The PII signal-transduction superfamily is widespread in all domains of the life, representing one of the largest and most ancient families of signaling proteins in nature. Signaling proteins of the PII superfamily are characterized by their highly conserved trimeric structure. Canonical PII proteins sense the cellular energy state through competitive binding of ATP and ADP and sense the C/N balance through 2-oxoglutarate binding (2-OG). The ancestor of Archaeplastida inherited the PII signal transduction protein from the ancient cyanobacterial endosymbiont. In plants, the major interaction partner of PII is the controlling enzyme of arginine synthesis, N-acetyl-L-glutamate kinase (NAGK). The plant PII proteins are not covalently modified and its mode of action has been shown to require direct binding of effector molecules. The results suggest that PII signalling system of red algae represents an intermediary state between Cyanobacteria and Chlorophyta.To our data, in the course of evolution, plant PII proteins acquired a glutamine-sensing C-terminal extension, present in all Chloroplastida PII proteins (except Brassicaceae family). Sensing glutamine as the primary product of nitrogen assimilation indicates that in the Chloroplastida, PII became specialized to respond to the nitrogen status. In agreement with glutamine becoming the dominant signal for plant PII proteins, the sensory properties of PII proteins that were determined from different Chlorophyta towards the ATP/ADP status or towards 2-OG are quite variable. Among these organisms, the colorless alga Polytomella parva is a special case, as its the PII-NAGK system has lost the ability to estimate the cellular energy and carbon status but has specialized to provide an entirely glutamine-dependent arginine-feedback control. The observed differences towards the effector molecules between PII proteins from different representatives of Chlorophyta and higher plants demonstrate the evolutionary plasticity of PII signaling system. (This research was funded by Russian Science Foundation, N 16-14-10004, and DFG, Fo195/9-2, Fo195/13-1).