The adults are talking: parental genetic conflict in seed development

In a new paper from the lab of Whitehead Institute Member Mary Gehring, researchers examined the mechanisms by which genetic parental conflict impacts which genes are expressed in a tissue called the endosperm, which plays a similar role to the placenta in humans.

Developing plant embryos depend on the endosperm for their nutrients — and so do people. “Endosperm provides 60 percent of the world's nutrition in one way or another,” said Satyaki Rajvasireddy, the first author of the new paper. “If you're eating popcorn, if you’re eating rice or cereal, if you're drinking beer, you’re really consuming endosperm.”

Epigenetic pathways play key roles in regulating gene expression in the endosperm, meaning that each cell controls which genes are expressed and which are silenced through strategies that do not change the sequence of its DNA. Gehring and Satyaki had long been curious about how the plants choose which genes to express in this tissue. Their new research, published online April 7 in PLOS Biology, reveals the role of RNA Polymerase IV, or RNA Pol IV for short, as a tool used by both mother and father plant genomes to competitively influence expression of endosperm genes. 

A ‘selfish’ struggle

Many plant species are polyandrous — the eggs carried in a mother’s flower can be fertilized by sperm from different fathers. This creates a perfect setup for conflict. 

Because there are multiple fathers involved, all of which could have slightly different adaptations, it is in the best interest of the mother plant to equally distribute her resources to all offspring. That way, she has the best chance of successfully passing on her genetic material in a variety of conditions. “In terms of her fitness, the more viable seeds she makes, the more of her progeny are produced,” Gehring said. 

For the fathers, the calculus is slightly different. Each father has a better chance of passing on his DNA if his seed becomes a nutrient hog. “It's in the interest of the paternal genome to influence nutrient resource transfer, such that their seed gets as many resources from the mother as possible,” Gehring said. 

That’s where the endosperm, which is responsible for nutrient transfer, emerges as a perfect stage for this conflict to play out. In each seed produced (and therefore in the endosperm) there are both maternal and paternal genomes. As the endosperm tissue is forming, the expression of different genes might benefit either the mother or father’s interest.

Tools of the conflict

In previous papers starting in 2017, Gehring and collaborators, working on a well-studied relative of Canola and mustard called Arabidopsis thaliana, discovered that the outcome of losing one specific RNA pathway — responsible for creating small RNAs, which work with other molecular players to methylate, or silence, genes —  was different depending on whether the mother’s or father’s copy of the key pathway genes were expressed. 

The genes affected by the small RNA pathway influenced various aspects of seed development, including, in some cases, seed abortion. For example, when researchers increased the ratio of paternal to maternal genomes in the endosperm under normal conditions, the seeds aborted before maturity. But when they disrupted the small RNA pathway, the seeds were suddenly viable. “That initial work suggested that this pathway that makes small RNAs is important for controlling the relative contribution of maternal and paternal genomes to endosperm gene expression,” Gehring said. 

This time around, Satyaki and Gehring wanted to perform similar experiments in plants that had the normal ratio of mother to father genomes. “In this paper, we essentially removed either the mother's or father's copy of the small RNA pathway and we looked at gene expression,” Satyaki said. “We also removed both copies of the small RNA pathway and looked at what was happening to small RNAs.”

When they removed the maternal copy of RNA Pol IV, several hundred genes were expressed in higher or lower quantities than normal. The difference was less extreme when they removed the father’s copy — only a few dozen genes were affected. In some cases, RNA Pol IV from the mother and father had opposite affects on the expression of specific genes — for example, one parent’s RNA Pol IV would promote expression of a gene in the endosperm, while the other would repress it.

When both parents’ copies of RNA Pol IV were removed, the antagonistic effects seemed to cancel each other out somewhat, and fewer genes were misregulated than when just the father’s copy was present.

These parentally influenced differences in gene expression could have various effects on how nutrients are divided among seedlings. For example, as the researchers previously found, the small RNA pathway that includes Pol IV affects genes essential in aborting seeds, but the mother and father have different interests in how many seeds to keep (keeping more seeds benefits the mother, but many seeds means each receives less nutrients, which is detrimental to the interests of the multiple fathers). 

Interestingly, RNA Pol IV, the same tool that drives these parental conflicts, may also be key in resolving the conflict. The parental conflict can be resolved if gene expression can be regulated at a level that is tolerable to both parents. Because both parental genomes use Pol IV as a regulatory tool, it may also serve as a system through which to negotiate the optimal gene expression levels.

“We're only ever looking at a snapshot of evolution, but it may be that [this interaction] is part of a stalemate, or some agreement has been reached that is acceptable to both maternal and paternal sides,” Gehring said. “Perhaps by using the same molecule, both sides become dependent on it and neither can give up that weapon. So it may be that this is the evolutionary stable strategy that has been reached."