Late blight caused by Phytophthora infestans greatly constrains potato production. Many Resistance (R) genes were cloned from wild Solanum species and/or introduced into potato cultivars by breeding. However, individual R genes have been overcome by P. infestans evolution; durable resistance remains elusive. We positionally cloned a new R gene, Rpi-amr1, from Solanum americanum , that encodes an NRC helper-dependent CC-NLR protein. Rpi-amr1 confers resistance in potato to all 19 P. infestans isolates tested. Using association genomics and long-read RenSeq, we defined eight additional Rpi-amr1 alleles from different S. americanum and related species.Despite only ~90% identity between Rpi-amr1 proteins, all confer late blight resistance but differentially recognize Avramr1 orthologs and paralogs. We propose that Rpi-amr1 gene family diversity assists detection of diverse paralogs and alleles of the recognized effector, facilitating durable resistance against P. infestans .
1 2 Late blight caused by Phytophthora infestans greatly constrains potato production. 3 Many Resistance (R) genes were cloned from wild Solanum species and/or introduced 4 into potato cultivars by breeding. However, individual R genes have been overcome by 5 P. infestans evolution; durable resistance remains elusive. We positionally cloned a 6 new R gene, Rpi-amr1, from Solanum americanum, that encodes an NRC helper-7 dependent CC-NLR protein. Rpi-amr1 confers resistance in potato to all 19 P. infestans 8 isolates tested. Using association genomics and long-read RenSeq, we defined eight 9 additional Rpi-amr1 alleles from different S. americanum and related species. Despite 10 only ~90% identity between Rpi-amr1 proteins, all confer late blight resistance but 11 differentially recognize Avramr1 orthologs and paralogs. We propose that Rpi-amr1 12 gene family diversity facilitates detection of diverse paralogs and alleles of the 13 recognized effector, enabling broad-spectrum and durable resistance against P. 14 infestans. Pathogen enrichment Sequencing) enable rapid definition of allelic variation 63 and mapping of plant NLRs, or discovery of variation in pathogen effectors 21-23 . 64 Combined with single-molecule real-time (SMRT) sequencing, SMRT RenSeq enabled 65 cloning of Rpi-amr3 from Solanum americanum 24 . Similarly, long read and cDNA 66 PenSeq enabled us to identify Avramr1 from P. infestans 25 . 67 4 68In this study, we further explored the genetic diversity of S. americanum, and by 69 applying sequence capture technologies, we fine-mapped and cloned Rpi-amr1 from S. 70 americanum, (usually) located on the short arm of chromosome 11. Multiple Rpi-amr1 71 homologs were found in different S. americanum accessions and in relatives, including 72Solanum nigrescens and Solanum nigrum. Functional alleles show extensive allelic 73 variation and confer strong, broad-spectrum resistance to all 19 tested diverse P. 74 infestans isolates. Although differential recognition was found between different Rpi-75 amr1 and Avramr1 homologs, all Rpi-amr1 alleles recognize the Avramr1 homologs 76 from Phytophthora parasitica and Phytophthora cactorum. Our study reveals unique 77properties of genetic variation of R genes from "non-host" species. 78 79
1 2 • Potato late blight, caused by the oomycete pathogen Phytophthora infestans, 3 significantly hampers potato production. Recently, a new Resistance to Phytophthora 4 infestans (Rpi) gene, Rpi-amr1, was cloned from a wild Solanum species, Solanum 5 americanum. Identification of the corresponding recognized effector (Avirulence, or 6Avr) genes from P. infestans is key to elucidating their naturally occurring sequence 7 variation, which in turn informs the potential durability of the cognate late blight 8 resistance. 9• To identify the P. infestans effector recognized by Rpi-amr1, we screened available 10 effector libraries and used long read and cDNA pathogen-enrichment sequencing 11 (PenSeq) on four P. infestans isolates to explore the untested effectors. 12• By using SMRT and cDNA PenSeq, we identified 47 highly expressed effectors from 13 P. infestans, including PITG_07569 which triggers a highly specific cell death response 14 when transiently co-expressed with Rpi-amr1 in Nicotiana benthamiana, suggesting 15 that PITG_07569 is Avramr1. 16• Here we demonstrate that long read and cDNA PenSeq enables the identification of 17 full-length RxLR effector families, and their expression profile. This study has revealed 18 key insights into the evolution and polymorphism of a complex RxLR effector family 19 that is associated with the recognition by Rpi-amr1.
Albugo candida is an obligate oomycete pathogen that infects many plants in the Brassicaceae family. We re-sequenced the genome of isolate Ac2V using PacBio long reads and constructed an assembly augmented by Illumina reads. The Ac2VPB genome assembly is 10% larger and more contiguous compared to a previous version. Our annotation of the new assembly, aided by RNASeq information, revealed a 175% expansion (40 to 110) in the CHxC effector class, which we redefined as “CCG” based on motif analysis. This class of effectors consist of arrays of phylogenetically related paralogs residing in gene sparse regions, and shows signatures of positive selection and presence/absence polymorphism. This work provides a resource that allows the dissection of the genomic components underlying A. candida adaptation and particularly the role of CCG effectors in virulence and avirulence on different hosts.
Potato late blight, caused by the hemibiotrophic oomycete pathogen Phytophthora infestans, triggered the Irish and European famine in the late 1840s, and still causes severe losses to world potato production. To reduce losses, breeders sought resistance genes in wild relatives of potato. Early in the 20th century, Solanum demissum, a highly resistant hexaploid (2n = 72) wild potato, was found to be a useful source of resistance to P. infestans (Rpi) genes (Salaman, 1937). Since then, many resistance traits have been transferred to cultivated potatoes by introgression breeding (Toxopeus, 1956), and many Rpi genes have been cloned from wild potatoes, for example R1, R3a, R8, Rpi
SUMMARY The oomycete Albugo candida causes white rust of Brassicaceae, including vegetable and oilseed crops, and wild relatives such as Arabidopsis thaliana. Novel White Rust Resistance (WRR) genes from Arabidopsis enable new insights into plant/parasite co‐evolution. WRR4A from Arabidopsis accession Columbia (Col‐0) provides resistance to many but not all white rust races, and encodes a nucleotide‐binding, leucine‐rich repeat immune receptor. Col‐0 WRR4A resistance is broken by AcEx1, an isolate of A. candida. We identified an allele of WRR4A in Arabidopsis accession Øystese‐0 (Oy‐0) and other accessions that confers full resistance to AcEx1. WRR4AOy‐0 carries a C‐terminal extension required for recognition of AcEx1, but reduces recognition of several effectors recognized by the WRR4ACol‐0 allele. WRR4AOy‐0 confers full resistance to AcEx1 when expressed in the oilseed crop Camelina sativa.
Late blight caused by the oomycete pathogen Phytophthora infestans continues to cause major worldwide losses in potato and tomato. Most accessions of Solanum americanum, a globally distributed, wild Solanaceae plant, are highly resistant to late blight. We generated high-quality reference genomes of four S. americanum accessions, re-sequenced 52 accessions, and we defined variation in the NLR immune receptor genes (the S. americanum NLRome). We further screened for variation in recognition of ~315 P. infestans RXLR effectors in 52 S. americanum accessions. Using these genotypic and phenotypic data, we cloned three novel NLR-encoding genes Rpi-amr4, Rpi-amr16 and Rpi-amr17, and determined their corresponding RXLR effector genes Avramr4 (PITG_22825), Avramr16 (PITG_02860) and Avramr17 (PITG_04373) from P. infestans. These genomic resources and methodology will support efforts to convert potato into a nonhost of late blight and can be applied to diseases of other crops.
The oomycete Albugo candida causes white blister rust, an important disease of Brassica crops. Distinct races of A. candida are defined by their specificity for infecting different host species. The White Rust Resistance 4 (WRR4) locus in Col-0 accession of Arabidopsis thaliana contains three genes that encode TIR-NLR resistance proteins. The Col-0 alleles of WRR4A and WRR4B confer resistance to at least four A. candida races (2, 7 and 9 from B. juncea, B. rapa and B. oleracea, respectively, and Race 4 from Capsella bursa-pastoris). Resistance mediated by both paralogs can be overcome by Col-0-virulent isolates of Race 4. After comparing repertoires of candidate effectors in resisted and resistance-breaking strains, we used transient co-expression in tobacco or Arabidopsis to identify effectors recognized by WRR4A and WRR4B. A library of CCG effectors from four A. candida races was screened for WRR4A- or WRR4B- dependent elicitation of hypersensitive response (HR). These CCG genes were validated for WRR-dependent HR by bombardment assays in wild type Col-0, wrr4A or wrr4B mutants. Our analysis revealed eight WRR4A-recognized CCGs and four WRR4B-recognized CCGs. Remarkably, the N-terminal region of 100 amino acids after the secretion signal is sufficient for WRR4A recognition of these eight recognized effectors. This multiple recognition capacity potentially explains the broad-spectrum resistance to many A. candida races conferred by WRR4 paralogs.
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