Plasma membrane cyclic nucleotide gated calcium channels control land plant thermal sensing and acquired thermotolerance.
Typically at dawn on a hot summer day, land plants need precise molecular thermometers to sense harmless increments in the ambient temperature to induce a timely heat shock response (HSR) and accumulate protective heat shock proteins in anticipation of harmful temperatures at mid-day. Here, we found that the cyclic nucleotide gated calcium channel (CNGC) CNGCb gene from Physcomitrella patens and its Arabidopsis thaliana ortholog CNGC2, encode a component of cyclic nucleotide gated Ca(2+) channels that act as the primary thermosensors of land plant cells. Disruption of CNGCb or CNGC2 produced a hyper-thermosensitive phenotype, giving rise to an HSR and acquired thermotolerance at significantly milder heat-priming treatments than in wild-type plants. In an aequorin-expressing moss, CNGCb loss-of-function caused a hyper-thermoresponsive Ca(2+) influx and altered Ca(2+) signaling. Patch clamp recordings on moss protoplasts showed the presence of three distinct thermoresponsive Ca(2+) channels in wild-type cells. Deletion of CNGCb led to a total absence of one and increased the open probability of the remaining two thermoresponsive Ca(2+) channels. Thus, CNGC2 and CNGCb are expected to form heteromeric Ca(2+) channels with other related CNGCs. These channels in the plasma membrane respond to increments in the ambient temperature by triggering an optimal HSR, leading to the onset of plant acquired thermotolerance.
Department of Plant Molecular Biology, University of Lausane, CH-1015 Lausane, Switzerland.
Andrija
A
Finka
America Farinia Henriquez
AF
Cuendet
Frans J M
FJ
Maathuis
Younousse
Y
Saidi
Pierre
P
Goloubinoff
D000220:Adaptation, Biological; D000595:Amino Acid Sequence; D017360:Arabidopsis / Q000235:genetics / Q000254:growth & development / Q000502:physiology*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism; D019068:Bryopsida / Q000235:genetics / Q000254:growth & development / Q000502:physiology*; D002118:Calcium / Q000378:metabolism; D002462:Cell Membrane / Q000235:genetics / Q000378:metabolism*; D019295:Computational Biology; D054815:Cyclic Nucleotide-Gated Cation Channels / Q000235:genetics / Q000378:metabolism*; D003593:Cytoplasm / Q000235:genetics / Q000378:metabolism; D017353:Gene Deletion; D018506:Gene Expression Regulation, Plant; D017343:Genes, Plant; D018869:Heat-Shock Response; D006358:Hot Temperature; D008969:Molecular Sequence Data; D010641:Phenotype; D010802:Phylogeny; D030821:Plants, Genetically Modified / Q000235:genetics / Q000254:growth & development / Q000378:metabolism; D015398:Signal Transduction; D013997:Time Factors
C518230:ATCNGC4 protein, Arabidopsis; D029681:Arabidopsis Proteins; C518228:CNGC2 protein, Arabidopsis; D054815:Cyclic Nucleotide-Gated Cation Channels; D002118:Calcium