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Ncomms2427.Pdf ARTICLE Received 21 May 2012 | Accepted 31 Dec 2012 | Published 29 Jan 2013 DOI: 10.1038/ncomms2427 OPEN The evolution and pathogenic mechanisms of the rice sheath blight pathogen Aiping Zheng1,2,3,*, Runmao Lin1,*, Danhua Zhang1, Peigang Qin1, Lizhi Xu1, Peng Ai1, Lei Ding3, Yanran Wang1, Yao Chen1, Yao Liu1, Zhigang Sun1, Haitao Feng1, Xiaoxing Liang1, Rongtao Fu1, Changqing Tang1, Qiao Li1, Jing Zhang1, Zelin Xie3, Qiming Deng1,2,3, Shuangcheng Li1,2,3, Shiquan Wang1,2,3, Jun Zhu1,2,3, Lingxia Wang2, Huainian Liu2 & Ping Li1,2,3 Rhizoctonia solani is a major fungal pathogen of rice (Oryza sativa L.) that causes great yield losses in all rice-growing regions of the world. Here we report the draft genome sequence of the rice sheath blight disease pathogen, R. solani AG1 IA, assembled using next-generation Illumina Genome Analyser sequencing technologies. The genome encodes a large and diverse set of secreted proteins, enzymes of primary and secondary metabolism, carbohydrate-active enzymes, and transporters, which probably reflect an exclusive necrotrophic lifestyle. We find few repetitive elements, a closer relationship to Agaricomycotina among Basidiomycetes, and expand protein domains and families. Among the 25 candidate pathogen effectors identified according to their functionality and evolution, we validate 3 that trigger crop defence responses; hence we reveal the exclusive expression patterns of the pathogenic determinants during host infection. 1 State Key Laboratory of Hybrid Rice, Sichuan Agricultural University, Chengdu 611130, China. 2 Rice Research Institute of Sichuan Agricultural University, Chengdu 611130, China. 3 Key Laboratory of Southwest Crop Gene Resource and Genetic Improvement of Ministry of Education, Sichuan Agricultural University, Ya’an 625014, China. * These authors contributed equally to this work. Correspondence and requests for materials should be addressed to A.Z. (email: [email protected]) or to P.L. (email: [email protected]). NATURE COMMUNICATIONS | 4:1424 | DOI: 10.1038/ncomms2427 | www.nature.com/naturecommunications 1 & 2013 Macmillan Publishers Limited. All rights reserved. ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms2427 he soilborne Basidiomycete fungus Rhizoctonia solani The mitochondrial genome of R. solani AG1 IA assembled as a (teleomorph: Thanatephorus cucumeris) is a complex with circular molecule of 146 kb, with an overall G þ C content of Tmore than 100 species that attack all known crops, pastures 33.8%. In all, 21 ORFs were predicted. A total of 26 tRNAs, and horticultural species. R. solani is divided into 14 anastomosis 1 rRNA and 4 ribozymes were identified. Twenty-nine gaps were groups (AG1 to AG13 and AGBI)1. Among R. solani AG1 finally filled using the PCR technique (Table 1, Supplementary containing three main intraspecific groups (ISG), the subgroup Fig. S2, Supplementary Note 2). Indeed, it is the largest AG1 IA is one of the most important plant pathogens, which mitochondrial genome sequence among fungi thus far. causes diseases such as sheath blight, banded leaf, aerial blight Additionally, we adopted the comprehensive approaches and brown patch1–3 in many plants, including more than 27 to assess the large-scale and local assembly accuracy of the families of monocots and dicots. scaffolds including Sanger protocols (Fig. 1c, Supplementary Fig. As the agent of rice sheath blight, R. solani AG1 IA was S3, Supplementary Tables S2 and S3, Supplementary Note 2). It thought to be mainly an asexual fungus on rice (Oryza sativa L.), showed that we assembled the diploid multinuclei genome of although sexual structures from its teleomorph (T. cucumeris) R. solani AG1 IA, and the assembly was highly accurate. have been occasionally observed in fields. In nature, R. solani AG1 IA exists primarily as vegetative mycelium and sclerotia The R. solani AG1 IA repeat content. DNA transposons and (Supplementary Fig. S1). Each year, the blight causes up to a 50% retrotransposons including 81 families are identified in R. solani decrease in the rice yield under favourable conditions around the AG1 IA, which accounts for 5.27% of the 36.94-Mb genome world4,5. In Eastern Asia, it affects B15–20 million ha of paddy- sequence (Supplementary Table S4, Supplementary Note 3). irrigated rice and causes a yield loss of 6 million tons of rice Among the repetitive elements, Gypsy comprised 1,189,261 bp grains per year5. R. solani AG1 IA is also considered to be the and were the most abundant type of transposon elements (TEs). most destructive pathogen for other economically important They account for 65.18% of the TEs and 3.43% of the assembly, crops, including corn (Zea mays)3,6 and soybean (Glycine and when compared with the Gypsy LTR retrotransposons mined max)2,7. from 25 fungal species genomes from Ascomycota and Basidio- Highly resistant rice and corn cultivars have not been found for mycota12, more copies were detected in R. solani AG1 IA. use in breeding, but quantitative resistance exists8. Until now, Furthermore, tandem repeats of B55,417 bp were identified. control strategies have relied mainly on fungicides. Despite the In all, repeat elements were B5.43% of the assembly. The genome high worldwide rice yield losses caused by R. solani AG1 IA, only of R. solani AG1 IA showed no evidence of a whole-genome limited information is available about the genetic structure of its duplication. Among Basidiomycetes, the similarity of repeat populations and reproductive mode5,9. The main objective of our contents exists among R. solani AG1 IA, Postia placenta and study was to elucidate the possible molecular basis of host– Cryptococcus neoformans (5% of genome repeats). However, pathogen interactions and pathogenic mechanisms of the rice- TEs content in the R. solani AG1 IA genome is higher than the infecting pathogen R. solani AG1 IA, which could provide content of 2.5% observed in Coprinopsis cinerea and the 1.1% knowledge for improving the yield of food crop in agriculture. content in Ustilago maydis and is much lower than the 45% content in Melampsora larici-populina, the 43.7% content in Results Puccinia graminis f. sp. tritici, and the 21% content in Laccaria Genome sequencing and analysis. We used a whole- bicolor of Basidiomycetes. In general, the relatively low repeat genome shotgun (WGS) sequencing strategy and the Illumina content of the R. solani AG1 IA genome is similar to what Genome Analyser (GA) sequencing technology. A 36.94-Mb draft would be expected for small, rapidly reproducing eukaryotic genome sequence was assembled using the high-quality 13 10 organisms . We deduce that the R. solani AG1 IA contains DNA sequenced data (Supplementary Table S1) and SOAPdenovo . methylase genes (AG1IA_00169, AG1IA_00211, AG1IA_01948, The N50 sizes of the scaffold and contig were 474.50 Kb and AG1IA_05357), which may inhibit repeat element expansion14. 20,319 bp, respectively (Table 1, Fig. 1). The G þ C content of the genome was 47.61%. The heterozygosity in the R. solani AG1 IA genome was estimated to be 0.12%, and 43,121 SNPs were Evolution and comparative genomics. Comparative analyses detected in the assembly. The coding DNA sequences contain of the available Basidiomycete genomes show that L. bicolor, 10,489 open reading frames (ORFs)11(Supplementary Note 2). P. placenta and rusts M. laricis-populina, P. graminis have more Totally, 6,156 genes were annotated, and among these genes 257 genes (Supplementary Table S5). In all, 608 ortholog groups with genes were assigned to the pathogen–host interaction (PHI) only a single gene from each fungus and 102 ortholog groups of database. Moreover, 2 ribosomal RNAs and 102 transfer RNAs nine fungi were predicted, but no M. oryzae groups were found. were predicted. Among the 102 groups, only a single gene from each fungus was included in the 37 ortholog groups. The genes in these 102 groups were assigned to 426 KOG groups. Not surprisingly, the Table 1 | Description of R. solani AG1 IA genome assembly. Basidiomycete groups included many proteins involved in basic cellular processes. However, 33 KOG groups contained proteins Type Genome Mitochondria that were found in all species of these fungi, which were absent Scaffold number 2,648 1 from the of M. oryzae such as Gab-family adaptor protein, Scaffold length (bp) 36,938,120 147,264 protein tyrosine phosphatase. This number of conserved clusters Scaffold average length (bp) 13,949 147,264 reflects the small evolutionary distance between members of Scaffold N50 (bp) 474,500 147,264 Basidiomycete, as well as complex patterns of gene gains and Scaffold N90 (bp) 32,110 147,264 losses during the evolution of fungi. The differences and quan- Contigs number 6,452 6 tities of the ortholog groups among the fungi are shown using a Contigs length (bp) 34,639,994 146,906 Contig average length (bp) 5,068 24,484 Venn diagram (Fig. 2a). Contig N50 (bp) 20,319 30,515 The R. solani AG1 IA genes consist of 9,324 families, and of Contigs N90 (bp) 1,928 9,240 these families, 4,863 are unique, among which 4,538 are single- GC content 47.61 33.93 gene families (Supplementary Table S5). The R. solani AG1 IA undergoing genome reduction display a parallel process of 2 NATURE COMMUNICATIONS | 4:1424 | DOI: 10.1038/ncomms2427 | www.nature.com/naturecommunications & 2013 Macmillan Publishers Limited. All rights reserved. NATURE COMMUNICATIONS | DOI: 10.1038/ncomms2427 ARTICLE Sequence coverage 0.016 0.014 Frequency distribution of GC content 0.012 2.5 0.010 0.008 0.006 Proportion 2 0.004 0.002 0 02550 75 100 125 150 175 200 1.5 Coverage (X) Paired-reads coverage 0.020 1 0.018 0.016 0.014 0.012 % of total bin (width = 500 bp) 0.5 0.010 0.008 Proportion 0.006 0.004 0 0.002 20 25 30 35 40 45 50 55 60 65 70 75 0 % of GC content 0 255075100125 150 175 200 Coverage (X) cdsdaxa (bp) 100 1 5,000 10,000 15,000 20,000 25,000 30,000 35,000 36,848 90 A vs T 80 A vs C 70 A vs G 60 T vs C 50 T vs G 40 C vs G 30 Fosmid base Fosmid 20 230,761 235,761 240,761 245,761 250,761 255,761 260,761 265,761 269,062 10 genome sequence depth 0 Scaffold17 (bp) 01020 30 40 50 60 70 80 90 100 110 120 121 Assembly base genome sequence depth (X) Figure 1 | Genomic sequence and paired reads coverage.
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