Large gene family of phosphoenolpyruvate carboxylase in the crassulacean acid metabolism plant Kalanchoe pinnata (Crassulaceae) characterised by partial cDNA sequence analysis
Hans H. Gehrig A , Joshua A. Wood B , Mary Ann Cushman B , Aurelio Virgo A , John C. Cushman B C and Klaus Winter AA Smithsonian Tropical Research Institute, P.O. Box 2072, Balboa, Ancón, Republic of Panama.
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) 467-472 https://doi.org/10.1071/FP05079
Submitted: 4 April 2005 Accepted: 3 May 2005 Published: 27 May 2005
Abstract
Clones coding for a 1100-bp cDNA sequence of phosphoenolpyruvate carboxylase (PEPC) of the constitutive crassulacean acid metabolism (CAM) plant Kalanchoe pinnata (Lam.) Pers., were isolated by reverse transcription-polymerase chain reaction (RT–PCR) and characterised by restriction fragment length polymorphism analysis and DNA sequencing. Seven distinct PEPC isogenes were recovered, four in leaves and three in roots (EMBL accession numbers: AJ344052–AJ344058). Sequence similarity comparisons and distance neighbour-joining calculations separate the seven PEPC isoforms into two clades, one of which contains the three PEPCs found in roots. The second clade contains the four isoforms found in leaves and is divided into two branches, one of which contains two PEPCs most similar with described previously CAM isoforms. Of these two isoforms, however, only one exhibited abundant expression in CAM-performing leaves, but not in very young leaves, which do not exhibit CAM, suggesting this isoform encodes a CAM-specific PEPC. Protein sequence calculations suggest that all isogenes are likely derived from a common ancestor gene, presumably by serial gene duplication events. To our knowledge, this is the most comprehensive identification of a PEPC gene family from a CAM plant, and the greatest number of PEPC isogenes reported for any vascular plant to date.
Keywords: crassulacean acid metabolism, evolution, gene family, isogenes, Kalanchoe pinnata, phosphoenolpyruvate carboxylase.
Acknowledgements
This research was supported by grants from the Andrew W. Mellon Foundation through the Smithsonian Tropical Research Institute to JCC and KW, and by funds from the Smithsonian Tropical Research Institute to KW. Additional support was provided by the Nevada Agricultural Experiment Station and this article is published as publication No. 03055524 of the University of Nevada Agricultural Experiment Station.
Bläsing OE,
Ernst K,
Streubel M,
Westhoff P, Svensson P
(2002) The non-photosynthetic phosphoenolpyruvate carboxylases of the C4 dicot Flaveria trinervia — implications for the evolution of C4 photosynthesis. Planta 215, 448–456.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Chollet R,
Vidal J, O’Leary MH
(1996) Phosphoenolpyruvate carboxylase: a ubiquitous, highly regulated enzyme in plants. Annual Review of Plant Physiology and Plant Molecular Biology 47, 273–298.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Crayn DM,
Winter K, Smith JAC
(2004) Multiple origins of crassulacean acid metabolism and the epiphytic habit in the neotropical family Bromeliaceae. Proceedings of the National Academy of Sciences USA 101, 3703–3708.
| Crossref | GoogleScholarGoogle Scholar |
Crétin C,
Santi S,
Keryer E,
Lepiniec L,
Tagu D,
Vidal J, Gadal P
(1991) The phosphoenolpyruvate carboxylase gene family of Sorghum: promoter structures, amino acid sequences, and expression of genes. Gene 99, 87–94.
| Crossref | GoogleScholarGoogle Scholar | 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,
Meyer G,
Michalowski CB,
Schmitt JM, Bohnert HJ
(1989) Salt stress leads to the differential expression of two isogenes of phosphoenolpyruvate carboxylase during crassulacean acid metabolism induction in the common ice plant. The Plant Cell 1, 715–725.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Deleens E, Queiroz O
(1984) Effects of photoperiod and aging on the carbon isotope composition of Bryophyllum daigremontianum Berger. Plant, Cell & Environment 7, 279–283.
Edwards, G ,
and
Walker, DA (1983).
Engelmann S,
Bläsing OE,
Westhoff P, Svensson P
(2002) Serine 774 and amino acids 296 to 437 comprise the major C4 determinants of the C4 phosphoenolpyruvate carboxylase of Flaveria trinervia.
FEBS Letters 524, 11–14.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Felsenstein J
(1991) Counting phylogenetic invariants in some simple cases. Journal of Theoretical Biology 152, 357–376.
| PubMed |
Gehrig HH,
Taybi T,
Kluge M, Brulfert J
(1995) Identification of multiple PEPC isogenes in leaves of the facultative crassulacean acid metabolism (CAM) plant Kalanchoe blossfeldiana Poelln. cv. Tom Thumb. FEBS Letters 377, 399–402.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Gehrig HH,
Faist K, Kluge M
(1998) Identification of phosphoenolpyruvate carboxylase isoforms in leaf, stem and roots of the obligate CAM plant Vanilla planifolia Salib. (Orchidaceae): a physiological and molecular approach. Plant Molecular Biology 38, 1215–1223.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Gehrig H,
Heute V, Kluge M
(2001) New partial sequences of phosphoenolpyruvate carboxylase as molecular phylogenetic markers. Molecular Phylogenetics and Evolution 20, 262–274.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Gehrig HH,
Winter K,
Cushman J,
Borland AM, Taybi T
(2000) An improved RNA isolation method for succulent plant species rich in polyphenols and polysaccharides. Plant Molecular Biology Reporter 18, 369–376.
Gehrig HH,
Aranda J,
Cushman MA,
Virgo A,
Cushman JC,
Hammel BE, Winter K
(2003) Cladogram of Panamanian Clusia based on nuclear DNA: implications for the origins of crassulacean acid metabolism. Plant Biology 5, 59–70.
| Crossref | GoogleScholarGoogle Scholar |
Golombek S,
Heim U,
Horstmann C,
Wobus U, Weber H
(1999) Phosphoenolpyruvate carboxylase in developing seeds of Vicia faba L.: gene expression and metabolic regulation. Planta 208, 66–72.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Guillet C,
Just D,
Bénard N,
Destrac-Irvine A,
Baldet P,
Hernould M,
Causse M,
Raymond P, Rothan C
(2002) A fruit-specific phosphoenolpyruvate carboxylase is related to rapid growth of tomato fruit. Planta 214, 717–726.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hata S,
Izui K, Kouchi H
(1997) Expression of a soybean nodule-enhanced phosphoenolpyruvate carboxylase gene that shows striking similarity to another gene for a housekeeping isoform. The Plant Journal 7, 198–201.
Holmes DS, Quigley M
(1981) A rapid boiling method for the preparation of bacterial plasmids. Analytical Biochemistry 114, 193–197.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Holtum JAM, Winter K
(1999) Degrees of crassulacean acid metabolism in tropical epiphytic and lithophytic ferns. Australian Journal of Plant Physiology 26, 749–757.
Holtum JAM,
Aranda J,
Virgo A,
Gehrig HH, Winter K
(2004) δ13C values and crassulacean acid metabolism in Clusia species from Panama. Trees — Structure and Function 18, 658–668.
| Crossref | GoogleScholarGoogle Scholar |
Izui K,
Matsumura H,
Furumoto T, Kai Y
(2004) Phosphoenolpyruvate carboxylase: a new era of structural biology. Annual Review of Plant Biology 55, 69–84.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Jones MB
(1975) The effect of leaf age on leaf resistance and CO2 exchange of the CAM plant Bryophyllum fedtschenkoi.
Planta 123, 91–96.
| Crossref | GoogleScholarGoogle Scholar |
Kimura M
(1980) A simple model for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111–120.
| PubMed |
Kopka J,
Provart NJ, Muller-Rober B
(1997) Potato guard cells respond to drying soil by a complex change in the expression of genes related to carbon metabolism and turgor regulation. The Plant Journal 11, 871–882.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lepiniec L,
Vidal J,
Chollet R,
Gadal P, Crétin C
(1994) Phosphoenolpyruvate carboxylase: structure, regulation, and evolution. Plant Science 99, 111–124.
| Crossref | GoogleScholarGoogle Scholar |
Nimmo HG
(2000) The regulation of phosphoenolpyruvate carboxylase in CAM plants. Trends in Plant Science 5, 75–80.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Nishida K
(1978) Effect of leaf age on light and dark 14CO2 fixation in a CAM plant, Bryophyllum calycinum.
Plant & Cell Physiology 19, 935–941.
Pathirana MS,
Samac DA,
Roeven R,
Yoshioka H,
Vance CP, Gantt JS
(1997) Analyses of phosphoenolpyruvate carboxylase gene structure and expression in alfalfa nodules. The Plant Journal 12, 293–304.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Rao SK,
Magnin NC,
Reiskind JB, Bowes G
(2002) Photosynthetic and other phosphoenolpyruvate carboxylase isoforms in the single-cell, facultative C(4) system of Hydrilla verticillata.
Plant Physiology 130, 876–886.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sanchez R, Cejudo FJ
(2003) Identification and expression analysis of a gene encoding a bacterial-type phosphoenolpyruvate carboxylase from Arabidopsis and rice. Plant Physiology 132, 949–957.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Schaffner AR, Sheen J
(1992) Maize C4 photosynthesis involves differential regulation of phosphoenolpyruvate carboxylase genes. The Plant Journal 2, 221–232.
| PubMed |
Silvera K,
Santiago LS, Winter K
(2005) Distribution of crassulacean acid metabolism in orchids of Panama: evidence of selection for weak and strong modes. Functional Plant Biology 32, 397–407.
| Crossref | GoogleScholarGoogle Scholar |
Smart LB,
Vodjani F,
Maeshima M, Wilkins TA
(1998) Genes involved in osmoregulation during turgor-driven cell expansion of developing cotton fibers are differentially regulated. Plant Physiology 116, 1539–1549.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Winter K, Holtum JAM
(2002) How closely do the δ13C values of crassulacean acid metabolism plants reflect the proportion of CO2 fixed during day and night? Plant Physiology 129, 1843–1851.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Winter, K ,
and
Smith, JAC (1996).
Winter K,
Zotz G,
Baur B, Dietz KJ
(1992) Light and dark CO2 fixation in Clusia uvitana as affected by plant water status and CO2 availability. Oecologia 91, 47–51.
| Crossref | GoogleScholarGoogle Scholar |
Winter K,
Richter A,
Engelbrecht B,
Posada J,
Virgo A, Popp M
(1997) Effect of elevated CO2 on growth and crassulacean-acid-metabolism activity of Kalanchöe pinnata under tropical conditions. Planta 201, 389–396.
| Crossref | GoogleScholarGoogle Scholar |