Dissection of two major components of the post‐zygotic hybridization barrier in rice endosperm

Abstract

SUMMARYA post-zygotic hybridization barrier is often observed in the endosperm of seeds produced by interspecific or interploidy crosses. In Arabidopsis thaliana, for example, hybrid endosperm from both types of cross shows altered timing of cellularization and an altered rate of nuclear divisions. Therefore, it has been proposed that interspecific and interploidy crosses share common molecular mechanisms for establishment of an effective species barrier. However, these two types of hybridization barrier may be initiated by different intrinsic cues: the interspecific cross barrier arises after hybridization of genomes with differences in DNA sequences, while the interploidy cross barrier arises after hybridization of genomes with the same DNA sequences but differences in ploidy levels. In this study, we performed interploidy crosses to identify components of the post-hybridization barrier in the endosperm of rice. We performed an intra-cultivar cross of autotetraploid (4n) 3 diploid (2n) rice, and found precocious cellularization and a decreased rate of nuclear division in the syncytial endosperm. By contrast, seeds from the reciprocal cross showed delayed cellularization and an increased rate of nuclear division. This differential effect on nuclear division rates contrasts with the outcome of rice interspecific crosses, which were previously shown to have altered timing of cellularization without any change in nuclear division rates. Thus, we propose that the post-zygotic hybridization barrier in rice endosperm has two separable components, namely control of the timing of cellularization and control of the nuclear division rates in the syncytial stage of endosperm development.

Endosperm-based hybridization barriers explain the pattern of gene flow between Arabidopsis lyrata and Arabidopsis arenosa in Central Europe

“…Interploidy hybridizations disrupt the 2:1 ratio in the endosperm, leading to asymmetric endosperm developmental failure depending on the direction of hybridization. Increased ploidy of the paternal parent causes delayed or failed endosperm cellularization, whereas increased maternal ploidy induces precocious endosperm cellularization (29)(30)(31). Endosperm cellularization is a major developmental transition that, if impaired, leads to embryo arrest and seed lethality (32)(33)(34).…”

Heat stress yields a unique MADS box transcription factor in determining seed size and thermal sensitivity

“…Typically, in rice, cellularization is initiated 48 h after fertilization (HAF) and the endosperm is fully cellularized by 96 HAF (Ishikawa et al, 2011;Folsom et al, 2014). Either precocious or delayed syncytium/ cellularization transition in endosperm can cause abnormal rice seeds and possibly lead to seed abortion (Ishikawa et al, 2011;Sekine et al, 2013).…”

“…The expression of OsMADS87 is specific to the syncytial stage and is suppressed during endosperm cellularization (Ishikawa et al, 2011;Sekine et al, 2013). More pertinently, the expression of OsMADS87 shows temperature sensitivity and is negatively associated with an increased expression of OsFIE1, the only PRC2 complex member exhibiting thermal sensitivity in developing rice seeds (Folsom et al, 2014).…”

Ectopic application of the repressive histone modification H3K9me2 establishes post-zygotic reproductive isolation inArabidopsis thaliana

“…While hybridizations of maternal plants with pollen donors of increased ploidy delay endosperm cellularization, the reciprocal hybridization causes precocious endosperm cellularization (Scott et al 1998;Lafon-Placette and Köhler 2016). Interspecies hybridizations cause similar effects on endosperm cellularization (Woodell and Valentine 1961;Ishikawa et al 2010;Sekine et al 2013;Rebernig et al 2015;Lafon-Placette et al 2017), suggesting that the genes underpinning this hybridization barrier are dosage-sensitive genes (Birchler et al 2001;Birchler and Veitia 2012). Imprinted genes are expressed predominantly from one of the parental genomes and as a consequence of their monoallelic expression, which is predicted to be dosage-sensitive (Bartolomei and Ferguson-Smith 2011;Patten et al 2014).…”