Genetic differences between Arabidopsis thaliana accessions underlie the plant’s extensive phenotypic variation, and until now these have been interpreted largely in the context of the annotated reference accession Col-0. Here we report the sequencing, assembly and annotation of the genomes of 18 natural A. thaliana accessions, and their transcriptomes. When assessed on the basis of the reference annotation, one-third of protein-coding genes are predicted to be disrupted in at least one accession. However, re-annotation of each genome revealed that alternative gene models often restore coding potential. Gene expression in seedlings differed for nearly half of expressed genes and was frequently associated with cis variants within 5 kilobases, as were intron retention alternative splicing events. Sequence and expression variation is most pronounced in genes that respond to the biotic environment. Our data further promote evolutionary and functional studies in A. thaliana, especially the MAGIC genetic reference population descended from these accessions.

Identifying natural allelic variation that underlies quantitative trait variation remains a fundamental problem in genetics. Most studies have employed either simple synthetic populations with restricted allelic variation or performed association mapping on a sample of naturally occurring haplotypes. Both of these approaches have some limitations, therefore alternative resources for the genetic dissection of complex traits continue to be sought. Here we describe one such alternative, the Multiparent Advanced Generation Inter-Cross (MAGIC). This approach is expected to improve the precision with which QTL can be mapped, improving the outlook for QTL cloning. Here, we present the first panel of MAGIC lines developed: a set of 527 recombinant inbred lines (RILs) descended from a heterogeneous stock of 19 intermated accessions of the plant Arabidopsis thaliana. These lines and the 19 founders were genotyped with 1,260 single nucleotide polymorphisms and phenotyped for development-related traits. Analytical methods were developed to fine-map quantitative trait loci (QTL) in the MAGIC lines by reconstructing the genome of each line as a mosaic of the founders. We show by simulation that QTL explaining 10% of the phenotypic variance will be detected in most situations with an average mapping error of about 300 kb, and that if the number of lines were doubled the mapping error would be under 200 kb. We also show how the power to detect a QTL and the mapping accuracy vary, depending on QTL location. We demonstrate the utility of this new mapping population by mapping several known QTL with high precision and by finding novel QTL for germination data and bolting time. Our results provide strong support for similar ongoing efforts to produce MAGIC lines in other organisms.

Pathogens can be an important selective agent in plant evolution because they can severely reduce plant fitness and growth. However, the role of pathogen selection on plant evolution depends on the extent of genetic variation for resistance traits and their covariance with host fitness. Although it is usually assumed that resistance traits will covary with plant fitness, this assumption has not been tested rigorously in plant-pathogen interactions. Many plant species are tolerant to herbivores, decoupling the relationship between resistance and fitness. Tolerance to pathogens can reduce selection for resistance and alter the effect of pathogens on plant evolution. In this study, we measured three components of Arabidopsis thaliana resistance (pathogen growth, disease symptoms, and host fitness) to the bacteria Pseudomonas syringae and investigated their covariation to determine the relative importance of resistance and tolerance. We observed extensive quantitative variation in the severity of disease symptoms, the bacterial population size, and the effect of infection on host fitness among 19 accessions of A. thaliana infected with P. syringae. The severity of disease symptoms was strongly and positively correlated with bacterial population size. Although the average fitness of infected plants was smaller than noninfected plants, we found no correlation between the bacterial growth or symptoms expressed by different accessions of A. thaliana and their relative fitness after infection. These results indicate that the accessions studied vary in tolerance to P. syringae, reducing the strength of selection on resistance traits, and that symptoms and bacterial growth are not good predictors of host fitness.

The Red Queen Hypothesis (RQH) explains how pathogens may maintain sexual reproduction in hosts. It assumes that parasites become specialized on common host genotypes, reducing their fitness. Such frequency-dependent selection favors sexual reproduction in host populations. Necessary conditions are that resistance and virulence are genotype specific so that host genotype frequencies respond to changes in pathogen genotype frequencies, and vice versa. Empirical evidence on the genetic basis of disease, variation in resistance and virulence, and patterns of infection in sexual and asexual plants support certain features of the hypothesis. However, gene-for-gene interactions are generally not consistent with the RQH because they do not result in cycling of gene frequencies, unlike a matching allele mechanism. A conclusion of whether the RQH can explain the maintenance of sexual reproduction cannot be reached at present. Nevertheless, the RQH theory has shed light on many aspects of plant/pathogen interactions important for reducing pathogen damage in agricultural systems.