Constitutive Negative Regulation of R Proteins in Arabidopsis also via Autophagy Related Pathway?
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
26973696
PubMed Central
PMC4777726
DOI
10.3389/fpls.2016.00260
Knihovny.cz E-zdroje
- Klíčová slova
- Avr, ETI, R, autophagy, dwarf, exocyst, lesions, resistance,
- Publikační typ
- časopisecké články MeSH
Even though resistance (R) genes are among the most studied components of the plant immunity, there remain still a lot of aspects to be explained about the regulation of their function. Many gain-of-function mutants of R genes and loss-of-function of their regulators often demonstrate up-regulated defense responses in combination with dwarf stature and/or spontaneous leaf lesions formation. For most of these mutants, phenotypes are a consequence of an ectopic activation of R genes. Based on the compilation and comparison of published results in this field, we have concluded that the constitutively activated defense phenotypes recurrently arise by disruption of tight, constitutive and multilevel negative control of some of R proteins that might involve also their targeting to the autophagy pathway. This mode of R protein regulation is supported also by protein-protein interactions listed in available databases, as well as in silico search for autophagy machinery interacting motifs. The suggested model could resolve some explanatory discrepancies found in the studies of the immunity responses of autophagy mutants.
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Afzal A. J., da Cunha L., Mackey D. (2011). Separable fragments and membrane tethering of Arabidopsis RIN4 regulate its suppression of PAMP-triggered immunity. Plant Cell 23 3798–3811. 10.1105/tpc.111.088708 PubMed DOI PMC
Afzal A. J., Kim J. H., Mackey D. (2013). The role of NOI-domain containing proteins in plant immune signaling. BMC Genomics 14:327 10.1186/1471-2164-14-327 PubMed DOI PMC
Anderson J. C., Bartels S., Gonzalez Besteiro M. A., Shahollari B., Ulm R., Peck S. C. (2011). Arabidopsis MAP Kinase Phosphatase 1 (AtMKP1) negatively regulates MPK6-mediated PAMP responses and resistance against bacteria. Plant J. 67 258–268. 10.1111/j.1365-313X.2011.04588.x PubMed DOI
Axtell M. J., Staskawicz B. J. (2003). Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112 369–377. 10.1016/S0092-8674(03)00036-9 PubMed DOI
Azevedo C., Sadanandom A., Kitagawa K., Freialdenhoven A., Shirasu K., Schulze-Lefert P. (2002). The RAR1 interactor SGT1, an essential component of R gene-triggered disease resistance. Science 295 2073–2076. 10.1126/science.1067554 PubMed DOI
Bartels S., Anderson J. C., Gonzalez Besteiro M. A., Carreri A., Hirt H., Buchala A., et al. (2009). MAP kinase phosphatase1 and protein tyrosine phosphatase1 are repressors of salicylic acid synthesis and SNC1-mediated responses in Arabidopsis. Plant Cell 21 2884–2897. 10.1105/tpc.109.067678 PubMed DOI PMC
Bonardi V., Tang S., Stallmann A., Roberts M., Cherkis K., Dangl J. L. (2011). Expanded functions for a family of plant intracellular immune receptors beyond specific recognition of pathogen effectors. Proc. Natl. Acad. Sci. U.S.A. 108 16463–16468. 10.1073/pnas.1113726108 PubMed DOI PMC
Bowling S. A., Guo A., Cao H., Gordon A. S., Klessig D. F., Dong X. (1994). A mutation in Arabidopsis that leads to constitutive expression of systemic acquired resistance. Plant Cell 6 1845–1857. 10.1105/tpc.6.12.1845 PubMed DOI PMC
Brodersen P., Petersen M., Pike H. M., Olszak B., Skov S., Odum N., et al. (2002). Knockout of Arabidopsis accelerated-cell-death11 encoding a sphingosine transfer protein causes activation of programmed cell death and defense. Genes Dev. 16 490–502. 10.1101/gad.218202 PubMed DOI PMC
Carviel J. L., Al-Daoud F., Neumann M., Mohammad A., Provart N. J., Moeder W., et al. (2009). Forward and reverse genetics to identify genes involved in the age-related resistance response in Arabidopsis thaliana. Mol. Plant Pathol. 10 621–634. 10.1111/j.1364-3703.2009.00557.x PubMed DOI PMC
Century K. S., Holub E. B., Staskawicz B. J. (1995). NDR1, a locus of Arabidopsis thaliana that is required for disease resistance to both a bacterial and a fungal pathogen. Proc. Natl. Acad. Sci. U.S.A. 92 6597–6601. 10.1073/pnas.92.14.6597 PubMed DOI PMC
Century K. S., Shapiro A. D., Repetti P. P., Dahlbeck D., Holub E., Staskawicz B. J. (1997). NDR1, a pathogen-induced component required for Arabidopsis disease resistance. Science 278 1963–1965. 10.1126/science.278.5345.1963 PubMed DOI
Chatre L., Wattelet-Boyer V., Melser S., Maneta-Peyret L., Brandizzi F., Moreau P. (2009). A novel di-acidic motif facilitates ER export of the syntaxin SYP31. J. Exp. Bot. 60 3157–3165. 10.1093/jxb/erp155 PubMed DOI PMC
Collier S. M., Hamel L. P., Moffett P. (2011). Cell death mediated by the N-terminal domains of a unique and highly conserved class of NB-LRR protein. Mol. Plant Microbe Interact. 24 918–931. 10.1094/MPMI-03-11-0050 PubMed DOI
Cvrčková F., Zárský V. (2013). Old AIMs of the exocyst: evidence for an ancestral association of exocyst subunits with autophagy-associated Atg8 proteins. Plant Signal. Behav. 8 e27099. 10.4161/psb.27099 PubMed DOI PMC
Dagdas Y. F., Belhaj K., Maqbool A., Chaparro-Garcia A., Pandey P., Petre B., et al. (2016). An effector of the Irish potato famine pathogen antagonizes a host autophagy cargo receptor. Elife 5 e10856 10.7554/eLife.10856 PubMed DOI PMC
Damer C. K., Bayeva M., Hahn E. S., Rivera J., Socec C. I. (2005). Copine A, a calcium-dependent membrane-binding protein, transiently localizes to the plasma membrane and intracellular vacuoles in Dictyostelium. BMC Cell Biol. 6:46 10.1186/1471-2121-6-46 PubMed DOI PMC
Debener T., Lehnackers H., Arnold M., Dangl J. L. (1991). Identification and molecular mapping of a single Arabidopsis thaliana locus determining resistance to a phytopathogenic Pseudomonas syringae isolate. Plant J. 1 289–302. 10.1046/j.1365-313X.1991.t01-7-00999.x PubMed DOI
Doelling J. H., Walker J. M., Friedman E. M., Thompson A. R., Vierstra R. D. (2002). The APG8/12-activating enzyme APG7 is required for proper nutrient recycling and senescence in Arabidopsis thaliana. J. Biol. Chem. 277 33105–33114. 10.1074/jbc.M204630200 PubMed DOI
Engelhardt S., Boevink P. C., Armstrong M. R., Ramos M. B., Hein I., Birch P. R. (2012). Relocalization of late blight resistance protein R3a to endosomal compartments is associated with effector recognition and required for the immune response. Plant Cell 24 5142–5158. 10.1105/tpc.112.104992 PubMed DOI PMC
Feys B. J., Moisan L. J., Newman M. A., Parker J. E. (2001). Direct interaction between the Arabidopsis disease resistance signaling proteins, EDS1 and PAD4. EMBO J. 20 5400–5411. 10.1093/emboj/20.19.5400 PubMed DOI PMC
Feys B. J., Wiermer M., Bhat R. A., Moisan L. J., Medina-Escobar N., Neu C., et al. (2005). Arabidopsis SENESCENCE-ASSOCIATED GENE101 stabilizes and signals within an ENHANCED DISEASE SUSCEPTIBILITY1 complex in plant innate immunity. Plant Cell 17 2601–2613. 10.1105/tpc.105.033910 PubMed DOI PMC
Fujiki Y., Yoshimoto K., Ohsumi Y. (2007). An Arabidopsis homolog of yeast ATG6/VPS30 is essential for pollen germination. Plant Physiol. 143 1132–1139. 10.1104/pp.106.093864 PubMed DOI PMC
Fujisaki K., Abe Y., Ito A., Saitoh H., Yoshida K., Kanzaki H., et al. (2015). Rice Exo70 interacts with a fungal effector, AVR-Pii, and is required for AVR-Pii-triggered immunity. Plant J. 83 875–887. 10.1111/tpj.12934 PubMed DOI
Gao M., Wang X., Wang D., Xu F., Ding X., Zhang Z., et al. (2009). Regulation of cell death and innate immunity by two receptor-like kinases in Arabidopsis. Cell Host Microbe 6 34–44. 10.1016/j.chom.2009.05.019 PubMed DOI
Gomez-Gomez L., Boller T. (2000). FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol. Cell 5 1003–1011. 10.1016/S1097-2765(00)80265-8 PubMed DOI
Gou M., Hua J. (2012). Complex regulation of an R gene SNC1 revealed by auto-immune mutants. Plant Signal. Behav. 7 213–216. 10.4161/psb.18884 PubMed DOI PMC
Gou M., Shi Z., Zhu Y., Bao Z., Wang G., Hua J. (2012). The F-box protein CPR1/CPR30 negatively regulates R protein SNC1 accumulation. Plant J. 69 411–420. 10.1111/j.1365-313X.2011.04799.x PubMed DOI
Grant J. J., Chini A., Basu D., Loake G. J. (2003). Targeted activation tagging of the Arabidopsis NBS-LRR gene, ADR1, conveys resistance to virulent pathogens. Mol. Plant Microbe Interact. 16 669–680. 10.1094/MPMI.2003.16.8.669 PubMed DOI
Hanaoka H., Noda T., Shirano Y., Kato T., Hayashi H., Shibata D., et al. (2002). Leaf senescence and starvation-induced chlorosis are accelerated by the disruption of an Arabidopsis autophagy gene. Plant Physiol. 129 1181–1193. 10.1104/pp.011024 PubMed DOI PMC
He Y., Gan S. (2002). A gene encoding an acyl hydrolase is involved in leaf senescence in Arabidopsis. Plant Cell 14 805–815. 10.1105/tpc.010422 PubMed DOI PMC
Hofius D., Schultz-Larsen T., Joensen J., Tsitsigiannis D. I., Petersen N. H., Mattsson O., et al. (2009). Autophagic components contribute to hypersensitive cell death in Arabidopsis. Cell 137 773–783. 10.1016/j.cell.2009.02.036 PubMed DOI
Hua J., Grisafi P., Cheng S. H., Fink G. R. (2001). Plant growth homeostasis is controlled by the Arabidopsis BON1 and BAP1 genes. Genes Dev. 15 2263–2272. 10.1101/gad.918101 PubMed DOI PMC
Huang X., Li J., Bao F., Zhang X., Yang S. (2010). A gain-of-function mutation in the Arabidopsis disease resistance gene RPP4 confers sensitivity to low temperature. Plant Physiol. 154 796–809. 10.1104/pp.110.157610 PubMed DOI PMC
Jacob F., Vernaldi S., Maekawa T. (2013). Evolution and conservation of plant NLR functions. Front. Immunol. 4:297 10.3389/fimmu.2013.00297 PubMed DOI PMC
Janda M., Ruelland E. (2014). Magical mystery tour: salicylic acid signaling. Environ. Exp. Bot. 114 117–128. 10.1016/j.envexpbot.2014.07.003 DOI
Jirage D., Tootle T. L., Reuber T. L., Frost L. N., Feys B. J., Parker J. E., et al. (1999). Arabidopsis thaliana PAD4 encodes a lipase-like gene that is important for salicylic acid signaling. Proc. Natl. Acad. Sci. U.S.A. 96 13583–13588. 10.1073/pnas.96.23.13583 PubMed DOI PMC
Jones J. D., Dangl J. L. (2006). The plant immune system. Nature 444 323–329. 10.1038/nature05286 PubMed DOI
Kato H., Saito T., Ito H., Komeda Y., Kato A. (2014). Overexpression of the TIR-X gene results in a dwarf phenotype and activation of defense-related gene expression in Arabidopsis thaliana. J. Plant Physiol. 171 382–388. 10.1016/j.jplph.2013.12.002 PubMed DOI
Ketelaar T., Voss C., Dimmock S. A., Thumm M., Hussey P. J. (2004). Arabidopsis homologues of the autophagy protein Atg8 are a novel family of microtubule binding proteins. FEBS Lett. 567 302–306. 10.1016/j.febslet.2004.04.088 PubMed DOI
Kim H. S., Desveaux D., Singer A. U., Patel P., Sondek J., Dangl J. L. (2005). The Pseudomonas syringae effector AvrRpt2 cleaves its C-terminally acylated target, RIN4, from Arabidopsis membranes to block RPM1 activation. Proc. Natl. Acad. Sci. U.S.A. 102 6496–6501. 10.1073/pnas.0500792102 PubMed DOI PMC
Kim S. H., Gao F., Bhattacharjee S., Adiasor J. A., Nam J. C., Gassmann W. (2010). The Arabidopsis resistance-like gene SNC1 is activated by mutations in SRFR1 and contributes to resistance to the bacterial effector AvrRps4. PLoS Pathog. 6:e1001172 10.1371/journal.ppat.1001172 PubMed DOI PMC
Kliebenstein D. J., Dietrich R. A., Martin A. C., Last R. L., Dangl J. L. (1999). LSD1 regulates salicylic acid induction of copper zinc superoxide dismutase in Arabidopsis thaliana. Mol. Plant Microbe Interact. 12 1022–1026. 10.1094/MPMI.1999.12.11.1022 PubMed DOI
Kong Q., Qu N., Gao M., Zhang Z., Ding X., Yang F., et al. (2012). The MEKK1-MKK1/MKK2-MPK4 kinase cascade negatively regulates immunity mediated by a mitogen-activated protein kinase kinase kinase in Arabidopsis. Plant Cell 24 2225–2236. 10.1105/tpc.112.097253 PubMed DOI PMC
Kreibich S., Emmenlauer M., Fredlund J., Ramo P., Munz C., Dehio C., et al. (2015). Autophagy proteins promote repair of endosomal membranes damaged by the Salmonella type three secretion system 1. Cell Host Microbe 18 527–537. 10.1016/j.chom.2015.10.015 PubMed DOI
Kulich I., Pecenkova T., Sekeres J., Smetana O., Fendrych M., Foissner I., et al. (2013). Arabidopsis exocyst subcomplex containing subunit EXO70B1 is involved in autophagy-related transport to the vacuole. Traffic 14 1155–1165. 10.1111/tra.12101 PubMed DOI
Kulich I., Zarsky V. (2014). Autophagy-related direct membrane import from ER/cytoplasm into the vacuole or apoplast: a hidden gateway also for secondary metabolites and phytohormones? Int. J. Mol. Sci. 15 7462–7474. 10.3390/ijms15057462 PubMed DOI PMC
Levine B., Klionsky D. J. (2004). Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev. Cell 6 463–477. 10.1016/S1534-5807(04)00099-1 PubMed DOI
Li F., Vierstra R. D. (2012). Regulator and substrate: dual roles for the ATG1-ATG13 kinase complex during autophagic recycling in Arabidopsis. Autophagy 8 982–984. 10.4161/auto.20240 PubMed DOI PMC
Li J., Wen J., Lease K. A., Doke J. T., Tax F. E., Walker J. C. (2002). BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110 213–222. 10.1016/S0092-8674(02)00812-7 PubMed DOI
Li Y., Pennington B. O., Hua J. (2009). Multiple R-like genes are negatively regulated by BON1 and BON3 in Arabidopsis. Mol. Plant Microbe Interact. 22 840–848. 10.1094/MPMI-22-7-0840 PubMed DOI
Li Y., Tessaro M. J., Li X., Zhang Y. (2010). Regulation of the expression of plant resistance gene SNC1 by a protein with a conserved BAT2 domain. Plant Physiol. 153 1425–1434. 10.1104/pp.110.156240 PubMed DOI PMC
Liu J., Liu X., Dai L., Wang G. (2007). Recent progress in elucidating the structure, function and evolution of disease resistance genes in plants. J. Genet. Genomics 34 765–776. 10.1016/S1673-8527(07)60087-3 PubMed DOI
Liu Y., Schiff M., Czymmek K., Talloczy Z., Levine B., Dinesh-Kumar S. P. (2005). Autophagy regulates programmed cell death during the plant innate immune response. Cell 121 567–577. 10.1016/j.cell.2005.03.007 PubMed DOI
Lorrain S., Vailleau F., Balague C., Roby D. (2003). Lesion mimic mutants: keys for deciphering cell death and defense pathways in plants? Trends Plant Sci. 8 263–271. 10.1016/S1360-1385(03)00108-0 PubMed DOI
Mackey D., Belkhadir Y., Alonso J. M., Ecker J. R., Dangl J. L. (2003). Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112 379–389. 10.1016/S0092-8674(03)00040-0 PubMed DOI
Mackey D., Holt B. F., III, Wiig A., Dangl J. L. (2002). RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108 743–754. 10.1016/S0092-8674(02)00661-X PubMed DOI
Martin G. B. (1999). Functional analysis of plant disease resistance genes and their downstream effectors. Curr. Opin. Plant Biol. 2 273–279. 10.1016/S1369-5266(99)80049-1 PubMed DOI
McDowell J. M., Woffenden B. J. (2003). Plant disease resistance genes: recent insights and potential applications. Trends Biotechnol. 21 178–183. 10.1016/S0167-7799(03)00053-2 PubMed DOI
Meyers B. C., Kozik A., Griego A., Kuang H., Michelmore R. W. (2003). Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15 809–834. 10.1105/tpc.009308 PubMed DOI PMC
Minina E. A., Bozhkov P. V., Hofius D. (2014). Autophagy as initiator or executioner of cell death. Trends Plant Sci. 19 692–697. 10.1016/j.tplants.2014.07.007 PubMed DOI
Moreau K., Rubinsztein D. C. (2012). The plasma membrane as a control center for autophagy. Autophagy 8 861–863. 10.4161/auto.20060 PubMed DOI PMC
Mukhtar M. S., Carvunis A. R., Dreze M., Epple P., Steinbrenner J., Moore J., et al. (2011). Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science 333 596–601. 10.1126/science.1203659 PubMed DOI PMC
Munch D., Teh O. K., Malinovsky F. G., Liu Q., Vetukuri R. R., El Kasmi F., et al. (2015). Retromer contributes to immunity-associated cell death in Arabidopsis. Plant Cell 27 463–479. 10.1105/tpc.114.132043 PubMed DOI PMC
Nandety R. S., Caplan J. L., Cavanaugh K., Perroud B., Wroblewski T., Michelmore R. W., et al. (2013). The role of TIR-NBS and TIR-X proteins in plant basal defense responses. Plant Physiol. 162 1459–1472. 10.1104/pp.113.219162 PubMed DOI PMC
Nawrath C., Metraux J. P. (1999). Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. Plant Cell 11 1393–1404. 10.2307/3870970 PubMed DOI PMC
Noutoshi Y., Ito T., Seki M., Nakashita H., Yoshida S., Marco Y., et al. (2005). A single amino acid insertion in the WRKY domain of the Arabidopsis TIR-NBS-LRR-WRKY-type disease resistance protein SLH1 (sensitive to low humidity 1) causes activation of defense responses and hypersensitive cell death. Plant J. 43 873–888. 10.1111/j.1365-313X.2005.02500.x PubMed DOI
Ohtomo I., Ueda H., Shimada T., Nishiyama C., Komoto Y., Hara-Nishimura I., et al. (2005). Identification of an allele of VAM3/SYP22 that confers a semi-dwarf phenotype in Arabidopsis thaliana. Plant Cell Physiol. 46 1358–1365. 10.1093/pcp/pci146 PubMed DOI
Palma K., Thorgrimsen S., Malinovsky F. G., Fiil B. K., Nielsen H. B., Brodersen P., et al. (2010). Autoimmunity in Arabidopsis acd11 is mediated by epigenetic regulation of an immune receptor. PLoS Pathog. 6:e1001137 10.1371/journal.ppat.1001137 PubMed DOI PMC
Patel S., Dinesh-Kumar S. P. (2008). Arabidopsis ATG6 is required to limit the pathogen-associated cell death response. Autophagy 4 20–27. 10.4161/auto.5056 PubMed DOI
Petersen M., Brodersen P., Naested H., Andreasson E., Lindhart U., Johansen B., et al. (2000). Arabidopsis map kinase 4 negatively regulates systemic acquired resistance. Cell 103 1111–1120. 10.1016/S0092-8674(00)00213-0 PubMed DOI
Pontier D., Balague C., Roby D. (1998). The hypersensitive response. A programmed cell death associated with plant resistance. C. R. Acad. Sci. III 321 721–734. 10.1016/S0764-4469(98)80013-9 PubMed DOI
Qi Y., Tsuda K., Glazebrook J., Katagiri F. (2011). Physical association of pattern-triggered immunity (PTI) and effector-triggered immunity (ETI) immune receptors in Arabidopsis. Mol. Plant Pathol. 12 702–708. 10.1111/j.1364-3703.2010.00704.x PubMed DOI PMC
Qiu J. L., Zhou L., Yun B. W., Nielsen H. B., Fiil B. K., Petersen K., et al. (2008). Arabidopsis mitogen-activated protein kinase kinases MKK1 and MKK2 have overlapping functions in defense signaling mediated by MEKK1, MPK4, and MKS1. Plant Physiol. 148 212–222. 10.1104/pp.108.120006 PubMed DOI PMC
Reggiori F., Klionsky D. J. (2013). Autophagic processes in yeast: mechanism, machinery and regulation. Genetics 194 341–361. 10.1534/genetics.112.149013 PubMed DOI PMC
Roberts M., Tang S., Stallmann A., Dangl J. L., Bonardi V. (2013). Genetic requirements for signaling from an autoactive plant NB-LRR intracellular innate immune receptor. PLoS Genet. 9:e1003465 10.1371/journal.pgen.1003465 PubMed DOI PMC
Rogers E. E., Ausubel F. M. (1997). Arabidopsis enhanced disease susceptibility mutants exhibit enhanced susceptibility to several bacterial pathogens and alterations in PR-1 gene expression. Plant Cell 9 305–316. 10.1105/tpc.9.3.305 PubMed DOI PMC
Sasek V., Janda M., Delage E., Puyaubert J., Guivarc’h A., Lopez Maseda E., et al. (2014). Constitutive salicylic acid accumulation in pi4kIIIbeta1beta2 Arabidopsis plants stunts rosette but not root growth. New Phytol. 203 805–816. 10.1111/nph.12822 PubMed DOI
Sekine K. T., Nandi A., Ishihara T., Hase S., Ikegami M., Shah J., et al. (2004). Enhanced resistance to Cucumber mosaic virus in the Arabidopsis thaliana ssi2 mutant is mediated via an SA-independent mechanism. Mol. Plant Microbe Interact. 17 623–632. 10.1094/MPMI.2004.17.6.623 PubMed DOI
Shirano Y., Kachroo P., Shah J., Klessig D. F. (2002). A gain-of-function mutation in an Arabidopsis Toll Interleukin1 receptor-nucleotide binding site-leucine-rich repeat type R gene triggers defense responses and results in enhanced disease resistance. Plant Cell 14 3149–3162. 10.1105/tpc.005348 PubMed DOI PMC
Spoel S. H., Dong X. (2012). How do plants achieve immunity? Defence without specialized immune cells. Nat. Rev. Immunol. 12 89–100. 10.1038/nri3141 PubMed DOI
Stark C., Breitkreutz B. J., Reguly T., Boucher L., Breitkreutz A., Tyers M. (2006). BioGRID: a general repository for interaction datasets. Nucleic Acids Res. 34 D535–D539. 10.1093/nar/gkj109 PubMed DOI PMC
Stegmann M., Anderson R. G., Westphal L., Rosahl S., McDowell J. M., Trujillo M. (2013). The exocyst subunit Exo70B1 is involved in the immune response of Arabidopsis thaliana to different pathogens and cell death. Plant Signal. Behav. 8 e27421. 10.4161/psb.27421 PubMed DOI PMC
Synek L., Schlager N., Elias M., Quentin M., Hauser M. T., Zarsky V. (2006). AtEXO70A1, a member of a family of putative exocyst subunits specifically expanded in land plants, is important for polar growth and plant development. Plant J. 48 54–72. 10.1111/j.1365-313X.2006.02854.x PubMed DOI PMC
Takemoto D., Jones D. A. (2005). Membrane release and destabilization of Arabidopsis RIN4 following cleavage by Pseudomonas syringae AvrRpt2. Mol. Plant Microbe Interact. 18 1258–1268. 10.1094/MPMI-18-1258 PubMed DOI
Teh O. K., Hofius D. (2014). Membrane trafficking and autophagy in pathogen-triggered cell death and immunity. J. Exp. Bot. 65 1297–1312. 10.1093/jxb/ert441 PubMed DOI
Thompson A. R., Doelling J. H., Suttangkakul A., Vierstra R. D. (2005). Autophagic nutrient recycling in Arabidopsis directed by the ATG8 and ATG12 conjugation pathways. Plant Physiol. 138 2097–2110. 10.1104/pp.105.060673 PubMed DOI PMC
Tomsig J. L., Creutz C. E. (2002). Copines: a ubiquitous family of Ca(2+)-dependent phospholipid-binding proteins. Cell. Mol. Life Sci. 59 1467–1477. 10.1007/s00018-002-8522-7 PubMed DOI PMC
Trujillo M., Ichimura K., Casais C., Shirasu K. (2008). Negative regulation of PAMP-triggered immunity by an E3 ubiquitin ligase triplet in Arabidopsis. Curr. Biol. 18 1396–1401. 10.1016/j.cub.2008.07.085 PubMed DOI
Tzfadia O., Galili G. (2013). The Arabidopsis exocyst subcomplex subunits involved in a golgi-independent transport into the vacuole possess consensus autophagy-associated atg8 interacting motifs. Plant Signal. Behav. 8 e26732-1–e26732-3. 10.4161/psb.26732 PubMed DOI PMC
Vlot A. C., Liu P. P., Cameron R. K., Park S. W., Yang Y., Kumar D., et al. (2008). Identification of likely orthologs of tobacco salicylic acid-binding protein 2 and their role in systemic acquired resistance in Arabidopsis thaliana. Plant J. 56 445–456. 10.1111/j.1365-313X.2008.03618.x PubMed DOI
Vogelmann K., Drechsel G., Bergler J., Subert C., Philippar K., Soll J., et al. (2012). Early senescence and cell death in Arabidopsis saul1 mutants involves the PAD4-dependent salicylic acid pathway. Plant Physiol. 159 1477–1487. 10.1104/pp.112.196220 PubMed DOI PMC
Wagner S., Stuttmann J., Rietz S., Guerois R., Brunstein E., Bautor J., et al. (2013). Structural basis for signaling by exclusive EDS1 heteromeric complexes with SAG101 or PAD4 in plant innate immunity. Cell Host Microbe 14 619–630. 10.1016/j.chom.2013.11.006 PubMed DOI
Wang Y., Nishimura M. T., Zhao T., Tang D. (2011). ATG2, an autophagy-related protein, negatively affects powdery mildew resistance and mildew-induced cell death in Arabidopsis. Plant J. 68 74–87. 10.1111/j.1365-313X.2011.04669.x PubMed DOI
Yang H., Shi Y., Liu J., Guo L., Zhang X., Yang S. (2010). A mutant CHS3 protein with TIR-NB-LRR-LIM domains modulates growth, cell death and freezing tolerance in a temperature-dependent manner in Arabidopsis. Plant J. 63 283–296. 10.1111/j.1365-313X.2010.04241.x PubMed DOI
Yang S., Hua J. (2004). A haplotype-specific Resistance gene regulated by BONZAI1 mediates temperature-dependent growth control in Arabidopsis. Plant Cell 16 1060–1071. 10.1105/tpc.020479 PubMed DOI PMC
Yang S., Yang H., Grisafi P., Sanchatjate S., Fink G. R., Sun Q., et al. (2006). The BON/CPN gene family represses cell death and promotes cell growth in Arabidopsis. Plant J. 45 166–179. 10.1111/j.1365-313X.2005.02585.x PubMed DOI
Yoshimoto K., Hanaoka H., Sato S., Kato T., Tabata S., Noda T., et al. (2004). Processing of ATG8s, ubiquitin-like proteins, and their deconjugation by ATG4s are essential for plant autophagy. Plant Cell 16 2967–2983. 10.1105/tpc.104.025395 PubMed DOI PMC
Yoshimoto K., Jikumaru Y., Kamiya Y., Kusano M., Consonni C., Panstruga R., et al. (2009). Autophagy negatively regulates cell death by controlling NPR1-dependent salicylic acid signaling during senescence and the innate immune response in Arabidopsis. Plant Cell 21 2914–2927. 10.1105/tpc.109.068635 PubMed DOI PMC
Yu G. L., Katagiri F., Ausubel F. M. (1993). Arabidopsis mutations at the RPS2 locus result in loss of resistance to Pseudomonas syringae strains expressing the avirulence gene avrRpt2. Mol. Plant Microbe Interact. 6 434–443. 10.1094/MPMI-6-434 PubMed DOI
Yu I. C., Parker J., Bent A. F. (1998). Gene-for-gene disease resistance without the hypersensitive response in Arabidopsis dnd1 mutant. Proc. Natl. Acad. Sci. U.S.A. 95 7819–7824. 10.1073/pnas.95.13.7819 PubMed DOI PMC
Zhang Y., Goritschnig S., Dong X., Li X. (2003). A gain-of-function mutation in a plant disease resistance gene leads to constitutive activation of downstream signal transduction pathways in suppressor of npr1-1, constitutive 1. Plant Cell 15 2636–2646. 10.1105/tpc.015842 PubMed DOI PMC
Zhang Z., Lenk A., Andersson M. X., Gjetting T., Pedersen C., Nielsen M. E., et al. (2008). A lesion-mimic syntaxin double mutant in Arabidopsis reveals novel complexity of pathogen defense signaling. Mol. Plant 1 510–527. 10.1093/mp/ssn011 PubMed DOI
Zhang Z., Wu Y., Gao M., Zhang J., Kong Q., Liu Y., et al. (2012). Disruption of PAMP-induced MAP kinase cascade by a Pseudomonas syringae effector activates plant immunity mediated by the NB-LRR protein SUMM2. Cell Host Microbe 11 253–263. 10.1016/j.chom.2012.01.015 PubMed DOI
Zhao T., Rui L., Li J., Nishimura M. T., Vogel J. P., Liu N., et al. (2015). A truncated NLR protein, TIR-NBS2, is required for activated defense responses in the exo70B1 mutant. PLoS Genet. 11:e1004945 10.1371/journal.pgen.1004945 PubMed DOI PMC
Zhou F., Menke F. L., Yoshioka K., Moder W., Shirano Y., Klessig D. F. (2004). High humidity suppresses ssi4-mediated cell death and disease resistance upstream of MAP kinase activation, H2O2 production and defense gene expression. Plant J. 39 920–932. 10.1111/j.1365-313X.2004.02180.x PubMed DOI
Zhou J., Yu J. Q., Chen Z. (2014). The perplexing role of autophagy in plant innate immune responses. Mol. Plant Pathol. 15 637–645. 10.1111/mpp.12118 PubMed DOI PMC
Tethering Complexes in the Arabidopsis Endomembrane System