The dissection of R genes and locus Pc5.1 in Phytophthora capsici infection provides a novel view of disease resistance in peppers

Abstract

Background Phytophthora capsici root rot (PRR) is a disastrous disease in peppers (Capsicum spp.) caused by soilborne oomycete with typical symptoms of necrosis and constriction at the basal stem and consequent plant wilting. Most studies on the QTL mapping of P. capsici resistance suggested a consensus broad-spectrum QTL on chromosome 5 named Pc.5.1 regardless of P. capsici isolates and resistant resources. In addition, all these reports proposed NBS-ARC domain genes as candidate genes controlling resistance. Results We screened out 10 PRR-resistant resources from 160 Capsicum germplasm and inspected the response of locus Pc.5.1 and NBS-ARC genes during P. capsici infection by comparing the root transcriptomes of resistant pepper 305R and susceptible pepper 372S. To dissect the structure of Pc.5.1, we anchored genetic markers onto pepper genomic sequence and made an extended Pc5.1 (Ext-Pc5.1) located at 8.35 Mb–38.13 Mb on chromosome 5 which covered all Pc5.1 reported in publications. A total of 571 NBS-ARC genes were mined from the genome of pepper CM334 and 34 genes were significantly affected by P. capsici infection in either 305R or 372S. Only 5 inducible NBS-ARC genes had LRR domains and none of them was positioned at Ext-Pc5.1. Ext-Pc5.1 did show strong response to P. capsici infection and there were a total of 44 differentially expressed genes (DEGs), but no candidate genes proposed by previous publications was included. Snakin-1 (SN1), a well-known antimicrobial peptide gene located at Pc5.1, was significantly decreased in 372S but not in 305R. Moreover, there was an impressive upregulation of sugar pathway genes in 305R, which was confirmed by metabolite analysis of roots. The biological processes of histone methylation, histone phosphorylation, DNA methylation, and nucleosome assembly were strongly activated in 305R but not in 372S, indicating an epigenetic-related defense mechanism. Conclusions Those NBS-ARC genes that were suggested to contribute to Pc5.1 in previous publications did not show any significant response in P. capsici infection and there were no significant differences of these genes in transcription levels between 305R and 372S. Other pathogen defense-related genes like SN1 might account for Pc5.1. Our study also proposed the important role of sugar and epigenetic regulation in the defense against P. capsici.

Insights into the genetic architecture of Phytophthora capsici root rot resistance in chile pepper (Capsicum spp.) from multi-locus genomewide association study

“…GBS-derived-SNPs on chromosome 5 detected by Siddique et al [9] at 27.0 to 29.5 Mb, were also located ~ 1.4 Mb downstream to the S5_25470050. Three SNP markers (S5_9345710, S5_14665044, and S5_25470050) detected using GWAS in this study coincide with the extended Pc5.1 (Ext-Pc5.1) region on chromosome 5 that is located between 8.35 Mb and 38.13 Mb [73]. These SNPs also coincide with the MQTL5.1 identi ed from meta-QTL analysis in chile pepper [71].…”

Phytophthora capsici: Recent Progress on Fundamental Biology and Disease Management 100 Years After Its Description

“…In addition to targeted QTL regions, general receptor classes and gene families known to be involved in plant development, growth, and stress response have shown differential expression and regulation during P. capsici infection of pepper (29). Tissue-specific activation of ethylene response factors (ERFs) was associated with improved resistance to P. capsici and silencing of select ERFs weakened the defense response (56).…”

Chile Pepper (Capsicum) Breeding and Improvement in the “Multi-Omics” Era

“…While management practices can help mitigate the effects of P. capsici on chile pepper production ( Sanogo and Ji, 2012 ), breeding and selection for disease-resistant cultivars are still the most cost-effective approach ( Xu et al, 2016 ; Siddique et al, 2019 ). The short arm of chromosome P5 is a major genetic hotspot containing QTL for P. capsici resistance ( Mallard et al, 2013 ; Rehrig et al, 2014 ; Siddique et al, 2019 ; Du et al, 2021 ; Lozada et al, 2021b , c ), and this information facilitates breeding efforts for resistance to P. capsici . A set of New Mexico recombinant inbred lines (NMRIL) derived from the hybridization between the resistant landrace, CM-334, and the susceptible cultivar “Early Jalapeno” was previously developed at NMSU to facilitate a better understanding of the complex inheritance of P. capsici root rot resistance and the characterization of different races for breeding resistant cultivars ( Sy et al, 2008 ).…”

“…There has been growing evidence on the potential involvement of epigenetic factors, such as DNA methylation, histone acetylation, and chromatin remodeling, specifically on conferring P. capsici resistance in chile pepper ( Du et al, 2021 ; Lozada et al, 2021b , 2021c ). Examining the chile pepper epigenome using various techniques, such as DNA methylation PCR-based bisulfite sequencing and chromatin immunoprecipitation assays ( Cazaly et al, 2019 ; Li, 2021 ), could therefore be relevant in breeding and selection for P. capsici resistant lines.…”