Mechanisms driving endosperm-based hybrid incompatibilities: insights from hybrid monkeyflowers

Abstract

Angiosperm endosperm requires genomic and epigenomic interactions between maternal and paternal genomes for proper seed development. Genomic imprinting, an epigenetic phenomenon where the expression of certain genes is predominantly contributed by one parent, is an essential part of this process and unique to endosperm. Perturbation of imprinting can be fatal to developing seeds, and can be caused by interspecific or interploidy hybridization. However, underlying mechanisms driving these endosperm-based hybridization barriers are not well understood or described. Here we investigate the consequences of genomic imprinting in a naturally occurring interploidy and interspecies hybrid between the diploid, Mimulus guttatus, and the allotetraploid (with two subgenomes), M. luteus (Phrymaceae). We find that the two parental species differ in patterns of DNA methylation, gene expression, and imprinting. Hybrid crosses in both directions, which suffer from endosperm abnormalities and decreased germination rates, display altered methylation patterns compared to parent endosperm. Furthermore, imprinting and expression patterns appear perturbed in hybrid endosperm, where we observe global expression dominance of each of the two M. luteus subgenomes, which share similar expression patterns, over the M. guttatus genome, regardless of crossing direction. We suggest that epigenetic repatterning within the hybrid may drive global shifts in expression patterns and be the result of diverged epigenetic/regulatory landscapes between parental genomes. This may either establish or exacerbate dosage-based epistatic incompatibilities between the specific imprinting patterns that have diverged between parental species, thus driving potentially rapid endosperm-based hybridization barriers.

Effect of Whole-Genome Duplication on the Evolutionary Rescue of Sterile Hybrid Monkeyflowers

“…luteus is the maternal parent produces more viable hybrids (46%) than the opposite cross (0.3%). The asymmetry in hybrid formation and its response to the ploidy level of the parents suggests that inviability in hybrid seeds is mediated by parental conflict resulting in endosperm development failure ( Lafon-Placette and Kohler, 2014 ; Kinser et al., 2018 ; Coughlan et al., 2020 ). The inter-ploidy barrier between M .…”

Developmental Analysis of Mimulus Seed Transcriptomes Reveals Functional Gene Expression Clusters and Four Imprinted, Endosperm-Expressed Genes

“…In general, surveys of imprinted genes have found little overlap in imprinting status of loci between closely related (Wolff et al, 2011) or distantly related taxa (Luo et al, 2011;Waters et al, 2013;Yoshida et al, 2018), however, some loci are imprinted in several different species. Here we report the first validated imprinted genes in M. guttatus [(but see (Kinser et al, 2018)]. We found that all four of our validated paternally imprinted genes (PEGs) have homologues that are imprinted in other species, including maize, sorghum, and rice ( Table 2).…”

“…Disruption in the allelic dosage of paternally and maternally imprinted genes in endosperm can lead to dysfunctional endosperm development and ultimately, seed abortion, and is associated with hybrid seed failure (Haig and Westoby, 1989;Haig and Westoby, 1991;Scott et al, 1998;Kinser et al, 2018). Postzygotic isolation via such hybrid seed inviability is widespread in Solanum (Baek et al, 2016), and imprinted loci have been implicated in this process (Florez-Rueda et al, 2016;Roth et al, 2018;Roth et al, 2019).…”

“…Second, because hybrid seed inviability is a common outcome of hybridization and may be a major cause of speciation in plants, including Mimulus, characterizing the transcriptional dynamics of normally developing seeds will provide context for future studies on gene expression changes associated with hybrid seed lethality. Imprinted loci may play key roles in the proper development of endosperm (Grossniklaus et al, 1998) and divergence in the imprinting status of genes has been linked to the rapid emergence of reproductive barriers between even closely related species (Florez-Rueda et al, 2016;Lafon-Placette et al, 2018) including Mimulus (Kinser et al, 2018). Thus, although our study design prohibits a systematic screening for imprinted loci, we examine our data for genes exhibiting paternally imprinted expression in endosperm, as such genes have been implicated in the emergence of hybrid seed inviability.…”

“…We identify genes whose expression exhibits significant temporal changes associated with key developmental shifts and characterize their patterns of co-expression and biological functions using K-means clustering and gene ontology enrichment analyses. We also identify and validate four genes (ATRX5, MBD13, DnaJ, BGAL11) that are paternally imprinted and whose homologues are imprinted in other plants, but which are not linked to hybrid endosperm failure in Mimulus (Kinser et al, 2018) or other taxa (Hatorangan et al, 2016;Florez-Rueda et al, 2016;Lafon-Placette et al, 2018). Our study represents an important first step in illustrating the gene regulatory dynamics of Mimulus seeds, is the first to identify and validate genes with imprinted endosperm expression in Mimulus guttatus, and will inform future studies on the genetic causes of seed failure in this model system.…”