Overcoming the species hybridization barrier by ploidy manipulation in the genus Oryza

Abstract

In most eudicot and monocot species, interspecific and interploidy crosses generally display abnormalities in the endosperm that are the major cause of a post-zygotic hybridization barrier. In some eudicot species, however, this type of hybridization barrier can be overcome by the manipulation of ploidy levels of one parental species, suggesting that the molecular mechanisms underlying the species hybridization barrier can be circumvented by genome dosage. We previously demonstrated that endosperm barriers in interspecific and interploidy crosses in the genus Oryza involve overlapping but different mechanisms. This result contrasts with those in the genus Arabidopsis, which shows similar outcomes in both interploidy and interspecific crosses. Therefore, we postulated that an exploration of pathways for overcoming the species hybridization barrier in Oryza endosperm, by manipulating the ploidy levels in one parental species, might provide novel insights into molecular mechanisms. We showed that fertile hybrid seeds could be produced by an interspecific cross of female tetraploid Oryza sativa and male diploid Oryza longistaminata. Although the rate of nuclear divisions did not return to normal levels in the hybrid endosperm, the timing of cellularization, nucellus degeneration and the accumulation of storage products were close to normal levels. In addition, the expression patterns of the imprinted gene MADS87 and YUCCA11 were changed when the species barrier was overcome. These results suggest that the regulatory machinery for developmental transitions and imprinted gene expression are likely to play a central role in overcoming species hybridization barriers by genome dosage in the genus Oryza.

A high maternal genome excess causes severe seed abortion leading to ovary abscission in Nicotiana interploidy‐interspecific crosses

“…Coordinated embryo, endosperm, and maternal seed coat development is necessary for normal seed formation. However, seed abortion, a typical postzygotic reproductive barrier preventing seed development or seed germination, is widely observed in interspecific and interploidy crosses (Baek et al, 2016;Coughlan et al, 2020;Oneal et al, 2016;Rebernig et al, 2015;Roth et al, 2018;Scott et al, 1998;Sekine et al, 2013;Tonosaki et al, 2018;). Studies on Arabidopsis, Solanum, Mimulus, and other species have strongly suggested that endosperm developmental failure is the primary cause of seed abortion, as this failure leads to embryo arrest and seed abortion (Hehenberger et al, 2012;Rebernig et al, 2015;Scott et al, 1998;Sekine et al, 2013;Tonosaki et al, 2018;Oneal et al, 2016;Coughlan et al, 2020;Roth et al, 2018).…”

“…In these cases, it has been suggested that the influence of maternal and paternal genomes on endosperm development may not be balanced or that parental species have different EBNs or "effective ploidy," leading to endosperm developmental failure (Baek et al, 2016;Bushell et al, 2003;Coughlan et al, 2020;Ishikawa et al, 2011;Johnston et al, 1980;). The abnormal endosperm development in interspecific crosses between species with the same ploidy level can be bypassed by changing the ploidy of one parental species (Bushell et al, 2003;Johnston and Hanneman, 1982;Lafon-Placette et al, 2017;Tonosaki et al, 2018). Moreover, genome-wide studies on endosperm gene expression have revealed that genomic imprinting is extensively perturbed in failing hybrid endosperm in Solanum, Capsella and several other species (Lafon-Placette et al, 2018;Roth et al, 2019;Tonosaki et al, 2018).…”

“…The abnormal endosperm development in interspecific crosses between species with the same ploidy level can be bypassed by changing the ploidy of one parental species (Bushell et al, 2003;Johnston and Hanneman, 1982;Lafon-Placette et al, 2017;Tonosaki et al, 2018). Moreover, genome-wide studies on endosperm gene expression have revealed that genomic imprinting is extensively perturbed in failing hybrid endosperm in Solanum, Capsella and several other species (Lafon-Placette et al, 2018;Roth et al, 2019;Tonosaki et al, 2018).…”

Interspecific Hybridization for Brassica Crop Improvement

“…Resynthesis as a tool of crop improvement has many benefits. Polyploidy induced during the process of resynthesis can overcome crossing barriers due to endosperm failure in interploidy crosses [93]. The genetic diversity of some Brassica allotetraploid crops is limited due to the few hybridization events that gave rise to these species [12].…”

Functional divergence of two duplicatedFertilization Independent Endospermgenes in rice with respect to seed development

“…As a nutritional supply tissue, the endosperm is indispensable for embryo development. Either delayed or accelerated cellularization can lead to seed failure in interploidy and interspecific hybrids (Walia et al , 2009; Ishikawa et al , 2011; Kradolfer et al , 2013; Tonosaki et al , 2018). Developmental defects in the endosperm will cause embryo abortion, which has been found to occur in many plant species, where it acts as an important reproductive barrier (Chen et al , 2016b).…”