How Amphibious Plants Rewired a Gas Exchange Pathway to Survive in Water

January 24, 2023 • by Emily Engelbart

Just as humans cannot breathe underwater, the tiny pores of plants can't exchange air underwater.

When grown on land, the amphibious plant Rorippa aquatica produces pores called stomata (left); but grown in water, it does not. Credit: Shuka Ikematsu.

Even worse, having pores under water promotes the entry of water, microbes and other undesirable things inside the leaf. Amphibious plants—those adapted to the edges of rivers and lakes where water levels can change easily—like Rorippa aquatica, adapt to life underwater by not producing these pores, called stomata.

Keiko Torii, a professor of molecular biosciences at The University of Texas at Austin, and her team wondered what molecular changes happen within amphibious plants to block stomata production underwater. What they found led to a new understanding about how amphibious plants have adapted to live both on land and in water, and their results have been published in Current Biology this week.

Stomata are necessary for terrestrial plants to efficiently acquire carbon dioxide for photosynthesis while minimizing the loss of water vapor. Plants have developed special sensors for blue light and others for red light, both of which signal the plant to produce stomata.

As the team expected, Rorippa aquatica uses blue light to promote stomatal development, whether on land or in water. But Rorippa aquatica's reaction to red light when submerged highlights the difference between itself and terrestrial plants. When Torii and her team tested the reaction of Rorippa aquatica to red light when submerged in water, they found that the leaf did not develop stomata.

Through further experiments, the researchers discovered the process of adaptation to submergence: When Rorippa aquatica is submerged and is exposed to red light, it rapidly represses master regulatory genes called SPEECHLESS and MUTE, which normally tell cells to become stomata. In other words, the molecular pathway that normally uses red light as a trigger to produce stomata on land acts in the opposite way when this amphibious plant is underwater. Furthermore, when red and blue light are both present at the same time, red overrides blue, leading to a shutdown of stomata production.

How does this happen? The group found that in Rorippa aquatica, the red light triggers the production of ethylene, a gaseous hormone of plants that is normally associated with hypoxia stress (due to a lack of oxygen) or fruit ripening. In this case, ethylene is causing Rorippa to repress stomatal master regulators SPEECHLESS and MUTE.

"So, it's completely opposite of the dogma," Torii said. "It is surprising and fascinating that the amphibious plant Rorippa aquatica invented a new way to connect light cues to hormone production in order to rapidly adapt to submergence. As global climate changes dramatically, causing heavy rains and flooding, what we found from Rorippa aquatica could be applied to modify terrestrial plants—making them highly adapted to both land and water."

Rorippa aquatica, like terrestrial plants, can sustain itself on land. But if they find themselves submerged in water, this amphibious plant can use its innovative approach to survive in its new environment. If only all life had the tools to adapt to underwater and terrestrial life, we, like Rorippa, could explore new frontiers and thrive in a changing world.

The work was in collaboration with researchers at Kyoto Sangyo University and Nagoya University, Japan. The research at The University of Texas at Austin was funded in part by the Japanese Ministry of Education, Culture, Sports, Science and Technology. Torii is a Howard Hughes Medical Investigator and the Johnson & Johnson Centennial Chair at UT Austin.

Graphical abstract

When the amphibious plant Rorippa aquatica is grown on land, red and blue light trigger genes called SPCH and MUTE to produce pores called stomata (left). But when the plant is growing underwater, red light causes the hormone ethylene to build up in its tissues, which suppresses the SPCH and MUTE genes and in turn inhibits the formation of stomata. Credit: Shuka Ikematsu and Issey Takahashi.