iTRAQ-based proteomics analysis of autophagy-mediated immune responses against the vascular fungal pathogen Verticillium dahliae in Arabidopsis

References

• Klionsky DJ, Emr SD. Autophagy as a regulated pathway of cellular degradation. Science. 2000;290:1717–1721. doi:10.1126/science.290.5497.1717. PMID:11099404
   PubMed Web of Science ®Google Scholar
• Thompson AR, Vierstra RD. Autophagic recycling: lessons from yeast help define the process in plants. Curr Opin Plant Biol. 2005;8:165–173. doi:10.1016/j.pbi.2005.01.013. PMID:15752997
   PubMed Web of Science ®Google Scholar
• Han S, Yu B, Wang Y, et al. Role of plant autophagy in stress response. Protein Cell. 2011;2:784–791. doi:10.1007/s13238-011-1104-4. PMID:22058033
   PubMed Web of Science ®Google Scholar
• Liu Y, Bassham DC. Autophagy: pathways for self-eating in plant cells. Annu Rev Plant Biol. 2012;63:215–237. doi:10.1146/annurev-arplant-042811-105441. PMID:22242963
   PubMed Web of Science ®Google Scholar
• Liu Y, Schiff M, Czymmek K, et al. Autophagy regulates programmed cell death during the plant innate immune response. Cell. 2005;121:567–577. doi:10.1016/j.cell.2005.03.007. PMID:15907470
   PubMed Web of Science ®Google Scholar
• Andrew PH, Dinesh-Kumar SP. What can plant autophagy do for an innate immune response? Annu Rev Phytopathol. 2011;49:557–576. doi:10.1146/annurev-phyto-072910-095333. PMID:21370973
   PubMed Web of Science ®Google Scholar
• Lenz HD, Haller E, Melzer E, et al. Autophagy controls plant basal immunity in a pathogenic lifestyle-dependent manner. Autophagy. 2011;7:773–774. doi:10.4161/auto.7.7.15535. PMID:21460628
   PubMed Web of Science ®Google Scholar
• Zhou J, Yu J-Q, Chen Z. The perplexing role of autophagy in plant innate immune responses. Mol Plant Pathol. 2014;15:637–645. doi:10.1111/mpp.12118. PMID:24405524
   PubMed Web of Science ®Google Scholar
• Hofius D, Schultz-Larsen T, Joensen J, et al. Autophagic components contribute to hypersensitive cell death in Arabidopsis. Cell. 2009;137:773–783. doi:10.1016/j.cell.2009.02.036. PMID:19450522
   PubMed Web of Science ®Google Scholar
• Wang Y, Wu Y, Tang D. The autophagy gene, ATG18a, plays a negative role in powdery milde resistance and mildew-induced cell death in Arabidopsis. Plant Signal Behav. 2011;6:1408–1410. doi:10.4161/psb.6.9.16967. PMID:21847024
   PubMedGoogle Scholar
• Wang Y, Nishimura MT, Zhao T, et al. ATG2, an autophagy-related protein, negatively affects powdery mildew resistance and mildew-induced cell death in Arabidopsis. Plant J. 2011;68:74–87. doi:10.1111/j.1365-313X.2011.04669.x. PMID:21645148
   PubMed Web of Science ®Google Scholar
• Yoshimoto K. Plant autophagy puts the brakes on cell death by controlling salicylic acid signaling. Autophagy. 2010;6:192–193. doi:10.4161/auto.6.1.10843. PMID:20023431
   PubMed Web of Science ®Google Scholar
• Yoshimoto K, Jikumaru Y, Kamiya Y, et al. Autophagy negatively regulates cell death by controlling NPR-dependent salicylic acid signaling during senescence and the innate immune response in Arabidopsis. Plant Cell. 2009;21:2914–2927. doi:10.1105/tpc.109.068635. PMID:19773385
   PubMed Web of Science ®Google Scholar
• Patel S, Dinesh-Kumar SP. Arabidopsis ATG6 is required to limit the pathogen-associated cell death response. Autophagy. 2008;4:20–27. doi:10.4161/auto.5056. PMID:17932459
   PubMed Web of Science ®Google Scholar
• Lai Z, Wang F, Zheng Z, et al. A critical role of autophagy in plant resistance to necrotrophic fungal pathogens. Plant J. 2011;66:953–968. doi:10.1111/j.1365-313X.2011.04553.x. PMID:21395886
   PubMed Web of Science ®Google Scholar
• Lenz HD, Haller E, Melzer E, et al Autophagy differentially controls plant basal immunity to biotrophic and necrotrophic pathogens. Plant J. 2011;66:818–830. doi:10.1111/j.1365-313X.2011.04546.x. PMID:21332848
   PubMed Web of Science ®Google Scholar
• Han S, Wang Y, Zheng X, et al. Cytoplastic glyceraldehyde-3-phosphate dehydrogenases interact with ATG3 to negatively regulate Autophagy and immunity in Nicotiana benthamiana. Plant Cell. 2015;27:1316–1331. doi:10.1105/tpc.114.134692. PMID:25829441
   PubMed Web of Science ®Google Scholar
• Zimmermann AC, Zarei M, Eiselein S, et al. Quantitative proteomics for the analysis of spatio-temporal protein dynamics during autophagy. Autophagy. 2010;6:1009–1016. doi:10.4161/auto.6.8.12786. PMID:20603599
   PubMed Web of Science ®Google Scholar
• Yadeta K, Thomma B. The xylem as battleground for plant hosts and vascular wilt pathogens. Front Plant Sci. 2013;4:97. doi:10.3389/fpls.2013.00097. PMID:23630534
   PubMed Web of Science ®Google Scholar
• Xu RQ, Blanvillain S, Feng JX, et al. AvrAC(Xcc8004), a type III Effector with a leucine-rich repeat domain from Xanthomonas campestris pathovar campestris confers avirulence in vascular tissues of Arabidopsis thaliana ecotype Col-0. J Bacteriol. 2008;190:343–355. doi:10.1128/JB.00978-07. PMID:17951377
   PubMed Web of Science ®Google Scholar
• Kawchuk LM, Hachey J, Lynch DR, et al. Tomato Ve disease resistance genes encode cell surface-like receptors. Proc Natl Acad Sci USA. 2001;98:6511–6515. doi:10.1073/pnas.091114198. PMID:11331751
   PubMed Web of Science ®Google Scholar
• Zhang Z, Fradin E, de Jonge R, et al. Optimized agroinfiltration and virus-induced gene silencing to study Ve1-mediated Verticillium resistance in tobacco. Mol Plant Microbe Interact. 2013;26:182–190. doi:10.1094/MPMI-06-12-0161-R. PMID:22991998
   PubMed Web of Science ®Google Scholar
• Klosterman SJ, Atallah ZK, Vallad GE, et al. Diversity, pathogenicity, and management of Verticillium species. Annu Rev Phytopathol. 2009;47:39–62. doi:10.1146/annurev-phyto-080508-081748. PMID:19385730
   PubMed Web of Science ®Google Scholar
• Pegg G, Brady B. Verticillium wilts. Wallingford (Oxfordshire): CABI Publishing; 2002.
   Google Scholar
• Schnathorst WC. Life cycle and epidemiology of Verticillium. In: Mace ME, Bell AA, Beckman CH, editors. Fungal wilt diseases of plants. New York (NY): Academic Press; 1981. p. 81–111.
   Google Scholar
• Fradin EF, Thomma BPHJ. Physiology and molecular aspects of Verticillium wilt diseases caused by V. dahliae and V. albo-atrum. Mol Plant Pathol. 2006;7:71–86. doi:10.1111/j.1364-3703.2006.00323.x. PMID:20507429
   PubMed Web of Science ®Google Scholar
• Phillips AR, Suttangkakul A, Vierstra RD. The ATG12-conjugating enzyme ATG10 is essential for autophagic vesicle formation in Arabidopsis thaliana. Genetics. 2008;178:1339–1353. doi:10.1534/genetics.107.086199. PMID:18245858
   PubMed Web of Science ®Google Scholar
• Yoshimoto K, Hanaoka H, Sato S, et al. Processing of ATG8s, ubiquitin-like proteins, and their deconjugation by ATG4s are essential for plant autophagy. Plant Cell. 2004;16:2967–2983. doi:10.1105/tpc.104.025395. PMID:15494556
   PubMed Web of Science ®Google Scholar
• Contento AL, Xiong Y, Bassham DC. Visualization of autophagy in Arabidopsis using the fluorescent dye monodansylcadaverine and a GFP-AtATG8e fusion protein. Plant J. 2005;42:598–608. doi:10.1111/j.1365-313X.2005.02396.x. PMID:15860017
   PubMed Web of Science ®Google Scholar
• Walczak M, Martens S. Dissecting the role of the Atg12-Atg5-Atg16 complex during autophagosome formation. Autophagy. 2013;9:424–425. doi:10.4161/auto.22931. PMID:23321721
   PubMed Web of Science ®Google Scholar
• Wang FX, Ma YP, Yang CL, et al. Proteomic analysis of the sea-island cotton roots infected by wilt pathogen Verticillium dahliae. Proteomics. 2011;11:4296–4309. doi:10.1002/pmic.201100062. PMID:21928292
   PubMedGoogle Scholar
• Parker J, Koh J, Yoo MJ, et al. Quantitative proteomics of tomato defense against Pseudomonas syringae infection. Proteomics. 2013;13:1934–1946. doi:10.1002/pmic.201200402. PMID:23533086
   PubMed Web of Science ®Google Scholar
• Reusche M, Thole K, Janz D, et al. Verticillium infection triggers VASCULAR-RELATED NAC DOMAIN7-dependent de novo xylem formation and enhances drought tolerance in Arabidopsis. Plant Cell. 2012;24:3823–3837. doi:10.1105/tpc.112.103374. PMID:23023171
   PubMed Web of Science ®Google Scholar
• Xie Q, Tzfadia O, Levy M, et al. hfAIM: A reliable bioinformatics approach for in silico genome-wide identification of autophagy-associated Atg8-interacting motifs in various organisms. Autophagy. 2016;12:876–887. doi:10.1080/15548627.2016.1147668. PMID:27071037
   PubMed Web of Science ®Google Scholar
• Kalvari I, Tsompanis S, Mulakkal NC, et al. iLIR: A web resource for prediction of Atg8-family interacting proteins. Autophagy. 2014;10:913–925. doi:10.4161/auto.28260. PMID:24589857
   PubMed Web of Science ®Google Scholar
• Popelka H, Klionsky DJ. Analysis of the native conformation of the LIR/AIM motif in the Atg8/LC3/GABARAP-binding proteins. Autophagy. 2015;11:2153–2159. doi:10.1080/15548627.2015.1111503. PMID:26565669
   PubMed Web of Science ®Google Scholar
• Wu S, Xu Y, Feng Z, et al. Multiple-platform data integration method with application to combined analysis of microarray and proteomic data. BMC Bioinformatics. 2012;13:320. doi:10.1186/1471-2105-13-320. PMID:23198695
   PubMed Web of Science ®Google Scholar
• Mathew R, Khor S, Hackett SR, et al. Functional role of autophagy-mediated proteome remodeling in cell survival signaling and innate immunity. Mol Cell. 2014;55:916–930. doi:10.1016/j.molcel.2014.07.019. PMID:25175026
   PubMed Web of Science ®Google Scholar
• Li J, Liu R, Lei Y, et al. Proteomic analysis revealed association of aberrant ROS signaling with suberoylanilide hydroxamic acid-induced autophagy in Jurkat T-leukemia cells. Autophagy. 2015;6:711–724. doi:10.4161/auto.6.6.12397. PMID:20543569
   PubMedGoogle Scholar
• Mehta A, Magalhães BS, Souza DS, et al. Rooteomics: the challenge of discovering plant defense-related proteins in roots. Curr Protein Pept Sci. 2008;9:108–116. doi:10.2174/138920308783955225. PMID:18393883
   PubMed Web of Science ®Google Scholar
• Koers S, Guzel-Deger A, Marten I, et al. Barley mildew and its elicitor chitosan promote closed stomata by stimulating guard-cell S-type anion channels. Plant J. 2010;68:670–680. doi:10.1111/j.1365-313X.2011.04719.x. PMID:21781196
   PubMed Web of Science ®Google Scholar
• Bartels S, Lori M, Mbengue M, et al. The family of Peps and their precursors in Arabidopsis: differential expression and localization but similar induction of pattern-triggered immune responses. J Exp Bot. 2013;64:5309–5321. doi:10.1093/jxb/ert330. PMID:24151300
   PubMed Web of Science ®Google Scholar
• Bartels S, Boller T. Quo vadis, Pep? Plant elicitor peptides at the crossroads of immunity, stress, and development. J Exp Bot. 2015;66:5183–5193. doi:10.1093/jxb/erv180. PMID:25911744
   PubMed Web of Science ®Google Scholar
• Kadota Y, Sklenar J, Derbyshire P, et al. Direct regulation of the NADPH oxidase RBOHD by the PRR-associated kinase BIK1 during plant immunity. Mol Cell. 2014;54:43–55. doi:10.1016/j.molcel.2014.02.021. PMID:24630626
   PubMed Web of Science ®Google Scholar
• Straus MR, Rietz S, Ver Loren van Themaat E, et al. Salicylic acid antagonism of EDS1-driven cell death is important for immune and oxidative stress responses in Arabidopsis. Plant J. 2010;62:628–640. doi:10.1111/j.1365-313X.2010.04178.x. PMID:20163553
   PubMed Web of Science ®Google Scholar
• Palma K, Thorgrimsen S, Malinovsky FG, et al. Autoimmunity in Arabidopsis acd11 is mediated by epigenetic regulation of an immune receptor. Plos Pathogens. 2010;6:e1001137. doi:10.1371/journal.ppat.1001137. PMID:20949080
   PubMed Web of Science ®Google Scholar
• Gomes LC, Scorrano L. Mitochondrial morphology in mitophagy and macroautophagy. Biochim Biophys Acta. 2013;1833:205–212. doi:10.1016/j.bbamcr.2012.02.012. PMID:22406072
   PubMed Web of Science ®Google Scholar
• Jones A. Does the plant mitochondrion integrate cellular stress and regulate programmed cell death? Trends Plant Sci. 2000;5:225–230. doi:10.1016/S1360-1385(00)01605-8. PMID:10785669
   PubMed Web of Science ®Google Scholar
• Maxwell DP, Nickels R, McIntosh L. Evidence of mitochondrial involvement in the transduction of signals required for the induction of genes associated with pathogen attack and senescence. Plant J. 2002;29:269–279. doi:10.1046/j.1365-313X.2002.01216.x. PMID:11844105
   PubMed Web of Science ®Google Scholar
• Dutilleul C, Garmier M, Noctor G, et al. Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulation. Plant Cell. 2003;15:1212–1226. doi:10.1105/tpc.009464. PMID:12724545
   PubMed Web of Science ®Google Scholar
• Swidzinski JA, Leaver CJ, Sweetlove LJ. A proteomic analysis of plant programmed cell death. Phytochemistry. 2004;65:1829–1838. doi:10.1016/j.phytochem.2004.04.020. PMID:15276441
   PubMed Web of Science ®Google Scholar
• Cvetkovska M, Vanlerberghe GC. Alternative oxidase impacts the plant response to biotic stress by influencing the mitochondrial generation of reactive oxygen species. Plant Cell Environ. 2013;36:721–732. doi:10.1111/pce.12009. PMID:22978428
   PubMed Web of Science ®Google Scholar
• Twig G, Hyde B, Shirihai OS. Mitochondrial fusion, fission and autophagy as a quality control axis: the bioenergetic view. Biochim Biophys Acta. 2008;1777:1092–1097. doi:10.1016/j.bbabio.2008.05.001. PMID:18519024
   PubMed Web of Science ®Google Scholar
• Wei Y, Chiang WC, Sumpter R Jr, et al. Prohibitin 2 is an inner mitochondrial membrane mitophagy receptor. Cell. 2017;168:224–238. doi:10.1016/j.cell.2016.11.042. PMID:28017329
   PubMed Web of Science ®Google Scholar
• van Doorn WG. Classes of programmed cell death in plants, compared to those in animals. J Exp Bot. 2011;62:4749–4761. doi:10.1093/jxb/err196. PMID:21778180
   PubMed Web of Science ®Google Scholar
• Barceló AR. Lignification in plant cell walls. Int Rev Cytol. 1997;176:87–132. doi:10.1016/S0074-7696(08)61609-5. PMID:9394918
   PubMedGoogle Scholar
• Xu L, Zhu L, Tu L, Liu L, et al. Lignin metabolism has a central role in the resistance of cotton to the wilt fungus Verticillium dahliae as revealed by RNA-Seq-dependent transcriptional analysis and histochemistry. J Exp Bot. 2011;62:5607–5621. doi:10.1093/jxb/err245. PMID:21862479
   PubMed Web of Science ®Google Scholar
• Pomar F, Novo M, Bernal MA, et al. Changes in stem lignins (monomer composition and crosslinking) and peroxidase are related with the maintenance of leaf photosynthetic integrity during Verticillium wilt in Capsicum annuum. New Phytol. 2004;163:111–123. doi:10.1111/j.1469-8137.2004.01092.x.
   PubMed Web of Science ®Google Scholar
• Kwon SI, Cho HJ, Kim SR, et al. The Rab GTPase RabG3b positively regulates autophagy and immunity-associated hypersensitive cell death in Arabidopsis. Plant Physiol. 2013;161:1722–1736. doi:10.1104/pp.112.208108. PMID:23404918
   PubMed Web of Science ®Google Scholar
• Nelson BK, Cai X, Nebenführ A. A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J. 2007;51:1126–1136. doi:10.1111/j.1365-313X.2007.03212.x. PMID:17666025
   PubMed Web of Science ®Google Scholar
• Chaudhary P, Godara S, Cheeran AN, et al. Fast and accurate method for leaf area measurement. IJCA. 2012;49:22–25. doi:10.5120/7655-0757.
   Google Scholar
• Wang ZQ, Xu XY, Gong QQ, et al. Root proteome of rice studied by iTRAQ provides integrated insight into aluminum stress tolerance mechanisms in plants. J Proteomics. 2014;98:189–205. doi:10.1016/j.jprot.2013.12.023. PMID:24412201
   PubMed Web of Science ®Google Scholar
• Nesvizhskii AI, Keller A, Kolker E, et al. A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem. 2003;75:4646–4658. doi:10.1021/ac0341261. PMID:14632076
   PubMed Web of Science ®Google Scholar
• Shadforth IP, Dunkley TPJ, Lilley KS, et al. i-Tracker: For quantitative proteomics using iTRAQ (TM). BMC Genomics. 2005;6:145. doi:10.1186/1471-2164-6-145. PMID:16242023
   PubMed Web of Science ®Google Scholar
• Du Z, Zhou X, Ling Y, et al. agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res. 2010;38:W64–W70. doi:10.1093/nar/gkq310. PMID:20435677
   PubMed Web of Science ®Google Scholar
• Kanehisa M, Goto S, Sato Y, et al. KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res. 2012;40:D109–D114. doi:10.1093/nar/gkr988. PMID:22080510
   PubMed Web of Science ®Google Scholar
• Wang HY, Wang J, Gao P, et al. Down-regulation of GhADF1 gene expression affects cotton fibre properties. Plant Biotechnol J. 2009;7:13–23. doi:10.1111/j.1467-7652.2008.00367.x. PMID:18761653
   PubMed Web of Science ®Google Scholar
• Pantelides IS, Tjamos SE, Paplomatas EJ. Ethylene perception via ETR1 is required in Arabidopsis infection by Verticillium dahliae. Mol Plant Pathol. 2010;11:191–202. doi:10.1111/j.1364-3703.2009.00592.x. PMID:20447269
   PubMed Web of Science ®Google Scholar
• Li F, Vierstra RD. Arabidopsis ATG11, a scaffold that links the ATG1-ATG13 kinase complex to general autophagy and selective mitophagy. Autophagy. 2014;10:1466–1467. doi:10.4161/auto.29320. PMID:24991832
   PubMed Web of Science ®Google Scholar
• Klionsky DJ, Abdelmohsen K, Abe A, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy. 2016;12:1–222. doi:10.1080/15548627.2015.1100356. PMID:26799652
   PubMed Web of Science ®Google Scholar
• Moreira-Vilar FC, Siqueira-Soares RdC, Finger-Teixeira A, et al. The acetyl bromide method is faster, simpler and presents best recovery of lignin in different herbaceous tissues than Klason and thioglycolic acid methods. PLoS One. 2014;9:e110000. doi:10.1371/journal.pone.0110000. PMID:25330077
   PubMed Web of Science ®Google Scholar
• Han LB, Li YB, Wang HY, et al. The dual functions of WLIM1a in cell elongation and secondary wall formation in developing cotton fibers. Plant Cell. 2013;25:4421–4438. doi:10.1105/tpc.113.116970. PMID:24220634
   PubMed Web of Science ®Google Scholar
• Song X, Guo H, Zhang G, et al. OsPRA2 fine-tunes rice brassinosteroid receptor. Plant Sign Behav. 2017;4:e1257455. doi:10.1080/15592324.2016.1257455. PMID:28402719
   PubMedGoogle Scholar
• Dagdas YF, Belhaj K, Maqbool A, et al. An effector of the Irish potato famine pathogen antagonizes a host autophagy cargo receptor. eLife. 2016;5:e10856. doi:10.7554/eLife.10856. PMID:26765567
   PubMed Web of Science ®Google Scholar