How cucumbers got longer - and why it's a big deal for farming

Cucumbers, a summer staple of salads and sandwiches, are a valuable commercial crop. They also have a less well-known role as valuable model plants which are helping researchers to extend the boundaries of genomic discovery. 

A research collaboration between the John Innes Centre and the Chinese Academy of Agricultural Sciences (CAAS) used an array of experiments and genomic analysis to probe the differences between wild cucumbers and their domestic relatives at a molecular level. 

They targeted the genetics that underpin fruit elongation in domesticated cucumbers which are longer than their stubby, bitter tasting wild relatives.  

Their findings shed light on an increasingly important area of genetics and may allow us to breed bigger, higher yielding crops with much greater precision and variety. 

Much of modern plant breeding targets mutations in DNA sequences which encode proteins, the cellular machines that deliver traits in the field, such as long or short fruits, bitter or sweet flavours, and round or wrinkled seeds.  

But these protein encoding genes only account for a small proportion of the genome. Increasingly, researchers are using modern tools to explore DNA sequences that do not code for proteins. 

Synonymous mutations, previously known as silent mutations, are an example of non-coding regions in the genome that are increasingly attracting the interest of biologists.  

Previous studies have shown that they play a role in cellular functions, but there is little evidence of them shaping biological traits in a multi-cellular organism.  

In this study, which appears in the journal Cell, the researchers investigated how silent mutations might drive traits by altering the structure and function of RNA, a molecule found in cells.  

With the help of a genomic variation map based on cucumber populations, fruit length was identified as a key domestication trait of cucumber. 

The research team then used molecular and genetic analysis to reveal the precise mechanism that leads to cucumber elongation. 

They show that a single synonymous mutation in a gene was a key driver of fruit elongation during cucumber domestication, leading to fruits growing up to 70% longer. 

 Crucially, the mutation does not lead to the production of a protein as would be the case with most agricultural and biologically important traits. Instead, the gene acts on a different molecule, RNA, reshaping it, and repressing production of the protein that in wild cucumber gives the ‘short’ trait.  

“A tiny ‘silent’ change in a cucumber gene - once thought to be innocuous - is the key player in making modern cucumbers longer,” said Dr Yueying Zhang, postdoctoral researcher at the John Innes Centre and first author of the study.  

“Remarkably this silent mutation, long thought to be biologically neutral, rewired RNA regulation and contributed directly to the development of a domesticated trait,” added Dr Zhang. 

The findings provide valuable insights into crop breeding programmes, offering potential ways for engineering traits in the future. This study is especially relevant to traits like fruit size, which are crucial for improving crop yield and reaping commercial benefits for growers. 

The study also paves the way for more research targeting synonymous sites, using precision crop improvement techniques such as gene editing to improve traits in the field across a range of crops. 

This groundbreaking research was a collaborative effort between Professor Yiliang Ding’s group at the John Innes Centre, UK, and teams led by Professor Xueyong Yang at the Institute of Vegetables and Flowers and Academician Sanwen Huang, FRS, President of the Chinese Academy of Agricultural Sciences (CAAS). The study was initiated and led by CAAS, with Professor Ding’s group contributing critical insights into RNA structure and translation regulation. 

Recessive epistasis of a synonymous mutation confers cucumber domestication through epitranscriptomic regulation, appears in Cell.