The Zygotic Transition from Gametes By Single Cell Transcriptomics

Plant reproduction involves the fusion of two highly differentiated gametic cells, an egg cell and a sperm cell, to generate the zygote, a single totipotent cell that will regenerate a new plant. The transition from fertilized egg to autonomous embryo requires extensive changes at the genomic level, including reprogramming of the chromatin, activation of zygotic genes, and removal of maternally-supplied RNA. We have investigated the dynamics of this transition in rice by transcriptome characterization of individual male and female gametes, and isolated time-staged zygotes.  The transcriptomes of the gametes, i.e. the egg and the sperm cell reveal major differences in expression of genes regulating epigenetic modifications and in the RNAi pathways, suggesting differential silencing of genes and transposons in the two germlines.  Although studies in Arabidopsis have proposed delayed activation of the paternal genome as a feature of plant embryogenesis, high expression of genes promoting active chromatin configurations in the rice sperm cell suggests that the paternal genome is ready for activation.  Preliminary analysis of time-staged zygotes indicates that partial activation of the zygotic genome and loss of maternal transcripts takes place prior to the division of the unicellular zygote.  We conclude that flowering plants, in contrast to animals, initiate the zygotic transition during the earliest cell cycle after fertilization.  Further characterization of isolated zygotes, currently in progress, should help elucidate the nature of the genetic and epigenetic factors promoting this fundamental transition in the plant life cycle.