Plant Hormone Transporters: What We Know and What We Would Like to Know Jiyoung Park1*, Youngsook Lee2, Enrico Martinoia3 and Markus Geisler4*
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Park et al. BMC Biology (2017) 15:93 DOI 10.1186/s12915-017-0443-x REVIEW Open Access Plant hormone transporters: what we know and what we would like to know Jiyoung Park1*, Youngsook Lee2, Enrico Martinoia3 and Markus Geisler4* Abstract inputs with plant endogenous signaling requires the action of hormone transporting proteins. Evidence for this in- Hormone transporters are crucial for plant hormone cludes severe developmental and physiological impact that action, which is underlined by severe developmental is caused by hormone transporter loss-of-function muta- and physiological impacts caused by their loss-of- tions: without transport, no correct hormone action. function mutations. Here, we summarize recent Long distance transport has been demonstrated for knowledge on the individual roles of plant hormone many plant hormones, including auxins, abscisic acid transporters in local and long-distance transport. Our (ABA), cytokinins, gibberellins (GAs), strigolactones, inventory reveals that many hormones are transported and salicylic acid. Hormones transported with the tran- by members of distinct transporter classes, with an spiration stream have to be loaded into the xylem and apparent dominance of the ATP-binding cassette unloaded at the target cells. Similarly, hormones trans- (ABC) family and of the Nitrate transport1/Peptide ported through the phloem may also require loading and transporter family (NPF). The current need to explore unloading steps. Transporters involved in long distance further hormone transporter regulation, their transfer of auxin, ABA, cytokinins, and strigolactones functional interaction, transport directionalities, and have been reported, and further investigation would substrate specificities is briefly reviewed. allow us to understand fully how individual transporters cooperate to achieve a systemic level of transport includ- ing via xylem or phloem. In cases where long-distance Plants need many hormone transporters transport is achieved by cell-to-cell transport, such as The hormone concept was coined in the beginning of for auxins, the highly coordinated action of import and the 20th century, although it had been already postu- export transporters at the contact surfaces of neighbor- lated by the Darwins based on their observation that ing cells is needed. For local action of hormones (para- phototropic bending of coleoptiles employs a spatial sep- crine-like in animals) in some tissues such as seeds, aration between the place of sensing in the shoot tip and short-distance transport between cells is sufficient, the place of bending in the shoot below [1]. Today we which could be carried out by exporter and importer ‘ ’ know that what Darwin called certain influence [1] is proteins in adjacent cells (for example, see “Abscisic the phytohormone auxin, which is synthesized in the acid” section). Furthermore, in most cases plant hor- coleoptile tip, where light is sensed, and transported mones do not have only one target cell; therefore, sev- down to the appropriate site of action in the shoot [2]. eral pairs of importers and exporters are required for the Since then, many plant hormones have been identified correct allocation and in order to guarantee the function and most have been found to be synthesized at different of a complex hormonal network. sites from their actions. Thus, it has become evident that Only in a few cases has it been demonstrated that a hormones are transported, and consequently, hormone plant hormone is synthesized in the same cells where its transporters are essential for precise regulation of plant function is required, and these may not require intercellu- growth and development by plant hormones. Now we lar transport mechanisms. A well-documented example understand that the proper integration of environmental regards ABA. Guard cells are able to synthesize ABA autonomously upon drought, thus rapidly closing stomata * Correspondence: [email protected]; [email protected] to prevent water loss [3]. Another case is ethylene, which 1Division of Biological Sciences, University of California, San Diego, 9500 Gilman Drive, La Jolla, CA 92093-0116, USA is highly volatile and diffuses freely through lipid 4Department of Biology, University of Fribourg, 1700 Fribourg, Switzerland membranes. Therefore, ethylene synthesized at a specific Full list of author information is available at the end of the article © Park et al. 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Park et al. BMC Biology (2017) 15:93 Page 2 of 15 location could be perceived by other cells far away from with respect to their discrete regulation, functional inter- its site of synthesis as well as in the same cells without the action, transport directionality, and substrate specificity. need for a transporter [4]. However, it should be mentioned that the ethylene precursor ACC is mobile, What we know about plant hormone transporters and hence in this case it is not the hormone itself that is Auxins transported, but its precursor [5, 6]. Natural auxins represent a surprisingly heterogeneous Several hormones such as auxin and ABA are weak group of small aromatic carboxylic acids that act as a acids and hence partially present in their protonated forms main coordinative signal for virtually all plant growth in physiological pH conditions, which can diffuse quite and development processes [9]. The most abundant easily through membranes [7, 8]. Therefore, originally it auxin, IAA (indole-3-acetic acid), controls transcrip- has been postulated that transport of auxin and ABA from tional regulation of multiple developmental processes via the apoplast into cells would occur by diffusion through activation of a nuclear co-receptor complex (for a the plasma membrane. Nowadays we know that diffusion review, see [9]) but seems to regulate plant performance of these hormones over the plasma membrane plays only also on the post-transcriptional level [10]. a minor role in vivo and that transporters are required for Auxin responses depend on local auxin concentrations proper delivery of auxin and ABA (see “Auxin” and that are created by combinations of auxin biosynthesis, “Abscisic acid” sections for details). metabolism, and transport [7, 9]. In higher plants, IAA In this review, identification of plant transporters im- is translocated by two pathways: first, a fast, non- plicated in hormone transport and their individual and directional passive transport through the phloem vascu- overlapping roles will be discussed. The transporters lature from biosynthetically active source tissues (such range from primary active pumps belonging to the ATP as young shoots) towards sink tissues (such as the root) binding cassette (ABC) transporter family (which couple [7]. Second, a slow, directional cell-to-cell transport of hormone translocation to direct ATP hydrolysis); anti- IAA, usually referred to as polar auxin transport (PAT), porters and symporters from the NITRATE TRANS- that is provided by active movement of IAA over the PORTER (NRT) and Multidrug and toxic compound plasma membrane by auxin transporter proteins [9]. The extrusion (MATE) transporter families (which use the directional, cell-to-cell transport is also possible for proton motive force to create hormone concentration other plant hormones (such as jasmonic acids or strigo- gradients); and facilitators of the SWEET family. This re- lactones [11]), but has not yet been clearly demonstrated view will highlight how hormone transporters have been [12]. During PAT, local auxin minima and maxima, initially identified and—if so—how their individual activ- which are thought to be responsible for many develop- ities and their substrate specificities have been verified. mental cues, are established, maintained, and fine-tuned This would be crucial because deducing transport activ- by independent and combined action of members of at ities from protein sequence alignments or mutant phe- least three major families of auxin transporters [13] notypes can have many pitfalls. For example, large (Fig. 1): AUXIN1-RESISTANT1 (AUX1)/LIKE AUX1 substrate ranges of ABC, NRT, and MATE transporter (hereafter AUX1/LAX), PIN-FORMED proteins (here- families make it difficult to predict a specific function of after PINs), and members of the B subfamily of ATP a transporter in hormone transport without adequate binding cassette (ABC) transporters (hereafter ABCBs) biochemical analyses. In cases where a protein of interest [14, 15]. While the aux1 and pin1 mutants were first functions as a modulator of other transporters, it is ne- identified in genetic screens for auxin (2,4-D) resistance cessary to carefully interpret transport activities/mutant [16] and developmental (flower) phenotypes [17], re- phenotypes to elucidate functions of the modulator spectively, ABCB19/MDR1/PGP19 was originally iso- itself. Furthermore, phenotypes of transporter mutant lated in a screen for genes differentially expressed in plants need to be carefully examined since they may re-