The Peaceable Genomes of Pumpkins

Anyone who’s tossed a pumpkin onto the lawn after Halloween to discover vines snaking along the ground the next summer knows how easy it is to grow the plant. Pumpkins have an intriguing history and fascinating genetics.

A Brief History of Pumpkins and Us

Pumpkins arose in South America, about 30 million years ago, as two older species merged.

At first Native Americans sprinkled pumpkin seeds along river and stream banks. Once these early farmers began to cultivate corn, they realized that the broad pumpkin leaves spread on the soil surface kept weeds out and moisture in, enabling the maize roots to anchor the towering plants.

The early Native Americans found many uses for pumpkins. They roasted seeds, ate strips of the succulent orange flesh, added the flowers to soups and stews, ground flour from saved seeds, and used the outsides as bowls.

The pumpkin became a Thanksgiving staple at the second celebration, after the immigrants to the New World had learned about its nutritional value and versatility from the original Americans. The pilgrims devised their own recipes. One favorite was to hollow a pumpkin out and stuff it with eggs, cream, honey, and spices and bury it in hot ashes. Hours later they hauled out the soot-encrusted squash and scooped out the delicious innards. The pilgrims also used pumpkin to make beer, and inverted the fruits and plunked them on heads to guide bowl-like haircuts.

Early explorers brought pumpkin seeds back to Europe and beyond. But Jack O’Lanterns came in the opposite direction, hailing from Ireland, where people carved faces into hefty potatoes and turnips, and from England, where they carved beets. Here’s an intriguing history.

Today most pumpkins are grown in India and China. The word “pumpkin” comes from the Greek Pepõn, for large melon. It’s in genus Cucurbita and in a “tribe” with muskmelons, cucumbers, and watermelons.

Modern pumpkins are of two species. Cucurbita maxima has nutritious, orange flesh with an appealing texture and flavor. C. moschata is known for its resistance to stress, from insect pests to non-biological threats like extreme temperatures. Crossing the species yields the hardy hybrid Shintosa, which has such terrific resistance to pests and stress that growers graft melons and cucumber stems to its seedlings to tap into its superb roots.

Doubling Genomes

Many modern species arose from doubling genomes. Some have even doubled twice, including the genomes of all vertebrates and of pumpkins. An article from 2017 unveiled the genome sequences of the two pumpkin species, from researchers at the Cornell-affiliated Boyce Thompson Institute (BTI) and the National Engineering Research Center for Vegetables in Beijing.

The idea of genome doubling goes back to a 1970 book, Evolution by Gene Duplications, by geneticist Susumu Ohno, which became known as the 2R hypothesis.

The genomes of the ancestors of all flowering plants doubled about 160 million years ago. The grasses are pros at it: the genomes of corn, rice, wheat, and sugarcane doubled some 70 million years ago, those of corn and sugarcane doubling again.

In most cases of genome doubling, over time, genes that duplicated functions were lost, usually from one ancestral genome. Corn, cotton, mustard weed, and some cabbages, and even with our own genomes, have also jettisoned most of one ancestral genome.

A Genetic Tale of Two Pumpkins

Sequencing of the two pumpkin genomes enabled researchers to better pinpoint the times of genome duplication, and to flesh out the genetic characteristics and adaptive traits of each species.

Both species have 20 chromosomes, which represent two “paleo-subgenomes.” The first genome diverged about 31 million years ago and the second between 3.04 and 3.84 million years ago. Geneticists figure this out using genes with known mutation rates coupled with comparisons of chromosome configurations as well as archaeological data.

But the pumpkins are unusual. Since about 3 million years ago, the genomes of the two ancestors from the more recent doubling have peacefully co-existed within the same nucleus, unlike the other double-doublers that have selectively lost most of the contributions of one parent species. This makes pumpkins “paleotetraploid.” (“Ploid” refers to one full set of chromosomes, so paleotetraploid means “old four sets.”) Other genomically peaceable paleotetraploids are wheat and the African clawed frog Xenopus laevis, the model organism on which biologists have worked out many of the details of animal development.

“We were excited to find out that the current two subgenomes in pumpkin largely maintain the chromosome structures of the two progenitors despite sharing the same nucleus for at least 3 million years,” said Shan Wu, first author of the paper and a BTI postdoc.

Drilling down to the details, C. maxima’s genome is about 387 million bases to C. moschata’s 372 million. C. maxima, the tasty one, has 30 disease resistance genes to C. moschata’s 57. And the ultra-resistant hybrid Shintosa has even more.

Each pumpkin genome has about 4 dozen genes that show signs of positive selection – persisting because they provide a reproductive advantage. And more than 40% of each genome consists of repeated sequences, holdovers from the most ancient doubling.

Sequencing the genomes of this favorite fruit will have practical repercussions, such as breeding for resistance to powdery mildew and increased carotenoid levels, making the pumpkin more nutritious.

Said Zhangjun Fei, associate professor at BTI and senior author of the paper, “The high-quality pumpkin genome sequences will lead to more efficient dissection of the genetics underlying important agronomic traits, thus accelerating the breeding process for pumpkin improvement.”

The new insights into the past of pumpkins might also improve the pie that we’ll be eating in a few weeks.

Happy Halloween!

(This article originally appeared for Thanksgiving, 2017.)