plasma membrane transport in context — making sense …directory.umm.ac.id/data...

236

Major advances in our understanding of the transport ofinorganic nutrient ions across plant plasma membranes haveemerged from recent studies on the control of the dominantH+-pumping ATPase and from identification of a range ofnew transporters for divalent cations, potassium, phosphateand nitrate. In many cases, multiple transporter isoformshave been described. An appreciation of the physiologicalroles of these transporters demands combined genetic andphysiological approaches, which, in the case of an outwardrectifying K+ channel, have already been used to yield anintriguing insight into root-mediated K+ release into thexylem. In this review we attempt to place some of thosedevelopments in a physiological context.

AddressesThe Plant Laboratory, Department of Biology, University of York,PO Box 373, York YO1 5YW, UK*e-mail: [email protected]

Current Opinion in Plant Biology 1999, 2:236–243

http://biomednet.com/elecref/1369526600200236

© Elsevier Science Ltd ISSN 1369-5266

AbbreviationsHAK high affinity K+ transporterKIRC K+ selective inward rectifying channelKORC K+ selective outward rectifying channelLCT low affinity cation transporterPMF protonmotive forceZIP ZRT, IRP-like protein

IntroductionPlant growth depends on the acquisition and appropriatepartitioning of inorganic solutes from the soil. The prin-cipal inorganic nutrients are potassium, nitrogen,phosphate and sulphate [1]. The latter three nutrientsare metabolised and incorporated into organic com-pounds, while K+ plays a key role in generating osmoticpressure and in compensating net negative charge ofcytosolic constituents [2]. Other essential nutrients,which are absorbed to a lesser extent, include divalentcations required as enzyme cofactors (iron, zinc, copper)or for signal transduction (calcium).

Absorption of all nutrients is energised, ultimately, by pro-ton pumps [3]. H+-ATPases are ubiquitous in plant plasmamembranes and generate an electrochemical potential dif-ference for H+ (i.e. protonmotive force [PMF]). Theelectrical component of the PMF — the membrane poten-tial — is typically of the order –150 mV, and tends to drivecation uptake requiring only the presence of a pore, orchannel. By contrast, accumulation of anionic nutrientsrequires additional energization, which is provided by cou-pling their transport to the re-uptake of H+.

This simplistic picture for cation and anion transport —although broadly correct — requires refinement. Whenpresent at very low concentrations, transport of cationssuch as K+ will require energisation by both components ofthe PMF [4]. In such cases transport requires the operationof more than one class of transport system. Furthermore,many of the proteins which catalyse transport for a givenion are expressed as a variety of isoforms. These findingsdemand that the significance of multiple pathways for iontransport be considered in a physiological context. Newinsights are also emerging into the mechanisms of controlof the activities of H+-pumping ATPases, which underlieplasma membrane energisation.

Important families of transporters for ammonium and sul-phate have been identified some years ago and have beendiscussed previously [5]. In this review we consider theproperties of recently-identified transporters for a numberof nutrient ions, including divalent cations, K+, Pi andnitrate. Their physiological roles are considered in relationto their expression patterns and, where studied, theirkinetic properties.

Regulation of H+ transportThe H+-ATPase reaction cycle includes a phosphorylat-ed intermediate state. Both the phosphorylation andATP-binding domains are conserved. The H+-ATPaseexhibits a long hydrophilic extension around the car-boxyl-terminus (Figure 1). Truncation of thecarboxyl-terminus elicits constitutive activity of theenzyme, indicating that the carboxyl-terminus is a regu-latory domain [6]. It has also been known for many yearsthat activity of the H+-ATPase is increased by the fungaltoxin fusicoccin [7], and that one potential site of inter-action of fusicoccin is with 14-3-3 proteins [8]. 14-3-3proteins are ubiquitous in all eukaryotic organisms wherethey play essential roles in cell signalling, possibly bymodulating protein phosphorylation. Only recently, how-ever, has the mode of action of fusicoccin on theH+-ATPase been explained in a molecular context, thathas general relevance to the control of H+ pumping atthe plasma membrane.

Co-purification of an active H+-ATPase and a 14-3-3 pro-tein from fusicoccin-treated tissue, but not from controltissue, indicates that direct interaction between the H+-ATPase and 14-3-3 proteins is mediated by fusicoccin[9•,10•,11]. Furthermore, cleavage of a 10 kDa fragmentfrom the carboxy-terminal of the H+-ATPase abolishedinteraction with the 14-3-3 protein, reinforcing thenotion that fusicoccin-induced stimulation is related torelief of auto-inhibition by the carboxy-terminal domain[9•]. Expression in yeast of one isoform of the H+-

Plasma membrane transport in context — making sense outof complexityFrans JM Maathuis* and Dale Sanders

Plasma membrane transport in context Maathuis and Sanders 237

ATPase from Arabidopsis thaliana, AHA2, has providedfurther evidence for functional interactions between theenzyme and 14-3-3 proteins [12••]. Thus, fusicoccinbinding activity was conferred by the carboxy-terminaldomain of AHA2, but only in the presence of 14-3-3 pro-teins. The fusicoccin binding site appears to be sharedbetween the H+-ATPase and the 14-3-3, althoughwhether an endogenous small molecule fulfils this func-tion in planta is not known.

Emerging classes of divalent cation transporterThe molecular identity of plant uptake systems for divalentcations has, until recently, been a mystery. Several develop-ments in the past few years have, however, resulted in thecharacterisation of divalent cation transporters, predomi-nantly via functional complementation of yeast mutants.

An iron-regulated metal transporter gene (IRT1), encodinga protein with eight putative transmembrane spans, has

Figure 1

The modulation of H+-ATPase activity byfusicoccin (FC) and 14-3-3 proteins. TheATPase activity shifts from low to high afterbinding of both FC plus 14-3-3 to thecarboxyl-terminus (Ct) of the pump. Neitherthe ATPase nor the 14-3-3 protein is capableof FC binding on its own (see [3]).

Ct

Low-activity state High-activity state

FC

14-3-3

Current Opinion in Plant Biology

Figure 2

Genes that encode transport systems in theplant plasma membrane and their putativefunctions as discussed in the text. CDPK;calcium/calmodulin domain protein kinase.

NRT1NRT2

Vacuole

Root symplast

AHA

APTPHTLePTMePT

Root apoplast

ZIP

H+?K+

H+

K+

K+

Zn2+

Na+/K+

Na+

Ca2+

Ca2+

Ca2+

nH+?Pi H+? NO3–

KUPHAKAtKT

SKOR

Guard cell

HKT

LCT1

ATP

Cd2+/ Ca2+?

ADP

CDPKKAT

ATP ADP

Xylem


been identified in Arabidopsis [13]. Yeast complementationexperiments suggest that IRT1 is involved in Fe2+ trans-port. Expression is most marked in roots, and is induced byiron deficiency. The IRT1 gene is a member of a familywhich includes Zn2+ transporters encoded by the ZRTgenes of yeast, known as the ZIP (for ZRT, IRP-like pro-tein) family (Figure 2).

In the case of Fe, transporter activity in delivering the ion tothe root cell is often supplemented by secretion of chelatorswhich mobilise Fe3+ from the soil. Further insights into themechanism of Fe uptake have emerged from the recentidentification of a membrane-bound ferric-chelate reductasein Arabidopsis ( see Note added in proof). At the root surface,Fe3+ → Fe2+ reduction reduces affinity for the chelator,thereby increasing the concentration of Fe2+ for subsequentuptake. The FRO2 gene was identified on the basis ofhomology with human and yeast plasma membrane enzymesthat transfer electrons from FADH2 to an acceptor on theopposing side of the membrane via two intramembrane haemgroups. FRO2 transcripts accumulate in roots in response toFe deficiency. Furthermore, FRO2 complements mutantswhich are defective in ferric chelate reductase activity. Thededuced structure of FRO2 contains a cytosolic binding sitefor FAD and conserved intramembrane His residues thoughtto be involved in coordination of the two haems.

In complementation studies using yeast zrt mutants, fourgenes (ZIP1–4), which encode transporters involved inZn2+ uptake, were identified in Arabidopsis [14••]. Each ofthese transporters is predicted to possess 7–9 transmem-brane spans, and expression of two (ZIP1 and ZIP3) ispreferential in root tissue and enhanced by Zn2+ starvation.These findings suggest that ZIP1 and ZIP3 are involved in

Zn2+ uptake from the soil. The differential substrate speci-ficity and expression patterns of ZIP isoforms might pointto their discrete physiological roles. Competition experi-ments with other divalent cations also indicate that ZIP1and ZIP3 are distinctly Zn2–-specific, while ZIP2 exhibitsequal or greater affinity for Cu2+ and Cd2+.

Sequence analysis of ZIP family members demonstrates adegree of conservation in putative transmembrane spansIV, V and VI, possibly associated with an intramembranemetal binding site [15•]. Furthermore, in the majority ofmembers, a possible heavy metal binding site has beenidentified in the extramembrane loop between transmem-brane spans III and IV. This conserved sequence has theform HXHXH, a motif found in another, otherwise unre-lated family of heavy metal transporters from bacteria.

A completely different type of transporter involved incation uptake has been identified in wheat roots andshoots. The LCT1 (for low affinity cation transporter) genewas originally identified by virtue of its ability to restoregrowth of a K+ uptake-deficient yeast in low millimolar K+

concentrations [16]. LCT1 was originally shown to trans-port K+ and Na+ in yeast; however, further workdemonstrated an ability also to transport Ca2+ and Cd2+

[17••]. Although the physiological function of LCT1 isunknown, this is the first transport system identified as acandidate for mediating Ca2+ uptake by plant cells.

Our knowledge of the pathways for divalent cation transportacross the plasma membrane therefore remains fragmentary,yet, significant advances can be expected in the comingyears, not only from complementation screens, but also frombioinformatic approaches to genome sequences.

238 Physiology and metabolism

Table 1

Gene products involved in the uptake and translocation of K+ in plants.

Protein Species Type Expression Inhibitors Function Reference

AKT1 A. thaliana Channel Root cortex Cs+/TEA/Ba2+ Low and high [18••]affinity uptake

SKOR A. thaliana Channel Root pericycle Translocation [25••]Xylem parenchyma to shoot

HvHAK1–2 Barley Carrier Root Na+/NH4+ High affinity uptake [19••]

Wheat (Km of 27 µM)Rice

A. thaliana

AtKUP1–4 A. thaliana Carrier Flower/leaf Cs+ High affinity uptake [21•](AtKT1–2) Root/stem (Km of 22 µM) with

low affinity component

AtKUP1 A. thaliana Carrier Root Cs+/Ba2+ Dual affinity uptake [20•](Kms of 44 µM and 11mM)

HKT1 Wheat Carrier Root High affinity uptake [22–24]Barley (Km of 3 µM), low

affinity Na+ uptakeRice Na+ uptake

Potassium transportTo maintain the essential roles that K+ plays in cellularhomeostasis requires sophisticated means to move K+ atkey locations throughout the plant, which include thesoil/root interface, the xylem, and cells involved in move-ment, for example in guard cells, which are responsible forthe opening and closing of stomatas.

K+ transport at the soil/root interfaceThe process of K+ uptake in plant roots has been a majorfocus of plant physiology. Conventionally, K+ accumulationat various ambient K+ concentrations is perceived as occur-ring at the root cell plasma membrane through two or moreindependent influx systems with respectively high and lowaffinities. Traditionally, low affinity K+ uptake is believedto be mediated by K+ selective ion channels, a notion sup-ported by both patch clamp characterisation of root K+

channels and yeast complementation studies [2].Thermodynamic constraints require energisation of highaffinity K+ uptake via carriers [4].

The convenient notion of a channel and carrier mediatedlow and high affinity K+ uptake is rapidly crumbling in theface of recent data. Functional analysis of the role of AKT1(a K+ selective inward rectifying channel or KIRC) in plan-ta has been advanced [18••] by identifying an AKT1 nullmutant (akt1-1) from an Arabidopsis T-DNA mutagenisedpopulation. Surprisingly, differences in growth betweenwild type and akt1-1 were apparent only in the presence ofmillimolar ammonium and with K+ levels of >1 mM. In thepresence of ammonium, Rb+ uptake from external solu-tions was reduced, but progressively so at lower Rb+

concentrations. A reduced Rb+ influx in the mutant alsooccurred in the absence of ammonium conditions where nophenotype was observed. The combined results of thisstudy indicate that, in the presence of ammonium, theAKT1 channel plays a role in high affinity K+ uptake.They also indicate that AKT1 may not be the predomi-nant low affinity K+ influx pathway in A. thaliana roots, asat 1 mM external Rb+ concentrations the mutant showsaround 70% of the wild-type uptake.

With a sufficiently negative membrane potential, theinflux of K+, even from lower micromolar concentrations,can proceed ‘down hill’ and this obviates the requirement

for an energised carrier mechanism. Nevertheless, a largenumber of carrier type K+ transporters has now beenidentified (Table 1, Figure 2). In barley, HvHAK wascloned [19••] using degenerate primers for conservedregions of the Schwanniomyces HAK (high affinity K+)transporter. Complementation of K+ transport deficientyeast restored high affinity Rb+ uptake, which, in agree-ment with the observations of Hirsch et al. [18••], wassensitive to ammonium. The HvHAK1 protein has 12putative membrane spanning regions and is a member ofa large conserved family of transporters that are highly K+

selective and probably function as H+ coupled systems[19••]. The barley member of this family shows homolo-gy to HAK/KUP transporters found in bacteria(Escherichia coli), fungi (Schwanniomyces occidentalis),plants (Lyphopyrum, wheat, rice and Arabidopsis) and ani-mals (Homo sapiens). HvHAK1 transcript is exclusivelyfound in roots and highly induced by K+ starvation, whichis in agreement with the frequently observed induction ofhigh affinity K+ uptake in intact plants.

By searching for HAK/KUP homologues in A. thalianaEST databases, several groups isolated a number ofHAK/KUP isoforms (AtKUP 1–4). The Rb+ and K+ trans-port capacity of AtKUP1 was analysed in homologousand heterologous expression systems [20•,21•]. In bothexpression systems AtKUP1 mediated high affinity Rb+

transport with a micromolar Km indicating a role in highaffinity K+ transport in vivo. In addition to high affinityK+ transport, AtKUP1 expressing yeast cells showed arise in Rb+ uptake from millimolar concentrations [20•].The latter suggests that HAK/KUP type proteins mayalso contribute to low affinity K+ transport. Expressionpatterns of AtKUP1 differ in various reports (Table 1) andexpression of at least one isoform (AtKUP3) is up regu-lated upon K+-starvation [21•].

A class of putative high affinity K+ transporters, not relat-ed to HAK/KUP, is provided by HKT1 type mechanisms[22]. Originally cloned from wheat, HKT1 catalysesK+:Na+ (µM ambient Na+) or Na+:Na+ (mM ambient Na+)symport. Homologues of HKT1 have been found in bar-ley [23], rice [24] and A. thaliana [22] and in both barleyand wheat mRNA levels increase in K+ starvation condi-tions [23]. The physiological relevance of HKT1 remains


Table 2

Gene products involved in the uptake of phosphate in plants.

Protein Species Expression Transport Km Reference

APT1–2 (APT1–4) A. thaliana Root/low level in leaf – [33,35•]

PHT1 A. thaliana Root 3 µM [34]

StPT1–2 Potato Root/tuber/leaf flower 280 and 130 µM [31•]

LePT1 Tomato Root/mature leaf 31 µM [30•]

MtPT1–2 M. trunculata Root 192 µM [32•]

to be clarified but may be in providing a pathway for Na+

entry into the plant [24].

K+ release into the xylemSKOR [25••] is an Arabidopsis K+ selective channel and amember of the Shaker gene family (Figure 3). Shaker typechannels are K+ selective, voltage gated outward rectifyingchannels that were first identified in Drosophila shakermutants. In spite of the large degree of homology to KATand AKT inward rectifying channels, SKOR mediates K+

efflux. How such similar primary protein structures resultin K+ channels with contrasting voltage sensitivity remainsto be explained. Expression patterns and gene disruptionmutants imply a clearly defined function for SKOR inxylem loading of K+: GUS constructs with the SKOR pro-moter show expression restricted to the root pericycle andxylem parenchyma cells. Disruption of the SKOR gene did

not affect root K+ levels but caused a decrease in xylem sapK+ and a reduction in shoot K+ contents, consistent with afunction in K+ release into the xylem. Exposure of plantsto the stress hormone ABA, which is believed to play a rolein ion translocation to the shoot, resulted in a rapiddecrease of SKOR transcript.

K+ transport in guard cellsThe first plant K+ channels were identified in guard cellswhich control stomatal aperture by osmotic swelling andshrinking caused by the movement of large amounts ofK+. Via the membrane voltage, either inward or outwardrectifying channels are activated to allow a sustained inwardor outward flux of K+ for stomatal opening or closing,respectively. A variety of stimuli such as ABA, CO2 andoxidative stress promote stomatal closure, probably via araise in cytosolic Ca2+. A direct target for cytosolic Ca2+


Figure 3

Model according to Doyle et al. 1998 [44] forthe permeation of K+ ions through an inwardrectifying K+ channel with a pore regionsimilar to that of the Shaker family K+

channels. Ions traverse a narrow pore withinthe channel, which forms the selectivity filter(SF) and can hold two ions simultaneously.The large aqueous cavity helps to stabilisecation(s) in the middle of the membrane bythe dipole action of the depicted helices.

SF


– –

Figure 4

Generalised model for the topology of highaffinity phosphate carriers. Transmembranespans show an internal repeat and arearranged in a typical 6+6 structurecharacteristic of many carriers belonging tothe major facilitator superfamily. The largecytoplasmic loop contains a putativephosphorylation site for kinase C.

COOHNH2


has now been described in Vicia faba guard cells [26] as aCa2+ dependent protein kinase that phosphorylates anddown regulates KAT1, the predominant KIRC in guardcell plasma membranes.

Cytosolic Ca2+ also affects the activity of a newly identifiedK+ selective outward rectifying channel (KORC) [27]. Incontrast to previously described KORCs that show sus-tained currents, this particular type of KORC rapidlyinactivates. The physiological role of this channel remainsto be elucidated, but may be in the transduction of signalsduring stomatal closing. Additional potential modulators ofstomatal aperture that act on K+ channels are agents thataffect the polymerisation of actin filaments [28] and theosmolarity of solutions facing the membrane [29].

Phosphate uptake in plant rootsPhosphate is an essential macronutrient and plant cells con-trol cytosolic phosphate within narrow limits by balancingimport and export. Rates of phosphate uptake depend ongrowth demand and phosphate supply, the latter frequent-ly being inadequate due to the low mobility of phosphatein the soil. At the prevailing soil pH, phosphate is mostreadily taken up by plants as H2PO4–. External concentra-tions of this nutrient are typically a few micromolar inphysiological conditions, whereas cytosolic levels are a1000-fold higher. Phosphate transport shows a pronouncedpH optimum, is highly sensitive to uncouplers [30•] and isgenerally assumed to occur via H+ coupled symport.

Several genes encoding high affinity phosphate trans-porters have been cloned (Table 2; [30•–32•,33,34,35•]).The proteins encoded by these genes are around 60 kD,and show high levels of homology to each other and to thehigh affinity phosphate transporters of yeast PHO84 [36]and mycorrhizal fungi GvPT [37]. APT1 and APT2 [35•] forexample, are both expressed in Arabidopsis root tissue andshare 99% identity in their coding regions; however, theirpromoter regions are very different, pointing to cell-type-specific or development-specific expression for either gene.

Hydrophobicity plots show a common structure of12 transmembrane spans that contain an internal repeat of6 + 6 transmembrane spans (Figure 4) with a large centralhydrophobic region protruding into the cytosol that carriesa highly conserved putative kinase phosphorylation site. Insome cases transcript levels were shown to be sensitive tothe phosphate status of the plant (e.g. for APT1, APT2)whereas other genes appear to be constitutively expressed(e.g. for StPT2).

The functional analysis of LePT1 from tomato [30•] and ofMtPT1 from Medicago [32•] was carried out in the yeastpho84 strain. In both cases, yeast growth was restored onmicromolar phosphate and transport assays confirmed therestoration of phosphate uptake with an apparent Km of 31µM for LePT1 and 192 µM for MtPT1. Both Km values aremuch higher than those established in intact plants and may

result from the use of Saccharomyces as expression systemwhere the interaction of several proteins is necessary for theproper functioning of high affinity phosphate transport [36].

The relative contribution of these gene products to theoverall uptake of phosphate by plants will be affected bythe formation of mycorrhizae, which can drasticallyimprove plant phosphate nutrition. The presence of myc-orrhizae will shift phosphate uptake to GvPT-typetransporters at the soil/fungus interface and can reduce theamount taken up by the plant root to almost nil. Themechanism of phosphate transfer from fungus to rootremains unknown but probably involves separate geneproducts as was shown for Medicago where MtPT transcriptwas significantly reduced after mycorrhiza formation [32•].

Nitrate uptake Nitrate uptake from the soil has long been suspected,from kinetic studies, to involve an array of different trans-port systems. Thus, constitutive high affinity andnon-saturable kinetic phases exist in roots along with ahigh affinity phase, which is induced by nitrate [38]. Theproperties of the transport systems that underlie thiskinetic complexity are beginning to be elucidated withcandidate genes falling into two families.

The first family of nitrate transporters is identified by aconsensus motif (FYXXINXGSL), characteristic of thePTR family of peptide transporters present in yeast,plants and mammals. At least two members of this fami-ly are present in Arabidopsis: NRT1 (or CHL1) andNRT3 (or NLT3) [38]. NRT1 expression is inducible bynitrate, whereas that of NRT3 appears to be constitutive.Until recently both transport systems were thought to beinvolved only in low affinity transport. Careful analysisof one chl1 mutant line containing an active transposableelement in CHL1, however, revealed defects in both lowand high affinity transport [39••]. The extent to whichCHL1 participates in high affinity transport dependscritically on growth conditions: the presence of ammoni-um ions results in a marked contribution of CHL1 tohigh affinity uptake, whereas in the absence of ammoni-um no contribution is apparent. CHL1, therefore,appears to behave as a dual affinity transporter, a phe-nomenon that can be explained by random binding of H+

and nitrate to the carrier [40].

A CHL1 homologue from Brassica napus has been func-tionally characterised in oocytes with respect to substratespecificity [41••]. Generally, transport carriers exhibit ahigh degree of substrate specificity and it was, therefore,surprising to find that CHL1 not only translocates nitrate,but also histidine and to a lesser extent, other basic aminoacids. The physiological significance of this observationis not known but could relate to delivery of amino acidsto growing cells. Resolution of expression patterns at acellular level could help resolve this issue; it is alreadyknown that two putative nitrate transporters in the PTR



family exhibit differential expression patterns in tomatoroots [42].

Members of the second nitrate transporter family (NRT2)are nitrate inducible, belong to the major facilitator super-family and were identified originally on the basis ofhomologies to fungal and algal nitrate transporters [38].Confirmation of a role in nitrate transport awaits their func-tional expression or the identification of mutants in thesegenes. The high degree of correlation between expressionlevels of the tobacco transporter NRT2 with high affinitynitrate transport activity, however, provides evidence for afunction in inducible, high affinity nitrate transport [43•].

Conclusions and prospectsThe number of transporters identified at a molecularlevel has increased dramatically over the past years. Forany given nutrient, an array of potential transport path-ways is present at the plasma membrane, even within asingle species.

At one level, this complexity reflects the presence of iso-forms that are often expressed on a tissue- or celltype-specific basis. Isoforms enable transport to be con-trolled at a transcriptional level in response todevelopmental or environmental signals. At a secondlevel, different classes of transporter are apparent for ionslike K+ and nitrate which may reflect the wide range ofnutrient concentrations to which plants are exposed.Although the complexity of multiple transport pathwayswill doubtless increase as genomic information expands,we can expect marked advances in our understanding ofthe functional attributes of transporters with the combina-tion of reverse genetic and physiological approaches overthe coming years.

Considerable effort and expense is required for the inor-ganic fertilisation of many agricultural systems. Manysuch systems are, indeed, over-fertilised, with devastatingconsequences for water courses which become eutrophic.Identification of those transporters which are pivotal inthe uptake of inorganic nutrients from the soil and thesubsequent redistribution of nutrients around the plantoffers the exciting possibility of engineering more effi-cient strategies for fertiliser application. Such strategiesshould focus not only on the mechanisms for soluteuptake, involving, for example, the affinity of the trans-porter for the ion. In addition the clear implication of thepresence of multiple isoforms is that transcriptional and/orpost-translational controls might differ, and elucidatingthe pathways leading to regulation of transporter activitycan be predicted to become a new and major goal of stud-ies in nutrient acquisition.

Note added in proofFurther insights into the mechanism of Fe uptake haveemerged from the recent identification of a membrane-bound ferric-chelate reductase in Arabidopsis [45••].

References and recommended readingPapers of particular interest, published within the annual period of review,have been highlighted as:

• of special interest••of outstanding interest

1. Marschner H: Mineral Nutrition of Higher Plants. London: AcademicPress; 1995

2. Maathuis FJM, Sanders D: Mechanisms of potassium absorption byhigher plant roots. Physiol Plant 1996, 96:158-168.

3. Palmgren MG, Fuglsang AT, Jahn T: Deciphering the role of 14-3-3-proteins. Exp Biol On line 1998, 3:1-20.

4. Maathuis FJM, Sanders D: Energization of potassium uptake inArabidopsis thaliana. Planta 1993, 191:302-307.

5. Assmann SM, Haubrick LL: Transport proteins of the plant plasmamembrane. Curr Opin Cell Biol 1996, 8:458-467.

6. Palmgren MG, Larsson C, Sommarin M: Proteolytic activation of theplant plasma-membrane H+-ATPase by removal of a terminalsegment. J Biol Chem 1990, 265:13423-13426.

7. Radice M, Scacchi A, Pesci P, Beffagna N, Marre MT: Comparative-analysis of the effects of fusicoccin (fc) and of its derivativedideacetylfusicoccin (daf) on maize leaves and roots. Physiol Plant1981, 51:215-221.

8. Korthout HAAJ, deBoer AH: A fusicoccin binding-protein belongsto the family of 14-3-3-brain protein homologs. Plant Cell 1994,6:1681-1692.

9. Jahn T, Fuglsang AT, Olsson A, Bruntrup IM, Collinge DB,• Volkmann D, Sommarin M, Palmgren MG, Larsson C: The 14-3-3

protein interacts directly with the c-terminal region of the plantplasma membrane H+-ATPase. Plant Cell 1997, 9:1805-1814.

In this study, detergent-solubilised plasma membrane H+-ATPase isolatedfrom fusicoccin-treated maize was copurified with the 14-3-3 protein, yield-ing H+-ATPase in an activated state. In the absence of fusicoccin treatment,H+-ATPase was recovered in a nonactivated form.

10. Oecking C, Piotrowski M, Hagemeier J, Hagemann K: Topology and• target interaction of the fusicoccin-binding 14-3-3 homologs of

Commelina communis. Plant J 1997, 12:441-453.Experiments carried out with sealed plasma membrane vesicles show thatthe fusicoccin-binding site faces the cytoplasmic surface of the membrane.Stabilisation of the labile ATPase–14-3-3 complex in plasma membranescould be achieved by fusicoccin treatment in vivo or in vitro. The carboxyl-terminus probably represents the binding domain for 14-3-3 homologues.

11. Oecking C, Hagemann K: Association of 14-3-3 proteins with theC-terminal antoinhibitory domain of the plant plasma-membraneH+-ATPase generates a fusicoccin-binding complex. Planta 1999,207:480-482.

12. Baunsgaard L, Fuglsang AT, Jahn T, Korthout HAAJ, deBoer AH,•• Palmgren MG: The 14-3-3 proteins associate with the plant plasma

membrane H+-ATPase to generate a fusicoccin binding complexand a fusicoccin responsive system. Plant J 1998, 13:661-671.

By testing the fusicoccin binding activity of yeast membranes, the carboxy-termi-nal regulatory domain of AHA2 was found to be part of a functional fusicoccinreceptor, a component of which was the 14-3-3 protein. ATP hydrolytic activity ofAHA2 expressed in yeast internal membranes was activated by all tested isoformsof the 14-3-3 protein of yeast and Arabidopsis, but only in the presence of fusic-occin.

13. Eide D, Broderius M, Fett J, Guerinot ML: A novel iron-regulatedmetal transporter from plants identified by functional expressionin yeast. Proc Natl Acad Sci USA 1996, 93:5624-5628.

14. Grotz N, Fox T, Connolly E, Park W, Guerinot ML, Eide D: Identification•• of a family of zinc transporter genes from Arabidopsis that respond

to zinc deficiency. Proc Natl Acad Sci USA 1998, 95:7220-7224.Report on the identification of ZIP genes from Arabidopsis as encoding Zn2+

transporters. Expression in yeast reveals high specificity of two members of thefamily for Zn2+, and transcript levels are upregulated in roots on Zn2+ starvation.The plant ZIP transporters are related to metal transporters found in many othereukaryotes, including yeast, protozoa and — more distantly — humans.

15. Eng BH, Guerinot ML, Eide D, Saier MH: Sequence analyses and• phylogenetic characterization of the ZIP family of metal ion

transport proteins. J Membr Biol 1998, 166:1-7.Review about heavy metal ion transporters in plants and yeast that are mem-bers of the ZIP family.

16. Schachtman DP, Kumar R, Schroeder JI, Marsch EL: Molecular andfunctional characterization of a novel low-affinity cationtransporter (LCT1) in higher plants. Proc Natl Acad Sci USA 1997,94:11079-11084.


17. Clemens S, Antosiewicz DM, Ward JM, Schachtman DP: The •• plant cDNA LCT1 mediates the uptake of calcium and cadmium in

yeast. Proc Natl Acad Sci USA 1998, 95:12043-12048.Expression of LCT1 in yeast renders growth of yeast more sensitive to Cd2+.Ion flux assays showed an increase in Cd2+ uptake. Growth assays alsodemonstrate a sensitivity of LCT1-expressing yeast cells to extracellular mil-limolar Ca2+ concentrations. It is concluded that LCT1 can mediate uptakeof Ca2+ and Cd2+ in yeast and possibly also in plants.

18. Hirsch RE, Lewis BD, Spalding EP, Sussman MR: A role for the AKT1•• potassium channel in plant nutrition. Science 1998, 280:918-921.Reverse genetic screening identified an Arabidopsis thaliana mutant inwhich the AKT1 channel gene was disrupted. Roots of this mutant lackedinward-rectifying potassium channels and displayed reduced potassium(rubidium-86) uptake in the presence of ammonium.

19. Santa-Maria G, Rubio F, Dubcovsky J, Rodriguez-Navarro A: The•• HAK1 gene of barley is a member of a large gene family and

encodes a high-affinity potassium transporter. Plant Cell 1997,Cloning and partial characterisation are described for a barley high affinityK+ transporter that is expressed in root cells and which shows a high degreeof homology to bacterial high affinity K+ transporters.

20. Fu H, Luan S: AtKUP1: a dual affinity K+ transporter from• Arabidopsis. Plant Cell 1998, 10:63-67.Characterisation of AtKUP3 — a K+ transporter — in yeast. When expressedin yeast, AtKUP3 functions in both high-and low-affinity uptake.

21. Kim EJ, Kwak JM, Uozumi N, Schroeder JI: AtKUP1: an Arabidopsis• gene encoding high-affinity potassium transport activity. Plant

Cell 1998, 10:51-62.The identification of AtKUP from Arabidopsis thaliana via homology screeningof non-plant Kup and of HAK1 potassium transporters from Escherichia coliand Schwanniomyces occidentalis. AtKUP1 and AtKUP2 are able to comple-ment a potassium transport deficient E. coli triple mutant. Kinetic characterisa-tion and expression patterns are reported. Through sequence analysis a familyspecific signature sequence and metol-binding domains are described.

22. Schachtman DP, Schroeder JI: Structure and transport mechanismof a high-affinity potassium uptake transporter from higherplants. Nature 1994, 370:655-658.

23. Wang TB, Gassmann W, Rubio F, Schroeder JI, Glass ADM: Rapidupregulation of HKT1, a high-affinity potassium transporter gene,in roots of barley and wheat following withdrawal of potassium.Plant Physiol 1998, 118:651-659.

24. Golldack D, Kamasani UR, Quigley F, Bennett J, Bohnert HJ: Saltstress-dependent expression of a HKT1-type high affinitypotassium transporter in rice. Plant Physiol 1997, 114:529

25. Gaymard F, Pilot G, Lacombe B, Bouchez D, Bruneau D, Boucherez J,•• Michaux-Ferriere M, Thibaud J, Sentenac H: Identification and

disruption of a plant Shaker-like outward channel involved in K+

release into the xylem sap. Cell 1998, 94:647-655.SKOR, a K+ channel identified in Arabidopsis, displays the typical hydrophobiccore of the Shaker channel superfamily. Expression in Xenopus oocytes identi-fied SKOR as the first member of the Shaker family in plants to be outwardlyrectifying. SKOR expression is localised in root stelar tissues and evidence indi-cates that SKOR is involved in K+ release into the xylem sap toward the shoots.

26. Li J, Lee YR, Assmann SM: Guard cells possess a calcium-dependentprotein kinase that phosphorylates the KAT1 potassium channel.Plant Physiol 1998, 116:785-795.

27. Pei Z, Baizabal-Aguirre VM, Allen GJ, Schroeder JI: A transientoutward rectifying K+ channel current down-regulated by cytosolicCa2+ in Arabidopsis thaliana guard cells. Proc Natl Acad Sci USA1998, 95:6548-6553.

28. Hwang J, Suh S, Yi H, Kim J, Lee Y: Actin filaments modulate bothstomatal opening and inward K+ channel activities in guard cellsof Vicia faba L. Plant Physiol 1997, 115:335-342.

29. Liu K, Luan S: Voltage-dependent K+ channels as a target ofosmosensing in guard cells. Plant Cell 1998, 10:1957-1970.

30. Daram P, Brunner S, Persson PL, Amrhein N, Bucher M: Functional• analysis and cell-specific expression of a phosphate transporter

from tomato. Planta 1998, 206:225-233. Expression of LePT1, high affinity phosphate transporter from tomato, in aphosphate-uptake-deficient yeast mutant. Phosphate transport shows a Kmof 31 µM and is highly dependent on the external pH. The work presentsmolecular and biochemical evidence for distinct root cells playing an impor-tant role in phosphate acquisition at the root/soil interface.

31. Leggewie G, Wilmitzer L, Riesmeier JW: Two cDNAs from potato are• able to complement a phosphate uptake-deficient yeast mutant:

identification of phosphate transporters from higher plants. PlantCell 1997, 9:381-392.

Description and isolation of two cDNAs, StPT1 and StPT2, from potato thatshow homology to the phosphate/proton cotransporter from yeast.

32. Liu H, Trieu AT, Blaylock LA, Harrison MJ: Cloning and• characterization of two phosphate transporters from Medicago

trunculata roots: regulation in response to phosphate andcolonization by arbuscular mycorrhizal (AM) fungi. MolPlant–Microbe Interact 1998, 11:14-22.

Identification of two cDNA clones (MtPT1 and MtPT2) encoding phosphatetransporters from a mycorrhizal root cDNA library (Medicago truncatula/Glomusversiforme). The cDNAs represent M. truncatula genes and the encoded pro-teins share identity with high-affinity phosphate transporters from Arabidopsis,potato, yeast, Neurospora, and the arbuscular mycorrhizal fungus G. versiforme.

33. Lu YP, Zhen RG, Rea PA: AtPT4: a fourth member of theArabidopsis phosphate transporter gene family. Plant Physiol1997, 114:747-751.

34. Mitsukawa N, Okumura S, Shirano Y, Sato S, Kato T, Harashima S,Shibata D: Overexpression of an Arabidopsis thaliana high-affinityphosphate transporter gene in tobacco cultured cells enhancescell growth under phosphate-limited conditions. Proc Natl AcadSci USA 1997, 94:7098-7102.

35. Smith FW, Ealing PM, Dong B, Delhaize E: The cloning of two• Arabidopsis genes belonging to a phosphate transporter family.

Plant J 1997, 11:83-92.Two genes, APT1 and APT2, with DNA sequences that exhibit significantsequence identity to yeast and fungal H+/orthophosphate co-transporters,isolated from Arabidopsis thaliana are described. Both are predominantlyexpressed in root tissues and the level of expression is regulated by thephosphorus status of the plant.

36. Yompakdee C, Ogawa N, Harashima S, Oshima Y: A putativemembrane protein, PHO88p, involved in inorganic phosphatetransport in Saccharomyces cerevisiae. Mol Gen Genetics 1996,251:580-590.

37. Harrison MJ, VanBuuren ML: A phosphate transporter from themycorrhizal fungus Glomus versiforme. Nature 1995, 378:626-629.

38. Crawford NM, Glass ADM: Molecular and physiological aspects ofnitrate uptake in plants. Trends Plant Sci 1998, 3:389-395.

39. Wang RC, Liu D, Crawford NM: The Arabidopsis CHL1 protein•• plays a major role in high-affinity nitrate uptake. Proc Natl Acad

Sci USA 1998, 95:15134-15139.A search performed to find high-affinity phosphate uptake mutants by usingchlorate selections on plants containing Tag1 transposable elements yield-ed a chlorate-resistant mutant with a Tag1 insertion in CHL1. Analysisshowed that chl1 mutants have reduced high-affinity uptake in addition toreduced low-affinity uptake.

40. Sanders D: Generalized kinetic analysis of ion driven cotransportsystems: II. Random ligand binding as a simple explanation fornon-Michaelis kinetics. J Membr Biol 1986, 90:67-87.

41. Zhou JJ, Theodoulou FL, Muldin I, Ingemarsson B, Miller AJ: Cloning•• and functional characterization of a Brassica napus transporter

that is able to transport nitrate and histidine. J Biol Chem 1998,273:12017-12023.

A full-length cDNA for a membrane transporter was isolated from Brassicanapus by its sequence homology to a previously cloned Arabidopsis lowaffinity nitrate transporter. The properties of the transporter are consistentwith a proton cotransport mechanism for nitrate. Histidine is also transport-ed with an affinity was in the millimolar range.

42. Lauter FR, Ninnemann O, Bucher M, Riesmeier JW, Frommer WB:Preferential expression of an ammonium transporter and of twoputative nitrate transporters in root hairs of tomato. Proc NatlAcad Sci USA 1996, 93:8139-8144.

43. Krapp A, Fraisier V, Scheible WR, Quesada A, Gojon A, Stitt M,• Caboche M, Daniel-Vedele F: Expression studies of NRT2:1NP, a

putative high-affinity nitrate transporter: evidence for its role innitrate uptake. Plant J 1998, 14:723-731.

Expression levels of the gene Nrt2Np, a putative high-affinity nitrate transporterof Nicotiana plumbaginifolia, are studied under variable physiological conditions.

44. Doyle DA, Cabral JM, Pfeutzner RA, Kuo A, Gulbis JM, Cohen SL, ChaitBT, MacKinnon R: The structure of the potassium channel: molecularbasis of K+ conduction and selectivity. Science 1998, 280:69-77.

45. Robinson NJ, Proctor CM, Connolly EL, Guerinot ML: A ferric-chelate•• reductase for ion uptake from soils. Nature 1998, 397:694-697.Identification and characterisation of a gene involved in the reduction of fer-ric chelates in Arabidopsis roots. The gene product, FRO2, has a putativebinding site for FAD on the cytosolic side of the membrane, and coordina-tion sites for two intramembrane haems which are thought to be involved inreduction of Fe3+ on the external surface.

plasma membrane transport in context — making sense …directory.umm.ac.id/data...

Documents