title: Functional characterization of the plastidic phosphate translocator gene family from the thermo-acidophilic red alga Galdieria sulphuraria reveals specific adaptations of primary carbon partitioning in green plants and red algae.
abstract: In chloroplasts of green plants and algae, CO(2) is assimilated into triose-phosphates (TPs); a large part of these TPs is exported to the cytosol by a TP/phosphate translocator (TPT), whereas some is stored in the plastid as starch. Plastidial phosphate translocators have evolved from transport proteins of the host endomembrane system shortly after the origin of chloroplasts by endosymbiosis. The red microalga Galdieria sulphuraria shares three conserved putative orthologous transport proteins with the distantly related seed plants and green algae. However, red algae, in contrast to green plants, store starch in their cytosol, not inside plastids. Hence, due to the lack of a plastidic starch pool, a larger share of recently assimilated CO(2) needs to be exported to the cytosol. We thus hypothesized that red algal transporters have distinct substrate specificity in comparison to their green orthologs. This hypothesis was tested by expression of the red algal genes in yeast (Saccharomyces cerevisiae) and assessment of their substrate specificities and kinetic constants. Indeed, two of the three red algal phosphate translocator candidate orthologs have clearly distinct substrate specificities when compared to their green homologs. GsTPT (for G. sulphuraria TPT) displays very narrow substrate specificity and high affinity; in contrast to green plant TPTs, 3-phosphoglyceric acid is poorly transported and thus not able to serve as a TP/3-phosphoglyceric acid redox shuttle in vivo. Apparently, the specific features of red algal primary carbon metabolism promoted the evolution of a highly efficient export system with high affinities for its substrates. The low-affinity TPT of plants maintains TP levels sufficient for starch biosynthesis inside of chloroplasts, whereas the red algal TPT is optimized for efficient export of TP from the chloroplast.
authors.affiliation: Institut für Biochemie der Pflanzen, Heinrich-Heine-Universität, 40225 Duesseldorf, Germany.
authors.forename: Marc
authors.initials: M
authors.lastname: Linka
authors.forename: Aziz
authors.initials: A
authors.lastname: Jamai
authors.forename: Andreas P M
authors.initials: AP
authors.lastname: Weber
mesh_terms: D002244:Carbon / Q000378:metabolism*; D060365:Chloroplast Proteins; D026901:Membrane Transport Proteins / Q000235:genetics / Q000502:physiology*; D008969:Molecular Sequence Data; D005810:Multigene Family; D010940:Plant Proteins / Q000235:genetics / Q000502:physiology*; D010944:Plants / Q000378:metabolism*; D018087:Plastids; D000461:Rhodophyta / Q000235:genetics*; D012441:Saccharomyces cerevisiae / Q000235:genetics; D014306:Trioses / Q000378:metabolism
chemical_list: D060365:Chloroplast Proteins; D026901:Membrane Transport Proteins; D010940:Plant Proteins; D014306:Trioses; D002244:Carbon
references.citation: Plant Physiol. 2005 Feb;137(2):460-74
references.pmid: 15710685
references.citation: Plant Cell. 1998 Jan;10(1):105-17
references.pmid: 9477574
references.citation: Bioessays. 2007 Dec;29(12):1239-46
references.pmid: 18027391
references.citation: Plant Mol Biol. 2006 Oct;62(3):339-49
references.pmid: 16915520
references.citation: J Mol Evol. 2005 Feb;60(2):257-67
references.pmid: 15785854
references.citation: Annu Rev Plant Biol. 2005;56:133-64
references.pmid: 15862092
references.citation: J Eukaryot Microbiol. 2005 Sep-Oct;52(5):399-451
references.pmid: 16248873
references.citation: Anal Biochem. 1987 Apr;162(1):156-9
references.pmid: 2440339
references.citation: Physiol Plant. 2008 Jun;133(2):211-28
references.pmid: 18298409
references.citation: Bioinformatics. 2007 Nov 1;23(21):2947-8
references.pmid: 17846036
references.citation: Photosynth Res. 2004;79(1):1-24
references.pmid: 16228397
references.citation: Plant Physiol. 2003 Mar;131(3):1178-90
references.pmid: 12644669
references.citation: Annu Rev Plant Physiol Plant Mol Biol. 1999 Jun;50:27-45
references.pmid: 15012202
references.citation: Planta. 2000 Feb;210(3):371-82
references.pmid: 10750894
references.citation: Plant Cell Physiol. 2007 Sep;48(9):1359-73
references.pmid: 17698881
references.citation: J Plant Physiol. 2008 Mar 13;165(4):456-61
references.pmid: 17913294
references.citation: Plant Biol (Stuttg). 2005 Jan;7(1):91-7
references.pmid: 15666208
references.citation: Mol Biol Evol. 2004 May;21(5):809-18
references.pmid: 14963099
references.citation: Plant Cell Environ. 2007 Sep;30(9):1126-49
references.pmid: 17661751
references.citation: Plant Physiol. 1987 Feb;83(2):399-407
references.pmid: 16665257
references.citation: Plant Physiol. 2002 Feb;128(2):512-22
references.pmid: 11842155
references.citation: Plant Cell. 2006 Nov;18(11):3088-105
references.pmid: 17098813
references.citation: Plant Cell. 2005 Mar;17(3):760-75
references.pmid: 15722468
references.citation: Protein Eng. 1997 Jan;10(1):1-6
references.pmid: 9051728
references.citation: Curr Opin Plant Biol. 2002 Dec;5(6):536-42
references.pmid: 12393017
references.citation: Planta. 1994;194(2):181-5
references.pmid: 7765117
references.citation: Nucleic Acids Res. 2004 Jul 1;32(Web Server issue):W390-3
references.pmid: 15215417
references.citation: Annu Rev Genet. 2007;41:147-68
references.pmid: 17600460
references.citation: Annu Rev Plant Physiol Plant Mol Biol. 1996 Jun;47:185-214
references.pmid: 15012287
references.citation: Genome Biol. 2007;8(10):R212
references.pmid: 17919328
references.citation: Plant Cell. 2004 Feb;16(2):478-99
references.pmid: 14729914
references.citation: Bioessays. 2004 Jan;26(1):50-60
references.pmid: 14696040
references.citation: Plant Mol Biol. 2004 May;55(1):17-32
references.pmid: 15604662
references.citation: Plant Physiol. 1991 Apr;95(4):1131-7
references.pmid: 16668101
references.citation: Eukaryot Cell. 2006 Sep;5(9):1517-31
references.pmid: 16963634
references.citation: FEBS Lett. 2007 May 25;581(12):2215-22
references.pmid: 17316618
references.citation: Plant Mol Biol. 2006 Aug;61(6):945-57
references.pmid: 16927206
references.citation: Eukaryot Cell. 2006 Mar;5(3):609-12
references.pmid: 16524915
references.citation: Proc Biol Sci. 2001 Jul 7;268(1474):1417-22
references.pmid: 11429143
references.citation: Plant J. 2003 Nov;36(3):411-20
references.pmid: 14617097
references.citation: Biochem J. 1953 Aug;55(1):170-1
references.pmid: 13093635
references.citation: Annu Rev Plant Biol. 2006;57:805-36
references.pmid: 16669783
references.citation: Plant Physiol. 1993 Jan;101(1):209-16
references.pmid: 8278495
references.citation: Biochem J. 2007 Jan 1;401(1):13-28
references.pmid: 17150041
references.citation: Gene. 1999 Apr 1;230(1):7-14
references.pmid: 10196468
references.citation: Biochim Biophys Acta. 2003 Feb 21;1645(2):212-7
references.pmid: 12573251
references.citation: Plant J. 2003 Nov;36(3):301-17
references.pmid: 14617088
references.citation: Plant Cell. 1997 Mar;9(3):453-62
references.pmid: 9090886
references.citation: J Biol Chem. 1977 Oct 25;252(20):7384-90
references.pmid: 903365