Abstract
Antiviral RNA silencing and the resistance gene-conferred defense response are major antiviral immune systems in plants. Several of the components involved have been genetically or biochemically identified in Arabidopsis thaliana. One powerful tool to dissect antiviral immune systems involves a reverse genetic approach that analyzes Arabidopsis mutant lines with impaired antiviral defense responses. In particular, to better understand the signaling networks involved in the resistance gene-conferred antiviral response in host plants, establishment of mutant lines carrying the homozygous mutant allele and antiviral resistance gene is required. The information on well-characterized defense-related signaling mutant alleles and the PCR-based genotyping method provided in this chapter allows the efficient selection of Arabidopsis mutant lines that can be used to study antiviral resistance signaling networks and resistance mechanisms.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Voinnet O (2005) Induction and suppression of RNA silencing: insights from viral infections. Nat Rev Genet 6:206–220
Csorba T, Kontra L, Burgyán J (2015) Viral silencing suppressors: tools forged to fine-tune host-pathogen coexistence. Virology 479-480:85–103
de Ronde D, Butterbach P, Kormelink R (2014) Dominant resistance against plant viruses. Front Plant Sci 5:1–17
Hashimoto M, Neriya Y, Yamaji Y et al (2016) Recessive resistance to plant viruses: potential resistance genes beyond translation initiation factors. Front Microbiol 7:1695
Peláez P, Sanchez F (2013) Small RNAs in plant defense responses during viral and bacterial interactions: similarities and differences. Front Plant Sci 4:343
Cournoyer P, Dinesh-kumar SP (2011) NB-LRR immune receptors in plant virus defence. In: Caranta C, Aranda MA, Tepfer M, Lopez-Moya JJ (eds) Recent advances in plant virology, 1st edn. Caister Academic Press, Norfolk
Alonso JM, Stepanova AN, Leisse TJ et al (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301:653–657
Sessions A, Burke E, Presting G et al (2002) A high-throughput Arabidopsis reverse genetics system. Plant Cell 14:2985–2994
Rosso MG, Li Y, Strizhov N et al (2003) An Arabidopsis thaliana T-DNA mutagenized population (GABI-Kat) for flanking sequence tag-based reverse genetics. Plant Mol Biol 53:247–259
Kleinboelting N, Huep G, Kloetgen A et al (2012) GABI-Kat SimpleSearch: new features of the Arabidopsis thaliana T-DNA mutant database. Nucleic Acids Res 40:D1211–D1215
Woody ST, Austin-Phillips S, Amasino RM et al (2007) The WiscDsLox T-DNA collection: an arabidopsis community resource generated by using an improved high-throughput T-DNA sequencing pipeline. J Plant Res 120:157–165
Tissier AF, Marillonnet S, Klimyuk V et al (1999) Multiple independent defective suppressor-mutator transposon insertions in Arabidopsis: a tool for functional genomics. Plant Cell 11:1841–1852
Wisman E, Hartmann U, Sagasser M et al (1998) Knock-out mutants from an En-1 mutagenized Arabidopsis thaliana population generate phenylpropanoid biosynthesis phenotypes. Proc Natl Acad Sci U S A 95:12432–12437
Wang L, Tsuda K, Sato M et al (2009) Arabidopsis CaM binding protein CBP60g contributes to MAMP-induced SA accumulation and is involved in disease resistance against Pseudomonas syringae. PLoS Pathog 5:e1000301
Sun T, Zhang Y, Li Y et al (2015) ChIP-seq reveals broad roles of SARD1 and CBP60g in regulating plant immunity. Nat Commun 6:10159
Yang S, Hua J (2004) A haplotype-specific resistance gene regulated by BONZAI1 in Arabidopsis. Plant Cell 16:1060–1071
Chen QF, Xu L, Tan WJ et al (2015) Disruption of the Arabidopsis defense regulator genes SAG101, EDS1, and PAD4 confers enhanced freezing tolerance. Mol Plant 8:1536–1549
Glazebrook J, Rogers EE, Ausubel FM (1996) Isolation of Arabidopsis mutants with enhanced disease susceptibility by direct screening. Genetics 143:973–982
Reuber TL, Plotnikova JM, Dewdney J et al (1998) Correlation of defense gene induction defects with powdery mildew susceptibility in Arabidopsis enhanced disease susceptibility mutants. Plant J 16:473–485
Gou M, Su N, Zheng J et al (2009) An F-box gene, CPR30, functions as a negative regulator of the defense response in Arabidopsis. Plant J 60:757–770
Nawrath C, Métraux JP (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
Heck S, Grau T, Buchala A et al (2003) Genetic evidence that expression of NahG modifies defence pathways independent of salicylic acid biosynthesis in the Arabidopsis-Pseudomonas syringae pv. tomato interaction. Plant J 36:342–352
Century KS, Holubt EB, Staskawiczt BJ (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
Cao H, Bowling SA, Gordon AS et al (1994) Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6:1583–1592
Cao H, Glazebrook J, Clarke JD et al (1997) The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88:57–63
Nishimura MT, Stein M, Hou B-H et al (2003) Loss of callose synthase results in salicylic acid-dependent disease resistance. Science 301:969–972
Zhang Y, Cheng YT, Qu N et al (2006) Negative regulation of defense responses in Arabidopsis by two NPR1 paralogs. Plant J 48:647–656
Shi Z, Maximova S, Liu Y et al (2013) The salicylic acid receptor NPR3 is a negative regulator of the transcriptional defense response during early flower development in Arabidopsis. Mol Plant 6:802–816
Liu G, Holub EB, Alonso JM et al (2005) An Arabidopsis NPR1-like gene, NPR4, is required for disease resistance. Plant J 41:304–318
Jirage D, Tootle TL, Reuber TL 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
Hiruma K, Nishiuchi T, Kato T et al (2011) Arabidopsis ENHANCED DISEASE RESISTANCE 1 is required for pathogen-induced expression of plant defensins in nonhost resistance, and acts through interference of MYC2-mediated repressor function. Plant J 67:980–992
Huang J, Gu M, Lai Z et al (2010) Functional analysis of the Arabidopsis PAL gene family in plant growth, development, and response to environmental stress. Plant Physiol 153:1526–1538
Feys BJ, Wiermer M, Bhat RA 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
Langenbach C, Campe R, Schaffrath U et al (2013) UDP-glucosyltransferase UGT84A2/BRT1 is required for Arabidopsis nonhost resistance to the Asian soybean rust pathogen Phakopsora pachyrhizi. New Phytol 198:536–545
Zhang Y, Xu S, Ding P et al (2010) Control of salicylic acid synthesis and systemic acquired resistance by two members of a plant-specific family of transcription factors. Proc Natl Acad Sci U S A 107:18220–18225
Stein M, Dittgen J, Sánchez-Rodríguez C et al (2006) Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration. Plant Cell 18:731–746
Dewdney J, Reuber TL, Wildermuth MC et al (2000) Three unique mutants of Arabidopsis identify eds loci required for limiting growth of a biotrophic fungal pathogen. Plant J 24:205–218
Tsuda K, Sato M, Stoddard T et al (2009) Network properties of robust immunity in plants. PLoS Genet 5:e1000772
Gross J, Won KC, Lezhneva L et al (2006) A plant locus essential for phylloquinone (vitamin K1) biosynthesis originated from a fusion of four eubacterial genes. J Biol Chem 281:17189–17196
Miura K, Rus A, Sharkhuu A et al (2005) The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses. Proc Natl Acad Sci U S A 102:7760–7765
Lee J, Nam J, Park HC et al (2007) Salicylic acid-mediated innate immunity in Arabidopsis is regulated by SIZ1 SUMO E3 ligase. Plant J 49:79–90
Song JT, Lu H, McDowell JM et al (2004) A key role for ALD1 in activation of local and systemic defenses in Arabidopsis. Plant J 40:200–212
Xu E, Brosché M (2014) Salicylic acid signaling inhibits apoplastic reactive oxygen species signaling. BMC Plant Biol 14:155
Carella P, Kempthorne CJ, Wilson DC et al (2017) Exploring the role of DIR1, DIR1-like and other lipid transfer proteins during systemic immunity in Arabidopsis. Physiol Mol Plant Pathol 97:49–57
Bartsch M, Gobbato E, Bednarek P et al (2006) Salicylic acid-independent ENHANCED DISEASE SUSCEPTIBILITY1 signaling in Arabidopsis immunity and cell death is regulated by the monooxygenase FMO1 and the Nudix hydrolase NUDT7. Plant Cell 18:1038–1051
Kieber JJ, Rothenberg M, Roman G et al (1993) CTR1, a negative regulator of the ethylene pathway in Arabidopsis, encodes a member of the Raf family of protein kinases. Cell 72:427–441
Roman G, Lubarsky B, Kieber JJ et al (1995) Genetic analysis of ethylene signal transduction in Arabidopsis thaliana: five novel mutant loci integrated into a stress response pathway. Genetics 139:1393–1409
An F, Zhao Q, Ji Y et al (2010) Ethylene-induced stabilization of ETHYLENE INSENSITIVE3 and EIN3-LIKE1 is mediated by proteasomal degradation of EIN3 binding F-Box 1 and 2 that requires EIN2 in Arabidopsis. Plant Cell 22:2384–2401
Guo H, Ecker JR (2003) Plant responses to ethylene gas are mediated by SCFEBF1/EBF2- dependent proteolysis of EIN3 transcription factor. Cell 115:667–677
Alonso JM, Stepanova AN, Solano R et al (2003) Five components of the ethylene-response pathway identified in a screen for weak ethylene-insensitive mutants in Arabidopsis. Proc Natl Acad Sci U S A 100:2992–2997
Chang C, Kwok S, Bleecker A et al (1993) Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. Science 262:539–544
Hua J, Meyerowitz EM (1998) Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell 94:261–271
Kachroo P, Yoshioka K, Shah J et al (2000) Resistance to turnip crinkle virus in Arabidopsis is regulated by two host genes and is salicylic acid dependent but NPR1, ethylene, and jasmonate independent. Plant Cell 12:677–690
Guzmán P, Ecker JR (1990) Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2:513–523
Resnick JS, Wen C-K, Shockey JA et al (2006) REVERSION-TO-ETHYLENE SENSITIVITY1, a conserved gene that regulates ethylene receptor function in Arabidopsis. Proc Natl Acad Sci U S A 103:7917–7922
Alonso JM, Hirayama T, Roman G et al (1999) EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science 284:2148–2152
Chao Q, Rothenberg M, Solano R et al (1997) Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSITIVE3 and related proteins. Cell 89:1133–1144
Chen H, Xue L, Chintamanani S et al (2009) ETHYLENE INSENSITIVE3 and ETHYLENE INSENSITIVE3-LIKE1 repress SALICYLIC ACID INDUCTION DEFICIENT2 expression to negatively regulate plant innate immunity in Arabidopsis. Plant Cell 21:2527–2540
Potuschak T, Vansiri A, Binder BM et al (2006) The exoribonuclease XRN4 is a component of the ethylene response pathway in Arabidopsis. Plant Cell 18:3047–3057
Von Malek B, Van Der Graaff E, Schneitz K et al (2002) The Arabidopsis male-sterile mutant dde2-2 is defective in the ALLENE OXIDE SYNTHASE gene encoding one of the key enzymes of the jasmonic acid biosynthesis pathway. Planta 216:187–192
Xie D-X, Feys BF, James S et al (1998) COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280:1091–1094
Trusov Y, Sewelam N, Rookes JE et al (2009) Heterotrimeric G proteins-mediated resistance to necrotrophic pathogens includes mechanisms independent of salicylic acid-, jasmonic acid/ethylene- and abscisic acid-mediated defense signaling. Plant J 58:69–81
Staswick PE, Su W, Howell SH (1992) Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant. Proc Natl Acad Sci U S A 89:6837–6840
Reichheld J-P, Meyer E, Khafif M et al (2005) AtNTRB is the major mitochondrial thioredoxin reductase in Arabidopsis thaliana. FEBS Lett 579:337–342
Sweat TA, Wolpert TJ (2007) Thioredoxin h5 is required for victorin sensitivity mediated by a CC-NBS-LRR gene in Arabidopsis. Plant Cell 19:673–687
Torres MA, Dangl JL, Jones JDG (2002) Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc Natl Acad Sci U S A 99:517–522
Frye CA, Innes RW (1998) An Arabidopsis mutant with enhanced resistance to powdery mildew. Plant Cell 10:947–956
Nakagami H, Soukupová H, Schikora A et al (2006) A mitogen-activated protein kinase kinase kinase mediates reactive oxygen species homeostasis in Arabidopsis. J Biol Chem 281:38697–38704
Su S-H, Bush SM, Zaman N et al (2013) Deletion of a tandem gene gamily in Arabidopsis: increased MEKK2 abundance triggers autoimmunity when the MEKK1-MKK1/2-MPK4 signaling cascade is disrupted. Plant Cell 25:1895–1910
Bush SM, Krysan PJ (2010) iTILLING: a personalized approach to the identification of induced mutations in Arabidopsis. Plant Physiol 154:25–35
Gao M, Liu J, Bi D et al (2008) MEKK1, MKK1/MKK2 and MPK4 function together in a mitogen-activated protein kinase cascade to regulate innate immunity in plants. Cell Res 18:1190–1198
Yoo S-D, Cho Y-H, Tena G et al (2008) Dual control of nuclear EIN3 by bifurcate MAPK cascades in C2H4 signalling. Nature 451:789–795
Dóczi R, Brader G, Pettkó-Szandtner A et al (2007) The Arabidopsis mitogen-activated protein kinase kinase MKK3 is upstream of group C mitogen-activated protein kinases and participates in pathogen signaling. Plant Cell 19:3266–3279
Wang H, Ngwenyama N, Liu Y et al (2007) Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell 19:63–73
Bush SM, Krysan PJ (2007) Mutational evidence that the Arabidopsis MAP kinase MPK6 is involved in anther, inflorescence, and embryo development. J Exp Bot 58:2181–2191
Liu Y, Zhang S (2004) Phosphorylation of 1-aminocyclopropane-1-carboxylic acid synthase by MPK6, a stress-responsive mitogen-activated protein kinase, induces ethylene biosynthesis in Arabidopsis. Plant Cell 16:3386–3399
Barajas-López Jde D, Kremnev D, Shaikhali J et al (2013) PAPP5 is involved in the tetrapyrrole mediated plastid signalling during chloroplast development. PLoS One 8:e60305
Pruzinská A, Tanner G, Aubry S et al (2005) Chlorophyll breakdown in senescent Arabidopsis leaves. Characterization of chlorophyll catabolites and of chlorophyll catabolic enzymes involved in the degreening reaction. Plant Physiol 139:52–63
Greenberg JT, Guo A, Klessig DF et al (1994) Programmed cell death in plants: a pathogen-triggered response activated coordinately with multiple defense functions. Cell 77:551–563
Mène-Saffrané L, Dubugnon L, Chételat A et al (2009) Nonenzymatic oxidation of trienoic fatty acids contributes to reactive oxygen species management in Arabidopsis. J Biol Chem 284:1702–1708
Kaminaka H, Näke C, Epple P et al (2006) bZIP10-LSD1 antagonism modulates basal defense and cell death in Arabidopsis following infection. EMBO J 25:4400–4411
Coll NS, Vercammen D, Smidler A et al (2010) Arabidopsis type I metacaspases control cell death. Science 330:1393–1397
Yu I-C, Parker J, Bent AF (1998) Gene-for-gene disease resistance without the hypersensitive response in Arabidopsis dnd1 mutant. Proc Natl Acad Sci U S A 95:7819–7824
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 U S A 97:9323–9328
Genger RK, Jurkowski GI, McDowell JM et al (2008) Signaling pathways that regulate the enhanced disease resistance of Arabidopsis “defense, no death” mutants. Mol Plant-Microbe Interact 21:1285–1296
Yu I, Fengler KA, Clough SJ et al (2000) Identification of Arabidopsis mutants exhibiting an altered hypersensitive response in gene-for-gene disease resistance. Mol Plant-Microbe Interact 13:277–286
Jurkowski GI, Smith RK, Yu I et al (2004) Arabidopsis DND2, a second cyclic nucleotide-gated ion channel gene for which mutation causes the “defense, no death” phenotype. Mol Plant-Microbe Interact 17:511–520
Collins NC, Thordal-Christensen H, Lipka V et al (2003) SNARE-protein-mediated disease resistance at the plant cell wall. Nature 425:973–977
Johansson ON, Fantozzi E, Fahlberg P et al (2014) Role of the penetration-resistance genes PEN1, PEN2 and PEN3 in the hypersensitive response and race-specific resistance in Arabidopsis thaliana. Plant J 79:466–476
Lipka V, Dittgen J, Bednarek P et al (2005) Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 310:1180–1183
Kobae Y, Sekino T, Yoshioka H et al (2006) Loss of AtPDR8, a plasma membrane ABC transporter of Arabidopsis thaliana, causes hypersensitive cell death upon pathogen infection. Plant Cell Physiol 47:309–318
Cheng YT, Li Y, Huang S 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 U S A 108:14694–14699
Dong OX, Tong M, Bonardi V et al (2016) TNL-mediated immunity in Arabidopsis requires complex regulation of the redundant ADR1 gene family. New Phytol 210:960–973
Takahashi A, Casais C, Ichimura K et al (2003) HSP90 interacts with RAR1 and SGT1 and is essential for RPS2-mediated disease resistance in Arabidopsis. Proc Natl Acad Sci U S A 100:11777–11782
Hubert DA, Tornero P, Belkhadir Y et al (2003) Cytosolic HSP90 associates with and modulates the Arabidopsis RPM1 disease resistance protein. EMBO J 22:5679–5689
Hubert DA, He Y, McNulty BC et al (2009) Specific Arabidopsis HSP90.2 alleles recapitulate RAR1 cochaperone function in plant NB-LRR disease resistance protein regulation. Proc Natl Acad Sci 106:9556–9563
Palma K, Zhang Y, Li X (2005) An importin α homolog, MOS6, plays an important role in plant innate immunity. Curr Biol 15:1129–1135
Gu Y, Zebell SG, Liang Z et al (2016) Nuclear pore permeabilization is a convergent signaling event in effector-triggered immunity. Cell 166:1–13
Cheng YT, Germain H, Wiermer M et al (2009) Nuclear pore complex component MOS7/Nup88 is required for innate immunity and nuclear accumulation of defense regulators in Arabidopsis. Plant Cell 21:2503–2516
Zhang Y, Li X (2005) A putative nucleoporin 96 is required for both basal defense and constitutive resistance responses mediated by suppressor of npr1-1, constitutive 1. Plant Cell 17:1306–1316
Tornero P, Merritt P, Sadanandom A et al (2002) RAR1 and NDR1 contribute quantitatively to disease resistance in Arabidopsis, and their relative contributions are dependent on the R gene assayed. Plant Cell 14:1005–1015
Gloggnitzer J, Akimcheva S, Srinivasan A et al (2014) Nonsense-mediated mRNA decay modulates immune receptor levels to regulate plant antibacterial defense. Cell Host Microbe 16:376–390
Li Y, Li S, Bi D et al (2010) SRFR1 negatively regulates plant NB-LRR resistance protein accumulation to prevent autoimmunity. PLoS Pathog 6:e1001111
Gray WM, Muskett PR, Chuang H-W et al (2003) Arabidopsis SGT1b is required for SCF TIR1-mediated auxin response. Plant Cell 15:1310–1319
Kim SH, Gao F, Bhattacharjee S et al (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
Bohmert K, Camus I, Bellini C et al (1998) AGO1 defines a novel locus of Arabidopsis controlling leaf development. EMBO J 17:170–180
Arribas-Hernández L, Marchais A, Poulsen C et al (2016) The slicer activity of ARGONAUTE1 is required specifically for the phasing, not production, of trans-acting short interfering RNAs in Arabidopsis. Plant Cell 28:1563–1580
Morel J, Godon C, Mourrain P et al (2002) Fertile hypomorphic ARGONAUTE (ago1) mutants impaired in post-transcriptional gene silencing and virus resistance. Plant Cell 14:629–639
Mason GA, Vergara TL, Queitsch C (2016) The mechanistic underpinnings of an ago1-mediated, environmentally-dependent, and stochastic phenotype. Plant Physiol 170:2420–2431
Baumberger N, Baulcombe DC (2005) Arabidopsis ARGONAUTE1 is an RNA slicer that selectively recruits microRNAs and short interfering RNAs. Proc Natl Acad Sci U S A 102:11928–11933
Lam P, Zhao L, Eveleigh N et al (2015) The exosome and trans-acting small interfering RNAs regulate cuticular wax biosynthesis during Arabidopsis inflorescence stem development. Plant Physiol 167:323–336
Lobbes D, Rallapalli G, Schmidt DD et al (2006) SERRATE: a new player on the plant microRNA scene. EMBO Rep 7:1052–1058
Takeda A, Iwasaki S, Watanabe T et al (2008) The mechanism selecting the guide strand from small RNA duplexes is different among Argonaute proteins. Plant Cell Physiol 49:493–500
Oliver C, Santos JL, Pradillo M (2014) On the role of some ARGONAUTE proteins in meiosis and DNA repair in Arabidopsis thaliana. Front Plant Sci 5:1–10
Mi S, Cai T, Hu Y et al (2008) Sorting of small RNAs into Arabidopsis Argonaute complexes is directed by the 5´ terminal nucleotide. Cell 133:116–127
Wei W, Ba Z, Gao M et al (2012) A role for small RNAs in DNA double-strand break repair. Cell 149:101–112
Agorio A, Vera P (2007) ARGONAUTE4 is required for resistance to Pseudomonas syringae in Arabidopsis. Plant Cell 19:3778–3790
Strickler SR, Tantikanjana T, Nasrallah JB (2013) Regulation of the S-locus receptor kinase and self-incompatibility in Arabidopsis thaliana. Genes Genomes Genet 3:315–322
Hernández-Lagana E, Rodríguez-Leal D, Lúa J et al (2016) A multigenic network of ARGONAUTE4 clade members controls early megaspore formation in Arabidopsis. Genetics 204:1045–1056
Katiyar-Agarwal S, Gao S, Vivian-Smith A et al (2007) A novel class of bacteria-induced small RNAs in Arabidopsis. Genes Dev 21:3123–3134
Harvey JJW, Lewsey MG, Patel K et al (2011) An antiviral defense role of AGO2 in plants. PLoS One 6:e14639
Havecker ER, Wallbridge LM, Fedito P et al (2012) Metastable differentially methylated regions within Arabidopsis inbred populations are associated with modified expression of non-coding transcripts. PLoS One 7:e45242
Tucker MR, Okada T, Hu Y et al (2012) Somatic small RNA pathways promote the mitotic events of megagametogenesis during female reproductive development in Arabidopsis. Development 139:1399–1404
Zheng X, Zhu J, Kapoor A et al (2007) Role of Arabidopsis AGO6 in siRNA accumulation, DNA methylation and transcriptional gene silencing. EMBO J 26:1691–1701
Smith LM, Pontes O, Searle I et al (2007) An SNF2 protein associated with nuclear RNA silencing and the spread of a silencing signal between cells in Arabidopsis. Plant Cell 19:1507–1521
Hunter C, Sun H, Poethig RS et al (2003) The Arabidopsis heterochronic gene ZIPPY is an ARGONAUTE family member. Curr Biol 13:1734–1739
Peragine A, Yoshikawa M, Wu G et al (2004) SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNAs in Arabidopsis. Genes Dev 18:2368–2379
Vazquez F, Vaucheret H, Rajagopalan R et al (2004) Endogenous trans-acting siRNAs regulate the accumulation of Arabidopsis mRNAs. Mol Cell 16:69–79
Olmedo-Monfil V, Durán-Figueroa N, Arteaga-Vázquez M et al (2010) Control of female gamete formation by a small RNA pathway in Arabidopsis. Nature 464:628–632
Arribas-Hernández L, Kielpinski LJ, Brodersen P (2016) mRNA decay of most Arabidopsis miRNA targets requires slicer activity of AGO1. Plant Physiol 171:2620–2632
Elmayan T, Proux F, Vaucheret H (2005) Arabidopsis RPA2: a genetic link among transcriptional gene silencing, DNA repair, and DNA replication. Curr Biol 15:1919–1925
Zhang X, Yazaki J, Sundaresan A et al (2006) Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126:1189–1201
Xue W, Ruprecht C, Street N et al (2012) Paramutation-like interaction of T-DNA loci in Arabidopsis. PLoS One 7:e51651
Moissiard G, Bischof S, Husmann D et al (2014) Transcriptional gene silencing by Arabidopsis microrchidia homologues involves the formation of heteromers. Proc Natl Acad Sci U S A 111:7474–7479
Jacobsen SE, Running MP, Meyerowitz EM (1999) Disruption of an RNA helicase/RNAse III gene in Arabidopsis causes unregulated cell division in floral meristems. Development 126:5231–5243
Ye R, Chen Z, Lian B et al (2016) A dicer-independent route for biogenesis of siRNAs that direct DNA methylation in Arabidopsis. Mol Cell 61:222–235
Xie Z, Johansen LK, Gustafson AM et al (2004) Genetic and functional diversification of small RNA pathways in plants. PLoS Biol 2:642–652
Mlotshwa S, Pruss GJ, Peragine A et al (2008) DICER-LIKE2 plays a primary role in transitive silencing of transgenes in Arabidopsis. PLoS One 3:e1755
Mlotshwa S, Pruss GJ, Gao Z et al (2010) Transcriptional silencing induced by Arabidopsis T-DNA mutants is associated with 35S promoter siRNAs and requires genes involved in siRNA-mediated chromatin silencing. Plant J 64:699–704
Yoshikawa M, Peragine A, Park MY et al (2005) A pathway for the biogenesis of trans-acting siRNAs in Arabidopsis. Genes Dev 19:2164–2175
Yamamuro C, Miki D, Zheng Z et al (2014) Overproduction of stomatal lineage cells in Arabidopsis mutants defective in active DNA demethylation. Nat Commun 5:4062
Schoft VK, Chumak N, Choi Y et al (2011) Function of the DEMETER DNA glycosylase in the Arabidopsis thaliana male gametophyte. Proc Natl Acad Sci U S A 108:8042–8047
Adenot X, Elmayan T, Lauressergues D et al (2006) DRB4-dependent TAS3 trans-acting siRNAs control leaf morphology through AGO7. Curr Biol 16:927–932
Chan SWL, Henderson IR, Zhang X et al (2006) RNAi, DRD1, and histone methylation actively target developmentally important non-CG DNA methylation in Arabidopsis. PLoS Genet 2:e83
Vazquez F, Gasciolli V, Crété P et al (2004) The nuclear dsRNA binding protein HYL1 is required for microRNA accumulation and plant development, but not posttranscriptional transgene silencing. Curr Biol 14:346–351
Zhong S-H, Liu J-Z, Jin H et al (2013) Warm temperatures induce transgenerational epigenetic release of RNA silencing by inhibiting siRNA biogenesis in Arabidopsis. Proc Natl Acad Sci U S A 110:9171–9176
Saze H, Mittelsten Scheid O, Paszkowski J (2003) Maintenance of CpG methylation is essential for epigenetic inheritance during plant gametogenesis. Nat Genet 34:65–69
Habu Y, Mathieu O, Tariq M et al (2006) Epigenetic regulation of transcription in intermediate heterochromatin. EMBO Rep 7:1279–1284
Kang HG, Oh CS, Sato M et al (2010) Endosome-associated CRT1 functions early in Resistance gene-mediated defense signaling in Arabidopsis and tobacco. Plant Cell 22:918–936
Herr AJ, Jensen MB, Dalmay T et al (2005) RNA polymerase IV directs silencing of endogenous DNA. Science 308:118–120
Vu TM, Nakamura M, Calarco JP et al (2013) RNA-directed DNA methylation regulates parental genomic imprinting at several loci in Arabidopsis. Development 140:2953–2960
Pontier D, Yahubyan G, Vega D et al (2005) Reinforcement of silencing at transposons and highly repeated sequences requires the concerted action of two distinct RNA polymerases IV in Arabidopsis. Genes Dev 19:2030–2040
Mourrain P, Béclin C, Elmayan T et al (2000) Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell 101:533–542
Penterman J, Zilberman D, Huh JH et al (2007) DNA demethylation in the Arabidopsis genome. Proc Natl Acad Sci U S A 104:6752–6757
Hernandez-Pinzon I, Yelina NE, Schwach F et al (2007) SDE5, the putative homologue of a human mRNA export factor, is required for transgene silencing and accumulation of trans-acting endogenous siRNA. Plant J 50:140–148
Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4326
Konieczny A, Ausubel FM (1993) A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCR-based markers. Plant J 4:403–410
Neff MM, Neff JD, Chory J et al (1998) dCAPS, a simple technique for the genetic analysis of single nucleotide polymorphisms: experimental applications in Arabidopsis thaliana genetics. Plant J 14:387–392
Takahashi H, Miller J, Nozaki Y et al (2002) RCY1, an Arabidopsis thaliana RPP8/HRT family resistance gene, conferring resistance to cucumber mosaic virus requires salicylic acid, ethylene and a novel signal transduction mechanism. Plant J 32:655–667
Takahashi H, Kanayama Y, Zheng MS et al (2004) Antagonistic interactions between the SA and JA signaling pathways in Arabidopsis modulate expression of defense genes and gene-for-gene resistance to cucumber mosaic virus. Plant Cell Physiol 45:803–809
Takahashi H, Kai A, Yamashita M et al (2012) Cyclic nucleotide-gated ion channel-mediated cell death may not be critical for R gene-conferred resistance to Cucumber mosaic virus in Arabidopsis thaliana. Physiol Mol Plant Pathol 79:40–48
Ando S, Obinata A, Takahashi H (2014) WRKY70 interacting with RCY1 disease resistance protein is required for resistance to Cucumber mosaic virus in Arabidopsis thaliana. Physiol Mol Plant Pathol 85:8–14
Sekine K, Kawakami S, Hase S et al (2008) High level expression of a virus resistance gene, RCY1, confers extreme resistance to Cucumber mosaic virus in Arabidopsis thaliana. Mol Plant-Microbe Interact 21:1398–1407
Koiwa H, Barb AW, Xiong L et al (2002) C-terminal domain phosphatase-like family members (AtCPLs) differentially regulate Arabidopsis thaliana abiotic stress signaling, growth, and development. Proc Natl Acad Sci U S A 99:10893–13898
Sekine K-T, Ishihara T, Hase S et al (2006) Single amino acid alterations in Arabidopsis thaliana RCY1 compromise resistance to Cucumber mosaic virus, but differentially suppress hypersensitive response-like cell death. Plant Mol Biol 62:669–682
Acknowledgments
This work was supported by grants for JSPS Research Fellows (15J01964), for “Scientific Research on Innovative Areas” from the Ministry of Education, Culture, Sports, Science and Technology (MEXT) of Japan (Grant numbers: 16H06429, 16K21723, and 16H06435), and by the Japan Society for the Promotion of Science (JSPS) through the JSPS Core-to-Core Program (Advanced Research Networks) entitled “Establishment of International Agricultural Immunology Research-Core for Quantum Improvement in Food Safety.”
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2019 Springer Science+Business Media, LLC, part of Springer Nature
About this protocol
Cite this protocol
Sato, Y., Takahashi, H. (2019). Reverse Genetic Analysis of Antiviral Resistance Signaling and the Resistance Mechanism in Arabidopsis thaliana. In: Kobayashi, K., Nishiguchi, M. (eds) Antiviral Resistance in Plants. Methods in Molecular Biology, vol 2028. Humana, New York, NY. https://doi.org/10.1007/978-1-4939-9635-3_3
Download citation
DOI: https://doi.org/10.1007/978-1-4939-9635-3_3
Published:
Publisher Name: Humana, New York, NY
Print ISBN: 978-1-4939-9634-6
Online ISBN: 978-1-4939-9635-3
eBook Packages: Springer Protocols