Photosynthesis activates plasma membrane H+-ATPase via sugar accumulation

Plant Physiology

Volumn 171, Issue 1, 2016, Pages 580-589

  Okumura, Masaki ^a   Inoue, Shin ichiro ^a   Kuwata, Keiko ^a   Kinoshita, Toshinori ^a  

^a NAGOYA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE DEPENDENT PROTEINASE; ARABIDOPSIS PROTEIN; CARBOHYDRATE; CARRIER PROTEIN; DIURON; MEMBRANE PROTEIN; PLANT PROTEIN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE; SUCROSE TRANSPORT PROTEIN, PLANT; VAR2 PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; CELL MEMBRANE; DRUG EFFECTS; GENETICS; LIGHT; MESOPHYLL CELL; METABOLISM; MUTATION; PHOSPHORYLATION; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT LEAF; TRANSGENIC PLANT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; ATP-DEPENDENT PROTEASES; CELL MEMBRANE; DIURON; LIGHT; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; MESOPHYLL CELLS; MUTATION; PHOSPHORYLATION; PHOTOSYNTHESIS; PLANT LEAVES; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; PROTON-TRANSLOCATING ATPASES; SUGARS;

EID: 84964886710     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.16.00355     Document Type: Article

References (53)

1. Chen M, Choi Y, Voytas DF, Rodermel S (2000) Mutations in the Arabidopsis VAR2 locus cause leaf variegation due to the loss of a chloroplast FtsH protease. Plant J 22: 303-313
2. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacteriummediated transformation of Arabidopsis thaliana. Plant J 16: 735-743
3. Duby G, Boutry M (2009) The plant plasma membrane proton pump ATPase: a highly regulated P-type ATPase with multiple physiological roles. Pflugers Arch 457: 645-655
4. Fuglsang AT, Visconti S, Drumm K, Jahn T, Stensballe A, Mattei B, Jensen ON, Aducci P, Palmgren MG (1999) Binding of 14-3-3 protein to the plasma membrane H+-ATPase AHA2 involves the three C-terminal residues Tyr946-Thr-Val and requires phosphorylation of Thr947. J Biol Chem 274: 36774-36780
5. Gottwald JR, Krysan PJ, Young JC, Evert RF, Sussman MR (2000) Genetic evidence for the in planta role of phloem-specific plasma membrane sucrose transporters. Proc Natl Acad Sci USA 97: 13979-13984
6. Harada A, Okazaki Y, Takagi S (2002) Photosynthetic control of the plasma membrane H+-ATPase in Vallisneria leaves. I. Regulation of activity during light-induced membrane hyperpolarization. Planta 214: 863-869
7. Hayashi M, Inoue S, Takahashi K, Kinoshita T (2011) Immunohistochemical detection of blue light-induced phosphorylation of the plasma membrane H+-ATPase in stomatal guard cells. Plant Cell Physiol 52: 1238-1248
8. Hayashi Y, Nakamura S, Takemiya A, Takahashi Y, Shimazaki K, Kinoshita T (2010) Biochemical characterization of in vitro phosphorylation and dephosphorylation of the plasma membrane H+-ATPase. Plant Cell Physiol 51: 1186-1196
9. Kato Y, Miura E, Matsushima R, Sakamoto W (2007) White leaf sectors in yellow variegated2 are formed by viable cells with undifferentiated plastids. Plant Physiol 144: 952-960
10. Keifer DW, Spanswick RM (1979) Correlation of adenosine triphosphate levels in Chara corallina with the activity of the electrogenic pump. Plant Physiol 64: 165-168
11. Kinoshita T, Doi M, Suetsugu N, Kagawa T, Wada M, Shimazaki K (2001) Phot1 and phot2 mediate blue light regulation of stomatal opening. Nature 414: 656-660
12. Kinoshita T, Shimazaki K (1999) Blue light activates the plasma membrane H+-ATPase by phosphorylation of the C-terminus in stomatal guard cells. EMBO J 18: 5548-5558
13. Kusano M, Fukushima A, Arita M, Jonsson P, Moritz T, Kobayashi M, Hayashi N, Tohge T, Saito K (2007) Unbiased characterization of genotype-dependent metabolic regulations by metabolomic approach in Arabidopsis thaliana. BMC Syst Biol 1: 53
14. Lastdrager J, Hanson J, Smeekens S (2014) Sugar signals and the control of plant growth and development. J Exp Bot 65: 799-807
15. Lawson T (2009) Guard cell photosynthesis and stomatal function. New Phytol 181: 13-34
16. León P, Sheen J (2003) Sugar and hormone connections. Trends Plant Sci 8: 110-116
17. Lightner J, Caspar T (1998) Seed mutagenesis of Arabidopsis. In JM Martinez-Zapater, J Salinas, eds, Arabidopsis Protocols. Humana Press, Totowa, NJ, pp 91-102
18. Ljung K, Nemhauser JL, Perata P (2015) New mechanistic links between sugar and hormone signalling networks. Curr Opin Plant Biol 25: 130-137
19. Lloyd JC, Zakhleniuk OV (2004) Responses of primary and secondary metabolism to sugar accumulation revealed by microarray expression analysis of the Arabidopsis mutant, pho3. J Exp Bot 55: 1221-1230
20. Marten I, Deeken R, Hedrich R, Roelfsema MRG (2010) Light-induced modification of plant plasma membrane ion transport. Plant Biol (Stuttg) Suppl 1 12: 64-79
21. Maudoux O, Batoko H, Oecking C, Gevaert K, Vandekerckhove J, Boutry M, Morsomme P (2000) A plant plasma membrane H+-ATPase expressed in yeast is activated by phosphorylation at its penultimate residue and binding of 14-3-3 regulatory proteins in the absence of fusicoccin. J Biol Chem 275: 17762-17770
22. Mazzella MA, Alconada Magliano TM, Casal JJ (1997) Dual effect of phytochrome A on hypocotyl growth under continuous red light. Plant Cell Environ 20: 261-267
23. Mimura T, Tazawa M (1986) Light-induced membrane hyperpolarization and adenine nucleotide levels in perfused characean cells. Plant Cell Physiol 27: 319-330
24. Mockler T, Yang H, Yu X, Parikh D, Cheng YC, Dolan S, Lin C (2003) Regulation of photoperiodic flowering by Arabidopsis photoreceptors. Proc Natl Acad Sci USA 100: 2140-2145
25. Neumann J, Levine RP (1971) Reversible pH changes in cells of Chlamydomonas reinhardtii resulting from CO2 fixation in the light and its evolution in the dark. Plant Physiol 47: 700-704
26. Niittylä T, Fuglsang AT, Palmgren MG, Frommer WB, Schulze WX (2007) Temporal analysis of sucrose-induced phosphorylation changes in plasma membrane proteins of Arabidopsis. Mol Cell Proteomics 6: 1711-1726
27. Okumura M, Inoue S, Takahashi K, Ishizaki K, Kohchi T, Kinoshita T (2012a) Characterization of the plasma membrane H+-ATPase in the liverwort Marchantia polymorpha. Plant Physiol 159: 826-834
28. Okumura M, Takahashi K, Inoue S, Kinoshita T (2012b) Evolutionary appearance of the plasma membrane H+-ATPase containing a penultimate threonine in the bryophyte. Plant Signal Behav 7: 979-982
29. Palmgren MG (2001) Plant plasma membrane H+-ATPases: powerhouses for nutrient uptake. Annu Rev Plant Physiol Plant Mol Biol 52: 817-845
30. Prins HB, Harper JR, Higinbotham N (1980) Membrane potentials of Vallisneria leaf cells and their relation to photosynthesis. Plant Physiol 65: 1-5
31. Ren H, Gray WM (2015) SAUR proteins as effectors of hormonal and environmental signals in plant growth. Mol Plant 8: 1153-1164
32. Roitsch T (1999) Source-sink regulation by sugar and stress. Curr Opin Plant Biol 2: 198-206
33. Roitsch T, González MC (2004) Function and regulation of plant invertases: sweet sensations. Trends Plant Sci 9: 606-613
34. Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57: 675-709
35. Rolland F, Moore B, Sheen J (2002) Sugar sensing and signaling in plants. Plant Cell (Suppl) 14: S185-S205
36. Schmitz J, Schöttler MA, Krueger S, Geimer S, Schneider A, Kleine T, Leister D, Bell K, Flügge UI, Häusler RE (2012) Defects in leaf carbohydrate metabolism compromise acclimation to high light and lead to a high chlorophyll fluorescence phenotype in Arabidopsis thaliana. BMC Plant Biol 12: 8
37. Shabala S, Newman I (1999) Light-induced changes in hydrogen, calcium, potassium, and chloride ion fluxes and concentrations from the mesophyll and epidermal tissues of bean leaves: understanding the ionic basis of light-induced bioelectrogenesis. Plant Physiol 119: 1115-1124
38. Shimazaki K, Terada J, Tanaka K, Kondo N (1989) Calvin-Benson cycle enzymes in guard-cell protoplasts from Vicia faba L.: implications for the greater utilization of phosphoglycerate/dihydroxyacetone phosphate shuttle between chloroplasts and the cytosol. Plant Physiol 90: 1057-1064
39. Smeekens S (2000) Sugar-induced signal transduction in plants. Annu Rev Plant Physiol Plant Mol Biol 51: 49-81
40. Solfanelli C, Poggi A, Loreti E, Alpi A, Perata P (2006) Sucrose-specific induction of the anthocyanin biosynthetic pathway in Arabidopsis. Plant Physiol 140: 637-646
41. Spanswick RM (1981) Electrogenic ion pumps. Annu Rev Plant Physiol 32: 267-289
42. Spartz AK, Ren H, Park MY, Grandt KN, Lee SH, Murphy AS, Sussman MR, Overvoorde PJ, Gray WM (2014) SAUR inhibition of PP2C-D phosphatases activates plasma membrane H+-ATPases to promote cell expansion in Arabidopsis. Plant Cell 26: 2129-2142
43. Srivastava AC, Ganesan S, Ismail IO, Ayre BG (2008) Functional characterization of the Arabidopsis AtSUC2 sucrose/H+ symporter by tissuespecific complementation reveals an essential role in phloem loading but not in long-distance transport. Plant Physiol 148: 200-211
44. Stahlberg R, Van Volkenburgh E (1999) The effect of light on membrane potential, apoplastic pH and cell expansion in leaves of Pisum sativum L. var. Argenteum. Planta 208: 188-195
45. Stitt M, Lilley RM, Heldt HW (1982) Adenine nucleotide levels in the cytosol, chloroplasts, and mitochondria of wheat leaf protoplasts. Plant Physiol 70: 971-977
46. Svennelid F, Olsson A, Piotrowski M, Rosenquist M, Ottman C, Larsson C, Oecking C, Sommarin M (1999) Phosphorylation of Thr-948 at the C terminus of the plasma membrane H+-ATPase creates a binding site for the regulatory 14-3-3 protein. Plant Cell 11: 2379-2391
47. Takahashi K, Hayashi K, Kinoshita T (2012) Auxin activates the plasma membrane H+-ATPase by phosphorylation during hypocotyl elongation in Arabidopsis. Plant Physiol 159: 632-641
48. Takemiya A, Sugiyama N, Fujimoto H, Tsutsumi T, Yamauchi S, Hiyama A, Tada Y, Christie JM, Shimazaki K (2013) Phosphorylation of BLUS1 kinase by phototropins is a primary step in stomatal opening. Nat Commun 4: 2094
49. Uemura M, Yoshida S (1986) Studies on freezing injury in plant cells. II. Protein and lipid changes in the plasma membranes of Jerusalem artichoke tubers during a lethal freezing in vivo. Plant Physiol 80: 187-195
50. Ueno K, Kinoshita T, Inoue S, Emi T, Shimazaki K (2005) Biochemical characterization of plasma membrane H+-ATPase activation in guard cell protoplasts of Arabidopsis thaliana in response to blue light. Plant Cell Physiol 46: 955-963
51. Wippel K, Sauer N (2012) Arabidopsis SUC1 loads the phloem in suc2 mutants when expressed from the SUC2 promoter. J Exp Bot 63: 669-679
52. Yoshida K, Watanabe C, Kato Y, Sakamoto W, Noguchi K (2008) Influence of chloroplastic photo-oxidative stress on mitochondrial alternative oxidase capacity and respiratory properties: a case study with Arabidopsis yellow variegated 2. Plant Cell Physiol 49: 592-603
53. Zivanovic BD, Pang J, Shabala S (2005) Light-induced transient ion flux responses from maize leaves and their association with leaf growth and photosynthesis. Plant Cell Environ 28: 340-352