Evolution of photorespiration from cyanobacteria to land plants, considering protein phylogenies and acquisition of carbon concentrating mechanisms

Abstract

Photorespiration and oxygenic photosynthesis are intimately linked processes. It has been shown that under the present day atmospheric conditions cyanobacteria and all eukaryotic phototrophs need functional photorespiration to grow autotrophically. The question arises as to when this essential partnership evolved, i.e. can we assume a coevolution of both processes from the beginning or did photorespiration evolve later to compensate for the generation of 2-phosphoglycolate (2PG) due to Rubisco's oxygenase reaction? This question is mainly discussed here using phylogenetic analysis of proteins involved in the 2PG metabolism and the acquisition of different carbon concentrating mechanisms (CCMs). The phylogenies revealed that the enzymes involved in the photorespiration of vascular plants have diverse origins, with some proteins acquired from cyanobacteria as ancestors of the chloroplasts and others from heterotrophic bacteria as ancestors of mitochondria in the plant cell. Only phosphoglycolate phosphatase was found to originate from Archaea. Notably glaucophyte algae, the earliest branching lineage of Archaeplastida, contain more photorespiratory enzymes of cyanobacterial origin than other algal lineages or land plants indicating a larger initial contribution of cyanobacterial-derived proteins to eukaryotic photorespiration. The acquisition of CCMs is discussed as a proxy for assessing the timing of periods when photorespiratory activity may have been enhanced. The existence of CCMs also had marked influence on the structure and function of photorespiration. Here, we discuss evidence for an early and continuous coevolution of photorespiration, CCMs and photosynthesis starting from cyanobacteria via algae, to land plants.

Systems analysis of ethanol production in the genetically engineered cyanobacterium Synechococcus sp. PCC 7002

“…Because the ethanol-producer strain showed increasing 3PGA deficiency, we asked the question of whether the photorespiratory C2-cylce was activated, which converts two molecules of the oxygenase product 2PG into one molecule of 3PGA [38]. 2PG was found at increased levels throughout all phases of ethanol production, whereas glycolate levels increased from phase II onwards (Additional file 8).…”

Optimizing photorespiration for improved crop productivity

“…Deeper understanding of the role of photorespiratory intermediates in other metabolic pathways and determining how altered photorespiration will affect plant growth and yield under different growth environments is needed. Although photorespiration is involved in these aspects of plant metabolism, it is not clear if this is essential for plant function, or a result of the evolutionary pathway that led to the photorespiratory cycle in land plants (Hagemann et al ). It is well known, for example, that under many conditions, C3 plants benefit from reduced, including full suppression, of Rubisco oxygenation and subsequent photorespiratory metabolism (Wheeler et al ; Long et al ).…”

RubisCO Early Oxygenase Activity: A Kinetic and Evolutionary Perspective

“…A partial confirmation of this hypothesis is the oxygenase activity of all the other RubisCO forms, mainly form I (Figure ), and its involvement in photorespiration. On this view, the photorespiratory pathway in cyanobacteria/plants is not a wasteful process, but might be interpreted as a phylogenetically old part of the antioxidant system …”