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RNA silencing is required for Arabidopsis defence against Verticillium wilt disease.

Ellendorff U, Fradin EF, de Jonge R, Thomma BP - J. Exp. Bot. (2008)

Bottom Line: Recently, RNA silencing has been found to play a role in defence against bacterial plant pathogens in Arabidopsis through modulating host defence responses.Several components of RNA silencing pathways were tested, of which many were found to affect Verticillium defence.Since the observed differences in Verticillium susceptibility cannot be explained by notable differences in root architecture, it is speculated that the gene silencing mechanisms affect regulation of Verticillium-specific defence responses.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Phytopathology, Wageningen University, Binnenhaven 5, 6709 PD Wageningen, The Netherlands.

ABSTRACT
RNA silencing is a conserved mechanism in eukaryotes that plays an important role in various biological processes including regulation of gene expression. RNA silencing also plays a role in genome stability and protects plants against invading nucleic acids such as transgenes and viruses. Recently, RNA silencing has been found to play a role in defence against bacterial plant pathogens in Arabidopsis through modulating host defence responses. In this study, it is shown that gene silencing plays a role in plant defence against multicellular microbial pathogens; vascular fungi belonging to the Verticillium genus. Several components of RNA silencing pathways were tested, of which many were found to affect Verticillium defence. Remarkably, no altered defence towards other fungal pathogens that include Alternaria brassicicola, Botrytis cinerea, and Plectosphaerella cucumerina, but also the vascular pathogen Fusarium oxysporum, was recorded. Since the observed differences in Verticillium susceptibility cannot be explained by notable differences in root architecture, it is speculated that the gene silencing mechanisms affect regulation of Verticillium-specific defence responses.

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Typical symptoms caused by V. dahliae on various Arabidopsis silencing mutants. Arabidopsis gene-silencing mutants and the corresponding wild type Col-0 were inoculated with V. dahliae strain JR2, or mock-inoculated. (A) V. dahliae-inoculated ago7-2, dcl4-2, rdr6-11, rdr6-15, and sgs3-11 plants show enhanced symptom development, including more severe stunting, wilting, anthocyanin accumulation, and tissue necrosis, compared with inoculated Col-0 plants at 20 d post-inoculation. (B). V. dahliae-inoculated ago1-25, ago1-27, hen1-6, and hst-1 mutants develop fewer symptoms than inoculated Col-0 plants (A) at 25 d post-inoculation. (C) V. dahliae-inoculated dcl2-1, sde3-4, and sde3-5 mutants show similar disease symptoms as inoculated Col-0 plants (A) at 20 d post-inoculation.
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fig3: Typical symptoms caused by V. dahliae on various Arabidopsis silencing mutants. Arabidopsis gene-silencing mutants and the corresponding wild type Col-0 were inoculated with V. dahliae strain JR2, or mock-inoculated. (A) V. dahliae-inoculated ago7-2, dcl4-2, rdr6-11, rdr6-15, and sgs3-11 plants show enhanced symptom development, including more severe stunting, wilting, anthocyanin accumulation, and tissue necrosis, compared with inoculated Col-0 plants at 20 d post-inoculation. (B). V. dahliae-inoculated ago1-25, ago1-27, hen1-6, and hst-1 mutants develop fewer symptoms than inoculated Col-0 plants (A) at 25 d post-inoculation. (C) V. dahliae-inoculated dcl2-1, sde3-4, and sde3-5 mutants show similar disease symptoms as inoculated Col-0 plants (A) at 20 d post-inoculation.

Mentions: The enhanced susceptibility phenotype of the sgs mutants upon Verticillium inoculation directed us to assess susceptibility towards this pathogen in additional gene-silencing mutants. These comprised additional mutant alleles of SGS2 (also known as RDR6), namely rdr6-11 and rdr6-15, and for SGS3, namely sgs3-11. Furthermore, mutants of other components of RNA-silencing pathways were also included (Table 1). These included mutants of genes that encode different enzyme families, such as the argonautes AGO1 and AGO7, the dicers DCL2 and DCL4, the methyltransferase HEN1, the putative sRNA transporter HST, the DNA-dependent RNA polymerase NRPD1a, the RNA-dependent RNA polymerase RDR2, and the RNA helicase SDE3 that all have been implicated in different RNA-silencing pathways (Table 1; Voinnet, 2008). All mutants, derived from a Col-0 parental line, were challenged with V. dahliae strain JR2. As expected, additional mutant alleles of SGS2 and SGS3 (rdr6-11, rdr6-15, and sgs3-11) were more susceptible than Col-0 plants upon V. dahliae inoculation (Fig. 3A), thus confirming the enhanced susceptibility observed in the sgs2-1 and sgs3-1 mutants. The other PTGS mutants could be divided into three classes, based on the phenotypes after V. dahliae inoculation; those displaying enhanced susceptibility (Fig. 3A), mutants displaying enhanced resistance (Fig. 3B), and mutants displaying similar disease phenotypes as Verticillium-inoculated Col-0 plants (Fig. 3C). The mutants ago7-2, dcl4-2, nrpd1a-3, and rdr2-4 were found to be more susceptible to V. dahliae challenge by showing more severe stunting and necrosis when compared with inoculated Col-0 plants (Fig. 3A; see Supplementary Fig. S2 at JXB online). By contrast, the mutants ago1-25, ago1-27, hen1-6, and hst-1 were found to be more resistant because they displayed less necrosis and no anthocyanin production when compared with Col-0 plants upon V. dahliae inoculation (Fig. 3B; see Supplementary Fig. S2 at JXB online). Finally, the mutants dcl2-1, sde3-4, and sde3-5 showed a disease susceptibility phenotype that was similar to that of Col-0 with respect to severity of stunting, necrosis, and anthocyanin production (Fig. 3C; see Supplementary Fig. S2 at JXB online).


RNA silencing is required for Arabidopsis defence against Verticillium wilt disease.

Ellendorff U, Fradin EF, de Jonge R, Thomma BP - J. Exp. Bot. (2008)

Typical symptoms caused by V. dahliae on various Arabidopsis silencing mutants. Arabidopsis gene-silencing mutants and the corresponding wild type Col-0 were inoculated with V. dahliae strain JR2, or mock-inoculated. (A) V. dahliae-inoculated ago7-2, dcl4-2, rdr6-11, rdr6-15, and sgs3-11 plants show enhanced symptom development, including more severe stunting, wilting, anthocyanin accumulation, and tissue necrosis, compared with inoculated Col-0 plants at 20 d post-inoculation. (B). V. dahliae-inoculated ago1-25, ago1-27, hen1-6, and hst-1 mutants develop fewer symptoms than inoculated Col-0 plants (A) at 25 d post-inoculation. (C) V. dahliae-inoculated dcl2-1, sde3-4, and sde3-5 mutants show similar disease symptoms as inoculated Col-0 plants (A) at 20 d post-inoculation.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
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fig3: Typical symptoms caused by V. dahliae on various Arabidopsis silencing mutants. Arabidopsis gene-silencing mutants and the corresponding wild type Col-0 were inoculated with V. dahliae strain JR2, or mock-inoculated. (A) V. dahliae-inoculated ago7-2, dcl4-2, rdr6-11, rdr6-15, and sgs3-11 plants show enhanced symptom development, including more severe stunting, wilting, anthocyanin accumulation, and tissue necrosis, compared with inoculated Col-0 plants at 20 d post-inoculation. (B). V. dahliae-inoculated ago1-25, ago1-27, hen1-6, and hst-1 mutants develop fewer symptoms than inoculated Col-0 plants (A) at 25 d post-inoculation. (C) V. dahliae-inoculated dcl2-1, sde3-4, and sde3-5 mutants show similar disease symptoms as inoculated Col-0 plants (A) at 20 d post-inoculation.
Mentions: The enhanced susceptibility phenotype of the sgs mutants upon Verticillium inoculation directed us to assess susceptibility towards this pathogen in additional gene-silencing mutants. These comprised additional mutant alleles of SGS2 (also known as RDR6), namely rdr6-11 and rdr6-15, and for SGS3, namely sgs3-11. Furthermore, mutants of other components of RNA-silencing pathways were also included (Table 1). These included mutants of genes that encode different enzyme families, such as the argonautes AGO1 and AGO7, the dicers DCL2 and DCL4, the methyltransferase HEN1, the putative sRNA transporter HST, the DNA-dependent RNA polymerase NRPD1a, the RNA-dependent RNA polymerase RDR2, and the RNA helicase SDE3 that all have been implicated in different RNA-silencing pathways (Table 1; Voinnet, 2008). All mutants, derived from a Col-0 parental line, were challenged with V. dahliae strain JR2. As expected, additional mutant alleles of SGS2 and SGS3 (rdr6-11, rdr6-15, and sgs3-11) were more susceptible than Col-0 plants upon V. dahliae inoculation (Fig. 3A), thus confirming the enhanced susceptibility observed in the sgs2-1 and sgs3-1 mutants. The other PTGS mutants could be divided into three classes, based on the phenotypes after V. dahliae inoculation; those displaying enhanced susceptibility (Fig. 3A), mutants displaying enhanced resistance (Fig. 3B), and mutants displaying similar disease phenotypes as Verticillium-inoculated Col-0 plants (Fig. 3C). The mutants ago7-2, dcl4-2, nrpd1a-3, and rdr2-4 were found to be more susceptible to V. dahliae challenge by showing more severe stunting and necrosis when compared with inoculated Col-0 plants (Fig. 3A; see Supplementary Fig. S2 at JXB online). By contrast, the mutants ago1-25, ago1-27, hen1-6, and hst-1 were found to be more resistant because they displayed less necrosis and no anthocyanin production when compared with Col-0 plants upon V. dahliae inoculation (Fig. 3B; see Supplementary Fig. S2 at JXB online). Finally, the mutants dcl2-1, sde3-4, and sde3-5 showed a disease susceptibility phenotype that was similar to that of Col-0 with respect to severity of stunting, necrosis, and anthocyanin production (Fig. 3C; see Supplementary Fig. S2 at JXB online).

Bottom Line: Recently, RNA silencing has been found to play a role in defence against bacterial plant pathogens in Arabidopsis through modulating host defence responses.Several components of RNA silencing pathways were tested, of which many were found to affect Verticillium defence.Since the observed differences in Verticillium susceptibility cannot be explained by notable differences in root architecture, it is speculated that the gene silencing mechanisms affect regulation of Verticillium-specific defence responses.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Phytopathology, Wageningen University, Binnenhaven 5, 6709 PD Wageningen, The Netherlands.

ABSTRACT
RNA silencing is a conserved mechanism in eukaryotes that plays an important role in various biological processes including regulation of gene expression. RNA silencing also plays a role in genome stability and protects plants against invading nucleic acids such as transgenes and viruses. Recently, RNA silencing has been found to play a role in defence against bacterial plant pathogens in Arabidopsis through modulating host defence responses. In this study, it is shown that gene silencing plays a role in plant defence against multicellular microbial pathogens; vascular fungi belonging to the Verticillium genus. Several components of RNA silencing pathways were tested, of which many were found to affect Verticillium defence. Remarkably, no altered defence towards other fungal pathogens that include Alternaria brassicicola, Botrytis cinerea, and Plectosphaerella cucumerina, but also the vascular pathogen Fusarium oxysporum, was recorded. Since the observed differences in Verticillium susceptibility cannot be explained by notable differences in root architecture, it is speculated that the gene silencing mechanisms affect regulation of Verticillium-specific defence responses.

Show MeSH
Related in: MedlinePlus