Root Suberin Forms an Extracellular Barrier That Affects Water Relations and Mineral Nutrition in Arabidopsis

Abstract

Though central to our understanding of how roots perform their vital function of scavenging water and solutes from the soil, no direct genetic evidence currently exists to support the foundational model that suberin acts to form a chemical barrier limiting the extracellular, or apoplastic, transport of water and solutes in plant roots. Using the newly characterized enhanced suberin1 (esb1) mutant, we established a connection in Arabidopsis thaliana between suberin in the root and both water movement through the plant and solute accumulation in the shoot. Esb1 mutants, characterized by increased root suberin, were found to have reduced day time transpiration rates and increased water-use efficiency during their vegetative growth period. Furthermore, these changes in suberin and water transport were associated with decreases in the accumulation of Ca, Mn, and Zn and increases in the accumulation of Na, S, K, As, Se, and Mo in the shoot. Here, we present direct genetic evidence establishing that suberin in the roots plays a critical role in controlling both water and mineral ion uptake and transport to the leaves. The changes observed in the elemental accumulation in leaves are also interpreted as evidence that a significant component of the radial root transport of Ca, Mn, and Zn occurs in the apoplast. The root system is a highly specialized plant organ that works to get both water and essential mineral nutrients from the changing chemically and physically complex environment of the soil. Roots do this by both controlling the uptake of water and essential mineral ions, as well as regulating their movement to the central vascular system of the plant for long distance transport to the shoot. To allow the cellular control of water and mineral ion uptake and transport via specialized transport proteins, plant roots contain a waxy layer of suberin that acts to seal connections between cells, preventing uncontrolled leakage of water and mineral ions between cells. By screening thousands of mutant A. thaliana plants, we were able to identify a plant with elevated levels of suberin in the root. Using this mutant, we were able to uncover the importance of suberin in sealing connections between root cells to regulate water movement through the plant and accumulation of various essential and nonessential minerals in leaves, including sodium, sulfur, potassium, calcium, manganese, zinc, arsenic, selenium, and molybdenum.