Paternally expressed imprinted genes associate with hybridization barriers in Capsella

Abstract

Hybrid seed lethality is a widespread type of reproductive barrier among angiosperm taxa that contributes to species divergence by preventing gene flow between natural populations. Besides its ecological importance, it is an important obstacle to plant breeding strategies . Hybrid seed lethality is mostly due to a failure of the nourishing endosperm tissue, resulting in embryo arrest. The cause of this failure is a parental dosage imbalance in the endosperm that can be a consequence of either differences in parental ploidy levels or differences in the 'effective ploidy', also known as the endosperm balance number (EBN). Hybrid seed defects exhibit a parent-of-origin pattern, suggesting that differences in number or expression strength of parent-of-origin-specific imprinted genes underpin, as the primary or the secondary cause, the molecular basis of the EBN. Here, we have tested this concept in the genus Capsella and show that the effective ploidy of three Capsella species correlates with the number and expression level of paternally expressed genes (PEGs). Importantly, the number of PEGs and the effective ploidy decrease with the selfing history of a species: the obligate outbreeder Capsella grandiflora had the highest effective ploidy, followed by the recent selfer Capsella rubella and the ancient selfer Capsella orientalis. PEGs were associated with the presence of transposable elements and their silencing mark, DNA methylation in CHH context (where H denotes any base except C). This suggests that transposable elements have driven the imprintome divergence between Capsella species. Together, we propose that variation in transposable element insertions, the resulting differences in PEG number and divergence in their expression level form one component of the effective ploidy variation between species of different breeding system histories, and, as a consequence, allow the establishment of endosperm-based hybridization barriers.

Intercellular delivery of small RNAs in plant gametes

“…Besides the local role for gamete genome stability control, do gamete-delivered easiRNAs play a role in seed development? Hybrid reproductive barriers are a widespread mechanism that contribute to species divergence during evolution (Lafon-Placette et al, 2018). Hybrid seed lethality is due largely to a failure of the nourishing endosperm tissue, resulting in embryo arrest (Lafon-Placette et al, 2018).…”

“…Hybrid reproductive barriers are a widespread mechanism that contribute to species divergence during evolution (Lafon-Placette et al, 2018). Hybrid seed lethality is due largely to a failure of the nourishing endosperm tissue, resulting in embryo arrest (Lafon-Placette et al, 2018). The cause of this failure is mainly imbalanced dosage levels of the parental genomes (Lafon-Placette et al, 2018).…”

“…Hybrid seed lethality is due largely to a failure of the nourishing endosperm tissue, resulting in embryo arrest (Lafon-Placette et al, 2018). The cause of this failure is mainly imbalanced dosage levels of the parental genomes (Lafon-Placette et al, 2018). The mechanism by which the dosage imbalance of hybridization barriers is maintained has long been puzzling.…”

Patterns of hybrid seed inviability in perennials of theMimulus guttatussp. complex reveal a potential role of parental conflict in reproductive isolation

“…One hypothesis to explain the evolution of 55 early-onset hybrid inviability is that of parental conflict (Trivers 1974;Charnov 1979;56 be caused by either sequence change or duplication of specific genes. Whether parental 106 conflict is responsible for genic changes that contribute to HSI among diploids remains 107 relatively unexplored (but see Lafon-Placette et al 2018). 108…”

Agrobacterium-mediated floral-dip transformation of the obligate outcrosser Capsella grandiflora

“…Thus, these sister species have become important models for understanding the morphological and genomic consequences of the progression from SI to selfing. The loss of SI is associated with differences in floral morphology [18], reproductive imprinting [19], and cis-gene regulation [20,21]. To date, these differences have been examined at the genomic level but not at the functional and genetic levels because C. grandiflora has, to our knowledge, not previously been the subject of studies that require its transformation.…”