Centuries ago, ancient networks of the Silk Road facilitated political and economic openness between nations of Eurasia. This network also opened pathways for genetic exchange that shaped one of the world’s most popular fruits: the apple.

Silk Road travelers, trading their goods and ideas, brought with them hitchhiking apple seeds, discarded from the choicest fruit pulled from wild trees. This early selection would eventually lead to the 7,500 varieties of apple that exist today.

Cornell-affiliated Boyce Thompson Institute (BTI) researchers have been excavating mysteries of the apple’s evolutionary history, and an Aug. 15 publication in Nature Communications reveals insights into the genetic exchange that brought us today’s domesticated apple, Malus domestica.

In collaboration with scientists from Cornell University and Shandong Agricultural University in China, the researchers sequenced and compared the genomes of 117 diverse apple accessions representing 24 species, from North America, Europe, and East and Central Asia.

A tale of two roads

Previous studies have shown that the common apple, Malus domestica, arose from the Central Asian wild apple, Malus sieversii, with contributions from crabapples along the Silk Road as it was brought west to Europe.

The results of this new study have provided a much more comprehensive map of apple’s evolutionary history. “We narrowed down the origin of domesticated apple from very broad Central Asia to Kazakhstan area west of Tian Shan Mountain,” said Zhangjun Fei, BTI professor and lead author of this study.

Additionally, the authors discovered the first domesticated apple had also traveled east, hybridizing with wild apples to yield the ancestors of soft, dessert apples cultivated in China today.

“We pointed out two major evolutionary routes, west and east, along the Silk Road, revealing fruit quality changes in every step along the way,” Fei said.

The sour (but firm) side of the story

As the apple traveled west along the Silk Road in the hands of travelers, trees grew from dropped seeds and crossed with sour wild crabapples. The authors found that the European crabapple, Malus sylvestris contributed so extensively to the apple’s genome that the modern apple is more similar to this sour crabapple than to the Kazakhstani ancestor, M. sieversii.

“The [Malus sieversii] fruits are generally much larger than other wild apples. They are also soft and have a very plain flavor that people don’t like much,” said Yang Bai, a postdoctoral scientist at BTI.

The hybridization between ancient cultivated apples and M. sylvestris, followed by extensive human selection, produced larger apples that are fuller in flavor, crispier and firmer, giving them a longer shelf life.

Bai explained, “The modern domesticated apples have higher and well-balanced sugar and organic acid contents. That is how the apple started to become a popular and favored fruit.”

A sizeable discovery with big potential

In most cases of fruit domestication, the wild ancestor has tiny fruit that was shaped into its large, nutritious cultivated counterpart through centuries of selection. For example, the domesticated tomato is at least 100 times larger than its wild relatives.

“This is not quite the case for apple,” Bai said. “Its domestication started with a medium to large-sized fruit.”

Comparing the different apple genomes, the researchers found evidence supporting two evolutionary steps contributing to apple’s size increase – one before and one after domestication.

The large size of wild M. sieversii gave it an advantage. Having already evolved to a suitable size before cultivation, it was more attractive to growers who would not need to spend much effort selecting for larger fruits.

Such a lack of size selection also means that the genes responsible for size increase still retain variability with potential for future selection. The researchers identified several size-associated genetic markers, which is great news for breeders who want to further increase the apple’s girth.

“The genomic regions and candidate genes under human selection for a certain trait identified in this study will be very helpful and inspiring to breeders working on the same trait,” said Fei, who expects the results from this study will, “improve speed and accuracy of ‘marker-assisted selection’ in apple.”

By analyzing a diverse collection of representative apple genomes, Fei’s group has distinguished important genetic markers that will aid breeders in their quest for better apples – be it for disease resistance, shelf-life, taste or even size.

The research was supported by the National Natural Science Foundation of China, the Special Fund for Agro-Scientific Research in the Public Interest of China, and the U.S. National Science Foundation.

Alexa M. Schmitz is a communications associate at the Boyce Thompson Institute.