Small RNA mediates genetic parental conflict in seed endosperm

CAMBRIDGE, MA--When it comes to gene expression in the endosperm of seeds, gene provenance matters. In this specialized tissue, plants actively strive to keep the expression of genes inherited from the mother versus the father in balance, according to Whitehead Institute scientists.

The endosperm, the starchy part of a seed that envelopes and nourishes the developing embryo, comprises two-thirds of the calories in a typical human diet. It is the meat of a coconut and the sweet part of the corn on the cob we eat.  In a paper published online December 19 in the journal Cell Reports, Whitehead Member Mary Gehring, first author and former Gehring graduate student Robert Erdmann, and colleagues reveal that the endosperm is also the site where the plant must actively orchestrate a delicate balance between expression of genes inherited from the mother and those of the father.  If this critical balance errs toward one parent or the other, seeds can be too small or even abort.

Unlike most plant cells, which have two copies of the genome, cells within the endosperm have three copies: one inherited from the father, and two inherited from the mother. This ratio is established when a sperm cell in the fertilizing pollen grain fuses with the central cell associated with the egg cell in a flower’s ovule. Unlike most cells, the central cell has two nuclei, so when the sperm’s nucleus merges with the central cell, the resulting endosperm is triploid.

 The 2-to-1 ratio of maternal to paternal gene expression is crucial, and deviation can have dire consequences:  If maternal gene expression is too high, the seeds are too small; if paternal gene expression is too high, the seeds abort. Although plant biologists have known the importance of this ratio for seed viability, the balance was assumed to be passively maintained for the majority of genes.  Previously, Gehring determined that a subset of genes expressed in the endosperm are imprinted—their expression is inherited from their parent. But what about the remaining majority of the genome?

Now Gehring and colleagues have discovered a role for small RNAs—snippets of RNA that interfere with and can reduce gene expression—in actively maintaining this 2-to-1 balance in those genes that are not imprinted.  This the first time scientists have documented small RNAs maintaining such a ratio. Using Arabadopsis thaliana and Arabadopsis lyrata plants, Gehring and her lab determined that these small RNAs tamp down the expression of maternally inherited genes. When the enzyme that creates the small RNAs is mutated, fewer small RNAs are produced, and the plant’s carefully balanced gene expression is thrown off. The resulting seeds have excessive maternal gene expression. To understand the significance of this elevated maternal gene expression, Satyaki Rajavasireddy, a postdoctoral researcher in Gehring’s lab and an author of the Cell Reports paper, turned to plants with seeds that abort  because they have additional copies of paternal genes. When these plants with extra paternal DNA had their small-RNA-producing enzyme mutated, the outcome was striking: The seeds were rescued and developed to maturity.

Although the research analyzed this phenomenon in A. thaliana and A. lyrata, Gehring expects it to be a widespread manifestation of the tug-of-war between maternal and paternal genetic contributions.

“Maintaining this maternal/paternal balance is crucial for seed development, including in crop plants,” says Gehring, who is also an associate professor of biology at Massachusetts Institute of Technology.  “We’ve looked at two species that are separated by 10 million years of evolution, and I anticipate we will find this mechanism in other species as well.”

This work was supported by the National Science Foundation (NSF CAREER grant 1453459).

* * *

Mary Gehring's primary affiliation is with Whitehead Institute for Biomedical Research, where her laboratory is located and all her research is conducted. She is also an associate professor of biology at Massachusetts Institute of Technology.

* * *

Erdmann, R. et al. “A small RNA pathway mediates allelic dosage in endosperm." Cell Reports, online December 19, 2017.