Genotype-Specific Expression and NLR Repertoire Contribute to Phenotypic Resistance Diversity in Plantago lanceolata.

Pezhman Safdari,Layla Höckerstedt,Jarkko Salojärvi,Anna-Liisa Laine,Mikael Brosche

doi:10.3389/fpls.2021.675760

Abstract

High levels of phenotypic variation in resistance appears to be nearly ubiquitous across natural host populations. Molecular processes contributing to this variation in nature are still poorly known, although theory predicts resistance to evolve at specific loci driven by pathogen-imposed selection. Nucleotide-binding leucine-rich repeat (NLR) genes play an important role in pathogen recognition, downstream defense responses and defense signaling. Identifying the natural variation in NLRs has the potential to increase our understanding of how NLR diversity is generated and maintained, and how to manage disease resistance. Here, we sequenced the transcriptomes of five different Plantago lanceolata genotypes when inoculated by the same strain of obligate fungal pathogen Podosphaera plantaginis. A de novo transcriptome assembly of RNA-sequencing data yielded 24,332 gene models with N50 value of 1,329 base pairs and gene space completeness of 66.5%. The gene expression data showed highly varying responses where each plant genotype demonstrated a unique expression profile in response to the pathogen, regardless of the resistance phenotype. Analysis on the conserved NB-ARC domain demonstrated a diverse NLR repertoire in P. lanceolata consistent with the high phenotypic resistance diversity in this species. We find evidence of selection generating diversity at some of the NLR loci. Jointly, our results demonstrate that phenotypic resistance diversity results from a crosstalk between different defense mechanisms. In conclusion, characterizing the architecture of resistance in natural host populations may shed unprecedented light on the potential of evolution to generate variation.

Highlights

Parasitism is the most common life-style on Earth (Weinstein and Kuris, 2016), and parasitic species, including pathogens, play an important role in shaping biodiversity in natural populations (Kursar et al, 2009; Bever et al, 2015)
Transcript levels of the marker genes varied considerably in the susceptible plants and showed elevated levels only at time point 72 h post inoculation and this time point was selected for RNA sequencing
We identified 27 Nucleotide-binding leucine-rich repeat (NLR) transcripts with H values less than -3 (Figure 6; Supplementary Figure 4, FIGURE 5 | Redundancy analysis of NB-ARC domains. (A) (Genotype) redundancy analysis (RDA) analysis of the genotype effects of NB-ARC domain expression data explains 55% of the variation. (Phenotype) the same analysis shows that phenotype explains 15% of the variation that separates the resistant and susceptible phenotypes. (B) NB-ARC sequences contributing to the separation of the phenotypes (Resistant vs Susceptible); transcript2322 has the highest contribution to the separation

Summary

Introduction

Parasitism is the most common life-style on Earth (Weinstein and Kuris, 2016), and parasitic species, including pathogens, play an important role in shaping biodiversity in natural populations (Kursar et al, 2009; Bever et al, 2015). Relatively little is still understood of the molecular mechanisms that enable hosts and parasites to coexist in natural populations. In agriculture, increasing the diversity of crops – even from a monoculture to a mixture of two cultivars – has been shown to reduce disease levels (Zhu et al, 2000; Mundt, 2002). Natural host populations typically support diversity in resistance phenotypes (Salvaudon et al, 2008; Laine et al, 2011), and limited data available to date show that increasing resistance diversity decreases disease risk in the wild (Jousimo et al, 2014). Understanding how diversity in resistance is generated and maintained in natural populations can yield valuable insight into how to deploy durable resistance in crop plants

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Results

Discussion

Conclusion