Proteomic insights into trichome responses to elevated elemental stress in cation exchanger (CAX) mutants

Authors: GUO, QI - Southern Cross University; SHAYAN, SARKAR - Children'S Nutrition Research Center (CNRC); PUNSHON, TRACY - Dartmouth College; TAPPERO, RYANB - Brookhaven National Laboratory; BARKLA, BRONWYN - Southern Cross University; HIRSCHI, KENDAL - Children'S Nutrition Research Center (CNRC)

Submitted to: Plant and Cell Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/28/2024
Publication Date: 9/2/2024
Citation: Guo, Q., Shayan, S., Punshon, T., Tappero, R., Barkla, B.J., Hirschi, K.D. 2024. Proteomic insights into trichome responses to elevated elemental stress in cation exchanger (CAX) mutants. Plant and Cell Physiology. 65(12):1941-1957. https://doi.org/10.1093/pcp/pcae097.
DOI: https://doi.org/10.1093/pcp/pcae097

Interpretive Summary: Plants often face stressful conditions, such as salty soil, flooding, or low nutrients, which can hinder their growth. We studied tiny hair-like structures on plant leaves, called trichomes, to see how they manage important minerals during stress. Using advanced X-ray imaging, we discovered that even when specific nutrient transport proteins (called CAXs) were missing, the trichomes stored more calcium, potassium, and other elements than usual. The plants also changed which proteins they made to help move water and support communication between cells. This shows that plants have built-in backup systems to stay healthy when key parts aren’t working. Because trichomes are easy to see and study, they could be used as tools to understand stress in plants better—and may help scientists grow crops that can survive in harsh environments.

Technical Abstract: Research on elemental distribution in plants is crucial for understanding nutrient uptake, environmental adaptation and optimizing agricultural practices for sustainable food production. Plant trichomes, with their self-contained structures and easy accessibility, offer a robust model system for investigating elemental repartitioning. Transport proteins, such as the four functional cation exchangers (CAXs) in Arabidopsis, are low-affinity, high-capacity transporters primarily located on the vacuole. Mutants in these transporters have been partially characterized, one of the phenotypes of the CAX1 mutant being altered with tolerance to low-oxygen conditions. A simple visual screen demonstrated trichome density and morphology in cax1, and quadruple CAX (cax1-4: qKO) mutants remained unaltered. Here, we used synchrotron X-ray fluorescence (SXRF) to show that trichomes in CAX-deficient lines accumulated high levels of chlorine, potassium, calcium and manganese. Proteomic analysis on isolated Arabidopsis trichomes showed changes in protein abundance in response to changes in element accumulation. The CAX mutants showed an increased abundance of plasma membrane ATPase and vacuolar H-pumping proteins, and proteins associated with water movement and endocytosis, while also showing changes in proteins associated with the regulation of plasmodesmata. These findings advance our understanding of the integration of CAX transport with elemental homeostasis within trichomes and shed light on how plants modulate protein abundance under conditions of altered elemental levels.