How plants colonize the base of an active stratovolcano

New research on plants that colonized the base of an active stratovolcano reveals that two simple molecular steps rewired nutrient transport, enabling adaptation.

An international team led by Angela Hancock at the Max Planck Institute for Plant Breeding Research in Cologne (Germany) and including scientists from Associação Projecto Vitó and Parque Natural do Fogo (Cape Verde), University of Nottingham (Kingdom UK) and the University of Bochum (Germany) studied a wild Thalian watercress (Arabidopsis thaliana) population that colonized the base of an active stratovolcano. They found that a two-step molecular process reconnected nutrient transport in the population. The results, published today in the journal Scientists progress, reveal an exceptionally clear case of adaptive walking in a wild population. The finding has wider implications for evolutionary biology and crop improvement.

Adapt to a new soil environment

Nutrient homeostasis is crucial for good plant growth and therefore essential for crop productivity. Identifying the genetic changes that allow plants to thrive in new soil conditions provides insight into this important process. However, given the immense size of a genome, it is difficult to identify specific functional variants that enable adaptation.

Members of the research team have previously found that wild populations of the molecular model plant, Arabidopsis thaliana, commonly known as watercress thale, colonized the Cape Verde Islands from North Africa and adapted with the help of new mutations that emerged after the colonization of the islands. Here, scientists are focusing on the Fogo Island Arabid population, which grows at the base of Pico de Fogo, an active stratovolcano. “We wanted to know: What does it take to live at the foot of an active volcano? How the plants adapt Fogo’s volcanic soil?”Hancock said.

“What we found was surprising,” said Emmanuel Tergemina, the study’s first author. “While Fogo’s plants appeared to be healthy in their natural environment, they did poorly in standard potting soil.” Chemical analysis of the Fogo soils showed that they were severely depleted in manganese, a crucial element for energy production and good plant growth. In contrast, the leaves of Fogo plants grown on standard potting soil contained high levels of manganese, suggesting that the plants had evolved a mechanism to increase manganese uptake.

Two evolutionary steps towards a new adaptive peak

Scientists used a combination of genetic mapping and evolutionary analysis to uncover the molecular steps that allowed plants to colonize Fogo’s manganese-limited soil.

In a first evolutionary step, a mutation disrupted the primary iron transport gene (IRT1), eliminating its function. The disruption of this gene in a natural population was striking because this key gene exists intact in all other global populations of the Arabis species – no such disruption has been found elsewhere. Furthermore, patterns of genetic variation in the IRT1 genomic region suggest that the disrupted version of IRT1 was important in adaptation. Evolutionary reconstruction shows that the mutation quickly spread at settlement throughout the Fogo population, such that all Fogo Arabis plants now carry this mutation. Using gene editing technology (CRISPR-Cas9), researchers examined the functional effects of IRT1 disturbance at Fogo and found that it increases manganese accumulation in leaves, which may explain its role in adaptation. However, the loss of the IRT1 transporter came at a cost: it significantly reduced leaf iron.

In a second evolutionary step, the metal transporter gene NRAMP1 was duplicated in several side events. These duplications spread rapidly so that now almost all Fogo watercress plants carry multiple copies of NRAMP1 in their genomes. These duplications amplify NRAMP1 gene function, increasing iron transport and compensating iron deficiency induced by IRT1 disturbance. Moreover, amplification occurred through several independent duplication events in the island population. This was unexpected given the short time since colonization (about 5000 years) and the absence of similar events in other populations around the world. “The rapid increase in the frequency of these duplications as well as their beneficial effect on nutrient homeostasis indicate that they were important in adaptation,” Hancock explained. “Overall, our results provide an exceptionally clear example of how simple genetic changes can rewire nutrient processing in plants, enabling adaptation to a new soil environment.”

Implications for crop improvement

These results also provide encouraging news for plant breeding. Traditionally, information on gene function has come from studies of individual mutant lines. However, by using the variation that exists in nature, it is possible to uncover more complex multi-step processes that can lead to changes in traits relevant to agriculture. “The finding that a simple two-step process alters nutrient transport in this case may offer clues for approaches to improve crops to better adapt to local soil environments. Additionally, disturbance and l amplification of genes, as in the case of IRT1 and NRAMP1 in Fogo, are some of the easiest genetic changes to engineer, which makes them particularly exciting because it means they could be easily transferable to other species,” concluded Tergemina.

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