Transcriptional profiles of organellar metabolite transporters during induction of crassulacean acid metabolism in Mesembryanthemum crystallinum
Shin Kore-eda A , Chiyuki Noake A , Masahisa Ohishi A , Jun-ichi Ohnishi A and John C. Cushman B CA Department of Biochemistry and Molecular Biology, Saitama University, Saitama City, 338-8570, Japan.
B Department of Biochemistry and Molecular Biology, University of Nevada, Reno, NV, 89557-0014, USA.
C Corresponding author. Email: jcushman@unr.edu
D This paper originates from a presentation at the IVth International Congress on Crassulacean Acid Metabolism, Tahoe City, California, USA, July–August 2004
Functional Plant Biology 32(5) 451-466 https://doi.org/10.1071/FP04188
Submitted: 15 October 2004 Accepted: 3 March 2005 Published: 27 May 2005
Abstract
Metabolite transport across multiple organellar compartments is essential for the operation of crassulacean acid metabolism (CAM). To investigate potential circadian regulation of inter-organellar metabolite transport processes, we have identified eight full-length cDNAs encoding an organellar triose phosphate / Pi translocator (McTPT1), a phosphoenolpyruvate / Pi translocator (McPPT1), two glucose-6-phosphate / Pi translocators (McGPT1, 2), two plastidic Pi translocator-like proteins (McPTL1, 2), two adenylate transporters (McANT1, 2), a dicarboxylate transporter (McDCT2), and a partial cDNA encoding a second dicarboxylate transporter (McDCT1) in the model CAM plant, Mesembryanthemum crystallinum L. We next investigated day / night changes in steady-state transcript abundance of each of these transporters in plants performing either C3 photosynthesis or CAM induced by salinity or water-deficit stress. We observed that the expression of both isogenes of the glucose-6-phosphate / Pi translocator (McGPT1, 2) was enhanced by CAM induction, with McGPT2 transcripts exhibiting much more pronounced diurnal changes in transcript abundance than McGPT1. Transcripts for McTPT1, McPPT1, and McDCT1 also exhibited more pronounced diurnal changes in abundance in the CAM mode relative to the C3 mode. McGPT2 and McDCT1 transcripts exhibited sustained oscillations for at least 3 d under constant light and temperature conditions suggesting their expression is under circadian clock control. McTPT1 and McGPT2 transcripts were preferentially expressed in leaf tissues in either C3 or CAM modes. The leaf-specific and / or circadian controlled gene expression patterns are consistent with McTPT1, McGPT2 and McDCT1 playing CAM-specific metabolite transport roles.
Key words: circadian clock, common ice plant, crassulacean acid metabolism, metabolite transporters, salinity stress, transcript abundance.
Acknowledgments
The authors are grateful to Dr James Hartwell (University of Liverpool, UK) for providing the contig sequence and information about the expression properties of UBI1. We appreciate Dr Ikuo Nishida (Saitama University, Japan) for valuable and helpful discussions. We also thank Ms. Yuki Matsushima for technical support. This work was supported, in part, by funding from the Asahi Glass Foundation (to S.K.) and the National Science Foundation (IBN-0196070 and DBI-9813360) to J.C.C. Research supported in part by the Nevada Agricultural Experiment Station, publication # 03055492.
Altschul SF,
Gish W,
Miller W,
Meyers EW, Lipman DJ
(1990) Basic Local Alignment Search Tool. Journal of Molecular Biology 215, 403–410.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Amiri H,
Karlberg O, Andersson SE
(2003) Deep origin of plastid / parasite ATP / ADP translocases. Journal of Molecular Evolution 56, 137–150.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Borland AM, Taybi T
(2004) Synchronization of metabolic processes in plants with Crassulacean acid metabolism. Journal of Experimental Botany 55, 1255–1265.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Boxall, SF ,
Bohnert, HJ ,
Cushman, JC ,
Nimmo, HG ,
and
Hartwell, J (2001). The circadian clock and Crassulacean acid metabolism in Mesembryanthemum crystallinum. In ‘Proceedings of the 12th international congress on photosynthesis, Brisbane, Australia’. Poster S-18-012..
Boxall SF,
Foster JM,
Bohnert HJ,
Cushman JC,
Nimmo HG, Hartwell J
(2005) Conservation and divergence of circadian clock operation in a stress-inducible Crassulacean acid metabolism species reveals clock compensation against abiotic stress. Plant Physiology 137, 969–982.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Chen L-S,
Lin Q, Nose A
(2002) A comparative study of diurnal changes in metabolite levels in the leaves of three crassulacean acid metabolism (CAM) species, Ananas comosus, Kalanchoë daigremontiana and K. pinnata.
Journal of Experimental Botany 53, 341–350.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Cushman JC, Bohnert HJ
(1989) Nucleotide sequence of the gene encoding a CAM specific isoform of phosphoenolpyruvate carboxylase from Mesembryanthemum crystallinum.
Nucleic Acids Research 17, 6745–6746.
| PubMed |
Cushman JC, Bohnert HJ
(1999) Crassulacean acid metabolism: molecular genetics. Annual Review of Plant Physiology and Plant Molecular Biology 50, 305–332.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Cushman JC, Borland AM
(2002) Induction of crassulacean acid metabolism by water limitation. Plant, Cell & Environment 25, 295–310.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Dodd AN,
Griffiths H,
Taybi T,
Cushman JC, Borland AM
(2003) Integrating diel starch metabolism with the circadian and environmental regulation of Crassulacean acid metabolism in Mesembryanthemum crystallinum.
Planta 216, 789–797.
| PubMed |
Emanuelsson O,
Nielsen H,
Brunak S, von Heijne G
(2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. Journal of Molecular Biology 300, 1005–1016.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Epimashko S,
Meckel T,
Fischer-Schliebs E,
Lüttge U, Thiel G
(2004) Two functionally different vacuoles for static and dynamic purposes in one plant mesophyll leaf cell. The Plant Journal 37, 294–300.
| PubMed |
Felsenstein, J (2004).
Fischer K,
Kammerer B,
Gutensohn M,
Arbinger B,
Weber A,
Häusler RE, Flügge U-I
(1997) A new class of plastidic phosphate translocators: a putative link between primary and secondary metabolism by the phosphoenolpyruvate / phosphate antiporter. The Plant Cell 9, 453–462.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Fißlthaler B,
Meyer G,
Bohnert HJ, Schmitt JM
(1995) Age-dependent induction of pyruvate, orthophosphate dikinase in Mesembryanthemum crystallinum L. Planta 196, 492–500.
| Crossref |
PubMed |
Fliege R,
Flügge U-I,
Werden K, Heldt HW
(1978) Specific transport of inorganic phosphate, 3-phosphoglycerate and triosephosphates across the inner membrane of the envelope in spinach chloroplasts. Biochimica et Biophysica Acta 502, 232–247.
| PubMed |
Flügge U-I, Weber A
(1994) A rapid method for measuring organelle-specific substrate transport in homogenates from plant tissues. Planta 194, 181–185.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Flügge U-I,
Woo KC, Heldt HW
(1988) Characteristics of 2-oxoglutarate and glutamate transport in spinach chloroplasts. Planta 174, 534–541.
| Crossref | GoogleScholarGoogle Scholar |
Flügge U-I,
Fischer K,
Gross A,
Sebald W,
Lottspeich F, Eckerskorn C
(1989) The triose phosphate-3-phosphoglycerate-phosphate translocator from spinach chloroplasts: nucleotide sequence of a full-length cDNA clone and import of the in vitro synthesized precursor protein into chloroplasts. EMBO Journal 8, 39–46.
| PubMed |
Hafke JB,
Hafke Y,
Smith JAC,
Lüttge U, Thiel G
(2003) Vacuolar malate uptake is mediated by an anion-selective inward rectifier. The Plant Journal 35, 116–128.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hirokawa T,
Boon-Chieng S, Mitaku S
(1998) SOSUI: classification and secondary structure prediction system for membrane proteins. Bioinformatics 14, 378–379.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Häusler RE,
Baur B,
Scharte J,
Teichmann T,
Eicks M,
Fischer KL,
Flügge U-I,
Schubert S,
Weber A, Fischer K
(2000) Plastidic metabolite transporters and their physiological functions in the inducible crassulacean acid metabolism plant Mesembryanthemum crystallinum.
The Plant Journal 24, 285–296.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Holtum JAC, Winter K
(1982) Activities of enzymes of carbon metabolism during the induction of crassulacean acid metabolism in Mesembryanthemum crystallinum L. Planta 155, 8–16.
| Crossref | GoogleScholarGoogle Scholar |
Jack DL,
Yang NM, Saier MH
(2001) The drug / metabolite transporter superfamily. European Journal of Biochemistry 268, 3620–3639.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kammerer B,
Fischer K,
Hilpert B,
Schubert S,
Gutensohn M,
Weber A, Flügge U-I
(1998) Molecular characterization of a carbon transporter in plastids from heterotrophic tissues: the glucose 6-phosphate / phosphate antiporter. The Plant Cell 10, 105–117.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Knappe S,
Flügge U-I, Fischer K
(2003) Analysis of the plastidic phosphate translocator gene family in Arabidopsis and identification of new phosphate translocator-homologous transporters, classified by their putative substrate-binding site. Plant Physiology 131, 1178–1190.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kolarov J,
Kolarova N, Nelson N
(1990) A third ADP / ATP translocator gene in yeast. The Journal of Biological Chemistry 265, 12711–12716.
| PubMed |
Kore-eda S, Kanai R
(1997) Induction of glucose 6-phosphate transport activity in chloroplasts of Mesembryanthemum crystallinum by the C3–CAM transition. Plant & Cell Physiology 38, 895–901.
Kore-eda S,
Yamashita T, Kanai R
(1996) Induction of light dependent pyruvate transport into chloroplasts of Mesembryanthemum crystallinum by salt stress. Plant & Cell Physiology 37, 257–262.
Kore-eda S,
Cushman MA,
Akselrod I,
Bufford D,
Fredrickson M,
Clark E, Cushman JC
(2004) Transcript profiling of salinity stress responses by large-scale expressed sequence tag analysis in Mesembryanthemum crystallinum.
Gene 341, 83–92.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Krogh A,
Larsson B,
von Heijne G, Sonnhammer ELL
(2001) Predicting transmembrane protein topology with a hidden markov model: application to complete genomes. Journal of Molecular Biology 305, 567–580.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Linka N,
Hurka H,
Lang FB,
Burger G,
Winkler HH,
Stamme C,
Urbany C,
Seil I,
Kusch J, Neuhaus HE
(2003) Phylogenetic relationships of non-mitochondrial nucleotide transport proteins in bacteria and eukaryotes. Gene 306, 27–35.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lüttge U
(2004) Ecophysiology of crassulacean acid metabolism. Annals of Botany 93, 629–652.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lüttge U,
Pfeifer T,
Fischer-Schliebs E, Ratajczak R
(2000) The role of vacuolar malate-transport capacity in crassulacean acid metabolism and nitrate nutrition. Higher malate-transport capacity in ice plant after crassulacean acid metabolism-induction and in tobacco under nitrate nutrition. Plant Physiology 124, 1335–1347.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Maia IG,
Benedetti CE,
Leite A,
Turcinelli SR,
Vercesi AE, Arruda P
(1998) AtPUMP: an Arabidopsis gene encoding a plant uncoupling mitochondrial protein. FEBS Letters 429, 403–406.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Maxwell K,
Borland AM,
Haslam RP,
Helliker BR,
Roberts A, Griffiths H
(1999) Modulation of rubisco activity during the diurnal phases of the Crassulacean acid metabolism plant Kalanchoë daigremontiana.
Plant Physiology 121, 849–856.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Millar AH, Heazlewood JL
(2003) Genomic and proteomic analysis of mitochondrial carrier proteins in Arabidopsis.
Plant Physiology 131, 443–453.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Möhlmann T,
Tjaden J,
Schwuöppe C,
Winkler HH,
Kampfenkel K, Neuhaus HE
(1998) Occurrence of two plastidic ATP / ADP transporters in Arabidopsis thaliana L. — molecular characterization and comparative structural analysis of similar ATP / ADP translocators from plastids and Rickettsia prowazekii.
European Journal of Biochemistry 252, 353–359.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Möllering, H (1974).
l-(-)-malate, determination with malate dehydrogenase and glutamate–oxaloacetate transaminase. In ‘Methods of enzymatic analysis’. pp. 163–181. (Academic Press: New York)
Neuhaus HE, Schulte N
(1996) Starch degradation in chloroplasts isolated from C3 or CAM (crassulacean acid metabolism)-induced Mesembryanthemum crystallinum L. The Biochemical Journal 318, 945–953.
| PubMed |
Neuhaus HE,
Holtum JAM, Latzko E
(1988) Transport of phosphoenolpyruvate by chloroplasts from Mesembryanthemum crystallinum L. exhibiting Crassulacean acid metabolism. Plant Physiology 87, 64–68.
Niewiadomska E,
Miszalski Z,
Slesak I, Ratajczak R
(1999) Catalase activity during C3–CAM transition in Mesembryanthemum crystallinum L. leaves. Free Radical Research 31, S251–S256.
| PubMed |
Paul MJ,
Loos K,
Stitt M, Ziegler P
(1993) Starch-degrading enzymes during the induction of CAM in Mesembryanthemum crystallinum.
Plant, Cell & Environment 16, 531–538.
Picault N,
Palmieri L,
Pisano I,
Hodges M, Palmieri F
(2002) Identification of a novel transporter for dicarboxylates and tricarboxylates in plant mitochondria. Bacterial expression, reconstitution, functional characterization, and tissue distribution. The Journal of Biological Chemistry 277, 24204–24211.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Reiser J,
Linka N,
Lemke L,
Jeblick W, Neuhaus HE
(2004) Molecular physiological analysis of the two plastidic ATP / ADP transporters from Arabidopsis.
Plant Physiology 136, 3524–3536.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sun C-W, Callis J
(1997) Independent modulation of Arabidopsis thaliana polyubiquitin mRNAs in different organs and in response to environmental changes. The Plant Journal 11, 1017–1027.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Taniguchi Y,
Nagasaki J,
Kawasaki M,
Miyake H,
Sugiyama T, Taniguchi M
(2004) Differentiation of dicarboxylate transporters in mesophyll and bundle sheath chloroplasts of maize. Plant & Cell Physiology 45, 187–200.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Taybi T, Cushman JC
(1999) Signaling events leading to Crassulacean acid metabolism induction in the common ice plant. Plant Physiology 121, 545–556.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Thompson J,
Gibson T,
Plewniak F,
Jeanmougin F, Higgins D
(1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Tóth R,
Kevei E,
Hall A,
Millar AJ,
Nagy F, Kozma-Bognar L
(2001) Circadian clock-regulated expression of phytochrome and cryptochrome genes in Arabidopsis.
Plant Physiology 127, 1607–1616.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Weber A, Flügge U-I
(2002) Interaction of cytosolic and plastidic nitrogen metabolism in plants. Journal of Experimental Botany 53, 865–874.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Weber APM,
Schneidereit J, Voll LM
(2004) Using mutants to probe the in vivo function of plastid envelope membrane metabolite transporters. Journal of Experimental Botany 55, 1231–1244.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Winkler HH, Neuhaus HE
(1999) Non-mitochondrial ATP transport. Trends in Biochemical Sciences 24, 64–68.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Winter K,
Foster JG,
Edwards GE, Holtum JAM
(1982) Intracellular localization of enzymes of carbon metabolism in Mesembryanthemum crystallinum exhibiting C3 photosynthetic characteristics or performing Crassulacean acid metabolism. Plant Physiology 69, 300–307.
