High-fertility individuals observed in the progeny of low-fertility Nicotiana F1 interspecific hybrid and mechanistic insights into their appearance.

Abstract

Interspecific hybrids with different genomes from their parents often result in hybrid sterility due to meiotic failure. This is a typical example of reproductive isolation that limits interspecific hybridization. Although a few progenies can be obtained in such cases, the inheritance pattern of fertility has not yet been studied in detail. Therefore, using Nicotiana as a model, the fertility of hybrids derived from crosses between species with different genomes was investigated up to the F₃ generation. In the F₂ population, which developed from selfing seeds obtained from the low-fertility F₁ generation, extremely large variation in pollen viability (1.2-82.9%, average 43.2%), fruit set rate (0-100%, average 69.3%), and seed number (16-185, average 63.5) were observed among individuals. In addition, some of the F₃ individuals from F₂ individuals with low fertility were high-fertility. Furthermore, it was suggested that not only pollen viability, but also pistil length and number of ovules may be involved in the variation in fertility. Genome-wide genotyping using GRAS-Di technology revealed that the genomes of high-fertility F₂ individuals had fewer heterozygous genomic regions, leading to a hypothesis regarding the association between the proportion of heterozygous regions in the genome and pollen viability. To our knowledge, this study represents the first experimental observation that high-fertility F₂ individuals can be obtained from interspecific F₁ hybrids carrying different genomes with extremely low fertility without change of ploidy. These findings can be considered basic insights that enhance our understanding of plant speciation and adaptation.