Discovery and genome-guided mapping of REN12 from Vitis amurensis, conferring strong, rapid resistance to grapevine powdery mildew

Authors: SAPKOTA, SURYA - Cornell University; ZOU, CHENG - Cornell University; Ledbetter, Craig; Underhill, Anna; SUN, QI - Cornell University; GADOURY, DAVID - Cornell University; Cadle-Davidson, Lance

Submitted to: Horticulture Research
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/12/2023
Publication Date: 5/5/2023
Citation: Sapkota, S., Zou, C., Ledbetter, C.A., Underhill, A.N., Sun, Q., Gadoury, D., Cadle Davidson, L.E. 2023. Discovery and genome-guided mapping of REN12 from Vitis amurensis, conferring strong, rapid resistance to grapevine powdery mildew. Horticulture Research. https://doi.org/10.1093/hr/uhad052.
DOI: https://doi.org/10.1093/hr/uhad052

Interpretive Summary: Different powdery mildew resistance genes allow the pathogen to grow to different extents. Here, a strong and rapid powdery mildew resistance was discovered from Vitis amurensis ‘PI 588631’. This resistance was effective across multiple years of vineyard evaluation on all plant tissues and in controlled experiments. Resistance was caused by a single, dominantly inherited DNA segment (here named REN12) on chromosome 13 for all plant tissues. REN12 explained nearly all of the variation in disease on leaves. Genome sequencing enabled REN12 to be defined to a DNA segment having 92 genes. RNA expression analysis narrowed that to 4 candidate resistance genes in this region. REN12 is one of the strongest powdery mildew resistance loci in grapevine, and the DNA sequences presented here can be directly used for grape breeding. We recommend stacking of REN12 with other resistance genes and minimal use of fungicides to make resistance last for decades. This approach could enable a 90% reduction in fungicides in low-rainfall climates where few other pathogens attack the foliage or fruit.

Technical Abstract: Powdery mildew resistance genes restrict infection attempts at different stages of pathogenesis. Here, a strong and rapid powdery mildew resistance phenotype was discovered from Vitis amurensis ‘PI 588631’ that rapidly stopped over 97% of Erysiphe necator conidia, before or immediately after emergence of a secondary hypha from appressoria. This resistance was effective across multiple years of vineyard evaluation on leaves, stems, rachises, and fruit and against a diverse array of E. necator laboratory isolates. Using core genome rhAmpSeq markers, resistance mapped to a single dominant locus (here named REN12) on chromosome 13 near 22.8-27.0 Mbp, irrespective of tissue type, explaining up to 86.9% of the phenotypic variation observed on leaves. Shotgun sequencing of recombinant vines using skim-seq technology enabled the locus to be further resolved to a 780 kbp region, from 25.15 to 25.93 Mbp. RNASeq analysis indicated the allele-specific expression of four resistance genes (NLRs) from the resistant parent. REN12 is one of the strongest powdery mildew resistance loci in grapevine yet documented, and the rhAmpSeq sequences presented here can be directly used for marker-assisted selection or converted to other genotyping platforms. While no virulent isolates were identified among the genetically diverse isolates and wild populations of E. necator tested here, NLR loci like REN12 are often race-specific. Thus, stacking of multiple resistance genes and minimal use of fungicides should enhance the durability of resistance and could enable a 90% reduction in fungicides in low-rainfall climates where few other pathogens attack the foliage or fruit.