Characterization of photosynthesis in Arabidopsis ER-to-plastid lipid trafficking mutants

Photosynthesis Research

Volumn 112, Issue 1, 2012, Pages 49-61

  Li, Ziru ^a   Gao, Jinpeng ^a,b   Benning, Christoph ^a   Sharkey, Thomas D ^a  

^a Michigan State University   (United States)

^b WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Electrochromic shift; Galactolipids; Photosynthesis; Proton motive force; tgd1 1; tgd2 1

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ARABIDOPSIS PROTEIN; CARBON; CARRIER PROTEIN; MEMBRANE LIPID; RIBULOSEBISPHOSPHATE CARBOXYLASE; TGD1 PROTEIN, ARABIDOPSIS; TGD2 PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; ARTICLE; ELECTRON TRANSPORT; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; GERMINATION; LIGHT; METABOLISM; OXIDATION REDUCTION REACTION; PHENOTYPE; PHOTOSYNTHESIS; PHOTOSYSTEM I; PHOTOSYSTEM II; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT LEAF; PLASTID; PROTON MOTIVE FORCE; TRANSPORT AT THE CELLULAR LEVEL;

ADENOSINE TRIPHOSPHATASES; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOLOGICAL TRANSPORT; CARBON; ELECTRON TRANSPORT; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; GERMINATION; LIGHT; MEMBRANE LIPIDS; MEMBRANE TRANSPORT PROTEINS; OXIDATION-REDUCTION; PHENOTYPE; PHOTOSYNTHESIS; PHOTOSYSTEM I PROTEIN COMPLEX; PHOTOSYSTEM II PROTEIN COMPLEX; PLANT LEAVES; PLASTIDS; PROTON-MOTIVE FORCE; RIBULOSE-BISPHOSPHATE CARBOXYLASE; STRESS, PHYSIOLOGICAL;

ARABIDOPSIS; EUKARYOTA; PROKARYOTA; TRACHEOPHYTA;

EID: 84862785584     PISSN: 01668595     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11120-012-9734-9     Document Type: Article

References (62)

1. H Aronsson MA Schöttler AA Kelly C Sundqvist P Dörmann S Karim P Jarvis 2008 Monogalactosyldiacylglycerol deficiency in Arabidopsis affects pigment composition in the prolamellar body and impairs thylakoid membrane energization and photoprotection in leaves Plant Physiol 148 580 592 18641085 10.1104/pp.108.123372 1:CAS:528:DC%2BD1cXhtFKnu7zP (Pubitemid 352847592)
2. TJ Avenson JA Cruz A Kanazawa DM Kramer 2005 Regulating the proton budget of higher plant photosynthesis Proc Natl Acad Sci USA 102 9709 9713 15972806 10.1073/pnas.0503952102 1:CAS:528:DC%2BD2MXmsVaktbk%3D (Pubitemid 40981745)
3. K Awai C Xu B Tamot C Benning 2006 A phosphatidic acid-binding protein of the chloroplast inner envelope membrane involved in lipid trafficking Proc Natl Acad Sci USA 103 10817 16818883 10.1073/pnas.0602754103 1:CAS:528: DC%2BD28XntFWmtrk%3D (Pubitemid 44078059)
4. NR Baker J Harbinson DM Kramer 2007 Determining the limitations and regulation of photosynthetic energy transduction in leaves Plant Cell Environ 30 1107 1125 17661750 10.1111/j.1365-3040.2007.01680.x 1:CAS:528: DC%2BD2sXhtVeiurrI (Pubitemid 47174272)
5. C Benning 2009 Mechanisms of lipid transport involved in organelle biogenesis in plant cells Annu Rev Cell Dev Biol 25 71 91 19572810 10.1146/annurev.cellbio.042308.113414 1:CAS:528:DC%2BD1MXhsVKisbrP
6. K Cline K Keegstra 1983 Galactosyltransferases involved in galactolipid biosynthesis are located in the outer membrane of pea chloroplast envelopes Plant Physiol 71 366 372 16662832 10.1104/pp.71.2.366 1:CAS:528: DyaL3sXhtVCgtL4%3D
7. JA Cruz CA Sacksteder A Kanazawa DM Kramer 2001 Contribution of electric field (Δψ) to steady-state transthylakoid proton motive force (pmf) in vitro and in vivo. Control of pmf parsing into Δψ and ΔpH by ionic strength Biochemistry 40 1226 1237 11170448 10.1021/bi0018741 1:CAS:528:DC%2BD3MXms1ymuw%3D%3D (Pubitemid 32142884)
8. P Dörmann C Benning 2002 Galactolipids rule in seed plants Trends Plant Sci 7 112 118 11906834 10.1016/S1360-1385(01)02216-6 (Pubitemid 36726436)
9. P Dörmann S Hoffmann-Benning I Balbo C Benning 1995 Isolation and characterization of an Arabidopsis mutant deficient in the thylakoid lipid digalactosyl diacylglycerol Plant Cell 7 1801 1810 8535135 10.1105/tpc.7.11.1801 (Pubitemid 3019799)
10. AJ Dorne MA Block J Joyard R Douce 1982 The galactolipid:galactolipid galactosyltransferase is located on the outer surface of the outer membrane of the chloroplast envelope FEBS Lett 145 30 34 10.1016/0014-5793(82)81200-3 1:CAS:528:DyaL38XlsF2ksb0%3D
11. 3 species Planta 149 78 90 10.1007/BF00386231 1:CAS:528:DyaL3cXksVWrt7w%3D
12. M Frentzen 1986 Biosynthesis and desaturation of the different diacylglycerol moieties in higher plants J Plant Physiol 124 193 209 10.1016/S0176-1617(86)80034-7 1:CAS:528:DyaL28XkvFCnt7o%3D
13. K Gounaris J Barber 1983 Monogalactosyldiacylglycerol: the most abundant polar lipid in nature Trends Biochem Sci 8 378 381 10.1016/0968-0004(83)90366-3 1:CAS:528:DyaL3sXmtV2ktbk%3D
14. H Härtel H Lokstein P Dörmann B Grimm C Benning 1997 Changes in the composition of the photosynthetic apparatus in the galactolipid-deficient dgd1 mutant of Arabidopsis thaliana Plant Physiol 115 1175 1184 9390443 10.1104/pp.115.3.1175 (Pubitemid 28378777)
15. H Härtel H Lokstein P Dörmann RN Trethewey C Benning 1998 Photosynthetic light utilization and xanthophyll cycle activity in the galactolipid deficient dgd1 mutant of Arabidopsis thaliana Plant Physiol Biochem 36 407 417 10.1016/S0981-9428(98)80204-0 (Pubitemid 28278477)
16. G Hölzl S Witt N Gaude M Melzer MA Schöttler P Dörmann 2009 The role of diglycosyl lipids in photosynthesis and membrane lipid homeostasis in Arabidopsis Plant Physiol 150 1147 1159 19403724 10.1104/pp.109.139758
17. AG Ivanov L Hendrickson M Krol E Selstam G Oquist V Hurry N Huner 2006 Digalactosyl-diacylglycerol deficiency impairs the capacity for photosynthetic intersystem electron transport and state transitions in Arabidopsis thaliana due to photosystem I acceptor-side limitations Plant Cell Physiol 47 1146 16854937 10.1093/pcp/pcj089 1:CAS:528:DC%2BD28XpsFKnsb8%3D (Pubitemid 44461763)
18. P Jarvis P Dörmann CA Peto J Lutes C Benning J Chory 2000 Galactolipid deficiency and abnormal chloroplast development in the Arabidopsis MGD synthase 1 mutant Proc Natl Acad Sci USA 97 8175 8179 10869420 10.1073/pnas.100132197 1:CAS:528:DC%2BD3cXkvFCmsb4%3D (Pubitemid 30460792)
19. P Jordan P Fromme HT Witt O Klukas W Saenger N Krausz 2001 Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution Nature 411 909 917 11418848 10.1038/35082000 1:CAS:528: DC%2BD3MXkvVWhs78%3D (Pubitemid 32601481)
20. J Joyard E Teyssier C Miège D Berny-Seigneurin E Maréchal MA Block A-J Dorne N Rolland G Ajlani R Douce 1998 The biochemical machinery of plastid envelope membranes Plant Physiol 118 715 723 9808715 10.1104/pp.118.3.715 1:CAS:528:DyaK1cXnsFektr4%3D (Pubitemid 128652996)
21. A Kanazawa DM Kramer 2002 In vivo modulation of nonphotochemical exciton quenching (NPQ) by regulation of the chloroplast ATP synthase Proc Natl Acad Sci USA 99 12789 12794 12192092 10.1073/pnas.182427499 1:CAS:528: DC%2BD38XnvFGhsLY%3D
22. T Katagiri K Ishiyama T Kato S Tabata M Kobayashi K Shinozaki 2005 An important role of phosphatidic acid in ABA signaling during germination in Arabidopsis thaliana Plant J 43 107 117 15960620 10.1111/j.1365-313X.2005.02431. x 1:CAS:528:DC%2BD2MXmsVehs7w%3D (Pubitemid 40962739)
23. AA Kelly JE Froehlich P Dörmann 2003 Disruption of the two digalactosyldiacylglycerol synthase genes DGD1 and DGD2 in Arabidopsis reveals the existence of an additional enzyme of galactolipid synthesis Plant Cell 15 2694 2706 14600212 10.1105/tpc.016675 1:CAS:528:DC%2BD3sXpt1Orurs%3D (Pubitemid 37470669)
24. C Klughammer U Schreiber 1994 An improved method, using saturating light pulses, for the determination of photosystem I quantum yield via P700+-absorbance changes at 830 nm Planta 192 261 268 10.1007/BF01089043 1:CAS:528:DyaK2cXnt1OjtA%3D%3D (Pubitemid 2002837)
25. S Krumova S Laptenok L Kovács T Tóth A van Hoek G Garab H van Amerongen 2010 Digalactosyl-diacylglycerol-deficiency lowers the thermal stability of thylakoid membranes Photosynth Res 105 229 242 20645128 10.1007/s11120-010-9581-5 1:CAS:528:DC%2BC3cXhtlWrtbjN
26. A Laisk V Oja B Rasulov H Rämma H Eichelmann I Kasparova H Pettai E Padu E Vapaavuori 2002 A computer-operated routine of gas exchange and optical measurements to diagnose photosynthetic apparatus in leaves Plant Cell Environ 25 923 943 10.1046/j.1365-3040.2002.00873.x 1:CAS:528:DC%2BD38XlslKqurg%3D (Pubitemid 34775989)
27. HK Lichtenthaler 1987 Chlorophyll and carotenoids: pigments of photosynthetic membranes Methods Enzymol 148 350 382 10.1016/0076-6879(87)48036- 1 1:CAS:528:DyaL1cXhs1Cgu78%3D
28. Z Liu H Yan K Wang T Kuang J Zhang L Gui X An W Chang 2004 Crystal structure of spinach major light-harvesting complex at 2.72 A resolution Nature 428 287 292 15029188 10.1038/nature02373 1:CAS:528:DC%2BD2cXitFCntbc%3D (Pubitemid 38418793)
29. B Loll J Kern W Saenger A Zouni J Biesiadka 2005 Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II Nature 438 1040 1044 16355230 10.1038/nature04224 1:CAS:528:DC%2BD2MXhtlSksrvK (Pubitemid 43093979)
30. B Lu C Benning 2009 A 25-amino acid sequence of the Arabidopsis TGD2 protein is sufficient for specific binding of phosphatidic acid J Biol Chem 284 17420 17427 19416982 10.1074/jbc.M109.016014 1:CAS:528:DC%2BD1MXnsVWlu7s%3D
31. B Lu C Xu K Awai AD Jones C Benning 2007 A small ATPase protein of Arabidopsis, TGD3, involved in chloroplast lipid import J Biol Chem 282 35945 35953 17938172 10.1074/jbc.M704063200 1:CAS:528:DC%2BD2sXhtlKrsbrE (Pubitemid 350277137)
32. DW Meinke LH Franzmann TC Nickle EC Yeung 1994 Leafy Cotyledon mutants of Arabidopsis Plant Cell 6 1049 1064 12244265 10.1105/tpc.6.8.1049 1:CAS:528:DyaK2cXmt1Kmtbo%3D (Pubitemid 2137210)
33. N Mizusawa H Wada 2011 The role of lipids in photosystem II Biochim Biophys Acta (BBA) 10.1016/j.bbabio.2011.1004.1008
34. ER Moellering B Muthan C Benning 2010 Freezing tolerance in plants requires lipid remodeling at the outer chloroplast membrane Science 330 226 228 20798281 10.1126/science.1191803 1:CAS:528:DC%2BC3cXht1Cgt77M
35. G Noctor AV Ruban P Horton 1993 Modulation of Delta pH-dependent nonphotochemical quenching of chlorophyll fluorescence in spinach chloroplasts Biochim Biophys Acta 1183 339 344 10.1016/0005-2728(93)90237-A 1:CAS:528:DyaK2cXntlKltA%3D%3D
36. 1, ATP synthase from spinach chloroplasts by chloroplast lipids Biochim Biophys Acta 765 12 20 10.1016/0005-2728(84)90151-8 1:CAS:528:DyaL2cXktVaqsrY%3D
37. U Pick M Weiss K Gounaris J Barber 1987 The role of different thylakoid glycolipids in the function of reconstituted chloroplast ATP synthase Biochim Biophys Acta 891 28 39 10.1016/0005-2728(87)90080-6 1:CAS:528:DyaL2sXksFClt7s%3D
38. M Rossak C Tietje E Heinz C Benning 1995 Accumulation of UDP-sulfoquinovose in a sulfolipid-deficient mutant of Rhodobacter sphaeroides J Biol Chem 270 25792 25797 7592762 10.1074/jbc.270.43.25792 1:CAS:528: DyaK2MXovFyksL4%3D
39. R Roston J Gao C Xu C Benning 2011 Arabidopsis chloroplast lipid transport protein TGD2 disrupts membranes and is part of a large complex Plant J 10.1111/j.1365-1313X.2011.04536.x 21309871
40. 2 assimilation, and plant growth by overacidification of the thylakoid lumen Plant Cell 23 304 321 21278125 10.1105/tpc.110.079111 1:CAS:528:DC%2BC3MXpsFCksbk%3D
41. PG Roughan CR Slack 1982 Cellular organization of glycerolipid metabolism Annu Rev Plant Physiol 33 97 132 10.1146/annurev.pp.33.060182.000525 1:CAS:528:DyaL38XktlKjs70%3D
42. CA Sacksteder DM Kramer 2000 Dark-interval relaxation kinetics (DIRK) of absorbance changes as a quantitative probe of steady-state electron transfer Photosynth Res 66 145 158 16228416 10.1023/A:1010785912271 1:CAS:528: DC%2BD3MXkslWkt7Y%3D (Pubitemid 32540456)
43. CA Sacksteder ME Jacoby DM Kramer 2001 A portable, non-focusing optics spectrophotometer (NoFOSpec) for measurements of steady-state absorbance changes in intact plants Photosynth Res 70 231 240 16228356 10.1023/A:1017906626288 1:CAS:528:DC%2BD38Xit1Cktrs%3D (Pubitemid 34196938)
44. A Sen WP Williams PJ Quinn 1981 The structure and thermotropic properties of pure 1,2-diacylgalactosylglycerols in aqueous systems Biochim Biophys Acta 663 380 389 7213776 1:CAS:528:DyaL3MXhsFahs7c%3D
45. KU Sewe R Reich 1977 Effect of molecular polarization on electrochromism of carotenoids. 2. Lutein-chlorophyll complexes-origin of field-indicating absorption-change at 520 nm in membranes of photosynthesis Zeitschrift Fur Naturforschung 32c 161 171 1:CAS:528:DyaE2sXktVamsLY%3D (Pubitemid 8073085)
46. 3 leaves Plant Cell Environ 30 1035 1040 17661745 10.1111/j.1365-3040.2007.01710.x 1:CAS:528:DC%2BD2sXhtVeiur3F (Pubitemid 47174279)
47. 2 fixed in photosystems I and II Plant Physiol 115 1163 12223865 1:CAS:528:DyaK2sXns1yktbc%3D
48. D Stroebel Y Choquet J-L Popot D Picot 2003 An atypical haem in the cytochrome b6f complex Nature 426 413 418 14647374 10.1038/nature02155 1:CAS:528:DC%2BD3sXpt1GlsLY%3D (Pubitemid 37490123)
49. K Takizawa JA Cruz A Kanazawa DM Kramer 2007 The thylakoid proton motive force in vivo. Quantitative, non-invasive probes, energetics, and regulatory consequences of light-induced pmf Biochim Biophys Acta 1767 1233 1244 17765199 10.1016/j.bbabio.2007.07.006 1:CAS:528:DC%2BD2sXhtFCjurfN (Pubitemid 47498308)
50. S Toni 1997 Galactolipid biosynthesis genes and endosymbiosis Trends Plant Sci 2 161 162 10.1016/S1360-1385(97)01029-7 (Pubitemid 27186090)
51. A van Besouw JFGM Wintermans 1978 Galactolipid formation in chloroplast envelopes: I. Evidence for two mechanisms in galactosylation Biochim Biophys Acta 529 44 53 638180 (Pubitemid 8314696)
52. Wang Z, Benning C (2011) Arabidopsis thaliana polar glycerolipid profiling by thin layer chromatography (TLC) coupled with gas-liquid chromatography (GLC). J Vis Exp 49:e2518. http://www.jove.com/details.stp?id= 2518
53. Z Wang C Xu C Benning 2012 TGD4 involved in endoplasmic reticulum-to-chloroplast lipid trafficking is a phosphatidic acid binding protein Plant J 10.1111/j.1365-1313X.2012.04900.x
54. AR Wellburn H Lichtenthaler 1984 Formulae and program to determine total carotenoids and chlorophylls a and b of leaf extracts in different solvents Adv Photosynth Res 2 9 12 1:CAS:528:DyaL2cXksFWjurc%3D
55. HT Witt 1979 Energy conversion in the functional membrane of photosynthesis. Analysis by light pulse and electric pulse methods. The central role of the electric field Biochim Biophys Acta 505 355 35227 1:CAS:528:DyaE1MXhs1CltLs%3D
56. C Xu J Fan W Riekhof JE Froehlich C Benning 2003 A permease-like protein involved in ER to thylakoid lipid transfer in Arabidopsis EMBO J 22 2370 2379 12743031 10.1093/emboj/cdg234 1:CAS:528:DC%2BD3sXjvV2gsLk%3D (Pubitemid 36604976)
57. C Xu J Fan JE Froehlich K Awai C Benning 2005 Mutation of the TGD1 chloroplast envelope protein affects phosphatidate metabolism in Arabidopsis Plant Cell 17 3094 3110 16199613 10.1105/tpc.105.035592 1:CAS:528: DC%2BD2MXht1OgtLjJ
58. 6 /f complexes in limiting chloroplast electron transport and determining photosynthetic capacity Plant Physiol 155 956 962 21177473 10.1104/pp.110.168435 1:CAS:528: DC%2BC3MXksFOqt74%3D
59. R Zhang TD Sharkey 2009 Photosynthetic electron transport and proton flux under moderate heat stress Photosynth Res 100 29 43 19343531 10.1007/s11120-009-9420-8 1:CAS:528:DC%2BD1MXltVyktL4%3D
60. W Zhang C Qin J Zhao X Wang 2004 Phospholipase Dα1-derived phosphatidic acid interacts with ABI1 phosphatase 2C and regulates abscisic acid signaling Proc Natl Acad Sci USA 101 9508 9513 15197253 10.1073/pnas.0402112101 1:CAS:528:DC%2BD2cXltlKjtr4%3D (Pubitemid 38812905)
61. R Zhang JA Cruz DM Kramer ME Magallanes-Lundback D Dellapenna TD Sharkey 2009 Moderate heat stress reduces the pH component of the transthylakoid proton motive force in light-adapted, intact tobacco leaves Plant Cell Environ 32 1538 1547 19558623 10.1111/j.1365-3040.2009.02018.x 1:CAS:528:DC%2BD1MXhsVKhtbbM
62. R Zhang RR Wise KR Struck TD Sharkey 2011 Moderate heat stress of Arabidopsis thaliana leaves causes chloroplast swelling and plastoglobule formation Photosynth Res 105 123 134 10.1007/s11120-010-9572-6