Plant ABC Transporters

Abstract

ABC transporters constitute one of the largest protein families found in all living organisms. ABC transporters are driven by ATP hydrolysis and can act as exporters as well as importers. The plant genome encodes for more than 100 ABC transporters, largely exceeding that of other organisms. In Arabidopsis, only 22 out of 130 have been functionally analyzed. They are localized in most membranes of a plant cell such as the plasma membrane, the tonoplast, chloroplasts, mitochondria and peroxisomes and fulfill a multitude of functions. Originally identified as transporters involved in detoxification processes, they have later been shown to be required for organ growth, plant nutrition, plant development, response to abiotic stresses, pathogen resistance and the interaction of the plant with its environment. To fulfill these roles they exhibit different substrate specifies by e.g. depositing surface lipids, accumulating phytate in seeds, and transporting the phytohormones auxin and abscisic acid. The aim of this review is to give an insight into the functions of plant ABC transporters and to show their importance for plant development and survival.

Figure 1.

Overview of the Arabidopsis ABC transporters characterized to date. ABC transporters whose functions and/or substrates have been reported are listed according to their tissue of action. Detailed information for each gene is described in the corresponding chapters. Figure modified from Kretzschmar et al. (2011).

Figure 2.

Arabidopsis thaliana ATP-binding cassette (ABC) protein subfamilies, with their maximum likelihood phylogenies, and a phylogeny of the NBDs of all Arabidopsis ABC proteins. For the ABCI subfamily, only the encoded domain is indicated, as their divergence is too large to resolve their phylogenetic relationships. In the NBD phylogeny, both NBDs of full-size ABCs were included. NBDs of full-size ABCB show little divergence compared to NBDs of ABCCs and full-size ABCGs. Phylogenies were estimated using PhyML3.0 (Guindon et al., 2010) and the model LG+G4+I+F from a truncated protein sequence alignment generated with MUSCLE 3.8 (http://www.drive5.com/muscle). Gaps of more than 80% were removed (Capella-Gutiérrez et al., 2009). Branch support values correspond to non-parametric bootstrap values from 100 replicates. Domain organizations are indicated by colored symbols (key, bottom right).

Figure 3.

ABC transporters involved in cellular detoxification. (A) At the plasma membrane, AtABCG36 mediates Cd export and is also involved in pathogen defense (Kobae et al., 2006; Stein et al., 2006; Kim et al., 2007; Bednarek et al., 2009; Clay et al., 2009). The bacterial-type ABC transporters, STAR1 and STAR2, confer aluminum tolerance by transporting UDP-glucose to the extracellular space (Huang et al., 2009; Huang et al., 2010). At the vacuolar membrane, AtABCC1 and AtABCC2 sequester arsenic-phytochelatin complexes in the vacuolar lumen and confer tolerance to toxic metals/metalloid (Song et al., 2010; Park et al., 2011). AtABCC1 is also implicated in folate transport (Raichaudhuri et al., 2009), while AtABCC2 is the major transporter of glutathione conjugate (Lu et al., 1998; Frelet-Barrand et al., 2008). AtABCC5 functions as a phytate transporter (Nagy et al., 2009). (B–C) Loss-of-function of AtABCC1 and AtABCC2 resulted in arsenic hypersensitivity (Song et al., 2010) (B) and inhibition of vacuolar sequestration of Cd (Park et al., 2011) (C).

Figure 4.

AtABCB1, AtABCB4, and AtABCB19 are auxin transporters. (A) Phenotypes of the loss-of-function mutants of AtABCB1 and AtABCB19. Image reprinted Geisler et al. (2005) with permission from Wiley-Blackwell Publishing. (B) Localization of AtABCB1, AtABCB4, and AtABCB19 in roots and auxin fluxes mediated by these three ABCB proteins. AtABCB1 is expressed in the root differentiation zone (orange, columella and root apical meristem; Sidler et al., 1998). AtABCB4 localizes mainly to the epidermis (purple; Terasaka et al., 2005; Wu et al., 2007). AtABCB19 is expressed from the stele to the cortex and weakly in epidermal cells of the root (pink; Wu et al., 2007; Blakeslee et al., 2007). St: stele, En: endodermis, C: cortex, and Ep: epidermis. The arrows represent auxin flux.

Figure 5.

Abscisic acid (ABA) fluxes and the role of the ABA efflux and influx transporter. AtABCG25 exports ABA from parenchyma cells in the vasculature into the xylem. ABA is directed with the transpiration stream to guard cells, where AtABCG40 mediates its uptake into guard cells.

Figure 6.

Surface lipids are secreted by ABC transporters of the ABCG family. (A) Loss-of-function mutants in AtABCG26 fail to self-pollinate due to defective pollen development caused by impaired sporopollenin formation. Scale bars = 100 µm. Figure taken from Choi et al. (2011). (B) Members of the ABCG family that participate in cuticle formation by transporting components of the cuticular wax and/or cutin. See text for details. (C) AtABCG26 is involved in pollen exine formation, possibly by transporting exine precursors from the tapetum to the locules.