REVIEW ARTICLE Towards closing the remaining gaps in photorespiration – the essential but unexplored role of transport proteins M. Eisenhut, T. R. Pick, C. Bordych & A. P. M. Weber Center of Excellence on Plant Sciences (CEPLAS), Institute of Plant Biochemistry, Heinrich-Heine-University, Du ¨ sseldorf, Germany Keywords Arabidopsis; compartments; metabolites; photorespiration; transporters. Correspondence Andreas P.M. Weber, Institute of Plant Biochemistry, Center of Excellence on Plant Sciences (CEPLAS), Heinrich-Heine-University, Universita ¨ tsstraße 1, D-40225 Du ¨ sseldorf, Germany. E-mail: Andreas.Weber@uni-duesseldorf.de Editor H. Rennenberg Received: 20 August 2012; Accepted: 13 September 2012 doi:10.1111/j.1438-8677.2012.00690.x ABSTRACT Photorespiration is an essential prerequisite for all autotrophic organisms performing oxygenic photosynthesis. In contrast to the well-characterised enzymes accomplishing photorespiratory metabolism, current knowledge on the involved transport processes and the respective proteins is still quite limited. In this review, we focus on the status quo of translocators involved in photorespiratory metabolism. Although the transport of some of the photorespiratory intermediates could be characterised biochemically, using isolated organelles, the genes encoding these transporters have to date not been identified in most cases. Here, we describe the postulated transport processes, present information on established or hypothetical photorespiratory transporters, depict strategies on how to identify the transport proteins on the molecular level and, finally, discuss strategies for how to find the remaining candidates. INTRODUCTION Plant cells are highly compartmentalised. The different com- partments are specialised in their physiological roles, and enzyme selection customised for distinct metabolic functions. In several cases the sequence of enzymatic reactions comprising a complete metabolic pathway is distributed over several com- partments. One prominent example is plant photorespiratory metabolism, which involves the four compartments: chloro- plast, peroxisome, mitochondrion and cytosol. Photorespira- tion is defined as a light-dependent process in which the plant consumes O 2 and simultaneously releases CO 2 . The starting point of photorespiration is the O 2 fixation by ribulose 1,5- bisphosphate carboxylase/oxygenase (Rubisco), which is the central enzyme that all oxygenic photoautotrophs use for CO 2 fixation. As its name implies, it has a dual function, using the atmospheric gases CO 2 and O 2 as substrates for either carbox- ylation or oxygenation of the acceptor molecule ribulose 1,5- bisphosphate (Ogren & Bowes 1971). The rate of carboxylation versus oxygenation reactions depends on the CO 2 /O 2 ratio at the active site of the enzyme. When CO 2 is fixed, Rubisco gen- erates two molecules of 3-phosphoglycerate (3-PGA). When O 2 is fixed, one molecule of 3-PGA and one molecule of 2-phosphoglycolate (2-PG) are formed. The latter cannot be used as a Calvin–Benson cycle substrate, and needs to be detoxified. The decomposition of 2-PG is accomplished by a series of at least eight enzymatic steps (reviewed in Tolbert 1997), and includes the passage of the intermediates from the chloroplast through the peroxisome, mitochondrion, back to the peroxisome, and finally re-entering the chloroplast. We will reconsider the single enzymatic steps later in this article. A detailed review of this pathway is presented in this issue by Timm & Bauwe (2012). As a consequence of photorespiratory metabolism, the plant detoxifies 2-PG (Tolbert 1997), recovers 75% of the carbon that is contained in 2-PG back to 3-PGA (Lorimer 1981), and consumes energy, which contributes to preventing photoinhibition (Kozaki & Takeba 1996; Wingler et al. 2000). Additionally, the photorespiratory pathway is the major source for the amino acids glycine and serine (Wingler et al. 2000). A functional photorespiratory metabolism is a prerequisite for the survival of all photoautotrophic organisms in an O 2 - containing atmosphere (Eisenhut et al. 2008; reviewed in Hagemann et al. 2010; Bauwe et al. 2012), including cyanobac- teria (Eisenhut et al. 2008) and plants (reviewed in Somerville 2001), as demonstrated by the fact that mutants with a mal- function in the photorespiratory metabolism cannot survive in normal air containing 0.038% CO 2 and 21% O 2 . In plant pho- tosynthetic tissues photorespiration is a major metabolic path- way, considering that the carboxylation reaction exceeds oxygenation only by approximately three-fold in a normal air atmosphere (Zeiger 2000). In order to permit the high flux of metabolites through the photorespiratory cycle and auxiliary metabolic pathways, the different compartments have to be connected. High photorespiratory flux is facilitated by the close juxtaposition of the three organelles involved – chloroplast, peroxisome, and mitochondrion (Noctor et al. 2007). How- ever, since the inner membranes of organelles are generally impermeable to bigger and charged molecules, transport pro- teins are required that catalyse the flux of metabolic intermedi- ates across the permeation barrier. In contrast to the well- studied enzymes catalysing the enzymatic reactions of the pho- Plant Biology © 2012 German Botanical Society and The Royal Botanical Society of the Netherlands 1 Plant Biology ISSN 1435-8603