Patterns of Chromosomal Variation, Homoeologous Exchange, and Their Relationship with Genomic Features in Early Generations of a Synthetic Rice Segmental Allotetraploid

Polyploidization is a driving force in plant evolution. Chromosomal variation often occurs at early generations following polyploid formation due to meiotic pairing irregularity that may compromise segregation fidelity and cause homoeologous exchange (HE). The trends of chromosomal variation and especially factors affecting HE remain to be fully deciphered. Here, by whole-genome resequencing, we performed nuanced analyses of patterns of chromosomal number variation and explored genomic features that affect HE in two early generations of a synthetic rice segmental allotetraploid. We found a wide occurrence of whole-chromosome aneuploidy and, to a lesser extent, also large segment gains/losses in both generations (S2 and S4) of the tetraploids. However, while the number of chromosome gains was similar between S2 and S4, that of losses in S4 was lower than in S2. HEs were abundant across all chromosomes in both generations and showed variable correlations with different genomic features at chromosomal and/or local scales. Contents of genes and transposable elements (TEs) were positively and negatively correlated with HE frequencies, respectively. By dissecting TEs into different classes, retrotransposons were found to be negatively correlated with HE frequency to a stronger extent than DNA transposons, whereas miniature terminal inverted elements (MITEs) showed a strong positive correlation. Local HE frequencies in the tetraploids and homologous recombination (HR) rates in diploids within 1 Mb sliding windows were significantly correlated with each other and showed similar overall distribution profiles. Nonetheless, non-concordant trends between HE and HR rates were found at distal regions in some chromosomes. At local scale, both shared and polymorphic retrotransposons between parents were negatively correlated with HE frequency; in contrast, both shared and polymorphic MITEs showed positive correlations with HE frequency. Our results shed new light on the patterns of chromosomal number variation and reveal genomic features influencing HE frequency in early generations following plant polyploidization.