A computational study of genomic rearrangements in plants

In plants, genetic diversity is important for species adaptation in nature and for crop improvement through breeding. For decades, genetic diversity was measured at the nucleotide and gene level. With the abundance of whole genome sequences and chromosome level genome assemblies, the importance of diversity at the genome level - due to rearrangements within genomes - became more obvious given its effect on phenotypic diversity. In genetics research it has become crucial to understand the role of rearrangements in genome evolution and environmental adaptation. Likewise in plant breeding, it is essential to inventory diversity in a wide range of plant varieties for crop improvement as well as to understand how to create new varieties. In this thesis, we touch upon three different genomic rearrangements: recombination, structural variations (SVs) and transposon insertions. We approach them from a fundamental point of view and consider their application to plant breeding. 

As a first step, we studied genomic recombination investigating the position, distribution and genomic patterns of recombination (crossovers) in offspring from interspecific crosses of tomato (chapter 2). Interspecific recombination is used to introgress wild alleles into elite crops, but this is often problematic, among others due to linkage drag. We learned that recombination in tomato occurs preferentially at the distal ends of chromosomes in open chromatin or euchromatin. On a closer look, at the sequence level, the crossover breakpoints showed preferential occurrence near certain sequence motifs and transcription start sites. The next step was to develop a genome-wide predictor for regions prone to recombination. In chapter 3, we developed a classifier based on genomic patterns associated with recombination based on results presented in the second chapter as well as from studies on other plants (such as Arabidopsis, rice and maize). This model not only accurately predicted recombination probability, it also linked new genomic features such as DNA shape to recombination. With the application of this model on different plants we found that particular genomic features were predictive across the plant kingdom. Breeders can use this information to estimate the outcome of breeding programs, prior to the beginning of lengthy crossing experiments. 

Given the known effects of collinearity and SVs on recombination, we turned our focus to SVs. In chapter 4, we identified and inventoried SVs in another model crop, melon, due to its intriguing phenotypic and genetic diversity and cross-pollinating behavior. We revealed genetic diversity in 94 melon lines and 6 wild relatives of melon from an SV point of view and unraveled the history of melon breeding. Due to significant overlap between certain SVs and agronomic traits such as fruit ripening, fragrance, and stress response, we were able to see footprints of selective breeding in melon subspecies. Studying inversions in melon in detail showed that they likely resulted from meiotic recombination events, as their breakpoints share the same sequence motif.

A specific subset of SVs, transposon insertions, were studied next. Transposons can create genetic diversity by moving along the genome (semi)autonomously. For the study of transposons, we returned to tomato, as knowledge on retrotransposons and related phenotypic changes is well established. In chapter 5, we surveyed the activity of retrotransposons in 60 cultivated tomato lines, with a focus on the Rider family of retrotransposons. We created an inventory of transposon insertion polymorphisms and reported the possible effect of insertions on the expression of agronomy-related genes. 

The thesis concludes with a general discussion on the genomic rearrangements studied, insights obtained to further fundamental research, the consequences for plant breeding and what is necessary from the research community to improve the fields of bioinformatics, genetics and plant breeding.