From cyanobacteria to plants: conservation of PII functions during plastid evolution

Abstract

This article reviews the current state-of-the-art concerning the functions of the signal processing protein PII in cyanobacteria and plants, with a special focus on evolutionary aspects. We start out with a general introduction to PII proteins, their distribution, and their evolution. We also discuss PII-like proteins and domains, in particular, the similarity between ATP-phosphoribosyltransferase (ATP-PRT) and its PII-like domain and the complex between N-acetyl-L-glutamate kinase (NAGK) and its PII activator protein from oxygenic phototrophs. The structural basis of the function of PII as an ATP/ADP/ 2-oxoglutarate signal processor is described for Synechococcus elongatus PII. In both cyanobacteria and plants, a major target of PII regulation is NAGK, which catalyzes the committed step of arginine biosynthesis. The common principles of NAGK regulation by PII are outlined. Based on the observation that PII proteins from cyanobacteria and plants can functionally replace each other, the hypothesis that PII-dependent NAGK control was under selective pressure during the evolution of plastids of Chloroplastida and Rhodophyta is tested by bioinformatics approaches. It is noteworthy that two lineages of heterokont algae, diatoms and brown algae, also possess NAGK, albeit lacking PII; their NAGK however appears to have descended from an alphaproteobacterium and not from a cyanobacterium as in plants. We end this article by coming to the conclusion that during the evolution of plastids, PII lost its function in coordinating gene expression through the PipX-NtcA network but preserved its role in nitrogen (arginine) storage metabolism, and subsequently took over the fine-tuned regulation of carbon (fatty acid) storage metabolism, which is important in certain developmental stages of plants.

PipX, the coactivator of NtcA, is a global regulator in cyanobacteria

“…1), and perhaps P II -modifying enzymes (43,44). This complexity makes it difficult to infer a potential role for P II in the proposed PipX complexes.…”

The Proteome and Lipidome of Synechocystis sp. PCC 6803 Cells Grown under Light-Activated Heterotrophic Conditions*

“…Increased abundance of proteins involved in N-metabolism was observed although the growth conditions are not N-limiting, most likely because of the increased metabolic flow through the glycolysis and TCA cycle and increased production of the regulatory metabolite 2-OG. In fact, PamA functionally interacts with the PII sensor protein, a protein highly conserved in prokaryotes and plant chloroplasts (50), which was also significantly more abundant under LAHG conditions. PII appears to monitor the cellular C-as well as the N-status by binding 2-OG in a cooperative manner together with ATP, and furthermore, phosphorylation might additionally trigger the PII sensory function (51).…”

Proteogenomic analysis and global discovery of posttranslational modifications in prokaryotes

“…It is estimated that more than half of the photosynthetic activity on Earth is contributed by cyanobacteria (12). Cyanobacteria make substantial contributions to global CO 2 assimilation, O 2 production, and N 2 fixation and are the progenitors of chloroplasts in higher plants (13). Cyanobacterial habitats are highly diverse, and cyanobacterial cells adjust their cellular activities in response to a wide range of environmental cues and stimuli.…”