Evolutionary genomics of two diploid goat grass species belonging to the section Sitopsis of Aegilops, Aegilops longissima, and Aegilops sharonensis.

Aegilops longissima and Ae. sharonensis, being classified into the Sitopsis section of genus Aegilops, are distinct species both taxonomically and ecologically. Nevertheless, earlier observations indicate that the two species are not reproductively isolated to full extent and can inter-bred upon secondary contact. However, the genomic underpinnings of the morpho-ecological differentiation between the two foci species remained unexplored. Here, we resequenced 31 representative accessions of the two species and conducted in-depth comparative genomic analyses. We demonstrate recurrent and ongoing natural hybridizations between Ae. longissima and Ae. sharonensis, and depict features of genome composition of the resultant hybrids at both individual and population levels. We also delineate genomic regions and candidate genes potentially underpinning the differential morphological and edaphic adaptations of the two species. Intriguingly, a binary morphology was observed in the hybrids, suggesting existence of highly diverged genomic regions that remain uneroded by the admixtures. Together, our results provide new insights into the molding effects of interspecific hybridization on genome composition and mechanisms preventing merge of the two species.

Genome shock in a synthetic allotetraploid wheat invokes subgenome-partitioned gene regulation, meiotic instability, and karyotype variation.

It is becoming increasingly evident that interspecific hybridization at the homoploid level or coupled with whole-genome duplication (i.e. allopolyploidization) has played a major role in biological evolution. However, the direct impacts of hybridization and allopolyploidization on genome structure and function, phenotype, and fitness remains to be fully understood. Synthetic hybrids and allopolyploids are trackable experimental systems that can be used to address this issue. In this study, we resynthesized a pair of reciprocal F1 hybrids and corresponding reciprocal allotetraploids using the two diploid progenitor species of bread wheat (Triticum aestivum, BBAADD), namely T. urartu (AA) and Aegilops tauschii (DD). By comparing phenotypes related to growth, development, and fitness, and by analysing genome expression in both hybrids and allotetraploids in relation to the parents, we found that the types and trends of karyotype variation in the immediately formed allotetraploids were correlated with both instability of meiosis and chromosome- and subgenome-biased expression. We determined clear advantages of allotetraploids over diploid F1 hybrids in several morphological traits including fitness that mirrored the tissue- and developmental stage-dependent subgenome-partitioning of the allotetraploids. The allotetraploids were meiotically unstable primarily due to homoeologous pairing that varied dramatically among the chromosomes. Nonetheless, the manifestation of organismal karyotype variation and the occurrence of meiotic irregularity were not concordant, suggesting a role of functional constraints probably imposed by subgenome- and chromosome-biased gene expression. Our results provide new insights into the direct impacts and consequences of hybridization and allopolyploidization that are relevant to evolution and likely to be informative for future crop improvement approaches using synthetic polyploids.

Developmental Instability and Gene Dysregulation in an Extracted Tetraploid from Hexaploid Wheat.

The BBAA subgenomes of hexaploid common wheat can be 'extracted' to constitute a viable and self-reproducing novel tetraploid wheat, termed extracted tetraploid wheat (ETW). Prior studies have shown ETW manifesting phenotypic abnormalities and alteration in gene expression and epigenetic modifications. No population level investigation has been conducted, leaving the issue unclear regarding whether developmental stability, an essential property evolved in all natural organisms, might have been undermined in ETW. Here, we measured variations in five morphological traits and somatic chromosomal stability in populations of ETW and of its hexaploid donor, a resynthesized hexaploid and a natural tetraploid wheat. We observed phenotypic defects in ETW. Meanwhile, we documented much greater within-population variations in ETW than in the other wheat genotypes, most probably due to disrupted developmental stability in ETW. Also, somatic structural chromosome variations were detected only in ETW. Comparative transcriptome analyses indicated that the disrupted developmental stability of ETW is likely linked to massive dysregulation of genome-wide gene expression rather than to genetic mutations. Population network analysis of gene expression implicated intrinsic connectivity among the variable traits, while gene set enrichment analysis provided possible links between dysregulated gene expression and interlaced trait variation.