Resistance to Botrytis cinerea in Solanum lycopersicoides involves widespread transcriptional reprogramming

Abstract

BackgroundTomato (Solanum lycopersicum), one of the world’s most important vegetable crops, is highly susceptible to necrotrophic fungal pathogens such as Botrytis cinerea and Alternaria solani. Improving resistance through conventional breeding has been hampered by a shortage of resistant germplasm and difficulties in introgressing resistance into elite germplasm without linkage drag. The goal of this study was to explore natural variation among wild Solanum species to identify new sources of resistance to necrotrophic fungi and dissect mechanisms underlying resistance against B. cinerea.ResultsAmong eight wild species evaluated for resistance against B. cinerea and A. solani, S. lycopersicoides expressed the highest levels of resistance against both pathogens. Resistance against B. cinerea manifested as containment of pathogen growth. Through next-generation RNA sequencing and de novo assembly of the S. lycopersicoides transcriptome, changes in gene expression were analyzed during pathogen infection. In response to B. cinerea, differentially expressed transcripts grouped into four categories: genes whose expression rapidly increased then rapidly decreased, genes whose expression rapidly increased and plateaued, genes whose expression continually increased, and genes with decreased expression. Homology-based searches also identified a limited number of highly expressed B. cinerea genes. Almost immediately after infection by B. cinerea, S. lycopersicoides suppressed photosynthesis and metabolic processes involved in growth, energy generation, and response to stimuli, and simultaneously induced various defense-related genes, including pathogenesis-related protein 1 (PR1), a beta-1,3-glucanase (glucanase), and a subtilisin-like protease, indicating a shift in priority towards defense. Moreover, cluster analysis revealed novel, uncharacterized genes that may play roles in defense against necrotrophic fungal pathogens in S. lycopersicoides. The expression of orthologous defense-related genes in S. lycopersicum after infection with B. cinerea revealed differences in the onset and intensity of induction, thus illuminating a potential mechanism explaining the increased susceptibility. Additionally, metabolic pathway analyses identified putative defense-related categories of secondary metabolites.ConclusionsIn sum, this study provided insight into resistance against necrotrophic fungal pathogens in the Solanaceae, as well as novel sequence resources for S. lycopersicoides.Electronic supplementary materialThe online version of this article (doi: 10.1186/1471-2164-15-334) contains supplementary material, which is available to authorized users.

BcSUN1, a B. cinerea SUN-Family Protein, Is Involved in Virulence

“…Previously, Smith et al (2014) identified Bcsun1 as one of the genes induced in planta during infection of Solanum lycopersicoides leaves. Altogether, these results suggested a role of BcSUN1 in fungal pathogenesis.…”

‘Omics’ and Plant Responses to Botrytis cinerea

“…Several studies focusing on the transcriptional regulation of responses to multiple stresses have identified commonly regulated genes responsive to both B. cinerea infection and simultaneous abiotic stresses, such as drought, heat, or salinity, in Arabidopsis using microarray analyses (Atkinson and Urwin, 2012; Sham et al, 2015). In tomato, a transcriptomic study using RNAseq has distinguished the natural variation among wild Solanum species (Smith et al, 2014). Following B. cinerea infection, photosynthetic and metabolic processes were suppressed, whereas defense-related genes, such as those encoding PR protein 1 (PR1), β-1,3-glucanase and subtilisin-like protease, were simultaneously induced in the highly B. cinerea -resistant species, S. lycopersicoides .…”

“…Advances in high-throughput DNA sequencing, RNA sequencing (RNAseq), mass spectrometry (MS), and nuclear magnetic resonance (NMR) at the genomic, transcriptomic, proteomic and metabolomic levels, and through the multi-omics (also known as integrated-omics) (Shiratake and Suzuki, 2016), have made possible the development of such data into a systems biology-based framework ( Figure 1 ). High-throughput-next generation sequencing (HT-NGS) technologies, ranging from RNAseq to whole-genome sequencing, are fast, sensitive and accurate tools for detection of B. cinerea genome from symptomatic or asymptomatic plants and understanding defense mechanisms associated with fungal infections in planta (Smith et al, 2014). Moreover, HT-NGS techniques have promising applications at the molecular plant- B. cinerea interaction research.…”

Tomato SlERF.A1, SlERF.B4, SlERF.C3 and SlERF.A3, Members of B3 Group of ERF Family, Are Required for Resistance to Botrytis cinerea

“…Several quantitative trait loci conferring resistance or susceptibility to B. cinerea have been identified and mapped in tomato (Finkers et al, 2007; Davis et al, 2009). Significant transcriptional reprogramming, metabolic and biochemical changes, and modification of signal pathways operated by different stress hormones such as ethylene (ET), salicylic acid (SA), jasmonic acid (JA), and abscisic acid (ABA) are involved in the response of tomato or its wild species to B. cinerea (Blanco-Ulate et al, 2013; Seifi et al, 2014; Smith et al, 2014; Camañes et al, 2015; Vega et al, 2015). During the infection process, B. cinerea can manipulate the antagonistic balance between the SA- and JA/ET-mediated signaling pathways and hijack the SA signaling pathway to accelerate disease development (El Oirdi et al, 2011; Rahman et al, 2012).…”