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J Exp Bot. 2016 May;67(10):2963-76. doi: 10.1093/jxb/erw063. Epub 2016 Mar 1.

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

Author information

1
Universität Rostock, Institut für Biowissenschaften, Abteilung Pflanzenphysiologie, A.- Einstein-Str. 3, D-18051 Rostock, Germany martin.hagemann@uni-rostock.de.
2
Universität Rostock, Institut für Biowissenschaften, Abteilung Pflanzenphysiologie, A.- Einstein-Str. 3, D-18051 Rostock, Germany.
3
University of Düsseldorf, Institute of Developmental and Molecular Biology of Plants and Biotechnology, Cluster of Excellence on Plant Science (CEPLAS), Universitätsstraße 1, 40225 Düsseldorf, Germany.
4
Department of Biology, University of New Mexico, Albuquerque, NM 87131, USA.
5
Institute of Plant Biochemistry, Cluster of Excellence on Plant Science (CEPLAS), Heinrich-Heine-Universität Düsseldorf, 40225 Düsseldorf, Germany.
6
Department of Ecology & Evolutionary Biology, University of Toronto, Toronto, ON M5S3B2, Canada.

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.

KEYWORDS:

2-phosphoglycolate phosphatase.; Algae; Archaeplastida; C2 pathway; carbon concentrating mechanism; cyanobacteria; glycolate oxidase; land plants; oxygenase; photorespiration; phylogeny

PMID:
26931168
DOI:
10.1093/jxb/erw063
[Indexed for MEDLINE]

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