Metal crossroads in plants: modulation of nutrient acquisition and root development by essential trace metals

A comprehensive review of how the availability of essential trace metals modulates nutrient acquisition by altering the rhizosphere environment, interfering with uptake and signaling mechanisms, and shaping root systems. The metals iron, zinc, manganese, copper, molybdenum, and nickel are essential for the growth and development of virtually all plant species. Although these elements are required at relatively low amounts, natural factors and anthropogenic activities can significantly affect their availability in soils, inducing deficiencies or toxicities in plants. Because essential trace metals can shape root systems and interfere with the uptake and signaling mechanisms of other nutrients, the non-optimal availability of any of them can induce multi-element changes in plants. Interference by one essential trace metal with the acquisition of another metal or a non-metal nutrient can occur prior to or during root uptake. Essential trace metals can also indirectly impact the plant's ability to capture soil nutrients by targeting distinct root developmental programs and hormone-related processes, consequently inducing largely metal-specific changes in root systems. The presence of metal binding domains in many regulatory proteins also enables essential trace metals to coordinate nutrient uptake by acting at high levels in hierarchical signaling cascades. Here, we summarize the known molecular and cellular mechanisms underlying trace metal-dependent modulation of nutrient acquisition and root development, and highlight the importance of considering multi-element interactions to breed crops better adapted to non-optimal trace metal availabilities.