Association of Wheat miRNAs with Hybrid Incompatibility in Interspecific Crosses of Triticum and Aegilops
Hybrid Incompatibility in Higher Plants
For successful speciation through allopolyploidization, normal growth and fertility of interspecific hybrids are essential. However, hybrid plants frequently fail to produce a next generation due to lethality and sterility. Such hybrid incompatabilities are considered a postzygotic reproductive barrier, and play important roles in differentiation and establishment of new genealogical lineages in plants. The Dobzhansky-Müller (DM) model simply explains the process for generating genetic incompatibility in hybrids between two diverging lineages (Bomblies and Weigel 2007). This model proposes that reduction of fitness in hybrids generally occurs due to interaction between at least two epistatic loci derived from divergent parents.
The molecular nature of the causal genes for DM-type hybrid incompatibilities, including hybrid sterility and hybrid lethality, was recently elucidated in some plant species (Bomblies and Weigel 2007). A nucleotide binding leucine rich repeat-type disease resistance (R) gene is necessary for induction of hybrid necrosis in some intraspecific crosses of Arabidopsis thaliana L. (Bomblies et al. 2007; Alcázar et al. 2009). The epistatic interaction of RPP1, the NB-LRR-type R gene, and SRF3, a receptor-like protein kinase gene, corresponds to the DM relationship for induction of hybrid necrosis in Arabidopsis (Alcázar et al. 2010). Therefore, it has been postulated that hybrid necrosis is caused by particular alleles of the R locus inducing autoimmune-like responses when interacting epistatically with particular alleles of genes elsewhere in the genome (Bomblies and Weigel 2007). On the other hand, gene duplication followed by reciprocal gene loss sometimes results in DM-type hybrid incompatibilities. Loss or silencing of different copies of a duplicated gene in genealogically separated populations contributes to reduced fitness of F2 progeny derived from F1 hybrids, which functions to accelerate genetic differentiation between the genealogically separated populations (Taylor et al. 2001). In intraspecific hybrids of A. thaliana, arrested embryo development and root growth impairment are induced by a lack of both duplicated gene copies (Bikard et al. 2009). Similarly, pollen sterility is induced by independent disruption of each copy of two paralogs in intersubspecific hybrids between Oryza sativa L. subspecies indica and japonica (Mizuta et al. 2010). These epistatic interactions of the paralogous DM genes result in segregation distortion in the progeny.
Some reproductive barriers in interploidy crosses are established in the endosperm, and parent-of-origin specific gene expression in the endosperm is related to reproductive barriers (Schatlowski and Köhler 2012). A maternally expressed WRKY transcription factor controls hybrid lethality during seed development in interploidy crosses between a tetraploid accession of A. thaliana and a diploid accession of Arabidopsis arenosa L. (Dilkes et al. 2008). Embryo arrest occurs, accompanied by abnormal proliferation of endosperm in interspecific crosses between this tetraploid accession of A. thaliana and diploid accession of A. arenosa, and increased expression of target genes of an imprinted Polycomb group protein gene is observed during seed development in the incompatible crosses (Walia et al. 2009). Therefore, precise expression of imprinted genes in the endosperm plays an important role in successful development and establishment of hybrid seeds, and seed arrest in incompatible crosses is explained by deregulation of the imprinted gene expression during endosperm development (Schatlowski and Köhler 2012). In addition, recent studies have shown association of small RNAs with failure of seed development in Arabidopsis hybrids (Ng et al. 2012). Paternal expression of the ATHILA retrotransposon is related to maternally expressed p4-siRNAs in developing endosperm (Mosher et al. 2009), which is essential for normal seed development in interploidy hybrids of Arabidopsis (Josefsson et al. 2006). Thus, disruption of parental genome balance in interploidy crosses could result in developmental failure of endosperm through imbalanced regulation of siRNA-mediated transcripts (Ng et al. 2012).