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When plant roots learned to follow gravity

Highly developed seed plants have developed deep root systems that are able to detect the Earth's gravity. The how and when of this stage of evolution has, until now, remained unknown. Phytobiologists at the Austrian Institute of Science and Technology (IST Austria) have identified crucial components and processes that only developed about 350 million years ago in seedlings to allow rapid and efficient root growth by gravity. The results were published in the journal Nature Communications.

One of the most important events in the history of evolution occurred about 500 million years ago with the spread of plant life from water to land. For plants to thrive in this new environment, the root system had to evolve to grow downwards, following gravity with two main objectives: to anchor itself in the soil and provide a source of water and nutrients for the growth of plant parts above the ground. This mechanism, called gravitropism, has been the subject of numerous studies on flowering plants such as Arabidopsis thaliana. However, it has never been systematically compared to the whole plant kingdom and its evolutionary origin remains a mystery.

Down, down, down, down, but at different speeds

Now, Yuzhou Zhang, postdoc in Professor Jirí Friml's group, and his team have acquired a broader vision of how and when root gravitropism evolved. The researchers selected multiple plant species representing lines of mosses, lycophytes (clovers and firmosses), ferns, gymnosperms (conifers) and flowering plants and allowed their roots to grow horizontally to observe if and when they began to bend down to follow gravity. The result: Root growth by gravity was very rudimentary and slow in the most primitive terrestrial plants (mosses) as well as in basal vascular plants (lycophytes and ferns). Only seed plants (gymnosperms and flowering plants), which appeared about 350 million years ago, have shown a faster and therefore more effective form of gravitropism.

The power of starch

But what stage of evolution has allowed this fast and effective root gravitropism in seedlings? By analyzing the different phases of gravitropism - the perception of gravity, the transmission of the gravitational signal and, finally, the growth response itself - the researchers discovered two essential components that evolved hand in hand. The first has proved to be an anatomical characteristic: Plant organelles called amyloplasts - densely filled with starch granules - are sediments in response to gravity and thus function as gravity sensors. However, this sedimentation process has only been observed in gymnosperms and flowering plants, with amyloplasts being highly concentrated at the bottom of the root tips. In earlier plants, however, amyloplasts remained randomly distributed in and above the root tip, thus not functioning as gravity sensors as was the case in seed plants.

A special PIN code for auxin

After perception by amyloplasts, the gravity signal is transmitted from cell to cell by the growth hormone auxin. In genetic experiments, researchers identified a specific transport molecule in the model plant Arabidopsis thaliana, PIN2, which directs the flow of auxins and thus root growth. While almost all green plants carry PIN proteins, only the PIN2 molecule specific to seed plants gathers on the growth side of the epidermal cells of the root. This specific location, unique to seed plants, leads to the polarization of carrier cells which, in turn, allows the root to transport auxin to the shoot and thus to the auxin-based signaling to move from the perception of the location of gravity to the regulation of the growth zone.

Plants as teachers for humanity

By identifying these two anatomical and functional components, the authors have gained valuable knowledge on the evolution of root gravitropism, which is one of the crucial adaptations of seed plants to the soil. But even the practical implications of these results are conceivable: "Now that we have begun to understand which plants need to grow a stable anchor to reach nutrients and water in the deep layers of the soil, we could eventually find ways to improve the growth of crops and other plants in very arid areas," says Zhang, who joined IST Austria in 2016. He adds: "Nature is much smarter than us; there are so many things we can learn from plants that can eventually be useful to us.