Recurrent evolution of cryptic triploids in cultivated enset increases yield

Abstract

The high incidence of polyploidy in crops could be explained if domestication involved the selection of polyploids (cytotypes with more than two sets of chromosomes). Ancestral horticulture could have targeted desirable traits including yield, robustness to stress and to disease, rather than requiring knowledge of polyploidy itself. We find evidence for this process underway in enset (Ensete ventricosum, Musaceae) - a highly resilient crop constituting the main staple for over 20 million people in Ethiopia, which is clonally propagated and cultivated for its starch-rich corm and pseudostem. Prior to this study, enset was thought to be exclusively diploid (2n = 2x = 18). Using a newly-assembled chromosome-scale reference genome, and sequence data from 723 wild and domesticated enset individuals from southwestern Ethiopia, we demonstrate that around 20% of cultivated enset clones are triploid. We show that triploidy has arisen multiple times independently, that the triploid lineages have been given distinct landrace names, and planted disproportionately frequently. As well as providing evidence for enduring selection on triploids, our results reveal valuable genetic diversity captured by these triploid lines. They represent key resources for scientifically directed breeding of this major crop in the Ethiopian agrosystem, and could improve food security in sub-saharan Africa. Author SummaryDuplication of a species entire genome (polyploidization) plays an important part in evolution. Domestication may have favoured polyploid crops including wheat, coffee, potato, cotton, strawberry, and banana. It has been proposed that this trend is explained by the selection of advantageous traits exhibited by polyploids compared to their relatives with unduplicated genomes. These desirable traits include bigger fruits, seeds or other edible organs, and better tolerance to stress and disease. We unexpectedly find that a large proportion of cultivated enset lines have three copies of their genome (triploidy) instead of two (diploid). Enset is a highly resilient crop in the banana family; its stem and leaves are processed to provide one of the main food sources for over 20 million people in Ethiopia. Prior to our study, enset was thought to be exclusively diploid. Farmers use landrace names that distinguish diploids from triploids without having this new genetic information, showing the differences between them are recognised and given importance. Triploids were planted disproportionately and appear to grow faster, suggesting they are being selected for their higher productivity. These triploid ensets are an important genetic resource for scientifically directed breeding of new varieties, which could improve food security in sub-saharan Africa.