Leaf structures thought to provide salt and drought protection actually defend against herbivores
by Science Writer Kim Woolcock
As the planet warms, highly resilient crops such as quinoa (Chenopodium quinoa) are attracting more and more attention, as are the traits that allow them to grow in harsh conditions. An ancient crop native to the Andean region of South America, quinoa is highly salt and drought tolerant. Its leaves are covered in tiny, fluid-filled balloons called epidermal bladder cells (EBCs) that were thought to be the source of its stress tolerance. A study published in Current Biology on October 17, 2023 reveals that EBCs actually do not protect against salt or drought, instead providing physical and chemical protection against insects and bacteria. The EBCs act as a shield, blocking access to the leaf surface, and are filled with compounds, including oxalic acid, that are toxic to herbivorous insects. Understanding the function of EBCs will help in breeding quinoa varieties adapted to specific conditions. The open-access Current Biology article is titled “Epidermal Bladder Cells As a Herbivore Defense Mechanism.”
EBCs are modified trichomes—leaf hairs—that cover the leaf surface. Although they were long thought to act in salt and drought tolerance, recent research indicated that they are filled with compounds that plants usually use to defend against herbivores, like oxalic acid and saponins. Max Moog and Michael Palmgren at the University of Copenhagen and coworkers decided to investigate their function using plants without EBCs: mutants that did not produce EBCs and plants that had their EBCs removed by scraping.
Comparing wild-type and EBC-free plants, they found that EBCs did not help quinoa plants against either drought or salt stress. In fact, the wild-type plants with EBCs were less drought tolerant, because the plants directed water into their EBCs at the expense of their leaf cells.
The plants for the drought and salt experiments were grown in the highly controlled environment of growth chambers. When the team grew quinoa plants in the greenhouse, they noticed something unexpected. The greenhouse sometimes had infestations of thrips, a common greenhouse pest. While the wild-type plants grew normally, the EBC-free plants were very stunted. Observing the plants, they found that new shoots of wild-type plants were densely covered in EBCs, and they only found thrips on older leaves, with less dense EBCs. New leaves of EBC-free plants, however, were thickly coated in thrips, and their new growth died within ~2 weeks of being infested.
Testing with another common insect pest, the two-spotted spider mite (Tetranychus urticae), showed that EBCs blocked the mites from accessing the leaf surface. Leaves with densely packed EBCs had no feeding damage because the mites simply could not access the leaf surface.
The researchers also noticed that the mites did not consume the EBCs. Examining their contents showed why not: they were full of oxalic acid, which is toxic to many insects, at much higher concentrations (100 mM) than in the leaves (10 mM). If they wounded the EBCs, the oxalic acid concentrations doubled within 24 h. When they fed spider mites oxalic acid at these concentrations, only ~5% survived.
Further testing showed that the EBCs also deterred a larger leaf-chewing herbivore, first instar larvae of the beet armyworm (Spodoptera exigua) and prevented infection by a common plant pathogenic bacterium Pseudomonas syringae pv. tomato DC300, probably by forming a physical barrier that prevented the bacteria from getting to the leaf surface.
Quinoa is an ancient crop that has been the subject of many studies, but we still have new things to learn about it. Understanding that EBCs guard against plant pests rather than drought could help in breeding new varieties more resistant to either pests or drought and that can be grown sustainably in an even wider variety of conditions.