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Maximizing Reproduction: How Flowers Do It

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This past Mother's Day, Americans spent approximately $18.6 billion on gifts for mom. The gift of choice? Flowers -- $2.2 billion dollars worth. It doesn't seem likely that during this flower frenzy many shoppers thought about how many species of flowers exist or how they've become so successful at reproducing. In fact, with about 300 thousand species, flowering plants have come to dominate the planet. Why are flowering plants so successful? Part of the answer is that the inner workings of a flower are as beautiful as their colorful petals.

As in humans, flower sperm and eggs must fuse to create a new organism with novel genetic material from both mother and father. Only one sperm cell must be allowed to fertilize one egg cell or else an unequal contribution from father and mother results, which can cause severe developmental defects. A lot of research has gone into figuring out how animal egg cells "block" multiple sperm from fusing, a process called polyspermy. This block to polyspermy is extremely important and must be tightly regulated because hundreds of sperm cells often compete for a single egg.

Less is known about how flowering plants prevent polyspermy, compared to animals. A major difference between them is that plant sperm, which develops within pollen, are unable to swim. To deliver sperm to the female "egg" cells the pollen grain must grow a specialized structure called a pollen tube, that grows through the female tissue to the right spot. This site of fusion is located within a structure called an ovule and once a pollen tube enters this structure, the tube bursts to release sperm. Each pollen tube only contains the precise number of sperm required for fertilization. So, if each pollen tube only targets one ovule, and each ovule receives only one pollen tube, the ratio of sperm to egg is maintained. However, there are often hundreds of pollen tubes competing for a limited number of ovules. So in flowers the key question is, how do plants prevent too many pollen tubes from entering a single ovule? And what if a sperm is defective?

As a PhD candidate working at Brown University I recently published a paper in Current Biology that brings new insight into this question. In this paper my advisor Mark Johnson, fellow graduate student Alexander Leydon and I showed that flowers have evolved a mechanism to ensure that only one effective pollen tube targets each ovule. Scientists have studied plant reproduction for centuries, but the tools that made this discovery possible have only recently become available. The most important tools are mutants -- plants with defective genes, expressed in sperm, required for sperm and egg fusion. These mutants with "dud" sperm allow us to halt the process of fertilization at this fusion step and analyze what happens when it fails.

Another advance has been the use of fluorescent proteins that allow us to visualize specific components in fertilization. These techniques, developed by the Berger lab in Singapore and the Higashiyama lab in Japan, have enabled scientists all over the world to learn about processes that have long been hidden within floral tissues.

While studying the mutant sperm I noticed something interesting -- multiple "dud" sperm piled up in ovules. If only one pollen tube was allowed to enter each ovule then I should not have seen multiple sperm. I also knew that these sperm were not fusing with the female cells so I made the hypothesis that sperm fusion was required to efficiently block multiple tubes from entering. I developed methods to count how many pollen tubes were entering a single ovule and found that when defective sperm were delivered first, the ovules did not block other tubes from entering. However, when functional sperm were delivered first this block was created. This meant that there was a safeguard in case the first tube contained bum sperm. The ovule wants to block other pollen tubes when functional sperm fuse to the egg, so they don't receive too many sperm, but they don't want to trigger the block when a pollen tube enters in case that tube contains bum sperm. They use successful fusion as their trigger. I was also pleased to find that the Higashiyama lab in Japan independently found similar results (also published in Current Biology).

These papers together really show that flowers have evolved a system in which they can "check" that fertilization was successful so that ovules don't get wasted. This mechanism ensures that the maximum number of seeds develop within each plant, which means maximum reproductive success, which means an abundance of flowers for mom.

The next big question is, what exactly is this block? We hypothesize that it has to be a small molecule that is released rapidly. We are excited about the possibility of applying this work to crop plants, which feed the majority of the world -- the better we understand the fertilization process in plants, the better we will be able to ensure that seed production is robust even in the harshest of conditions. After all, didn't we just thank millions of moms for, among many other things, keeping us fed?