Write ‘systemic small RNAs’: read ‘systemic immunity’
Alireza SeifiWageningen UR Plant Breeding, Wageningen University and Research Center, PO Box 386, 6700 AJ Wageningen, The Netherlands. Email: arseifi@yahoo.com
Functional Plant Biology 38(10) 747-752 https://doi.org/10.1071/FP11100
Submitted: 24 April 2011 Accepted: 28 June 2011 Published: 16 September 2011
Abstract
About 50 years ago, it was reported that pathogen-infected plants are less susceptible to a broad spectrum of the subsequent pathogen attacks. This form of induced resistance, which resembles the immunisation in mammalian cells, is called systemic acquired resistance (SAR). In the last 10 years, plant molecular biology has been revolutionised by the discovery of RNA silencing, which is also a systemic phenomenon and also contributes to plant immunity. Here, I review these two systemic phenomena in a comparative way to highlight the possibility that systemic silencing contributes to systemic immunity. This potential contribution could be in the process of gene expression reprogramming, which is needed for SAR induction, and/or in SAR signal complex, and/or in establishing SAR in remote tissues and forming priming status.
Additional keywords: gene silencing, plant defense mechanisms, plant–microbe interactions, systemic acquired resistance (SAR), systemic silencing, mobile small RNAs.
References
Agorio A, Vera P (2007) ARGONAUTE4 is required for resistance to Pseudomonas syringae in Arabidopsis. The Plant Cell 19, 3778–3790.| ARGONAUTE4 is required for resistance to Pseudomonas syringae in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXns1eksg%3D%3D&md5=37c97a1cc062738ec7d8e365dca393aeCAS |
Attaran E, Zeier TE, Griebel T, Zeier J (2009) Methyl salicylate production and jasmonate signalling are not essential for systemic acquired resistance in Arabidopsis. The Plant Cell 21, 954–971.
| Methyl salicylate production and jasmonate signalling are not essential for systemic acquired resistance in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlsFylurY%3D&md5=940e21d0cd251adac904efc840ac24eaCAS |
Baulcombe D (2004) RNA silencing in plants. Nature 431, 356–363.
| RNA silencing in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnsFaiu7c%3D&md5=ff3f13290c22d4bc2b47937ef5b8e9d4CAS |
Baulcombe DC (2007) Amplified silencing. Science 315, 199–200.
| Amplified silencing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnslWqsQ%3D%3D&md5=f1b5df42ea0ce9b162e161985b2cdab2CAS |
Butterbrodt T, Thurow C, Gatz C (2006) Chromatin immunoprecipitation analysis of the tobacco PR-1a and the truncated CaMV 35S promoter reveals differences in salicylic acid-dependent TGA factor binding and histone acetylation. Plant Molecular Biology 61, 665–674.
| Chromatin immunoprecipitation analysis of the tobacco PR-1a and the truncated CaMV 35S promoter reveals differences in salicylic acid-dependent TGA factor binding and histone acetylation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XnslShur8%3D&md5=da7c227eba8490cf7d888898a907cf05CAS |
Cameron RK, Dixon RA, Lamb CJ (1994) Biologically induced systemic acquired resistance in Arabidopsis thaliana. The Plant Journal 5, 715–725.
| Biologically induced systemic acquired resistance in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Champigny MJ, Cameron RK (2009) Action at a distance: long-distance signals in induced resistance. Advances in Botanical Research 51, 123–171.
| Action at a distance: long-distance signals in induced resistance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1Slsr%2FJ&md5=b44385341d31fd81ab6c5136ca7c51f7CAS |
Chapman EJ, Carrington JC (2007) Specialisation and evolution of endogenous small RNA pathways. Nature Reviews Genetics 8, 884–896.
| Specialisation and evolution of endogenous small RNA pathways.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFOksL7K&md5=716de4a9116b02be70d5580b848591a4CAS |
Chaturvedi R, Krothapalli K, Makandar R, Nandi A, Sparks AA, Roth MR, Welti R, Shah J (2008) Plastid 3 fatty acid desaturase dependent accumulation of a systemic acquired resistance inducing activity in petiole exudates of Arabidopsis thaliana is independent of jasmonic acid. The Plant Journal 54, 106–117.
| Plastid 3 fatty acid desaturase dependent accumulation of a systemic acquired resistance inducing activity in petiole exudates of Arabidopsis thaliana is independent of jasmonic acid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXltlertbs%3D&md5=729a622e36e50c9ac9d7ede3fd3c6ba9CAS |
Chellappan P, Xia J, Zhou X, Gao S, Zhang X, Coutino G, Vazquez F, Zhang W, Jin H (2010) siRNAs from miRNA sites mediate DNA methylation of target genes. Nucleic Acids Research 38, 6883–6894.
| siRNAs from miRNA sites mediate DNA methylation of target genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVektr7E&md5=1b5d4da7dde79e237f3297a673be2f08CAS |
Chen HM, Chen LT, Patel K, Li YH, Baulcombe DC, Wu SH (2010) 22-nucleotide RNAs trigger secondary siRNA biogenesis in plants. Proceedings of the National Academy of Sciences of the United States of America 107, 15269–15274.
| 22-nucleotide RNAs trigger secondary siRNA biogenesis in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFSnsb7F&md5=fe663bcdb669e788a3424ce2485244c0CAS |
Chern M, Canlas PE, Fitzgerald HA, Ronald PC (2005) Rice NRR, a negative regulator of disease resistance, interacts with Arabidopsis NPR1 and rice NH1. The Plant Journal 43, 623–635.
| Rice NRR, a negative regulator of disease resistance, interacts with Arabidopsis NPR1 and rice NH1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpvFKrsL0%3D&md5=956669596e9fec071e8dcd63ac8e9a86CAS |
Conrath U (2006) Systemic acquired resistance. Plant Signaling & Behavior 1, 179–184.
| Systemic acquired resistance.Crossref | GoogleScholarGoogle Scholar |
Dean RA, Kuc J (1986) Induced systemic protection in cucumbers – the source of the signal. Physiological and Molecular Plant Pathology 28, 227–233.
| Induced systemic protection in cucumbers – the source of the signal.Crossref | GoogleScholarGoogle Scholar |
Despres C, Chubak C, Rochon A, Clark R, Bethune T, Desveaux D, Fobert PR (2003) The Arabidopsis NPR1 disease resistance protein is a novel cofactor that confers redox regulation of DNA binding activity to the basic domain/leucine zipper transcription factor TGA1. The Plant Cell 15, 2181–2191.
| The Arabidopsis NPR1 disease resistance protein is a novel cofactor that confers redox regulation of DNA binding activity to the basic domain/leucine zipper transcription factor TGA1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnsV2gurY%3D&md5=d5e6a633c98a9975a9d6186a8c7458a6CAS |
Dong XN (2001) Genetic dissection of systemic acquired resistance. Current Opinion in Plant Biology 4, 309–314.
| Genetic dissection of systemic acquired resistance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXksVyktL4%3D&md5=30a6850ab490b280bdad8e5812bcf62eCAS |
Dong XN (2004) NPR1, all things considered. Current Opinion in Plant Biology 7, 547–552.
| NPR1, all things considered.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXntV2msLs%3D&md5=cd2aa4f23b1476c84708275d1f02ee5cCAS |
Dunoyer P, Himber C, Voinnet O (2006) Induction, suppression and requirement of RNA silencing pathways in virulent Agrobacterium tumefaciens infections. Nature Genetics 38, 258–263.
| Induction, suppression and requirement of RNA silencing pathways in virulent Agrobacterium tumefaciens infections.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XotlGksg%3D%3D&md5=d7a4e91294838147afb8f3215cbd9427CAS |
Dunoyer P, Schott G, Himber C, Meyer D, Takeda A, Carrington JC, Voinnet O (2010) Small RNA duplexes function as mobile silencing signals between plant cells. Science 328, 912–916.
| Small RNA duplexes function as mobile silencing signals between plant cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlvVelt70%3D&md5=eb5117bfa3f3c5363df61e97412377f1CAS |
Durrant WE, Dong X (2004) Systemic acquired resistance. Annual Review of Phytopathology 42, 185–209.
| Systemic acquired resistance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXotFyrtbs%3D&md5=a1468719ff80fefbaeb5cd6078206321CAS |
Fire A, Xu SQ, Montgomery MK, Kostas SA, Driver SE, Mello CC (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391, 806–811.
| Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXhtlCju74%3D&md5=2b9a6c4eaae724372485f546bd1feb03CAS |
Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annual Review of Phytopathology 43, 205–227.
| Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVOksrrN&md5=24b1f4ae6d066cd8397bbb74846acb69CAS |
Grant M, Lamb C (2006) Systemic immunity. Current Opinion in Plant Biology 9, 414–420.
| Systemic immunity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xmt1ylsLY%3D&md5=575f556766e69893514505726b2582a2CAS |
Hamilton AJ, Baulcombe DC (1999) A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286, 950–952.
| A species of small antisense RNA in posttranscriptional gene silencing in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXntFaktbY%3D&md5=eb8ac79118b8e287f80d43358223ceddCAS |
Hammerschmidt R (2009) Systemic acquired resistance. Advances in Botanical Research 51, 173–222.
| Systemic acquired resistance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1Slsr%2FK&md5=03fd2e8ee0593a1307873a072bc5bb11CAS |
Jenns AE, Kuc J (1979) Graft transmission of systemic resistance of cucumber to anthrocnose induced by Colletotrichum lagenarium and tobacco necrosis virus. Phytopathology 69, 753–756.
| Graft transmission of systemic resistance of cucumber to anthrocnose induced by Colletotrichum lagenarium and tobacco necrosis virus.Crossref | GoogleScholarGoogle Scholar |
Jin H (2008) Endogenous small RNAs and antibacterial immunity in plants. FEBS Letters 582, 2679–2684.
| Endogenous small RNAs and antibacterial immunity in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpsVGhsr4%3D&md5=1c4fab3d364271721c5a76f0448b8566CAS |
Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAs and their regulatory roles in plants. Annual Review of Plant Biology 57, 19–53.
| MicroRNAs and their regulatory roles in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XosVKhsb0%3D&md5=27ad002a6b275d426a535d36439a0060CAS |
Jung HW, Tschaplinski TJ, Wang L, Glazebrook J, Greenberg JT (2009) Priming in systemic plant immunity. Science 324, 89–91.
| Priming in systemic plant immunity.Crossref | GoogleScholarGoogle Scholar |
Katiyar-Agarwal S, Jin H (2010) Role of small RNAs in host-microbe interactions. Annual Review of Phytopathology 48, 225–246.
| Role of small RNAs in host-microbe interactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1Wgt7%2FO&md5=e860554fc1e6f18c98a9fc206e60b79dCAS |
Katiyar-Agarwal S, Morgan R, Dahlbeck D, Borsani O, Villegas A, Zhu JK, Staskawicz BJ, Jin H (2006) A pathogen-inducible endogenous siRNA in plant immunity. Proceedings of the National Academy of Sciences of the United States of America 103, 18002–18007.
| A pathogen-inducible endogenous siRNA in plant immunity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1Kmsr%2FL&md5=0b1af952cca67da82cd19db0e0426ad2CAS |
Katiyar-Agarwal S, Gao S, Vivian-Smith A, Jin H (2007) A novel class of bacteria-induced small RNAs in Arabidopsis. Genes & Development 21, 3123–3134.
| A novel class of bacteria-induced small RNAs in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVaht7vL&md5=e60887158b704d810a02bdc919ab2914CAS |
Koornneef A, Rindermann K, Gatz C, Pieterse CMJ (2008) Histone modifications do not play a major role in salicylate-mediated suppression of jasmonate-induced PDF1.2 gene expression. Communicative & Integrative Biology 1, 143–145.
| Histone modifications do not play a major role in salicylate-mediated suppression of jasmonate-induced PDF1.2 gene expression.Crossref | GoogleScholarGoogle Scholar |
Lam E, Kato N, Lawton M (2001) Programmed cell death, mitochondria and the plant hypersensitive response. Nature 411, 848–853.
| Programmed cell death, mitochondria and the plant hypersensitive response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXksF2nsrg%3D&md5=e8c62ae762b81d4427b2d11d06a5debcCAS |
Maldonado AM, Doerner P, Dixon RA, Lamb CJ, Cameron RK (2002) A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature 419, 399–403.
| A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XntlGgsLk%3D&md5=149b17f5c97fe966bf4699235df93e82CAS |
Matzke M, Kanno T, Daxinger L, Huettel B, Matzke AJM (2009) RNA-mediated chromatin-based silencing in plants. Current Opinion in Cell Biology 21, 367–376.
| RNA-mediated chromatin-based silencing in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmvFGgu7c%3D&md5=9eef3be29079d70007af6dbe4791119dCAS |
Moazed D (2009) Small RNAs in transcriptional gene silencing and genome defence. Nature 457, 413–420.
| Small RNAs in transcriptional gene silencing and genome defence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXotlOgtg%3D%3D&md5=a499b7b4ec21f7ecc169bf670405e43eCAS |
Molnar A, Melnyk CW, Bassett A, Hardcastle TJ, Dunn R, Baulcombe DC (2010) Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science 328, 872–875.
| Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlvVelt7s%3D&md5=ec727de6c01873db0b67212811c021a7CAS |
Molnar A, Melnyk C, Baulcombe DC (2011) Silencing signals in plants: a long journey for small RNAs. Genome Biology 12, 215–222.
| Silencing signals in plants: a long journey for small RNAs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXivVymt70%3D&md5=30a0b0c614015282417303238251ebe5CAS |
Mosher RA, Durrant WE, Wang D, Song J, Dong X (2006) A comprehensive structure-function analysis of Arabidopsis SNI1 defines essential regions and transcriptional repressor activity. The Plant Cell 18, 1750–1765.
| A comprehensive structure-function analysis of Arabidopsis SNI1 defines essential regions and transcriptional repressor activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmvV2qtLs%3D&md5=f183e492d534d6afdeaa5ba3a9fffb37CAS |
Mou Z, Fan WH, Dong XN (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113, 935–944.
| Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlsVSjur8%3D&md5=264fe58419f78d3a412e81b41a3388faCAS |
Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones J (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signalling. Science 312, 436–439.
| A plant miRNA contributes to antibacterial resistance by repressing auxin signalling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjslSktbw%3D&md5=e08b2e87be980b5e450fd7c37a51a0abCAS |
Notaguchi M, Daimon Y, Abe M, Araki T (2009) Adaptation of a seedling micro-grafting technique to the study of long-distance signalling in flowering of Arabidopsis thaliana. Journal of Plant Research 122, 201–214.
| Adaptation of a seedling micro-grafting technique to the study of long-distance signalling in flowering of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXitFKmsLo%3D&md5=f4f543d72878bcb20b136dc22a82c907CAS |
Nowara D, Gay A, Lacomme C, Shaw J, Ridout C, Douchkov D, Hensel G, Kumlehn J, Schweizer P (2010) HIGS: host-induced gene silencing in the obligate biotrophic fungal pathogen Blumeria graminis. The Plant Cell 22, 3130–3141.
| HIGS: host-induced gene silencing in the obligate biotrophic fungal pathogen Blumeria graminis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVKjs7vL&md5=225254a3f1085ebb4614d6d1436c1ea7CAS |
Padmanabhan C, Zhang X, Jin H (2009) Host small RNAs are big contributors to plant innate immunity. Current Opinion in Plant Biology 12, 465–472.
| Host small RNAs are big contributors to plant innate immunity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpsFyqt70%3D&md5=64b89410463d150f8b882700e4fb662aCAS |
Park SW, Kaimoyo E, Kumar D, Mosher S, Klessig DF (2007) Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318, 113–116.
| Methyl salicylate is a critical mobile signal for plant systemic acquired resistance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFWitb%2FF&md5=56dc72b0f4f476f2935ecd102fbf0f54CAS |
Parker JE (2009) The quest for long-distance signals in plant systemic immunity. Science Signaling 2, pe31
| The quest for long-distance signals in plant systemic immunity.Crossref | GoogleScholarGoogle Scholar |
Pavet V, Quintero C, Cecchini NM, Rosa AL, Alvarez ME (2006) Arabidopsis displays centromeric DNA hypomethylation and cytological alterations of heterochromatin upon attack by Pseudomonas syringae. Molecular Plant-Microbe Interactions 19, 577–587.
| Arabidopsis displays centromeric DNA hypomethylation and cytological alterations of heterochromatin upon attack by Pseudomonas syringae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XltVyrt7s%3D&md5=3783c96c7afa2ba11f51cb28edd15796CAS |
Plasterk RHA (2002) RNA silencing: the genome’s immune system. Science 296, 1263–1265.
| RNA silencing: the genome’s immune system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xjsl2qt7w%3D&md5=5a66a0c76a834ff5497c3a6b081edb21CAS |
Rasmussen JB, Hammerschmidt R, Zook MN (1991) Systemic induction of salicylic acid accumulation in cucumber after inoculation with Pseudomonas syringae pv. syringae. Plant Physiology 97, 1342–1347.
| Systemic induction of salicylic acid accumulation in cucumber after inoculation with Pseudomonas syringae pv. syringae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XlsFOgsw%3D%3D&md5=2d9c0e6c7b49dbbf64c86bafeaf42183CAS |
Ross AF (1961) Systemic acquired resistance induced by localised virus infections in plants. Virology 14, 340–358.
| Systemic acquired resistance induced by localised virus infections in plants.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF3c%2Fmtlaktg%3D%3D&md5=e3b51b6e8ac8f71faa9dd2814c8efb60CAS |
Ruiz-Ferrer V, Voinnet O (2009) Roles of plant small RNAs in biotic stress responses. Annual Review of Plant Biology 60, 485–510.
| Roles of plant small RNAs in biotic stress responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXntFGlsLk%3D&md5=4499e14f2bb217e2083c0e0b53612078CAS |
Ryals JA, Neuenschwander UH, Willits MG, Molina A, Steiner HY, Hunt MD (1996) Systemic acquired resistance. The Plant Cell 8, 1809–1819.
Smith JA, Hammerschmidt R, Fulbright DW (1991) Rapid induction of systemic resistance in cucumber by Pseudomonas syringae pv. syringae. Physiological and Molecular Plant Pathology 38, 223–235.
| Rapid induction of systemic resistance in cucumber by Pseudomonas syringae pv. syringae.Crossref | GoogleScholarGoogle Scholar |
Sticher L, Mauch-Mani B, Métraux JP (1997) Systemic acquired resistance. Annual Review of Phytopathology 35, 235–270.
| Systemic acquired resistance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmtVGhsrg%3D&md5=9ab5cacc9e137c4376355eb91fca2579CAS |
Truman W, Bennett MH, Kubigsteltig I, Turnbull C, Grant M (2007) Arabidopsis systemic immunity uses conserved defense signalling pathways and is mediated by jasmonates. Proceedings of the National Academy of Sciences of the United States of America 104, 1075–1080.
| Arabidopsis systemic immunity uses conserved defense signalling pathways and is mediated by jasmonates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVShuro%3D&md5=6352b71186da30367a5646c60f55adfaCAS |
Turnbull CGN, Booker JP, Leyser HMO (2002) Micrografting techniques for testing long-distance signalling in Arabidopsis. The Plant Journal 32, 255–262.
| Micrografting techniques for testing long-distance signalling in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovFGqtrc%3D&md5=23aa5904746ac692d46bba115dd28f2aCAS |
van den Burg HA, Takken FLW (2009) Does chromatin remodeling mark systemic acquired resistance? Trends in Plant Science 14, 286–294.
| Does chromatin remodeling mark systemic acquired resistance?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXls1OqtLg%3D&md5=87e21224bb45d9d81556ee851290bf2eCAS |
Vernooij B, Friedrich L, Morse A, Reist R, Kolditz-Jawhar R, Ward E, Uknes S, Kessmann H, Ryals J (1994) Salicylic acid is not the translocated signal responsible for inducing systemic acquired resistance but is required in signal transduction. The Plant Cell 6, 959–965.
Voinnet O (2008) Post-transcriptional RNA silencing in plant-microbe interactions: a touch of robustness and versatility. Current Opinion in Plant Biology 11, 464–470.
| Post-transcriptional RNA silencing in plant-microbe interactions: a touch of robustness and versatility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpsVamurg%3D&md5=c066d8cb76108bfd83920d7c8de656c9CAS |
Voinnet O, Vain P, Angell S, Baulcombe DC (1998) Systemic spread of sequence-specific transgene RNA degradation in plants is initiated by localised introduction of ectopic promoterless DNA. Cell 95, 177–187.
| Systemic spread of sequence-specific transgene RNA degradation in plants is initiated by localised introduction of ectopic promoterless DNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXntVSmu7o%3D&md5=1cc33955d4f208213b55b22a58450b6cCAS |
Wang D, Weaver ND, Kesarwani M, Dong X (2005) Induction of protein secretory pathway is required for systemic acquired resistance. Science 308, 1036–1040.
| Induction of protein secretory pathway is required for systemic acquired resistance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjvF2qsL8%3D&md5=5816b0a25732499b6b2951214f809b6bCAS |
Wassenegger M (2005) The role of the RNAi machinery in heterochromatin formation. Cell 122, 13–16.
| The role of the RNAi machinery in heterochromatin formation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmsFeitb0%3D&md5=6d66ed847ba065880263ed3cf3ccc3bdCAS |
Yi H, Richards E (2007) A cluster of disease resistance genes in Arabidopsis is co-ordinately regulated by transcriptional activation and RNA silencing. The Plant Cell 19, 2929–2939.
| A cluster of disease resistance genes in Arabidopsis is co-ordinately regulated by transcriptional activation and RNA silencing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlWhsr%2FL&md5=0dad4bbedbd7c6f4d0d9d31fcf9caa97CAS |