An outward-rectifying plant K⁺ channel SPORK2 exhibits temperature-sensitive ion-transport activity

Temperature sensing is critical for the survival of living organisms.^1,2 Thermosensitive transient receptor-potential (TRP) cation channels function as thermosensors in mammals.^2,3,4,5,6 In contrast to animals, land plants lack TRP genes.^7,8,9 Previous patch-clamp studies in plant cells suggested the presence of ion channels whose activities are related to temperature, implying the presence of TRP-like channels.^{10,11,12,13,14} However, the molecular entities of such temperature-sensitive ion channels were still unknown in land plants. In this study, we observed that the unique rainfall-induced leaf-folding movement of the legume tree Samanea saman¹⁵ was temperature-sensitive by using a rainfall-mimicking assay. Chilling-induced leaf folding in S. saman was shown to be related to the swelling of the motor cells^16,17 at the base of the leaflet. This swelling suggested involvement of temperature-sensitive inactivation of K⁺ currents, independent of fluctuations in ion channel gene expression in motor cells. These findings led us to examine the temperature sensitivity of an outward-rectifying K⁺ channel, SPORK2, which was reported as an ion channel responsible for the nyctinastic (circadian-rhythmic) leaf movement of S. saman.¹⁸ We also discovered that SPORK2 exhibits temperature-sensitive K⁺ transport activity in the Xenopus oocyte expression system. Using chimeric channels, we showed that two domains of SPORK2 regulated the temperature sensitivity. Furthermore, heterologously expressed SPORK2 in Arabidopsis guard cells induced temperature-dependent stomatal closure. Therefore, SPORK2 is an ion channel in land plants with temperature-sensitive ion-transport activity that functions similarly to mammalian TRP channels. Our current findings advance the molecular understanding of temperature-sensing mechanisms in plants.