Mechanosensation triggers enhanced heavy metal ion uptake by non-glandular trichomes

The trichomes of Arabidopsis thaliana serve as accumulation sites for heavy metals such as Cd²⁺, and thereby both help plants cope with heavy metal stress and detoxify the soil. These trichomes are also believed to prime plant defenses against insect herbivores in response to mechanical stimulation. Because Cd²⁺ in such trichomes may be beneficial for plant defenses, we hypothesized that mechanical stimulation would enhance sequestration of Cd²⁺ in trichomes. We quantified the distribution and concentration of Cd²⁺ in leaves of A. thaliana, of the glabrous mutant gl1–1 of A. thaliana, and Brassica rapa L. subsp. pekinensis (Lour.) Hanelt (Chinese cabbage) and examined how these changed following mechanical stimulation of the trichomes or leaves. Light brushing or exposure to caterpillars of Spodoptera exigua led trichomes of both A. thaliana and Chinese cabbage to accumulate Cd²⁺ complexes more rapidly and to a higher concentration than trichomes in unstimulated controls. Comparison to responses in leaves of gl1–1 mutants suggested that this acceleration and enhancement of Cd²⁺ storage requires signaling through trichomes. In wild type A. thaliana, Cd²⁺ was found exclusively in trichomes, whereas in gl1–1 mutants, Cd²⁺ was found mainly in the - mesophyll cells. Results suggest a mechanobiological pathway for improving heavy metal detoxification of soils through the action of hyperaccumulator plant leaves containing non-glandular trichomes.