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Autoimmunity in plants

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Abstract

Main conclusion

Attenuation in the activity of the negative regulators or the hyperactivity of plant innate immune receptors often causes ectopic defense activation manifested in severe growth retardation and spontaneous lesion formations, referred to as autoimmunity. In this review, we have described the cellular and molecular basis of the development of autoimmune responses for their useful applications in plant defense.

Plants are exposed to diverse disease-causing pathogens, which bring infections by taking over the control on host immune machineries. To counter the challenges of evolving pathogenic races, plants recruit specific types of intracellular immune receptors that mostly belong to the family of polymorphic nucleotide-binding oligomerization domain-containing leucine-rich repeat (NLR) proteins. Upon recognition of effector molecules, NLR triggers hyperimmune signaling, which culminates in the form of a typical programmed cell death, designated hypersensitive response. Besides, few plant NLRs also guard certain host proteins known as ‘guardee’ that are modified by effector proteins. However, this fine-tuned innate immune system can be lopsided upon knock-out of the alleles that correspond to the host guardees, which mimick the presence of pathogen. The absence of pathogens causes inappropriate activation of the respective NLRs and results in the constitutive activation of plant defense and exhibiting autoimmunity. In plants, autoimmune mutants are readily scorable due to their dwarf phenotype and development of characteristic macroscopic disease lesions. Here, we summarize recent reports on autoimmune response in plants, how it is triggered, and phenotypic consequences associated with this phenomenon.

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Abbreviations

ACD11:

Accelerated cell death 11

Avr:

Avirulence

CC:

Coiled-coil

CNL:

Coiled-coil NLR

EDS1:

Enhanced disease susceptibility

ETI:

Effector-triggered immunity

LOF:

Loss-of-function

LMMs:

Lesion mimic mutants

LRR:

Leucine-rich repeat

NLR:

Nucleotide-binding oligomerization domain-containing leucine-rich repeat

PCD:

Programmed cell death

PTI:

Pattern triggered immunity

RGA:

Resistance gene analog

RLP:

Receptor-like protein

TIR:

Toll-interleukin receptor

TNL:

TIR-NLR

UPS:

Ubiquitin proteasome system

References

  • Ali Z, Ali S, Tashkandi M, Zaidi SS, Mahfouz MM (2016) CRISPR/Cas9-mediated immunity to geminiviruses: differential interference and evasion. Sci Rep 6:26912

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aouida M, Piatek MJ, Bangarusamy DK, Mahfouz MM (2014) Activities and specificities of homodimeric TALENs in Saccharomyces cerevisiae. Curr Genet 60:61–74

    Article  CAS  PubMed  Google Scholar 

  • Baltes NJ, Hummel AW, Konecna E, Cegan R, Bruns AN, Bisaro DM et al (2015) Conferring resistance to geminiviruses with the CRISPR–Cas prokaryotic immune system. Nat Plants 1:15145

    Article  CAS  Google Scholar 

  • Bartels S, Anderson JC, Gonzalez Besteiro MA, 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baruah A, Simkova K, Hincha DK, Apel K, Laloi C (2009) Modulation of O-mediated retrograde signaling by the PLEIOTROPIC RESPONSE LOCUS 1 (PRL1) protein, a central integrator of stress and energy signaling. Plant J 60:22–32

    Article  CAS  PubMed  Google Scholar 

  • Beckers GJM et al (2009) Mitogen-activated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsis thaliana. Plant Cell 21:944–953

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bernoux M, Ve T, Williams S et al (2011) Structural and functional analysis of a plant resistance protein TIR domain reveals interfaces for self-association, signaling, autoregulation. Cell Host Microbe 9:200–211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhattacharjee S, Halane MK, Kim SH, Gassmann W (2011) Pathogen effectors target Arabidopsis EDS1 and alter its interactions with immune regulators. Science 334:1405–1408

    Article  CAS  PubMed  Google Scholar 

  • Bi D, Cheng YT, Li X, Zhang Y (2010) Activation of plant immune responses by again-of-function mutation in an atypical receptor-like kinase. Plant Physiol 153:1771–1779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bi D, Johnson K, Huang Y, Zhu Z, Li X, Zhang Y (2011) Mutations in an atypical TIR-NB-LRR-LIM resistance protein confers autoimmunity. Front Plant Sci 2:71

    Article  PubMed  PubMed Central  Google Scholar 

  • Boccara M, Sarazin A, Thiébeauld O, Jay F, Voinnet O, Navarro L, Colot V (2014) The Arabidopsis miR472-RDR6 silencing pathway modulates PAMP- and effector-triggered immunity through the posttranscriptional control of disease resistance genes. PLoS Pathog 10:e1003883

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bomblies K, Weigel D (2007) Hybrid necrosis: autoimmunity as a potential gene flow barrier in plant species. Nat Rev Genet 8:382–393

    Article  CAS  PubMed  Google Scholar 

  • Bomblies K, Lempe J, Epple P, Warthmann N, Lanz C, Dangl JL, Weigel D (2007) Autoimmune response as a mechanism for a Dobzhansky–Muller-type incompatibility syndrome in plants. PLoS Biol 5:1962–1972

    Article  CAS  Google Scholar 

  • Borhan MH, Gunn N, Cooper A et al (2008) WRR4 encodes a TIRNB-LRR protein that confers broad-spectrum white rust resistance in Arabidopsis thaliana to four physiological races of Albugo candida. Mol Plant Microbe Interact 21:757–768

    Article  CAS  PubMed  Google Scholar 

  • Borhan MH, Holub EB, Kindrachuk C et al (2010) WRR4, a broad spectrum TIR-NB-LRR gene from Arabidopsis thaliana that confers white rust resistance in transgenic oilseed Brassica crops. Mol Plant Pathol 11:283–291

    Article  CAS  PubMed  Google Scholar 

  • Brodersen P, Petersen M, Pike HM, Brodersen P, Petersen M, Pike HM, Olszak B, Skov S, Ødum N, Jørgensen LB et al (2002) Knockout of Arabidopsis encoding a sphingosine transfer protein causes activation of programmed cell death and defense. Genes Dev 16:490–502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brodersen P, Malinovsky FG, Hématy K, Newman MA, Mundy J (2005) The role of salicylic acid in the induction of cell death in Arabidopsis acd11. Plant Physiol 138:1037–1045

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bruggeman Q, Raynaud C, Benhamed M, Delarue M (2015) To die or not to die? Lessons from lesion mimic mutants. Front Plant Sci 6:1–22

    Article  Google Scholar 

  • Cesari S, Thilliez G, Ribot C, Chalvon V, Michel C, Jauneau A, Rivas S, Alaux L, Kanzaki H, Okuyama Y et al (2013) The rice resistance protein pair RGA4/RGA5 recognizes the Magnaporthe oryzae effectors AVR-Pia and AVR1-CO39 by direct binding. Plant Cell 25:1463–1481

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chakraborty J, Jain A, Mukherjee D, Ghosh S, Das S (2018) Functional diversification of structurally alike NLR proteins in plants. Plant Sci 269:85–93

    Article  CAS  PubMed  Google Scholar 

  • Cheng YT, Li Y, Huang S, Huang Y, Dong X, Zhang Y et al (2011) Stability of plant immune-receptor resistance proteins is controlled by SKP1-CULLIN1-F-box (SCF)-mediated protein degradation. Proc Natl Acad Sci USA 108:14694–14699

    Article  CAS  PubMed  Google Scholar 

  • Christian M, Cermak T, Doyle EL, Schmidt C, Zhang F, Hummel A et al (2010) Targeting DNA double-strand breaks with TAL effector nucleases. Genetics 186:757–761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clough SJ, Fengler KA, Yu IC et al (2000) The Arabidopsis dnd1 “defense, no death” gene encodes a mutated cyclic nucleotide-gated ion channel. Proc Natl Acad Sci USA 97:9323–9328

    Article  CAS  PubMed  Google Scholar 

  • Colinas M, Eisenhut M, Tohge T, Pesquera M, Fernie AR, Weber AP, Fitzpatrick TB (2016) Balancing of B6 vitamers is essential for plant development and metabolism in Arabidopsis. Plant Cell 28(2):439–453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dangl JL, Jones JD (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833

    Article  CAS  PubMed  Google Scholar 

  • de Oliveira MV, Xu G, Li B, deSouza Vespoli L, Meng X, Chen X et al (2016) Specific control of Arabidopsis BAK1/SERK4-regulated cell death by protein glycosylation. Nat Plants 2:15218

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Du L, Ali GS, Simons KA, Hou J, Yang T, Reddy ASN et al (2009) Ca2+/calmodulin regulates salicylic-acid-mediated plant immunity. Nature 457:1154–1158

    Article  CAS  PubMed  Google Scholar 

  • Du J, Gao Y, Zhan Y, Zhang S, Wu Y, Xiao Y et al (2016) Nucleocytoplasmic trafficking is essential for BAK1-and BKK1-mediated cell-death control. Plant J 85:520–531

    Article  CAS  PubMed  Google Scholar 

  • Epple P, Mack AA, Morris VR, Dangl JL (2003) Antagonistic control of oxidative stress-induced cell death in Arabidopsis by two related, plant- specific zinc finger proteins. Proc Natl Acad Sci USA 100:6831–6836

    Article  CAS  PubMed  Google Scholar 

  • Fan J, Doerner P (2012) Genetic and molecular basis of nonhost disease resistance: complex, yes; silver bullet, no. Curr Opin Plant Biol 15:400–406

    Article  CAS  PubMed  Google Scholar 

  • Fitzpatrick TB, Amrhein N, Kappes B, Macheroux P, Tews I, Raschle T (2007) Two independent routes of de novo vitamin B6 biosynthesis: notthat different after all. Biochem J 407:1–13

    Article  CAS  PubMed  Google Scholar 

  • Flor HH (1971) Current status of the gene-for-gene concept. Annu Rev Phytopathol 9:275–296

    Article  Google Scholar 

  • Fujioka S, Yokota T (2003) Biosynthesis and metabolism of brassinosteroids. Annu Rev Plant Biol 54:137–164

    Article  CAS  PubMed  Google Scholar 

  • Galon Y, Nave R, Boyce JM, Nachmias D, Knight MR, Fromm H (2008) Calmodulin-binding transcription activator (CAMTA) 3 mediates biotic defense responses in Arabidopsis. FEBS Lett 582:943–948

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez E, Danehower D, Daub ME (2007) Vitamer levels, stress response, enzyme activity, and gene regulation of Arabidopsis lines mutant in the pyridoxine/pyridoxamine 5′-phosphate oxidase (PDX3) and the pyridoxal kinase (SOS4) genes involved in the vitamin B6 salvage pathway. Plant Physiol 145:985–996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gupta S, Chakraborti D, Basu D, Das S (2010) In search of decoy/guardee to R genes: deciphering the role of sugars in defense against Fusarium wilt in chickpea. Plant Signal Behav 5:9

    Article  CAS  Google Scholar 

  • Haas BJ, Kamoun S, Zody MC et al (2009) Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461:393–398

    Article  CAS  PubMed  Google Scholar 

  • Hanley-Bowdoin L, Bejarano ER, Robertson D, Mansoor S (2013) Geminiviruses: masters at redirecting and reprogramming plant processes. Nat Rev Microbiol 11:777–788

    Article  CAS  PubMed  Google Scholar 

  • He K, Gou X, Yuan T, Lin H, Asami T, Yoshida S et al (2007) BAK1and BKK1 regulate brassinosteroid-dependent growth and brassinosteroid-independent cell-death pathways. Curr Biol 17:1109–1115

    Article  CAS  PubMed  Google Scholar 

  • Hofius D, Schultz-Larsen T, Joensen J, Tsitsigiannis DI, Petersen NH, Mattsson O, Jørgensen LB, Jones JD, Mundy J, Petersen M (2009) Autophagic components contribute to hypersensitive cell death in Arabidopsis. Cell 137:773–783

    Article  CAS  PubMed  Google Scholar 

  • Hua J, Grisafi P, Cheng SH, Fink GR (2001) Plant growth homeostasis is controlled by the Arabidopsis BON1 and BAP1 genes. Genes Dev 15:2263–2272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang Y, Minaker S, Roth C, Huang S, Hieter P, Lipka V, Wiermer M, Li X (2014) An E4 ligase facilitates polyubiquitination of plant immune receptor resistance proteins in Arabidopsis. Plant Cell 26:485–496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang S, Chen X, Zhong X, Li M, Ao K, Huang J, Li X (2016) Plant TRAF proteins regulate NLR immune receptor turnover. Cell Host Microbe 19(2):204–215

    Article  CAS  PubMed  Google Scholar 

  • Ji X, Zhang H, Zhang Y, Wang Y, Gao C (2015) Establishing a CRISPR- Cas-like immune system conferring DNA virus resistance in plants. Nat Plants 1:15144

    Article  CAS  PubMed  Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  CAS  PubMed  Google Scholar 

  • Jones JDG, Vance RE, Dangl JL (2016) Intracellular innate immune surveillance devices in plants and animals. Science 354:5

    Article  Google Scholar 

  • Kachroo A, Lapchyk L, Fukushige H, Hildebrand D, Klessig D, Kachroo P (2003a) Plastidial fatty acid signaling modulates salicylic acid- and jasmonic acid-mediated defense pathways in the Arabidopsis ssi2 mutant. Plant Cell 15:2952–2965

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kachroo P, Kachroo A, Lapchyk L, Hildebrand D, Klessig DF (2003b) Restoration of defective crosstalk in ssi2 mutants: role of salicylic acid, jasmonic acid, and fatty acids in SSI2-mediated signaling. Mol Plant Microbe Interact 16:1022–1029

    Article  CAS  PubMed  Google Scholar 

  • Kaminaka H, Nake C, Epple P, Dittgen J, Schutze K, Chaban C et al (2006) bZIP10-LSD1 antagonism modulates basal defense and cell death in Arabidopsis following infection. EMBO J 25:4400–4411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kemmerling B, Schwedt A, Rodriguez P, Mazzotta S, Frank M, Qamar SA et al (2007) The BRI1-associated kinase1, BAK1, has a brassinolide- independent role in plant cell-death control. Curr Biol 17:1116–1122

    Article  CAS  PubMed  Google Scholar 

  • Kim YG, Cha J, Chandrasegaran S (1996) Hybrid restriction enzymes: zinc finger fusions to Fok I cleavage domain. Proc Natl Acad Sci USA 93:1156–1160

    Article  CAS  PubMed  Google Scholar 

  • Kim MG, da Cunha L, McFall AJ, Belkhadir Y, DebRoy S, Dangl JL, Mackey D (2005) Two Pseudomonas syringae type III effectors inhibit RIN4-regulated basal defense in Arabidopsis. Cell 121:749–759

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lapidot M, Karniel U, Gelbart D, Fogel D, Evenor D, Kutsher Y et al (2015) A novel route controlling begomovirus resistance by the messenger RNA surveillance factor pelota. PLoS Genet 11:e1005538

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li F, Vierstra RD (2012) Regulator and substrate: dual roles for the ATG1- ATG13 kinase complex during autophagic recycling in Arabidopsis. Autophagy 8:982–984

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li X, Clarke JD, Zhang Y, Dong X (2001) Activation of an EDS1-mediated R-gene pathway in the snc1 mutant leads to constitutive, NPR1-independent pathogen resistance. Mol Plant Microbe Interact 14:1131–1139

    Article  CAS  PubMed  Google Scholar 

  • Li J, Wen JQ, Lease KA, Doke JT, Tax FE, Walker JC (2002) BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110:213–222

    Article  CAS  PubMed  Google Scholar 

  • Li B, Lu D, Shan L (2014a) Ubiquitination of pattern recognition receptors in plant innate immunity. Mol Plant Pathol 15:737–746

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li M, Ma X, Chiang Y-H, Yadeta KA, Ding P, Dong L, Zhao Y, Li X, Yu Y, Zhang L et al (2014b) Proline isomerization of the immune receptor-interacting protein RIN4 by a cyclophilin inhibits effector-triggered immunity in Arabidopsis. Cell Host Microbe 16:473–483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liebrand TW, van den Berg GC, Zhang Z, Smit P, Cordewener JH, America AH, Sklenar J, Jones AM, Tameling WI, Robatzek S, Thomma BP, Joosten MH (2013) Receptor-like kinase SOBIR1/EVR interacts with receptor-like proteins in plant immunity against fungal infection. Proc Natl Acad Sci USA 110:10010–10015

    Article  CAS  PubMed  Google Scholar 

  • Liebrand TW, van den Burg HA, Joosten MH (2014) Two for all: receptor-associated kinases SOBIR1 and BAK1. Trends Plant Sci 19:123–132

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Ding P, Sun T, Nitta Y, Dong O, Huang X et al (2013) Heterotrimeric G proteins serve as a converging point in plant defense signaling activated by multiple receptor-like kinases. Plant Physiol 161:2146–2158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lolle S, Greeff C, Petersen K, Roux M, Jensen MK, Bressendorff S, Rodriguez E, Sømark K, Mundy J, Petersen M (2017) Matching NLR immune receptors to autoimmunity in camta3 mutants using antimorphic NLR alleles. Cell Host Microbe 21(4):518–529

    Article  CAS  PubMed  Google Scholar 

  • Lu H, Rate DN, Song JT, Greenberg JT (2003) ACD6, a novel ankyrin protein, is a regulator and an effector of salicylic acid signalling in the Arabidopsis defense response. Plant Cell 15:2408–2420

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu H, Salimian S, Gamelin E, Wang G, Fedorowski J, LaCourse W et al (2009) Genetic analysis of acd6-1 reveals complex defense networks and leads to identification of novel defense genes in Arabidopsis. Plant J 58:401–412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mackey D, Holt BF, Wiig A, Dangl JL (2002) RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108:743–754

    Article  CAS  PubMed  Google Scholar 

  • Mackey D, Belkhadir Y, Alonso JM, Ecker JR, Dangl JL (2003) Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112:379–389

    Article  CAS  PubMed  Google Scholar 

  • Marzluf GA (1997) Genetic regulation of nitrogen metabolism in fungi. Microbiol Mol Biol Rev 61:17–32

    CAS  PubMed  PubMed Central  Google Scholar 

  • McHale L, Tan X, Koehl P et al (2006) Plant NBS-LRR proteins: adaptable guards. Genome Biol 7:212

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Monaghan J, Germain H, Weihmann T, Li X (2010) Dissecting plant defence signal transduction: modifiers of snc1 in Arabidopsis. Can J Plant Pathol 32:35–42

    Article  CAS  Google Scholar 

  • Munch D, Teh OK, Malinovsky FG, Liu Q, Vetukuri RR, El Kasmi F, Brodersen P, Hara-Nishimura I, Dangl JL, Petersen M et al (2015) Retromer contributes to immunity-associated cell death in Arabidopsis. Plant Cell 27:463–479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nodzynski T, Feraru MI, Hirsch S, De Rycke R, Niculaes C, Boerjan W, Van Leene J, De Jaeger G, Vanneste S, Friml J (2013) Retromer subunits VPS35A and VPS29 mediate prevacuolar compartment (PVC) function in Arabidopsis. Mol Plant 6:1849–1862

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Palma K, Thorgrimsen S, Malinovsky FG, Fiil BK, Nielsen HB, Brodersen P, Hofius D, Petersen M, Mundy J (2010) Autoimmunity in Arabidopsis acd11 is mediated by epigenetic regulation of an immune receptor. PLoS Pathog 6:e1001137

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pan H, Liu S, Tang D (2012) HPR1, a component of the THO/TREX complex, plays an important role in disease resistance and senescence in Arabidopsis. Plant J 69:831–843

    Article  CAS  PubMed  Google Scholar 

  • Park BS, Song JT, Seo H (2011) Arabidopsis nitrate reductase activity is stimulated by the E3 SUMO ligase AtSIZ1. Nat Commun 2:400

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pastor V, Gamir J, Camanes G, Cerezo M, Sanchez-Bel P, Flors V (2014) Disruption of the ammonium transporter AMT1.1 alters basal defenses generating resistance against Pseudomonas syringae and Plectosphaerella cucumerina. Front. Plant Sci 5:231

    Google Scholar 

  • Petutschnig EK, Stolze M, Lipka U, Kopischke M, Horlacher J, Valerius O et al (2014) A novel Arabidopsis CHITIN ELICITOR RECEPTOR KINASE 1 (CERK1) mutant with enhanced pathogen-induced cell death and altered receptor processing. New Phytol 204:955–967

    Article  CAS  PubMed  Google Scholar 

  • Piatek A, Mahfouz MM (2016) Targeted genome regulation via synthetic programmable transcriptional regulators. Crit Rev Biotechnol. https://doi.org/10.3109/07388551

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Reyes FC, Buono R, Otegui MS (2011) Plant endosomal trafficking pathways. Curr Opin Plant Biol 14:666–673

    Article  CAS  PubMed  Google Scholar 

  • Reyes MI, Nash TE, Dallas MM, Ascencio-Ibanez JT, Hanley-Bowdoin L (2013) Peptide aptamers that bind to geminivirus replication proteins confer a resistance phenotype to tomato yellow leaf curl virus and tomato mottle virus infection in tomato. J Virol 87:9691–9706

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riehs-Kearnan N, Gloggnitzer J, Dekrout B, Jonak C, Riha K (2012) Aberrant growth and lethality of Arabidopsis deficient in nonsense-mediated RNA decay factors is caused by autoimmune-like response. Nucleic Acids Res 40:5615–5624

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rioux JD, Abbas AK (2005) Paths to understanding the genetic basis of autoimmune disease. Nature 435(7042):584–589

    Article  CAS  PubMed  Google Scholar 

  • Robinson DG, Pimpl P, Scheuring D, Stierhof YD, Sturm S, Viotti C (2012) Trying to make sense of retromer. Trends Plant Sci 17:431–439

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez E, El Ghoul H, Mundy J, Petersen M (2016) Making sense of plant autoimmunity and ‘negative regulators’. FEBS J 283:1385–1391

    Article  CAS  PubMed  Google Scholar 

  • Sarris PF, Duxbury Z, Huh SU, Ma Y, Segonzac C, Sklenar J et al (2015) A plant immune receptor detects pathogen effectors that target WRKY transcription factors. Cell 161:1089–1100

    Article  CAS  PubMed  Google Scholar 

  • Saunders DG, Breen S, Win J et al (2012) Host protein BSL1 associates with Phytophthora infestans RXLR effector AVR2 and the Solanum demissum immune receptor R2 to mediate disease resistance. Plant Cell 24:3420–3434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shirasu K (2009) The HSP90–SGT1 chaperone complex for NLR immune sensors. Annu Rev Plant Biol 60:139–164

    Article  CAS  PubMed  Google Scholar 

  • Shivaprasad PV, Chen HM, Patel K, Bond DM, Santos BACM, Baulcombe BDC (2012) A microRNA superfamily regulates nucleotide binding site-leucine-rich repeats and other mRNAs. Plant Cell 24:859–887

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simanshu DK, Zhai X, Munch D, Hofius D, Markham JE, Bielawski J, Bielawska A, Malinina L, Molotkovsky JG, Mundy JW et al (2014) Arabidopsis accelerated cell death 11, ACD11, is a ceramide-1-phosphate transfer protein and intermediary regulator of phytoceramide levels. Cell Rep 6:388–399

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sohn KH, Segonzac C, Rallapalli G, Sarris PF, Woo JY, Williams SJ et al (2014) The nuclear immune receptor RPS4 is required for RRS1 SLH1- dependent constitutive defense activation in Arabidopsis thaliana. PLoS Genet 10:e1004655

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stegmann M, Anderson RG, Westphal L, Rosahl S, McDowell JM, 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stella S, Montoya G (2016) The genome editing revolution: a CRISPR-Cas TALE off-target story. BioEssays 38:4–13

    Article  CAS  Google Scholar 

  • Takemoto D, Jones DA (2005) Membrane release and destabilization of Arabidopsis RIN4 following cleavage by Pseudomonas syringae AvrRpt2. Mol Plant Microbe Interact 18:1258–1268

    Article  CAS  PubMed  Google Scholar 

  • Tateda C, Zhang Z, Greenberg JT (2015) Linking pattern recognition and salicylic acid responses in Arabidopsis through ACCELERATED CELL DEATH6 and receptors. Plant Signal Behav 10:e1010912

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • The OK, Hofius D (2014) Membrane trafficking and autophagyin pathogen-triggered cell death and immunity. J Exp Bot 65:1297–1312

    Article  CAS  Google Scholar 

  • Thompson AR, Doelling JH, Suttangkakul A, Vierstra RD (2005) Autophagic nutrient recycling in Arabidopsis directed by the ATG8 and ATG12 conjugation pathways. Plant Physiol 138:2097–2110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tran DTN, Chung E-H, Habring-Muller A, Demar M, Schwab R, Dangl JL, Weigel D, Chae E (2017) Activation of a plant NLR complex through heteromeric association with an autoimmune risk variant of another NLR. Curr Biol 27:1148–1160

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Undan JR, Tamiru M, Abe A, Yoshida K, Kosugi S, Takagi H et al (2012) Mutation in OsLMS, a gene encoding a protein with two double-stranded RNA binding motifs, causes lesion mimic phenotype and early senescence in rice (Oryza sativa L.). Genes Genet Syst 87:169–179

    Article  CAS  PubMed  Google Scholar 

  • van der Biezen EA, Jones JD (1998) The NB-ARC domain: a novel signalling motif shared by plant resistance gene products and regulators of cell death in animals. Curr Biol 8:226–228

    Article  Google Scholar 

  • van Ooijen G, Mayr G, Kasiem MM et al (2008) Structure–function analysis of the NB-ARC domain of plant disease resistance proteins. J Exp Bot 59:1383–1397

    Article  PubMed  CAS  Google Scholar 

  • van Wersch R, Li X, Zhang Y (2016) Mighty Dwarfs: Arabidopsis autoimmune mutants and their usages in genetic dissection of plant immunity. Front Plant Sci 7:1717

    PubMed  PubMed Central  Google Scholar 

  • Vanderschuren H, Stupak M, Futterer J, Gruissem W, Zhang P (2007) Engineering resistance to geminiviruses—review and perspectives. Plant Biotechnol J 5:207–220

    Article  CAS  PubMed  Google Scholar 

  • Wan J, Zhang XC, Neece D, Ramonell KM, Clough S, Kim SY et al (2008) A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell 20:471–481

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu F, Zhu C, Cevik V, Johnson K, Liu Y, Sohn K, Jones JD, Holub EB, Li X (2015) Autoimmunity conferred by chs3-2D relies on CSA1, its adjacent TNL-encoding neighbour. Sci Rep 5(5):8792

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang S, Hua JA (2004) Haplotype-specific Resistance gene regulated by BONZAI1 mediates temperature-dependent growth control in Arabidopsis. Plant Cell 16:1060–1071

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang H, Shi Y, Liu J et al (2010) A mutant CHS3 protein with TIRNB-LRR-LIM domains modulates growth, cell death and freezing tolerance in a temperature-dependent manner in Arabidopsis. Plant J 63:283–296

    Article  CAS  PubMed  Google Scholar 

  • Yoshioka K, Kachroo P, Tsui F, Sharma SB, Shah J, Klessig DF (2001) Environmentally sensitive, SA-dependent defense responses in the cpr22 mutant of Arabidopsis. Plant J 26:447–459

    Article  CAS  PubMed  Google Scholar 

  • Zhai C, Zhang Y, Yao N, Lin F, Liu Z, Dong Z et al (2014) Function and interaction of the coupled genes responsible for Pik-h encoded rice blast resistance. PLoS One 9(6):e98067

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang Y, Goritschnig S, Dong X, Li X (2003) (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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang ZG, Lenk A, Andersson MX, Gjetting T, Pedersen C, Nielsen ME et al (2008) A lesion-mimics syntaxin double mutant in Arabidopsis reveals novel complexity of pathogen defense signaling. Mol Plant 1:510–527

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Yang Y, Fang B, Gannon P, Ding P, Li X (2010) Arabidopsis snc2-1D activates receptor-like protein-mediated immunity transduced through WRKY70. Plant Cell 22:3153–3163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Z, Wu Y, Gao M, Zhang J, Kong Q, Liu Y, Ba H, Zhou J, Zhang Y (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

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Du L, Shen C, Yang Y, Poovaiah BW (2014) Regulation of plant immunity through ubiquitin-mediated modulation of Ca (2+)-calmodulin-AtSR1/CAMTA3 signaling. Plant J 78:269–281

    Article  CAS  PubMed  Google Scholar 

  • Zhang T, Chen S, Harmon AC (2016) Protein–protein interactions in plant mitogen-activated protein kinase cascades. J Exp Bot 67(3):607–618

    Article  CAS  PubMed  Google Scholar 

  • Zhao BY, Ardales E, Brasset E et al (2004a) The Rxo1/Rba1 locus of maize controls resistance reactions to pathogenic and nonhost bacteria. Theor Appl Genet 109:71–79

    Article  CAS  PubMed  Google Scholar 

  • Zhao BY, Ardales EY, Raymundo A et al (2004b) The avrRxo1 gene from the rice pathogen Xanthomonas oryzae pv. oryzicola confers a nonhost defense reaction on maize with resistance gene Rxo1. Mol Plant Microbe Interact 17:771–779

    Article  CAS  PubMed  Google Scholar 

  • Zhao B, Lin X, Poland J et al (2005) A maize resistance gene functions against bacterial streak disease in rice. Proc Natl Acad Sci USA 102:15383–15388

    Article  CAS  PubMed  Google Scholar 

  • Zhao T, Rui L, Li J, Nishimura MT, Vogel JP, 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zheng Q, Zhao Y (2007) The diverse biofunctions of LIM domain proteins: determined by subcellular localization and protein–protein interaction. Bio Cell 99:489–502

    Article  CAS  Google Scholar 

  • Zhou F, Menke FL, Yoshioka K, Moder W, Shirano Y, Klessig DF (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

    Article  CAS  PubMed  Google Scholar 

  • Zhou F, Mosher S, Tian M, Sassi G, Parker J, Klessig DF (2008) The Arabidopsis gain-of-function mutant ssi4 requires RAR1 and SGT1b differentially for defense activation and morphological alterations. Mol Plant Microbe Interact 21:40–49

    Article  CAS  PubMed  Google Scholar 

  • Zhu Z, Xu F, Zhang Y, Cheng YT, Wiermer M, Li X, Zhang Y (2010) Arabidopsis resistance protein SNC1 activates immune responses through association with a transcriptional corepressor. Proc Natl Acad Sci USA 107:13960–13965

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors are thankful to Bose institute for infrastructural supports. SD acknowledges Indian National Science Academy for funding through Senior Scientist scheme. The authors are thankful to professor Kalipada Das for critical reading of the manuscript.

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Chakraborty, J., Ghosh, P. & Das, S. Autoimmunity in plants. Planta 248, 751–767 (2018). https://doi.org/10.1007/s00425-018-2956-0

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