Over the span of 400 million years, more than two dozen species of flowering plants – including certain types of roses, eggplants, and Chinese pears – independently evolved to develop prickles. These sharp outgrowths – commonly, but inaccurately, referred to as “thorns” in roses – provide plants with a natural defense against hungry herbivores and can help plants retain water or compete with other plants for resources.
Yet, over a period of at least 150 million years, prickle-less species of many of these plants emerged, much to the benefit of humans who harvested crops of eggplants and other domesticated fruits, vegetables, and ornamental flowers. The loss of prickles occurred independently across several different plant species, leaving scientists to wonder if the initial gain – and later loss – of prickles in many of these plants could be linked to a mutation in the same gene.
To tackle this question, Howard Hughes Medical Institute Investigator Zachary Lippman – a plant geneticist at Cold Spring Harbor Laboratory – led a multinational team of collaborators to identify the mutation, or mutations, that caused these plants to lose their prickles. Their research may also help explain how these plants originally evolved to grow prickles. The group’s work, published in August 2024external link, opens in a new tab and previously shared as a preprintexternal link, opens in a new tab, shows that a specific mutation in what’s known as the LONELY GUY (LOG) gene family drove the independent losses of prickles in at least 16 cultivated and wild species of “spiny eggplants” in the nightshade family – which also includes tomato and potato, although the latter never evolved prickles. Remarkably, the authors found that LOG genes were responsible for the gain and loss of prickles in at least three other plants, including the “thornless rose.”
It all started with a discovery from James Satterlee, a postdoc in Lippman’s lab. Satterlee found that a LOG mutation caused certain species of eggplants to lose their prickles. Then, he and Lippman pondered if the same gene might drive the loss of prickles in other plants.
By digging deeper, the duo aimed to shed new light on convergent evolution: the process by which unrelated species develop the same – often extremely conspicuous – adaptive traits over time, such as when different species are confronted by similar ecological changes.
Traits can evolve within a species through natural selection of mutations that already exist in populations. But, as two or more populations of a species evolve in different ways over a long period of time – a process known as divergence – they can develop into new, different species that are increasingly unlikely to develop the same novel traits, driven by the same genes and genetic changes, as one another. This is because the genetic makeup and development processes of these now-distant relatives are so different.
“The thought has always been that the further you go in terms of evolutionary distance between species, the more the genetic architecture [of each species] has changed, and therefore, the genetic entry points [of their evolutionary changes] must be different,” says Lippman. “But our findings represent a concrete example showing that is not actually always true.”
Lippman and Satterlee worked with many collaborators at Cornell University, Johns Hopkins University, and New Mexico State University, as well as with scientists in Spain, France, Germany, Canada, the United Kingdom, and Israel. Together, the group connected the dots between different species of plants in the nightshade, or Solanaceae, family and proved that mutations in an ancient LOG gene could control the gain or loss of prickles. Using CRISPR-Cas9 genome-editing technology, Satterlee and Lippman tested their findings by successfully eliminating prickles in a desert raisin, a foraged berry among the “spiny eggplants” native to Australia. They were also able to “edit out” prickles without causing any unwanted effects on the plant’s growth or overall health.
The group’s work demonstrates the power of genome-editing to make crops easier to cultivate and harvest. Perhaps more significant, however, is that Lippman and his collaborators have now used genome-editing tools to tackle sweeping questions about how exactly traits emerge in different plants.
Kirsten Bombliesexternal link, opens in a new tab, deputy head of the Institute of Molecular Plant Biology at ETH Zurich, says that a strength of the group’s work is that they used an evolutionary lens to help them understand the molecular mechanism underlying a trait. Bomblies, who was not involved with this work, adds, “This is especially powerful for traits, like prickles, that our core model systems lack. Here the team used a smart approach, coupling genetic mapping in eggplant, and a deep evolutionary analysis of the literature, to identify the underlying mechanism of prickle formation.”
Moving forward, Lippman and his team hope to further investigate key questions about prickle formation and loss, including how and why prickles form in particular spots on certain plants. They hope their work will offer new insights into the driving factors for evolutionary novelties in plants – not just prickles – and further advance the field of plant genetics.
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Citations:
Preprint. Satterlee, James W., David Alonso, Pietro Gramazio, Katharine M. Jenike, Jia He, Andrea Arrones, Gloria Villanueva, et al. 2024. “Convergent Evolution of Plant Prickles Is Driven by Repeated Gene Co-Option over Deep Timeexternal link, opens in a new tab.” doi: 10.1101/2024.02.21.581474
Satterlee, James W., David Alonso, Pietro Gramazio, Katharine M. Jenike, Jia He, Andrea Arrones, Gloria Villanueva, et al. 2024. “Convergent Evolution of Plant Prickles by Repeated Gene Co-Option over Deep Timeexternal link, opens in a new tab.” PMID: 39088611