The evolutionary gain and loss of plant prickles – sharp pointed epidermal outgrowths – are controlled by a shared genetic program involving cytokinin biosynthesis, researchers report. The study sheds light on the genetic basis of the emergence of similar traits in distantly related organisms and reveals genomic targets for prickle removal for crop improvement. The genetic basis of trait convergence is a central question in evolutionary biology, and the extent to which it is driven by corresponding convergence in the same underlying genetic programs across species isn't fully understood. In plants, prickles convergently evolved in numerous plant lineages, like roses, over the past 400 million years. Despite prickles' broad origins and diverse roles – including herbivore defense, plant competition, water retention, and climbing support – they exhibit marked morphological similarity. Moreover, prickles have been lost or suppressed in numerous other lineages. Thus, according to the authors, prickle formation in plants is an ideal system to study whether repeated origins and losses of the trait rely on the same genetic mechanisms over short and long evolutionary timescales. James Satterlee and colleagues investigated the genetic control of prickles in the genus Solanum, which includes eggplants. Combining classical genetic mapping with chromosome-scale reference genome sequencing, Satterlee et al. performed phylogenetic analysis across a diverse range of eggplants and their wild relatives, including several indigenous African crop species. The authors discovered that some species have independent mutations in a LONELY GUY (LOG)-family gene, called PRICKLESSNESS (PL), affecting the hormone cytokinin. What's more, disruption of PL was found to drive prickle loss in at least 16 instances of prickle loss in both cultivated and wild Solanum species. Mutations in PL homologs were identified in flowering plants like rice and roses, indicating a shared genetic mechanism for prickle loss in species that diverged more than 150 million years ago. Using CRISPR-Cas9 experiments in several species, including desert raisin and tomato, Satterlee et al. found that loss of PL greatly reduces or eliminates prickles without off-target effects. Combined, the findings suggest that this genetic program underlies evolutionary widespread and recurrent instances of plant prickle formation over deep time. In a Perspective, Elizabeth Kellogg discusses the study and its findings in greater detail.
For reporters interested in research integrity issues, lead author Jack Satterlee notes, "As is standard, we have ensured that all data in the paper are available for readers and are committed to sharing all plant materials and lines generated in this work…We also respectfully acknowledge that some of the species studied here are available to us only through many centuries of Indigenous stewardship and non-Western cultivation histories. As a community, we must acknowledge the cultural heritages of the species we study. This, combined with data sharing and collaboration, are critical to ensuring research is honest and benefits communities around the world."
