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Species differ in their MAMP perception and immune response, thus suggesting that each MAMP recognition serves a distinct purpose. Here, we examine how MAMP perception and immune response mechanisms may influence herbivory. MAMPs are perceived by the pattern recognition receptors (PRRs) in the cell wall, and stimulation of the PRRs results in the production of immune marker proteins and upregulation of defense genes. Plants use a combination of the MAMP-PRR-interception system, transcription factors (TFs), and epigenetic regulators to respond to MAMPs. We focus on innate immunity, which involves the immune marker proteins, and on epigenetic modification of MAMP-responsive TFs. We distinguish between host defenses that involve MAMP perception and host defenses that involve MAMP-induced transcriptional changes. Finally, we integrate this knowledge with the current literature on and future considerations for future research on MAMP recognition. We conclude with questions to investigate.
The perception and molecular responses to MAMPs from oomycetes, bacteria, and fungi are the focus of this review. We have chosen these MAMPs because (i) they are among the most virulent MAMPs and thus are capable of triggering a robust immune response, (ii) they differ in molecular structure and are recognized by plant specific PRRs, thus acting as a tool to dissect MAMP perception and immune response mechanisms, and (iii) there are some sequence differences in the perception of the MAMPs between different plant species that can be exploited to study the genetic basis of MAMP perception and response.
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Previous research using a comparative genomics approach revealed FLS2 to be under diversifying selection [ 33 ]; however, the reason for this selection is unclear. In order to investigate the evolutionary drivers of FLS2 polymorphism, we performed an in depth phylogenetic analysis. We obtained sequences of the FLS2 genes from 38 accessions of A. thaliana (Arabidopsis lyrata 2 > 1.1, Capsella rubella 2 > 0.1, Arabidopsis halleri 0.1, Arabidopsis longifolia 1, Arabidopsis arenosa 1, Arabidopsis suecica 1, Arabidopsis thaliana Col-0 2, Arabidopsis lyrata ssp. eriantha 2, Arabidopsis suecica 2, Arabidopsis kamchatkensis 2, Arabidopsis littoralis 1, Arabidopsis thaliana Cvi-1, Arabidopsis halleri 0.1, Arabidopsis suecica 1, Arabidopsis mongolica 2). As SGI could not be measured for certain genotypes, particularly those related to Arabidopsis suecica, we were unable to include these accessions in our analysis. We obtained sequence data for the coding part of the kinase domain and two of the eight introns of FLS2 ( S1 Fig ). The tree obtained in the phylogenetic analysis show a high degree of divergence among A. thaliana accessions ( Fig 3 ) with the MAMP sensus specific clade and the accession specific clade (S1 File ). The A. thaliana phylogenetic tree also allowed us to estimate the divergence time between the accessions in the MAMP sensus specific clade. This information was used to assign the origin of the MAMP sensus specific clade to different time periods of speciation. Given that the region analysed in this study is relatively conserved, the placement of the MAMP sensus specific clade in the tree provides a lower bound for the date of speciation of this clade. Based on this lower bound, we estimated that the speciation of this clade occurred at about 90,000 to 150,000 years ago. We also found that intron-1-1 is the oldest intron in FLS2 ( Fig 3 and S1 File ). This intron has been present in all accessions of A. thaliana analysed in this study. In the region of the kinase domain, many amino acid sites ( Fig 4 ) were variable between accessions. The clade-specific amino acid sites show a particular pattern of amino acid variation ( S2 Text ).
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To measure the response of accessions to elf18 or flg22, we first determined a range of concentrations that would trigger substantial seedling growth inhibition. For elf18, this was 5 | 30 ng/ml, while for flg22 it was 300 | 3000 ng/ml. We tested the responses of populations of 186 accessions of A. thaliana to each of the MAMP variants elf18 and flg22 using batch culture. These data were used to test if accessions with similar growth responses to different MAMPs were correlated, or if accessions responded to each of the MAMPs independently. We observed no correlation between the responses to elf18 or flg22 (Pearson’s r: 0.039, P _ 0.59), indicating, consistent with a previous report [ 26 ], that responses to flagellin and EF-Tu in A. thaliana do not evolve redundantly. We then employed a maximum-likelihood association mapping approach to quantify the responses to elf18 or flg22, across all 186 accessions, as well as the responses to the variants of each MAMP. Mapping was performed on an overall correlation matrix of all 186 accessions, and on the correlation matrix conditioned for growth responses to either elf18 or flg22. We note that for mapping, any gene, variant, or combination of both, that is correlated with any of the four variables can be considered, with the caveat that signals, variants and strains present in the test material cannot be detected by any one of these. To achieve this goal we used multiple linear regression, and a Bonferroni-corrected P value of |0.01 (0.05/4), to determine which combinations of genetic variables were statistically significant. For each combination, the mapping output was converted to an odds ratio for binary (sensitive or not) variables, and weighted to apply any biases in the direction of the dependent variable. We then converted these odds ratios into chi-square statistics. This analysis revealed three loci whose responses were highly correlated across treatments, and moderately correlated with response to the respective MAMPs. As these loci had previously been implicated in responses to other MAMPs, we considered them to be novel loci. These loci are components of the so-called PTI, or PAMP-Triggered Immunity, signaling pathway [ 5 ]. Two of these loci are well characterized FLS2 variants, and the third is a MAP kinase kinase kinase (MAP3K). While the genetic architecture of the ELF18 system is understood, similar studies of the FLAG22 system have been limited, and until now, have not yielded evidence of genetic redundancy. Our results in A. thaliana show that the detection of flagellin and EF-Tu evolve largely independently.
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