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STV11 Encodes a Sulphotransferase and Confers Durable Resistance to Rice Stripe Virus

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STV11 Encodes a Sulphotransferase and Confers Durable Resistance to Rice Stripe Virus

Qi Wang et al. Nat Commun.

Abstract

Rice stripe virus (RSV) causes one of the most serious viral diseases of rice (Oryza sativa L.), but the molecular basis of RSV resistance has remained elusive. Here we show that the resistant allele of rice STV11 (STV11-R) encodes a sulfotransferase (OsSOT1) catalysing the conversion of salicylic acid (SA) into sulphonated SA (SSA), whereas the gene product encoded by the susceptible allele STV11-S loses this activity. Sequence analyses suggest that the STV11-R and STV11-S alleles were predifferentiated in different geographic populations of wild rice, Oryza rufipogon, and remained prevalent in cultivated indica and japonica rice varieties, respectively. Introgression of the STV11-R allele into susceptible cultivars or heterologous transfer of STV11-R into tobacco plants confers effective resistance against RSV. Our results shed new insights into plant viral defense mechanisms and suggest effective means of breeding RSV-resistant crops using molecular marker-assisted selection or genetic engineering.

Figures

Figure 1
Figure 1. Characterization of RSV resistance in KK34.
(a,b) Phenotypes of Kos and KK34 plants at 45 d.p.i. with non-virulent (mock) or RSV-carrying SBPH. (c) Representative images of Kos and KK34 leaves. (d) KK34 has similar SBPH susceptibility to Kos. WYJ3 (Wuyujing 3) and RH (Rathu Heenati) were used as the SBHP-susceptible and -resistant control, respectively. Error bars indicate s.e.m. (n=3), different letters at the top of each column indicate significant differences at P<0.01 (n=3) by the Student’s t-test. (e) RT–PCR assay showing accumulation of the RSV coat protein mRNA in whole seedling plant without roots of Kos and KK34 following RSV infection. m, mock seedlings were sampled 3 d.p.i. with RSV-free SBPH. The mean±s.e.m. was obtained from three technical repeats and three biological repeats. (f) ELISA assay showing replication of RSV in Kos and KK34 protoplasts. Mock, the protoplasts treated the PBS buffer. Error bars indicate s.e.m. (n=3), **indicates significant differences between Kos and KK34 inoculated with RSV at same time point at P<0.01 (n=3) by the Student’s t-test.
Figure 2
Figure 2. STV11 haplotypes and complementation tests.
(a) STV11 haplotypes identified in 24 rice varieties. AA changes are shown above the closed bar. *indicates non-synonymous polymorphisms. In, indica; Jp, japonica. (bg) Acquired RSV resistance of transgenic lines overexpressing STV11-R driven by the maize Ubiquitin-1 promoter (bd) or transformed with a genomic sequence of STV11-R (eg). NIP, the susceptible wild type NIP. (c,f) Quantification of RSV resistance. (d,g) Measurement of RSV by ELISA assay. One-week-old plants were used for RSV infection. Photographing, resistant evaluation and ELISA were performed 30 (bd) or 70 (eg) d.p.i. Data are shown as means±s.e.m. (n=3). Different letters at the top of each column indicate a significant difference at P<0.01 (n=3) by the Student’s t-test.
Figure 3
Figure 3. Effect of STV11-R on RSV resistance.
(a) Sulfotransferase activities of STV11-R and STV11-S. The insert shows HPLC detection of the SSA standard. (b) SA contents in KK34 and Kos following RSV infection. Mock, the 1-week-old rice plants were not infected with RSV. Data are shown as means±s.e.m. (n=3), **indicates significant difference between Kos and KK34 at same time point at P<0.01 by the Student’s t-test. (c) RSV replication is inhibited by SA or SSA in Kos protoplasts. Data are shown as means±s.e.m. (n=3). Different letters at the top of each column indicate a significant difference at P<0.05 (n=3) by the Student’s t-test. (d) Increased RSV replication in KK34 protoplasts expressing the bacterial salicylate hydroxylase gene (NahG) and co-expression of NahG reduces inhibition of RSV replication by STV11-R in Kos protoplasts. The protoplasts were collected at 16 h after infection of RSV. Mock (m), the protoplasts were not infected with RSV. Data are shown as means±s.e.m. (n=3). Different letters at the top of each column indicate a significant difference at P<0.05 (n=3) by the Student’s t-test.
Figure 4
Figure 4. Analysis of natural variation at the STV11 locus in rice cultivars and O. rufipogon.
(a) Geographical origin of rice landraces and cultivars used in this analysis. (b) Distribution of STV11-R and STV11-S in japonica, indica and O. rufipogon.

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