScNCX (Sodium/calcium exchanger) | MN167906 | Sorghum bicolor XM_021457777.1 | Maintenance of Ca2+ homeostasis | 95.14 | 1 | PM | [36] |
ScVHA-C (V-type proton ATPase C subunit) | MN167894 | Sorghum bicolor XM_002441847.2 | Required for the assembly of V-ATPase and proton channel formation and transmembrane transport of protons | 96.39 | 1 | V | [37] |
ScSULTR3-3 (Sulfate transporter 3-3) | MN167903 | Sorghum bicolor XM_002448617.2 | Transport of sulfate into chloroplast | 96.48 | 1 | Ch | [38] |
ScGONST4 (GDP-mannose transporter 4) | MN167897 | Sorghum bicolor XM_021454048.1 | Transport of GDP-mannose into Golgi for protein glycosylation | 96.67 | 1 | V | [39] |
ScPPT2 (Phosphoenolpyruvate/phosphate translocator 2) | MN167904 | Sorghum bicolor XM_002454771.2 | Transmembrane transport of phosphoglycerate | 94.73 | 1 | Ch | [40] |
ScTPT (Triose phosphate/phosphate translocator) | MN167912 | Sorghum bicolor XM_002454822.2 | Transport of triose phosphates derived from the Calvin cycle in the stroma into the cytosol for sucrose synthesis and other biosynthetic processes | 97.54 | 1 | Ch | [41,42] |
ScBGLU31 (beta-glucosidase 31) | MN167896 | Sorghum bicolor XM_002438540.2 | Involved in the glucose metabolism to supply acyl and glucosyl for glycosylation | 90.61 | 1 | V | [43] |
ScTMEM208 (Transmembrane protein 208) | MN167890 | Sorghum bicolor XM_002452735.2 | Transport of protein into ER | 97.52 | 1 | ER | [44] |
Photosynthesis | |||||||
ScPsbS (Photosystem II S subunit) | MN167889 | Sorghum bicolor XM_002456659.2 | Involved in nonphotochemical quenching | 96.41 | 3 | Ch | [45,46] |
ScPsbR (Photosystem II R subunit) | MN167892 | Sorghum bicolor XM_002443957.2 | Involved in the assembly of PSII, particularly that of the oxygen-evolving complex subunit PsbP | 94.66 | 1 | Ch | [47,48] |
ScVTE3 (2-methyl-6-phytyl-1,4-hydroquinone methyltransferase 2) | MN167899 | Sorghum bicolor XM_002443518.2 | Involved in the synthesis of vitamin E and plastoquinone | 94.38 | 3 | Ch | [49] |
ScCAB1 (Chlorophyll a/b binding protein 1) | MN167905 | Sorghum bicolor XM_002455856.2 | Involved in the formation of the LHCIIb complex | 97.11 | 1 | Ch | [50] |
© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Zhang, H.; Cheng, G.; Yang, Z.; Wang, T.; Xu, J. Identification of Sugarcane Host Factors Interacting with the 6K2 Protein of the Sugarcane Mosaic Virus. Int. J. Mol. Sci. 2019, 20, 3867. https://doi.org/10.3390/ijms20163867
Zhang H, Cheng G, Yang Z, Wang T, Xu J. Identification of Sugarcane Host Factors Interacting with the 6K2 Protein of the Sugarcane Mosaic Virus. International Journal of Molecular Sciences. 2019; 20(16):3867. https://doi.org/10.3390/ijms20163867
Chicago/Turabian StyleZhang, Hai, Guangyuan Cheng, Zongtao Yang, Tong Wang, and Jingsheng Xu. 2019. "Identification of Sugarcane Host Factors Interacting with the 6K2 Protein of the Sugarcane Mosaic Virus" International Journal of Molecular Sciences 20, no. 16: 3867. https://doi.org/10.3390/ijms20163867
APA StyleZhang, H., Cheng, G., Yang, Z., Wang, T., & Xu, J. (2019). Identification of Sugarcane Host Factors Interacting with the 6K2 Protein of the Sugarcane Mosaic Virus. International Journal of Molecular Sciences, 20(16), 3867. https://doi.org/10.3390/ijms20163867