Parental conflict in plants: Maternal factors silence paternal genes

May 31, 2011
This is a young plant embryo (8-cell stage) in a developing seed of Arabidopsis thaliana (thale cress). At this stage maternal gene activity predominates, while paternal genes will get activated gradually as embryogenesis proceeds. Credit: Michael T. Raissig, Institute of Plant Biology

In flowering plants, the beginning of embryogenesis is almost exclusively governed by maternal gene activity. Maternal factors regulate the development of the embryo and silence paternal genes during early stages of development. This finding – obtained using next generation sequencing technology – was reported by an international team of researchers including plant geneticists from the University of Zurich. This newly uncovered mechanism may be involved in the maintenance of species boundaries and could play an important role in the development of novel crop varieties.

Mother and father each contribute one half of the genetic information to their offspring. Thus, it was thought that both parents contribute equally to the development of the next generation. Indeed, this holds true for late stages of in plants, but early on, things are quite different: during the earliest phase of embryo development - from the fertilized egg to the globular stage - predominantly the maternal are active. This phase of development is controlled largely by maternal factors, which actively repress or silence the genes inherited from the father. This surprising finding was recently published in the renowned American journal Cell, by an international team of scientists led by plant geneticists from the Universities of Zurich and Montpellier.

Silenced Paternal Genes

For their analysis, the Zürich scientists crossed two genetically distinguishable races of the model plant Arabidopsis thaliana (tale cress) and analyzed the relative contributions of the parental genomes shortly after the first division of the fertilized egg. Such molecular genetic analyses of plant embryos at very early stages are technically challenging, which explains why up to now researchers resorted to studying embryos at later stages. But Ueli Grossniklaus, Professor for Plant Developmental Genetics at University of Zurich, has a marked preference for tackling experimentally challenging problems, including the study of gametes and very young embryos that are hard to obtain. Using "Next Generation Sequencing", a novel and powerful technology, Grossniklaus and colleagues were able to show that in an early phase of plant embryo development, predominantly maternal genes are active. Via small ribonucleic acid molecules (siRNAs), the maternal genome controls paternal genes to ensure that, initially, most remain inactive. In the course of development, are sucessively activated, which also requires the activity of maternal factors. This finding is surprising because it contradicts earlier findings, which suggested that these siRNAs have a specifc role in preventing "jumping genes" (transposons) to move within the genome.

The development of plant embryos (2-4 cell stage, left) in the thale cress (Arabidopsis thaliana) is predominantly governed by maternal genomic information, while later on (globular stage, right) both maternal and paternal gene expression is required to complete development. Credit: Michael T. Raissig, Institute of Plant Biology, UZH

According to Grossniklaus, the transient silencing of the paternal contribution during early development of the offspring is in the mother plant's best interest: the mother invests considerable resources into the formation of seeds. Before making this investment, the mother verifies the paternal contribution to the progeny for compatibility with her own genome. If the father's genome is too divergent from her own, e.g., originating from a different species, the embryo will die. In fact, the two parental plants have opposing interests with regard to their offspring. The pollen-donating father is interested in maximizing transfer of resources from the mother to the offspring. By contrast, the mother plant aims at optimizing the match with the fathers genome in order to prevent a waste of resources. „We are dealing with a classical parental conflict", Ueli Grossniklaus summarizes the opposing interests.

Maternal Control May Ensure the Maintenance of Species Boundaries

Maternally active genes direct and control early . Genetic incompatibility will cause embryos to abort, such that fertilization with pollen from other plant species is not successful. Therefore, the mechanism unraveled by Grossniklaus and colleagues may play an important role in the maintenance of species barriers. This may also explain why attempts to cross crop plants with their wild relatives, e.g., to transfer disease-resistance genes present in wild relatives to crops, often fail early in embryogenesis. A genetic divergence between the parents that is too large may be recognized by this novel mechanism, leading to embryo abortion. Commercial crop breeders will thus be interested in finding out how the maternal control of early plant embryo development can be circumvented in their breeding programs.

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