Parental Genome Imbalance Causes Hybrid Seed Lethality as Well as Ovary Abscission in Interspecific and Interploidy Crosses in Nicotiana

Abstract

Enhanced ovary abscission after pollination and hybrid seed lethality result in post-zygotic reproductive isolation in plant interspecific crosses. However, the connection between these barriers remains unclear. Here, we report that an imbalance in parental genomes or endosperm balance number (EBN) causes hybrid seed lethality and ovary abscission in both interspecific and intraspecific-interploidy crosses in the genus Nicotiana. Auxin treatment suppressed ovary abscission, but not hybrid seed lethality, in an interspecific cross between Nicotiana suaveolens and N. tabacum, suggesting that ovary abscission-related genes are located downstream of those involved in hybrid seed lethality. We performed interploidy crosses among N. suaveolens tetraploids, octoploids, and neopolyploids and revealed hybrid seed lethality and ovary abscission in interploid crosses. Furthermore, a higher maternal EBN than paternal EBN caused these barriers, as previously observed in N. suaveolens × N. tabacum crosses. Altogether, these results suggest that maternal excess of EBN causes hybrid seed lethality, which in turn leads to ovary abscission through the same mechanism in both interspecific and interploidy crosses.

Understanding and overcoming hybrid lethality in seed and seedling stages as barriers to hybridization and gene flow

“…Conversely, the paternal genome excess or paternally expressed genes (PEGs) promotes nutrient flow to the embryo and increases seed size and seed set ( Schatlowski and Köhler, 2012 ; Bai and Settles, 2015 ). This is consistent with the endosperm and embryo observation in interploidy hybridizations using parental plants with stepwise changes in EBN ( Scott et al., 1998 ; He et al., 2022 ).…”

“…The two types of hybrid seed lethality are reversed by an increase in ploidy levels of paternal parents. Thus, hybrid seed lethality in Nicotiana is well explained by EBN hypothesis and higher ploidy levels in maternal parents than in paternal parents cause type I or type II seed lethality ( He et al., 2020 ; He et al., 2022 ).…”

“…(2015) ). Abscission is also observed in developing ovaries (immature fruits) in interspecies and interploidy hybridizations in Nicotiana , which exhibit type II hybrid seed lethality ( He et al., 2020 ; He et al., 2022 ). The post-pollination developing fruit or pod abscission has also been reported in other interspecific crosses of the genera Cicer ( Mallikarjuna, 1999 ), Lupinus ( Gupta et al., 1996 ), Phaseolus ( Mok et al., 1978 ), and Vigna ( Barone et al., 1992 ), all of which belong to the Fabaceae family.…”

“…The post-pollination developing fruit or pod abscission has also been reported in other interspecific crosses of the genera Cicer ( Mallikarjuna, 1999 ), Lupinus ( Gupta et al., 1996 ), Phaseolus ( Mok et al., 1978 ), and Vigna ( Barone et al., 1992 ), all of which belong to the Fabaceae family. Studies in Nicotiana have clearly demonstrated that manipulation of parental ploidy levels not only affects hybrid seed lethality (type II, not type I, in the Nicotiana case) but also affects immature fruit abscission in interspecies and interploidy hybridizations ( He et al., 2020 ; He et al., 2022 ). This implies that the parental conflict hypothesis could also be applied to fruit maturation and abscission, which are maternal processes.…”

“…On the other hand, when the ovary was occupied by seeds exhibiting type II hybrid seed lethality, the supply of auxin from seeds or ovary might be insufficient, leading to immature fruit abscission. Although involvement of auxin in immature fruit abscission has been suggested because immature fruit abscission, but not type II hybrid seed lethality, was suppressed by exogenous auxin treatments ( He et al., 2022 ), further studies are needed to validate this hypothesis.…”