Genes of Both Parental Origins Are Differentially Involved in Early Embryogenesis of a Tobacco Interspecies Hybrid

Abstract

BackgroundIn animals, early embryonic development is largely dependent on maternal transcripts synthesized during gametogenesis. However, in higher plants, the extent of maternal control over zygote development and early embryogenesis is not fully understood yet. Nothing is known about the activity of the parental genomes during seed formation of interspecies hybrids.Methodology/Principal FindingsHere, we report that an interspecies hybridization system between SR1 (Nicotiana tabacum) and Hamayan (N. rustica) has been successfully established. Based on the system we selected 58 genes that have polymorphic sites between SR1 and Hamayan, and analyzed the allele-specific expression of 28 genes in their hybrid zygotes (Hamayan x SR1). Finally the allele-specific expressions of 8 genes in hybrid zygotes were repeatedly confirmed. Among them, 4 genes were of paternal origin, 1 gene was of maternal origin and 3 genes were of biparental origin. These results revealed obvious biparental involvement and differentially contribution of parental-origin genes to zygote development in the interspecies hybrid. We further detected the expression pattern of the genes at 8-celled embryo stage found that the involvement of the parental-origin genes may change at different stages of embryogenesis.Conclusions/SignificanceWe reveal that genes of both parental origins are differentially involved in early embryogenesis of a tobacco interspecies hybrid and functions in a developmental stage-dependent manner. This finding may open a window to seek for the possible molecular mechanism of hybrid vigor.

Environmental Heat and Salt Stress Induce Transgenerational Phenotypic Changes in Arabidopsis thaliana

“…One explanation may be parental imprinting, which leads to different expression of genes depending on whether they are maternally or paternally inherited. Such parental imprinting of genes in the endosperm or embryo has recently been detected in plants [60]-[63], although no effects beyond the embryos have so far been described. Alternatively the maternally inherited mitochondria and chloroplasts could lead to cytoplasmic differences between the two hybrid types.…”

The Maternal-to-Zygotic Transition in Higher Plants

“…Both parents contribute their transcripts (delivered directly or via de novo synthesis from parental alleles in the zygotic genome) to early embryonic development. Several parental-origin genes have been identified in early embryos of different species (Autran et al, 2011;Nodine & Bartel, 2012;Zhang et al, 2011). Work on the contributions made by parental transcripts to embryonic development in higher plants is just beginning; thus, no clear picture of the contributions of parental-origin genes to embryonic development can be drawn at this stage.…”

“…However, the principal limitation of this method is that SSR sites are fewer in number than SNPs. Nevertheless, the method was applied successfully to study activation of parental genomes in interspecific tobacco hybrids (Zhang et al, 2011). Four paternal-origin transcripts and one maternal-origin transcript were identified in hybrid zygotes (Hamayan  SR1) using SSR-based RT-PCR.…”

The Maternal‐to‐Zygotic Transition in Higher Plants

“…An A. thaliana transcriptome analysis indicated that transcripts are produced from both maternal and paternal alleles at a very early embryonic stage (Autran et al 2011; Nodine and Bartel 2012). Paternal originating transcripts could also be detected in hybrid zygotes shortly after fertilization, resulting from a cross between SR1 ( N. tabacum ) and Hamayan ( Nicotiana rustica ) (Zhang et al 2011). An expression profile analysis showed an increased paternal contribution from the 2‐ to 4‐cell stage to the globular embryo stage in A. thaliana (Autran et al 2011).…”