Diurnal expression of five protein phosphatase type 2C genes in the common ice plant, Mesembryanthemum crystallinum
Ko Sato A C , Hiroaki Ohsato A , Shunsuke Izumi A , Saori Miyazaki A B D , Hans J. Bohnert B , Hiromitsu Moriyama A and Toshiyuki Fukuhara A EA Department of Applied Biological Sciences, Tokyo University of Agriculture and Technology, 3-5-8 Saiwaicho, Fuchu, Tokyo 183-8509, Japan.
B Department of Plant Biology, Department of Crop Sciences, and Institute for Genome Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA.
C Present address: The Kitasato Institute Research Center for Biologicals, 6-111 Arai, Kitamoto-shi, Saitama 364-0026, Japan.
D Present address: National Institute for Basic Biology, Okazaki 444-8585, Japan.
E Corresponding author. Email: fuku@cc.tuat.ac.jp
Functional Plant Biology 34(7) 581-588 https://doi.org/10.1071/FP06342
Submitted: 28 December 2006 Accepted: 16 April 2007 Published: 4 July 2007
Abstract
The common ice plant, Mesembryanthemum crystallinum L., is a eu-halophytic model species with an environmental stress-initiated switch from C3 photosynthesis to crassulacean acid metabolism (CAM). Phosphoenolpyruvate carboxylase activity in 6-week-old plants exposed to salt stress for 5 days was ~15-fold higher than before stress, indicating the salinity-dependent induction of the C3 to CAM transition. Five plant protein phosphatase type 2C (PP2C) genes were cloned, representative of five of the 10 plant PP2C sub-families. We measured mRNA levels of these PP2Cs and of myo-inositol 1-phosphate synthase (Inps1) in 6-week-old plants before (C3) and after (CAM) salt stress. Remarkably, four PP2C genes and Inps1 were expressed with a diurnal fluctuation in plants in C3 mode. After salt-induced CAM induction, the six genes were expressed with more prominent fluctuations than before stress, suggesting that these PP2C genes may be involved in the diurnal regulation of protein phosphorylation in CAM. Under continuous light treatment the expression of two PP2C genes continued to fluctuate, indicating that their expression is controlled by circadian rhythm.
Additional keywords: circadian rhythm, crassulacean acid metabolism, diurnal rhythm, protein phosphatase type 2C, phosphoenolpyruvate carboxylase.
Acknowledgements
This research was supported in part by Grants-in-Aid for Scientific Research (No. 12025206 to TF) from the Ministry of Education, Science, Sports, Culture and Technology of Japan.
Adams P,
Nelson DE,
Yamada S,
Chmara W,
Jensen RG,
Bohnert HJ, Griffiths H
(1998) Growth and development of Mesembryanthemum crystallinum (Aizoaceae). New Phytologist 138, 171–190.
| Crossref | GoogleScholarGoogle Scholar |
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,
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 stress. Plant Physiology 137, 969–982.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Cushman JC
(2001) Crassulacean acid metabolism. A plastic photosynthetic adaptation to arid environments. Plant Physiology 127, 1439–1448.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Harmer SL,
Hogenesch JB,
Straume M,
Chang HS,
Han B,
Zhu T,
Wang X,
Kreps JA, Kay SA
(2000) Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290, 2110–2113.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ishitani M,
Majumder AL,
Bornhouser A,
Michalowski CB,
Jensen RG, Bohnert HJ
(1996) Coordinate transcriptional induction of myo-inositol metabolism during environmental stress. The Plant Journal 9, 537–548.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kerk D,
Bulgrien J,
Smith DW,
Barsam B,
Veretnik S, Gribskov M
(2002) The complement of protein phosphatase catalytic subunits encoded in the genome of Arabidopsis. Plant Physiology 129, 908–925.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kore-eda S,
Noake C,
Ohishi M,
Ohnishi J, Cushman JC
(2005) Transcriptional profiles of organellar metabolite transporters during induction of crassulacean acid metabolism in Mesembryanthemum crystallinum. Functional Plant Biology 32, 451–466.
| Crossref | GoogleScholarGoogle Scholar |
Kumar S,
Tamura K, Nei M
(2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Briefings in Bioinformatics 5, 150–163.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Leung J,
Bouvier-Durand M,
Morris PC,
Guerrier D,
Chefdor F, Giraudat J
(1994) Arabidopsis ABA-response gene ABI1: features of a calcium-modulated protein phosphatase. Science 264, 1448–1452.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lombardi LM, Brody S
(2005) Circadian rhythms in Neurospora crassa: clock gene homologues in fungi. Fungal Genetics and Biology 42, 887–892.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lüttge U
(2004) Ecophysiology of crassulacean acid metabolism (CAM). Annals of Botany 93, 629–652.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Meyer K,
Leube MP, Grill E
(1994) A protein phosphatase 2C involved in ABA signal transduction in Arabidopsis thaliana. Science 264, 1452–1455.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Miyazaki S,
Koga R,
Bohnert HJ, Fukuhara T
(1999) Tissue- and environmental response-specific expression of 10 PP2C transcripts in Mesembryanthemum crystallinum. Molecular & General Genetics 261, 307–316.
| Crossref | GoogleScholarGoogle Scholar |
Nagy F,
Kay SA, Chua NH
(1988) Analysis of gene expression in transgenic plants. Plant Molecular Biology Manual B4, 1–29.
Nelson DE,
Rammesmayer G, Bohnert HJ
(1998) Regulation of cell-specific inositol metabolism and transport in plant salinity tolerance. The Plant Cell 10, 753–764.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Nicholas KB,
Nicholas HB, Deerfield DW
(1997) GeneDoc: analysis and visualization of genetic variation. EMBnet NEWS 4, 14.
Nimmo HG
(2000) The regulation of phosphoenolpyruvate carboxylase in CAM plants. Trends in Plant Science 5, 75–80.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Parvathi K,
Bhagwat AS,
Ueno Y,
Izui K, Raghavendra AS
(2000) Illumination increases the affinity of phosphoenolpyruvate carboxylase to bicarbonate in leaves of a C4 plant, Amaranthus hypochondriacus. Plant & Cell Physiology 41, 905–910.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Schaffer R,
Landgraf J,
Accerbi M,
Simon V,
Larson M, Wisman E
(2001) Microarray analysis of diurnal and circadian-regulated genes in Arabidopsis. The Plant Cell 13, 113–124.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Schena M,
Shalon D,
Davis RW, Brown PO
(1995) Quantitative monitoring of gene expression patterns with a complementary DNA microarray. Science 270, 467–470.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Schweighofer A,
Hirt H, Meskiene I
(2004) Plant PP2C phosphatases: emerging functions in stress signaling. Trends in Plant Science 9, 236–243.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Stone JM,
Collinge MA,
Smith RD,
Horn MA, Walker JC
(1994) Interaction of a protein phosphatase with an Arabidopsis serine-threonine receptor kinase. Science 266, 793–795.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Taybi T,
Patil S,
Chollet R, Cushman JC
(2000) A minimal serine/threonine protein kinase circadianly regulates phosphoenolpyruvate carboxylase activity in crassulacean acid metabolism-induced leaves of the common ice plant. Plant Physiology 123, 1471–1482.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Thompson JD,
Gibson TJ,
Plewniak F,
Jeanmougin F, Higgins DG
(1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Yu LP,
Miller AK, Clark SE
(2003) POLTERGEIST encodes a protein phosphatase 2C that regulates CLAVATA pathways controlling stem cell identity at Arabidopsis shoot and flower meristems. Current Biology 13, 179–188.
| Crossref | GoogleScholarGoogle Scholar | PubMed |