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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 saman 15 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. [Display omitted] • Rainfall-induced leaf-folding movement of Samanea saman is temperature-sensitive • SPORK2 is identified as a temperature-sensitive K+ channel from Samanea motor cell • The temperature sensitivity is conserved among SPORK2 orthologs • TM3 and C-linker are essentially involved in the thermosensitivity of SPORK2 Transient receptor-potential ion channels are important for thermosensing in animals. In contrast, such temperature-sensitive ion channels in land plants are still mysterious. Muraoka et al. find that the rainfall-induced leaf-folding movement of Samanea saman is thermosensitive and identify SPORK2 as a temperature-sensitive K+ channel in land plants. [ABSTRACT FROM AUTHOR]

Summary The circadian leaf opening and closing (nyctinasty) of Fabaceae has attracted scientists’ attention since the era of Charles Darwin. Nyctinastic movement is triggered by the alternate swelling and shrinking of motor cells at the base of the leaf. This, in turn, is facilitated by changing osmotic pressures brought about by ion flow through anion and potassium ion channels. However, key regulatory ion channels and molecular mechanisms remain largely unknown. Here, we identify three key ion channels in mimosoid tree Samanea saman : the slow-type anion channels, SsSLAH1 and SsSLAH3, and the Shaker-type potassium channel, SPORK2. We show that cell-specific circadian expression of SsSLAH1 plays a key role in nyctinastic leaf opening. In addition, SsSLAH1 co-expressed with SsSLAH3 in flexor (abaxial) motor cells promoted leaf opening. We confirm the importance of SLAH1 in leaf movement using SLAH1-impaired Glycine max . Identification of this “master player” advances our molecular understanding of nyctinasty. [ABSTRACT FROM AUTHOR]