Ca2+-Mediated Thermal Sensing in Plants

Abstract

Temperature is an omnipresent environmental factor that shapes the growth, development and survival of plants. However, global warming has been an inevitable process and caused unusual temperature patterns across the world. As a consequence, forestry as well as agricultural plants are reportedly facing challenges from their environment. Several temperature responses in plant have been described, including short-term responses (such as acclimation) that increase tolerance towards sudden temperature stresses; as well as long-term responses (for example vernalization and flowering) that adjust growth and development to cope with seasonal temperature changes. However, the molecular mechanisms of how plants perceive temperature changes remain poorly understood. It has been observed for decades that one earliest response of plants towards low temperature is a transient increase of the cytosolic free Ca2+ concentration ([Ca2+]i). Considering the highly conserved role of [Ca2+]i increases in mediating thermal perception in animals, it has been speculated that [Ca2+]i increases may also play a role in thermal perception in plants. Nevertheless, despite intensive efforts, the molecular components responsible for cold-induced [Ca2+]i increases remain elusive. In this study, we carried out Ca2+-imaging-based forward genetic screen in Arabidopsis thaliana, isolated mutants defective in cold-induced [Ca2+]i increases (coca) and identified corresponding genes responsible for the coca phenotype through physical mapping. One of the mutants, named coca1, is highly specific to low temperature perception versus other stimuli, including osmotic, ionic and oxidative stimuli. coca1 displays compromised cold-induced [Ca2+] increases in both cotyledons and roots, as well as reduced growth fitness under ambient cool temperature. COCA1 encodes the dynamin-related protein 1A (DRP1A) and is localized on the plasma membrane. Our pharmacological studies showed that DRP1A acts upstream of plasma membrane rigidification and may mediate temperature perception by modification of membrane curvature which in turn opens Ca2+ channels. Alternatively, DRP1A may regulate endocytosis and channel activity through endocytosis signaling. Identification of coca1 as the first Arabidopsis mutant defective in cold-induced [Ca2+]i increases and DRP1A as a key player in thermal perception will greatly extend our understanding of plant adaptation to temperature changes, open up new avenues for studying Ca2+ signaling towards other stimuli and provide potential molecular genetic targets for engineering cold-resistant crops.