In eukaryotes, membrane contact sites (
MCS
) allow direct communication between organelles. Plants have evolved a unique type of
MCS
, inside intercellular pores, the plasmodesmata, where endoplasmic reticulum (
ER
)–plasma membrane (
PM
) contacts coincide with regulation of cell‐to‐cell signalling. The molecular mechanism and function of membrane tethering within plasmodesmata remain unknown. Here, we show that the multiple C2 domains and transmembrane region protein (
MCTP
) family, key regulators of cell‐to‐cell signalling in plants, act as
ER
‐
PM
tethers specifically at plasmodesmata. We report that
MCTP
s are plasmodesmata proteins that insert into the
ER
via their transmembrane region while their C2 domains dock to the
PM
through interaction with anionic phospholipids. A
Atmctp3/Atmctp4
loss of function mutant induces plant developmental defects, impaired plasmodesmata function and composition, while
MCTP
4 expression in a yeast Δtether mutant partially restores
ER
‐
PM
tethering. Our data suggest that
MCTP
s are unique membrane tethers controlling both
ER
‐
PM
contacts and cell‐to‐cell signalling.
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