Minireview Rhesus factors and ammonium: a function in efflux?
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1 Minireview Rhesus factors and ammonium: a function in efflux? 7MA K@AMEC E? L 9EH, HEI4A B* H AH )@@HAII A JHK B H A K =H>E CEA@AH2B = A ->AHD=H@ =H I 7 ELAHIEJ J )KB@AH HCA IJA A % %$6 >E CA /AH = O 9 B* H AH - =E M>B( >F K E JKA>E Published: 9 March 2001 Genome Biology 2001, 2(3):reviews The electronic version of this article is the complete one and can be found online at BioMed Central Ltd (Print ISSN ; Online ISSN ) Abstract Completion of fungal, plant and human genomes paved the way to the identification of erythrocytic rhesus proteins and their kidney homologs as ammonium transporters. ) EK EIJDAFHABAHHA@ EJH CA I KH?A BK CE = JI=?GKEHA EJH CA BH JDAI E E JDAB H B = EK 1 = E = = I =IIE E =JA@B H I B EJH CA = E =?E@I =HA K?D FHABAHHA@ B H KJHEJE E JDA?=IA B= JA E?= E = I = EK EIKIA@ B H JDA AN?HAJE B EJH CA E IJA=@ 1 JDA DK = E@ AO = EK HA=>I A= I J =E J=E F0 >= =?A J CAJ HE@ B IKHF KI E HC= E? EJH CA 9DAJDAH= EK JH= IF HJ= I D=I=H AE JDA F0HACK =JE B JDAH HC= IEI J M A?K =H A?D= EI IMAHA J KFJ Properties and role of ammonium 1 =GKA KI I KJE = EK 0 " EI E AGKE E>HEK MEJD = E= 0! MEJD = F = B ' # 6DKI =J JOFE?=?OJ I E? F0 =FFH NE =JA O '' EI FHAIA J E JDA?=JE E? B H ) E=?= F=IIJDH KCD EFE@>E =OAHI= CEJI??A JH=JE CH=@EA J MDAHA=I= EK EI H@AHI B =C E JK@A AII FAH A= J ) JH= I A >H= A A A?JHE?= F0 CH=@EA JME JDAHAB HA=BBA?J 0 " 0! AGKE E>HEK 2 = JI A E?H HC= EI I=?E@EBOJDAEHANJAH = A LEH A J E A A >H= A > EK JH= IF HJFH JAE I I E JAH = = E=??A JH=JE =O >A HA JD= JE AIA HE?DA@? F=HA@J JDAANJAH = IF=?A *AIE@AIF0 A >H= A F JA JE= JH= IF HJAHI A O =JE? HA=?JE I JD=J CA AH=JA H HA LA = EK =HA = I E F HJ= J E =E J=E E C EJI??A JH=JE H AN= F A E E?H HC= EI = JI = EK EIH=FE@ J O=IIE E =JA@>OA O AIIK?D=IC KJ= E AIO KJ= CA =IA )I DECD ALA I B = EK?= >A?OJ J NE??OJ F =I E?= EK D=IJ >A AFJ M 6 =E F =I E???A JH=JE I J FH JA EJH CA =IIE E =JE CH MJD E?H HC= EI I F = JI D=LA AL LA@ DECD O IFA?EBE? KFJ= A >A?=KIA B F=IIELA A= =CA B= E= KJ BJDA?A I HA KFJ= A A?D = EI I 6DA A?D= EI BJH= IF HJB HE F J IFA?EAI MDAJDAH JDA JH= IF HJAHI KIA = EK H= KF AJDAJH= I F HJJ FH J I H JDAHE I HA =E IJ >ABK OA K?E@=JA@ Transporters for ammonium ) EK JH= IF HJD=I>AA IJK@EA@B H = O@A?=@AIE E?H HC= EI I >KJ JDA A?K =H IJHK?JKHA B JDA JH= I F HJAHI JDA JH= IF HJ A?D= EI HA =E A@ >I?KHA /A AJE? IJK@EAI E -I?DAHE?DE=? E E@A JEBEA@ KJ= JELAE = EK JH= IF HJ >KJEJM=I JF IIE> AJ E@A JEBO => =BE@A CA C=F OJ FE? A >H= AFH JAE 1 JDA =JA'%I KIE C=JD H KCDI?HAA B HOA=IJ KJ= JI HAIEIJ= JJ AJDO = EK =J NE?= = C B= EK?=HHEA@>O IJ= EK JH= IF HJAHI = EK KFJ= AM=IE@A JEBEA@! 6DH KCD? F A A J= JE = EK JH= IF HJAH CA AI MAHA E@A JEBEA@ JDA HAIFA?JELAFH JAE IBH > JDOA=IJ = JI) 6 MAHA?D=H=?JAHE A@ " # 6DA CA AI BH JDA JM HC= EI I =HA? IA =I = A >H= AFH JAE IJD=J D=LA= ANJAH = = E JAH E KI = E JAH =?=H> NO JAH E I A >H= AIF= I $ ;A=IJM=IJDA KIA@=I= J J IJK@OJDA>E?DA E?= FH FAHJEAI B> JDJH= IF HJAHI
2 2 Genome Biology Vol 2 No 3 K@AMECAJ= 6H= IF HJM=II=JKH=> AMEJDDECD=BBE A?JELA B H= EK AJDO = EK % 1JM=I= I J M=I => A J??A JH=JA = EK IALAH= IE@AJDA?A I Selectivity of ammonium transporters 0 M?= JH= IF HJIOIJA I>AI IFA?EBE?B H= EK AJDO = EK ) JD KCD JDA FDOIE??DA E?= FH FAH JEAI B 0 " E =GKA KII KJE IK?D=I >E E? H=@EE J BH IJ JDAH >=IE??=JE I B H AN= F A = JDAO=HADECD OIE E =HJ 6DAIE E =HEJOEI HAB A?JA@E JDA MIA A?JELEJOID M >OF J=IIEK JH= IF HJ IOIJA IB H LAHIKI 0 " AI JIAA J >AHA? C E A@ >O AF H ) 6 JH= IF HJAHI D MALAH " # IKC CAIJE C JD=J?DA E?= E JAH=?JE I >AJMAA JDA JH= IF HJAH F HJ= JB HHA? C EJE IF HJ B JDA IK>IJH=JA 6DA B=?J JD=J JH= IF HJ EI J JH=JA= EK E JDA?OJ I IKCCAIJIJD=J JDA JH= IF HJ A?D= EI E L LAI = EK J= A KF = C JDA A A?JHE?= F0 CH=@EA J AIJ=> EIDA@ >O FH J )62=IAI ) JD KCD =L=E => A ANFAHE A B H = EK JH= IF HJAHI?= >AANF =E A@>O=K EF HJ A?D= EI B H 0 " ECKHA= EJD=I JOAJ>AA F IIE> CKEID = K EF HJ A?D= EI BH 0! 0? JH= IF HJ ANFAHE A J= O ECKHA > >A?=KIA JDA AJ B KN EI A A?JH?DA E?= OE@A JE?= 1 A?K =HJAH I D MALAH 0! 0 =O J IFA?EBE? IEJAI JDA JH= IF HJAH EJO BA=?DIEJAB HJDAHAIFA?JELAIK>IJH=JA =O C MDAJDAHJDA JDAHIEJAEI??KFEA@ = O D CI B JDA AF ) 6 = EK JH= I F HJAHI D=LA >AA E@A JEBEA@ E OA=IJ F = JI 5=??D= H O?AI?AHALEIE=A D=IJDHAAF=H= C KI AFFH JAE J =BBE EJEAI ' JDA DECDAH F = J )H=>E@ FIEI JD= E= = D=I IEN ) 6 F=H= CI % /A AJE? =J HOE JAH=?JE I>AJMAA JDA AF FH JAE I MDE?D =O F E J J = E JAH=?JE =I = EC AHE?? F AN KHJDAH HA EJ EI E JAHAIJE C J JA JD=J AF EI C O? IO =JA@ D=I >AA E F E?=JA@ E = EK IA IE C@KHE CFIAK@ DOFD= CH MJD 6DAE@A JEBE?=JE = JJH= IF HJAHI= I A@J JDA?D=H=?JAHE =JE B >=?JAHE= = EK JH= IF HJAHI >A?=KIA JDA CA AI B =H?D=A>=?JAHE= AK>=?JAHE=? J=E A@D C KIIAGKA?AI )>=?JAHE= D C E AOA=IJ AF F = J ) 6I >AD=LAI IJHE?J O E A = = EK JH= IF HJAH! 6DA FHAIA?A B D CI E = JDAIA IFA?EAI =@AEJFH >=> AJD=JHA =JA@FH JAE I ECDJ= I >A FHAIA JE = E = = I JDAO=HA =JE C IKHFHEIA M=I JD=J JDA = = E= D CI = JD KCD@EIJ= J OHA =JA@ D=@FHALE KI JH= IF HJBK?JE D=@>AA =IIEC A@ JDAOMAHAE@A JEBEA@ KF= JECA I " LAHIJHAJ?DAI B=FFH NE =JA O = E =?E@I E@A JEJO>AJMAA ) JAE I?= >A=IDECD=I # The rhesus blood group antigens 1 JAHAIJE C O 4D= JECA ID=@ C>AA HA? C E A@B HJDAEH H A E JH= IBKIE E? F=JE> A E K A HA=?JE I DA B AM> H >=>EAI ) JD KCD JDAO D=LA >AA >E?DA E?= O?D=H=?JAHE A@ =? A=HFDOIE CE?= H A? J>A=IIEC A@ # 6DA4D? F ANEIANFHAIIA@E AHOJDH?OJAI FAHD=FI IE E =H J AF FH JAE I EI = DAJAH JAJH= AH? IEIJE C B JM 4D)/ C O? FH JAE I = I M =I 4D# B H JDAEH A A?JH FD HAJE? >E EJO E 5,5 CA I MDE?D =HA C O? IO =JA@ E J F CE?= O IE E =H F IE JE IJ AF DECD OD C KI C O? IO =JA@ 4D- H 4D, IK>K EJI = I HABAHHA@ J =I 4D! -=?D AH? J=E I FKJ=JELA JH= I A >H= =E I JD= E NO JAH E E=HA?OJ I E? *=?JAHE= = EK JH= IF HJAHI D=LA = IE E =H IJHK?JKHA $ 6DA -,IK>K EJI BJDA? F ANFHAIA JJDAAFEJ FAI BJDA4D = JECA I, H- JDAEHANJAH = FI 6DA4D)/ IK>K EJI=HAAIIA JE= B HANFHAIIE BJDAMD A? F AN MDAHA=I JDA? >E =JE MEJD 4D- 4D, L=HEAI JCA AJE?@ABA?JI?= A=@J JDAH=HA4D MDE?DHAIK JIE?D= CA@AHOJDH?OJA HFD CO AEJDAH4D)/EI AI JJH= I?=JA JDA 4D? F AN J JDA?A IKHB=?A H 4D, AJA@ 4D-EIIE K J= A KI O KJ=JA@ # 6DA D CO B 4D FH JAE I MEJD AF ) 6 FH JAE I FH FJA@ =HE E AJ = % J E LAIJEC=JA MDAJDAH DK = 4D)/ANFHAIIA@= A?= A@E=JA= EK JH= IF HJE = EK KFJ= A@ABE?EA JOA=IJ 4D)/? BAHHA@CH MJD = EK =II A EJH CA I KH?A 5KHFHEIE C O JH=IJJ JDA AFFH JAE IE OA=IJ 4D)/= I? BAHHA@ HAIEIJ=?AJ LAHODECD??A JH=JE I BJ NE? AJDO = EK C EJ D=I = H A E ANF HJ 4D)/ FH JA@ ABB KN B= EK MDA?K JKHA@ = = E =?E@?=H> I KH?A JDA?=J=> EI BMDE?D A=@IJ = EK JE 6DAIAANFAHE A JIIKCCAIJJDAABB KNEI A@E=JA@AEJDAH >O K EF HJ B = E= H >O = = JEF HJ A?D= EI )I JDA F =I = A >H= A B AHOJDH?OJAI IAA IJ >AFAH A=> AJ 0! >KJ JJ 0 " & F0 B JDA?OJ I EI DECDAH B=?E B JDA K?D=HCA@ A?K A@ M EJI??A JH=JE CH=@EA J =O>A JDA=?JK= A?D= EI 5K?D= A?D= EI M =E JDA? E?E@A J= KFJ= KN?=F=>E EJEAI B4D)/ 4A?A J O JM D C KI C O? FH JAE I MAHA E@A JEBEA@ BH KIA DK = 4D*/ MDE?D EI FHA@ E = J O ANFHAIIA@ E E@ AO ELAH I E ' 4D/ = I M =I 4D/ MDE?D EI FHA@ E = J O ANFHAIIA@ E E@ % A role for RhBG and RhCG in kidney physiology ) EK AN?HAJE >OJDA E@ AOEIJECDJ O? KF A@J JDA =E JA =?A BIOIJA E?=?E@ >=IA>= =?A ) EK EI JFHE =HE O=? IJEJKA J BJDAK JH=BE JH=JA EJEICA AH =JA@>O AJ=> EI BC KJ= E AE FH NE = AFEJDA E=?A I
3 Import Export (a) (b) H ph 5 Figure 1 Models for and transport. (a) Channel- or carrier-mediated uniport for. Both concentration gradient and transmembrane voltage influence the direction of transport. A firmly established example of such transport is through potassium channels. (b) /H co-transporter. Driven by the ph gradient and transmembrane voltage, ammonia may be taken up against a concentration gradient for. The electrochemical situation is similar as for uniport in (a). (c) Carrier-mediated antiport for with unknown secondary substrate(s), for example, cation C. If both substrates are univalent only the concentration gradients determine the direction of transport. In the kidney, C could be sodium. (d) Channel- or carrier-mediated uniport for. Independent of the membrane potential, ammonia will equilibrate along its concentration gradient (depending on the external and internal ph). A net inflow of ammonium into the cytoplasm will depend on ammonium metabolism, which acts as a sink for /. EI HA A=IA@ E J JDA JK>K =H B KE@ 1 JAHAIJE C O 4D*/?= E AIJ FH NE = JK>K AI ' EK EI??A BJDAFH NE = JK>K A )IEC EB E?= J FH F HJE B = EK EI HA=>I H>A@ E JDA JDE? C E > BJDA F B0A A JDA=FE?= A >H= A B MDE?D EI DECD O FAH A=> A J 0 " >KJ J J 0! K A F IEJELA L F=H=?A K =H =>I HFJE B 0 " 6DABE = AFDH IAC A J JDA? A?JE C@K?J IAA I E FAH A=> A J 0 " >KJ FAH A=> A J 0! 2H J I =HA IA?HAJA@E J JDA K A E=HA A=IA@BH? HJE?= Cytosol 120mV ph 7 H (c) (d) C?A I ME >A FH J =JA@ J B H = EK JH=FFA@ E JDA K A AN?HAJA@ 4D/ MDE?D EI = I => A J ABB KN = EK %?= E AIJ JDA? A?JE C@K?J Functional and evolutionary relationships 6= A J CAJDAH JDAHAIK JIIKCCAIJJD=J@EBBAHA JJH= IF HJAHI BH JDAI= AIKFAHB= E O@ JH= IF HJJDAI= AIK>IJ=?AI >KJKIA@EBBAHA JJH= IF HJ A?D= EI I 6DEI =O J>AJ IKHFHEIE C IE?A@EBBAHA JBK?JE = HA =JE IDEFI=HAB C
4 4 Genome Biology Vol 2 No 3 K@AMECAJ= =IIAI B A >H= A JH= IF HJAHI IK?D =I C K? IA JH= IF HJAHI B JDA = H B=?E EJ=J H IKFAHB= E O B HAN= F A JDAOA=IJFH JAE 5?0:6? F=HA@MEJDJDA )H=>E@ FIEI FH JAE E =?E@JH= IF HJAHI B JDA = E =?E@ F O= E A?D E A )2 B= E O B H AN= F A JDA DK = FH JAE 0I)6? F=HA@ MEJD JDA )H=>E@ FIEI FH JAE )J)6 1 > JD?=IAI JDA F = J FH JAE FH >=> O A@E=JAI FH J? JH= IF HJ MDAHA=I JDA JDAH A@E=JAIK EF HJ A ECDJ IFA?K =JA JD=J 4D E A FH JAE I =HA 0! K E F HJAHI H 0 "?=JE = JEF HJAHI 1? JH=IJ AF ) 6 = EK JH= IF HJAHI =O AEJDAH BK?JE =I 0! 0? JH= IF HJAHI H=I 0 " K EF HJAHI ECKHA = > )?DA E?= E JAH=?JE B = EK H = E=MEJDJDAFH JAE I ECDJANF =E MDO= EK JH= IF HJAHI =HA I IA A?JELA B H = EK? F=HA@ MEJD B HAN= F A 1J ECDJ>AF IIE> AJD=J A >AHI J? =@AI B JDA IKFAHB= E O HA? C E A AEJDAH K?D=HCA@ H?D=HCA@B H I BJDAIK>IJH=JA, AIJDEIBEJ JDA AL KJE =HO F=JJAH 2DO CA AJE? = = OIAI IKCCAIJ JD=J4DFH JAE AF ) 6D=LA= =?AIJH= HA =JE IDEF ECKHA 1 JAHAIJE C O JDA A M H BHKEJB O? J=E > JD AF ) CIE JDAEH CA AI A DECDAH F = J IAGKA?A BH )H=>E@ FIEI JD=J B )J) 6 CH KFI? IA O J >=?JAHE= IAGKA?AI MDE?D=HA= I? IA OHA =JA@J OA=IJIAGKA?AI! 6DA =H?D=A>=?JAHE= IAGKA?AI=HA? IA OHA =JA@J I AF = J E = IAGKA?AI 9EJDE =IE C AIFA?EAI? =IIA > O J IK>K EJI E J = DAJAH AHE?? F AN =O A=@J BE AJK E C B= EK JH= IF HJ>O AF ) 6 JAE I Mep subfamily AbamtB ReamtB AvamtB AcamtB DdRh CeRh1 DmRh CeRh2 HsRhAG DrRh1 Rh subfamily GcRh HsRhBG HsRhCG ScMep1 ScMep3 EcamtB HsRhCE HsRhD ScMep2 AtAMT2 CgamtB CgamtP AtAMT1 50 changes 5 CeAMT2 SyAMT2 SyAMT3 SyAMT1 CeAMT1 CeAMT4 MjAMT2 MjAMT1 DmAMT AMT subfamily Figure 2 A phylogenetic tree of Mep, AMT and Rh-like proteins. Rh and AMT/Mep proteins are found in bacteria, archaebacteria and eukaryotes. The amino acid sequence alignment was created using the program ClustalW, and phylogenetic analysis was done using the program PAUP 4.0b4a. Highly variable amino- and carboxy-terminal sequences were removed before analysis. Only one archaebacterial sequence (Mj, Methanococchus janaschii) and those prokaryotic sequences that have been analyzed for ammonia transport have been included: Ec, Escherichia coli; Sy, Synechocystis sp.; Ac, Azorhizobium caulinodans; Av, Azotobacter vinelandii; Ab, Azospirillum brasilense; Re, Rhizobium etli; Cg, Corynebacterium glutamicum. With the exception of human (Hs, Homo sapiens), slime mold (Dd, Dictyostelium discoideum), marine sponge (Gc, Geodia cydonium), and zebrafish (Danio rerio), only eukaryotic sequences from fully sequenced organisms (Dm, Drosophila melanogaster (fruit fly); Ce, Caenorhabditis elegans (nematode); At, Arabidopsis thaliana (plant); Sc, Saccharomyces cerevisiae (yeast)) have been included.
5 6DA=>IA?A B4D E AFH JAE IE DECDAHF = JIIKCCAIJIJD=J AEJDAHI A BJDA) 6FH JAE I= I KIA=@EBBAHA J? KF E C A?D= EI H JD=J JDAH IAGKA?A K HA =JA@ FH JAE I =HA HAIF IE> A B H = EK = E= ANF HJ 1? JH=IJ J KHA= AN?HAJE C = = I BEID AN?HAJA =E O = EK JDH KCD JDA CE I 9A M JDAHAB HA FHA@E?J JD=J 4D E A FH JAE IIK?D=I)) $! #$ = I M =I,H4D =O>A DECD O ANFHAIIA@ E JDA CE I =O >A HAIF IE> A B H = EK = E= AN?HAJE E BEID? KJ KJ= JI E F = JI >AAN?A A JJ IB H@EIIA?JE C H AI B) 6 E AFH JAE IE J CA AI JDAEH HA =JELA? JHE>KJE J AJ = EK B KN? F=HA@ MEJD JDAH JH= IF HJAHI JD=J?= A@E=JA = EK JH= IF HJ IK?D =I F J=IIEK JH= I F HJAHI = 0 = JEF HJAHI H =? JH= IF HJAHI /A A ME@A= = OIEIME = I DA FJ K H=LA JDAAL KJE BJDA A?D= EI B= EK = E=JH= IF HJ Acknowledgements We are grateful for support by the GABI genome project funded by the BMBF. References 1. von Wiren N, Gazzarrini S, Gojon A, Frommer WB: The molecular physiology of ammonium uptake and retrieval. Curr Opin Plant Biol 2000, 3: Kleiner D: The transport of and across biological membranes. Biochim Biophys Acta 1981, 639: Dubois E, Grenson M: Methylamine/ammonia uptake systems in Saccharomyces cerevisiae: multiplicity and regulation. Mol Gen Genet 1979, 175: Marini AM, Vissers S, Urrestarazu A, Andre B: Cloning and expression of the MEP1 gene encoding an ammonium transporter in Saccharomyces cerevisiae. EMBO J 1994, 13: Ninnemann O, Jauniaux JC, Frommer WB: Identification of a high affinity transporter from plants. EMBO J 1994, 13: Marini AM, Andre B: In vivo N-glycosylation of the Mep2 highaffinity ammonium transporter of Saccharomyces cerevisiae reveals an extracytosolic N-terminus. Mol Microbiol 2000, 38: Gazzarrini S, Lejay L, Gojon A, Ninnemann O, Frommer WB, von Wiren N: Three functional transporters for constitutive, diurnally regulated, and starvation-induced uptake of ammonium into Arabidopsis roots. Plant Cell 1999, 11: White PJ: The permeation of ammonium through a voltageindependent K channel in the plasma membrane of rye roots. J Membr Biol 1996, 152: Marini AM, Soussi-Boudekou S, Vissers S, Andre B: A family of ammonium transporters in Saccharomyces cerevisiae. Mol Cell Biol 1997, 17: Marini AM, Springael JY, Frommer WB, Andre B: Cross-talk between ammonium transporters in yeast and interference by the soybean SAT1 protein. Mol Microbiol 2000, 35: Lorenz MC, Heitman J: The Mep2 ammonium permease regulates pseudohyphal differentiation in Saccharomyces cerevisiae. EMBO J 1998, 17: Meier-Wagner J, Nolden L, Jakoby M, Siewe R, Krämer R, Burkovski A: Multiplicity of ammonium uptake systems in Corynebacterium glutamicum: role of Amt and AmtB. Microbiology 2001, 147: Tate T, Riccio A, Merrick M, Patriarca EJ: The Rhizobium etli amtb gene coding for an transporter is down regulated early during bacteroid differentiation. Mol Plant Microbe Interact 1998, 11: Marini AM, Urrestarazu A, Beauwens R, Andre B: The Rh (rhesus) blood group polypeptides are related to transporters. Trends Biochem Sci 1997, 22: Avent ND, Reid ME: The Rh blood group system: a review. Blood 2000, 95: Thomas GH, Mullins JG, Merrick M.: Membrane topology of the Mep/Amt family of ammonium transporters. Mol Microbiol 2000, 37: Marini AM, Matassi G, Raynal V, Andre B, Cartron JP, Cherif-Zahar B: The human rhesus-associated RhAG protein and a kidney homologue promote ammonium transport in yeast. Nat Genet 2000, 26: Labotka RJ, Lundberg P, Kuchel PW: Ammonia permeability of erythrocyte membrane studied by 14 N and 15 N saturation transfer NMR spectroscopy. Am J Physiol 1995, 268:C686-C Liu Z, Peng J, Mo R, Hui Cc, Huang CH: Rh Type B glycoprotein is a new member of the Rh superfamily and a putative ammonia transporter in mammals. J Biol Chem 2001, 276: Liu Z, Chen Y, Mo R, Hui C, Cheng JF, Mohandas N, Huang CH: Characterization of human RhCG and mouse Rhcg as novel nonerythroid Rh glycoprotein homologues predominantly expressed in kidney and testis. J Biol Chem 2000, 275: Knepper MA, Packer R, Good DW: Ammonium transport in the kidney. Phys Rev 1989, 69: Kikeri D, Sun A, Zeidel ML, Hebert SC: Cell membranes impermeable to. Nature 1989, 339: Sohlenkamp C, Shelden M, Howitt S, Udvardi M: Characterization of Arabidopsis AtAMT2, a novel ammonium transporter in plants. FEBS Lett 2000, 467:
Rick Van Kooten, Indiana Univ., FNAL Users Meeting, HEPAP Session, June 27, 2000
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