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Transcriptional Activation of CAM Genes During Development and Environmental Stress

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Crassulacean Acid Metabolism

Part of the book series: Ecological Studies ((ECOLSTUD,volume 114))

Abstract

Crassulacean acid metabolism (CAM) can be defined as the ability to perform significant CO2 assimilation into C4 acids (mainly malic acid) in the dark. Reutilization of the stored C4 acids results in a characteristic diel (24 h) pattern of organic-acid fluctuation along with a reciprocal pattern of fluctuating levels of storage glucan. CAM is found primarily, although not exclusively, in succulent plants, particularly those having large chloroplast-containing parenchyma cells with the ability to store large amounts of malic acid and water. CAM plants are mainly tropical or subtropical in origin and typically inhabit arid environments with periodic water deficits such as semi-deserts, or regions with Mediterranean climates, or epiphytic habitats in tropical forests (Kluge and Ting 1978). Their ecological distribution and the observation that CAM plants open their stomata at night and close them during the day to avoid excessive evaporative water loss have led to the general consensus that CAM is a functional adaptation to dry environments and a means of water conservation. However, not all CAM plants occur in arid environments. Isoetes and related species which grow in aquatic environments display CAM (Keeley and Busch 1984). In these instances, CAM provides the plants with a source of carbon when levels of CO2 in the aquatic environment become limiting during the day.

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References

  • Adams P, Thomas JC, Vernon DM, Bohnert HJ, Jensen RG (1992) Distinct cellular and organismic responses to salt stress. Plant Cell Physiol 33: 1215–1223

    CAS  Google Scholar 

  • Andolfatto P, Bornhouser A, Bohnert HJ, Thomas JA (1993) Transformed hairy roots of Mesembryanthemum crystallinum: gene expression patterns upon salt stress. Physiol Plant 90: 708–714

    Article  Google Scholar 

  • Arndt K, Fink GR (1986) GCN4 protein, a positive transcription factor in yeast, binds general control promoters at all 5´-TGACTC-3´ sequences. Proc Natl Acad Sci USA 83: 8516–8520

    Article  PubMed  CAS  Google Scholar 

  • Bohnert HJ, Vernon DM, DeRocher EJ, Michalowski CB, Cushman JC (1992) Biochemistry and molecular biology of CAM. In: Wray JL (ed) Inducible plant proteins. Cambridge University Press, Cambridge, pp 113–137

    Chapter  Google Scholar 

  • Brulfert J, Müller M, Kluge M, Queiroz O (1982) Photoperiodism and crassulacean acid metabolism. Planta 154: 326–331

    Article  CAS  Google Scholar 

  • Chu C, Dai Z, Ku MSB, Edwards GE (1990) Induction of crassulacean acid metabolism in the facultative halophyte Mesembryanthemum crystallinum by abscisic acid. Plant Physiol 93: 1253–1260

    Article  PubMed  CAS  Google Scholar 

  • Cockburn W (1983) Stomatal mechanism as the basis of the evolution of CAM and C4 photosynthesis. Plant Cell Environ 6: 275–279

    CAS  Google Scholar 

  • Cushman JC (1992) Characterization and expression of NADP-malic enzyme cDNA induced by salt stress from the facultative CAM plant, Mesembryanthemum crystallinum. Eur J Biochem 208: 259–266

    Article  PubMed  CAS  Google Scholar 

  • Cushman JC (1993) Molecular cloning and expression of chloroplast NADP-malate dehydrogenase during crassulacean acid metabolism induction by salt stress. Photosynth Res 35: 15–27

    Article  CAS  Google Scholar 

  • Cushman JC, Bohnert HJ (1989a) Nucleotide sequence of the Ppc2 gene encoding a housekeeping isoform of phosphoenolpyruvate carboxylase from Mesembryanthemum crystallinum. Nucleic Acids Res 17: 6743–6744

    Article  PubMed  CAS  Google Scholar 

  • Cushman JC, Bohnert HJ (1989b) Nucleotide sequence of the gene encoding a CAM specific isoform of phosphoenolpyruvate carboxylase from Mesembryanthemum crystallinum. Nucleic Acids Res 17: 6745–6746

    Article  PubMed  CAS  Google Scholar 

  • Cushman JC, Bohnert HJ (1992) Salt stress alters A/T-rich DNA-binding factor interactions within the phosphoenolpyruvate carboxylase promoter from Mesembryanthemum crystallinum. Plant Mol Biol 20: 411–424

    Article  PubMed  CAS  Google Scholar 

  • Cushman JC, Meyer G, Michalowski CB, Schmitt JM, Bohnert HJ (1989) Salt stress leads to differential expression of two isogenes of phosphoenolpyruvate carboxylase during crassulacean acid metabolism induction in the common ice plant. Plant Cell 1: 715–725

    Article  PubMed  CAS  Google Scholar 

  • Cushman JC, Michalowski CB, Bohnert HJ (1990) Developmental control of crassulacean acid metabolism inducibility by salt stress in the common ice plant. Plant Physiol 94: 1137–1142

    Article  PubMed  CAS  Google Scholar 

  • Cushman JC, Meiners MS, Bohnert HJ (1993a) Expression of a phosphoenolpyruvate carboxylase promoter from Mesembryanthemum crystallinum is not salt-inducible in mature transgenic tobacco. Plant Mol Biol 21: 561–566

    Article  PubMed  CAS  Google Scholar 

  • Cushman JC, Vernon DM, Bohnert HJ (1993b) ABA and the transcriptional control of CAM induction during salt stress in the common ice plant. In: Verma DPS (ed) Control of plant gene expression. CRC Press, Boca Raton, pp 287–300

    Google Scholar 

  • Davidson I, Xiao JH, Rosales R, Staub A, Chambon P (1988) The HeLa cell protein TEF-1 binds specifically and cooperatively to two SV40 enhancer motifs of unrelated sequence. Cell 54: 931–942

    Article  PubMed  CAS  Google Scholar 

  • Demmig B, Winter K (1986) Sodium, potassium, chloride and proline concentrations of chloroplasts isolated from a halophyte, Mesembryanthemum crystallinum L. Planta 168: 421–426

    Article  CAS  Google Scholar 

  • DeRocher EJ, Bohnert HJ (1993) Expression of the rbcS gene family in Mesembryanthemum crystallinum during development and under environmental stress. Plant Cell 5: 1611–1625

    Article  PubMed  CAS  Google Scholar 

  • DeRocher EJ, Harkins KR, Galbraith DW, Bohnert HJ (1990) Developmentally regulated systemic endopolyploidy in succulents with small genomes. Science 250: 99–101

    Article  CAS  Google Scholar 

  • DeRocher EJ, Quigley F, Mache R, Bohnert HJ (1993) The six genes of the Rubisco small subunit multigene family from Mesembryanthemum crystallinum, a facultative CAM plant. Mol Gen Genet 239: 450–462

    Article  PubMed  CAS  Google Scholar 

  • Edwards GE, Foster JG, Winter K (1982) Activity and intracellular compartmentation of enzymes of carbon metabolism of CAM plants. In: Ting IP, Gibbs M (eds) Crassulacean acid metabolism. American Society of Plant Physiologists, Rockville, pp 92–111

    Google Scholar 

  • Fißlthaler B, Meyer G, Bohnert HJ, Schmitt JM (1995) Age-dependent induction of pyruvate, orthophosphate dikinase in Mesembryanthemum crystallinum L. Planta 196: 492–500

    Article  PubMed  Google Scholar 

  • Foster JG, Edwards GE, Winter K (1982) Changes in the levels of phosphoenolpyruvate carboxylase with induction of CAM in M. crystallinum L. Plant Cell Physiol 23: 585–594

    CAS  Google Scholar 

  • Galvez AF (1992) Genetic responses to salinity stress in halophytic Lophopyrum elongatum, glycophytic wheat and the L. elongatum × wheat amphiploid. PhD Thesis, University of California, Davis

    Google Scholar 

  • Gilmour DS, Thomas GH, Elgin SCR (1989) Drosophila nuclear proteins bind to regions of alternating C and T residues in gene promoters. Science 245: 1487–1490

    Article  PubMed  CAS  Google Scholar 

  • Goldstein JL, Brown MS (1990) Regulation of the mevalonate pathway. Nature 343: 425–430

    Article  PubMed  CAS  Google Scholar 

  • Groenhof AC, Bryant JA, Etherington JR (1986) Photosynthetic changes in the inducible CAM plant Sedum telephium L. following the imposition of water stress. Ann Bot 57: 689–695

    Google Scholar 

  • Gulick PJ, Dvorak J (1992) Coordinate gene response to salt stress in salt tolerant Lophopyrum elongatum immediately after initiation of stress. Plant Physiol 100: 1384–1388

    Article  PubMed  CAS  Google Scholar 

  • Guralnick LJ, Rorabaugh PA, Hanscom Z (1984) Seasonal shifts of photosynthesis in Portulacaria afra (L.) Jacq. Plant Physiol 76: 643–646

    Article  PubMed  CAS  Google Scholar 

  • Hai TW, Liu F, Coukos WJ, Green MR (1989) Transcription factor ATF cDNA clones: an extensive family of leucine zipper proteins able to selectively form DNA-binding heterodimers. Genes Dev 3: 2083–2090

    Article  PubMed  CAS  Google Scholar 

  • Hanscom Z, Ting IP (1978) Irrigation magnifies CAM-photosynthesis in Opuntia basilaris (Cactaceae). Oecologia 33: 1–15

    Article  Google Scholar 

  • Hermans J, Westhoff P (1992) Homologous gene for the C4 isoform of phosphoenolpyruvate carboxylase in a C3 and C4 Flaveria species. Mol Gen Genet 234: 275–284

    Article  PubMed  CAS  Google Scholar 

  • Heun AM, Gorham J, Lüttge U, Wyn Jones RG (1981) Changes of water-relation characteristics and levels of organic cytoplasmic solutes during salinity induced transition of M. crystallinum from C3-photosynthesis to crassulacean acid metabolism. Oecologia 50: 66–72

    Article  Google Scholar 

  • Höfner R, Vazquez-Moreno L, Winter K, Bohnert HJ, Schmitt JM (1987) Induction of crassulacean acid metabolism in M. crystallinum: mass increase and de-novo synthesis of PEP-carboxylase. Plant Physiol 83: 915–919

    Article  PubMed  Google Scholar 

  • Holthe PA, Sternberg LW, Ting IP (1987) Developmental control of CAM in Peperomia scandens. Plant Physiol 84: 743–747

    Article  PubMed  CAS  Google Scholar 

  • Holtum JAM, Winter K (1982) Activity of enzymes of carbon metabolism during the induction of crassulacean acid metabolism in Mesembryanthemum crystallinum L. Planta 155: 8–16

    Article  CAS  Google Scholar 

  • Hu YF, Lüscher B, Admon A, Mermod N, Tijan R (1990) Transcription factor AP-4 contains multiple dimerization domains that regulate dimer specificity. Genes Dev 4: 1741–1752

    Article  PubMed  CAS  Google Scholar 

  • Jiao J, Chollet R (1991) Posttranslational regulation of phosphoenolpyruvate carboxylase in C4 and crassulacean acid metabolism plants. Plant Physiol 95: 981–985

    Article  PubMed  CAS  Google Scholar 

  • Kadonaga JT, Jones KA, Tijan R (1986) Promoter-specific activation of RNA polymerase II transcription by Spl. Trends Biochem Sci 11: 20–33

    Article  CAS  Google Scholar 

  • Keeley JE, Busch G (1984) Carbon assimilation characteristics of the aquatic CAM plant Isoetes howellii. Plant Physiol 76: 525–530

    Article  PubMed  CAS  Google Scholar 

  • Kluge M, Ting IP (1978) Crassulacean acid metabolism. Analysis of an ecological adaptation. Springer, Berlin Heidelberg New York

    Book  Google Scholar 

  • Köster S, Anderson JA (1989) The photosynthetic apparatus of C3 and CAM-induced Mesembryanthemum crystallinum L. Photosynth Res 19: 251–264

    Google Scholar 

  • Langdale JA, Taylor WC, Nelson T (1991) Cell-specific accumulation of maize phosphoenolpyruvate carboxylase is correlated with demethylation at a specific site > 3kb upstream of the gene. Mol Gen Genet 225: 49–55

    Article  PubMed  CAS  Google Scholar 

  • Lee W, Mitchell P, Tijan R (1987) Purified transcription factor AP-1 interacts with TPA- inducible enhancer elements. Cell 49: 741–752

    Article  PubMed  CAS  Google Scholar 

  • Lepiniec L, Keryer E, Philippe H, Gadal P, Cretin C (1993) Sorghum PEPC gene family: structure, function and molecular evolution. Plant Mol Biol 21: 487–502

    Article  PubMed  CAS  Google Scholar 

  • Li Y, Sugiura M (1990) Three distinct ribonucleoproteins from tobacco chloroplasts: each contains a unique amino-terminal acidic domain and two ribonucleoprotein consensus motifs. EMBO J 9: 3059–3066

    PubMed  CAS  Google Scholar 

  • Lüttge U, Fischer E, Steudle E (1978) Membrane potential and salt distribution in epidermal bladders and photosynthetic tissue of Mesembryanthemum crystallinum. Plant Cell Environ 1: 121–129

    Article  Google Scholar 

  • Martin B, Nienhuis J, King G, Schaefer A (1989) Restriction fragment length polymorphisms associated with water use efficiency in tomato. Science 243: 1725–1728

    Article  PubMed  CAS  Google Scholar 

  • McElwain EF, Bohnert HJ, Thomas JC (1992) Light moderates the induction of phosphoenolpyruvate carboxylase by NaCl and abscisic acid in Mesembryanthemum crystallinum. Plant Physiol 99: 1261–1264

    Article  PubMed  CAS  Google Scholar 

  • Meiners MS, Thomas JC, Bohnert HJ, Cushman JC (1991) Regeneration of multiple shoots and plants from Mesembryanthemum crystallinum. Plant Cell Rep 9: 563–566

    Article  Google Scholar 

  • Meyer G, Schmitt JM, Bohnert HJ (1990) Direct screening of a small genome: estimation of the magnitude of plant gene expression changes during adaptation to high salt. Mol Gen Genet 224: 347–356

    Article  PubMed  CAS  Google Scholar 

  • Michalowski CB, Olson SW, Piepenbrock M, Schmitt JM, Bohnert HJ (1989a) Time course of mRNA induction elicited by salt stress in the common ice plant (M. crystallinum). Plant Physiol 89: 811–816

    Article  PubMed  CAS  Google Scholar 

  • Michalowski CB, Schmitt JM, Bohnert HJ (1989b) Expression during salt stress and nucleotide sequence of cDNA for ferredoxin-NADP+ reductase from Mesembryanthemum crystallinum. Plant Physiol 89:817–823

    Article  PubMed  CAS  Google Scholar 

  • Michalowski CB, DeRocher EJ, Bohnert HJ, Salvucci ME (1992) Phosphoribulokinase from ice plant: transcription, transcripts and protein expression during environmental stress. Photosynth Res 31: 127–138

    Article  CAS  Google Scholar 

  • Monson RK (1989) On the evolution of pathways resulting in C4 photosynthesis and crassulacean acid metabolism (CAM). Adv Ecol Res 19: 57–110

    Article  Google Scholar 

  • Moore PD (1982) Evolution of photosynthetic pathways in flowering plants. Nature 295: 647–648

    Article  Google Scholar 

  • Osmond CB (1978) Crassulacean acid metabolism: a curiosity in context. Annu Rev Plant Physiol 29: 379–414

    Article  CAS  Google Scholar 

  • Ostrem JA, Vernon DM, Bohnert HJ (1990) Increased expression of a gene coding for NAD: glyceraldehyde-3-phosphate dehydrogenase during the transition from C3 photosynthesis to crassulacean acid metabolism in Mesembryanthemum crystallinum. J Biol Chem 265: 3497–3502

    PubMed  CAS  Google Scholar 

  • Ottaviani E, Sari Gorla M, Pé E, Frova C (1991) Molecular markers (RFLPs and HSPs) for the genetic dissection of thermotolerance in maize. Theor Appl Genet 81: 713–719

    Article  Google Scholar 

  • Paul MJ, Cockburn W (1989) Pinitol, a compatible solute in Mesembryanthemum crystallium L. J Exp Bot 40: 1093–1098

    Article  CAS  Google Scholar 

  • Poethig RS (1990) Phase change and the regulation of shoot morphogenesis in plants. Science 250: 923–930

    Article  PubMed  CAS  Google Scholar 

  • Schmitt JM, Piepenbrock M (1992) Regulation of phosphoenolpyruvate carboxylase and crassulacean acid metabolism induction in Mesembryanthemum crystallinum L. by cytokinin. Plant Physiol 99: 1664–1669

    Article  PubMed  CAS  Google Scholar 

  • Schmitt JM, Höfner R, Abou-Mandour A A, Vazquez-Moreno L, Bohnert HJ (1989) CAM-induction in Mesembryanthemum crystallinum: protein expression. In: Singhal GS (ed) Photosynthesis-molecular biology and bioenergetics. Springer, Berlin Heidelberg New York, pp 259–268

    Google Scholar 

  • Sipes DL, Ting IP (1985) Crassulacean acid metabolism and crassulacean acid metabolism modifications in Peperomia camptotricha. Plant Physiol 77: 59–63

    Article  PubMed  CAS  Google Scholar 

  • Steudle E, Liittge U, Zimmermann U (1975) Water relations of the epidermal bladder cells of the halophytic species Mesembryanthemum crystallinum: direct measurements of hydrostatic pressure and hydraulic conductivity. Planta 126: 220–246

    Article  Google Scholar 

  • Sussex IM (1989) Developmental programing of the shoot meristem. Cell 56: 225–229

    Article  PubMed  CAS  Google Scholar 

  • Swofford DL (1993) PAUP: Phylogenetic analysis using parsimony, version 3.1. Computer program distributed by the Illinois Natural History Survey, Champaign, Illinois

    Google Scholar 

  • Tarczynski MC, Jensen RG, Bohnert HJ (1993) Stress protection in transgenic tobacco producing a putative osmoprotectant, mannitol. Science 259: 508–510

    Article  PubMed  CAS  Google Scholar 

  • Teeri JA (1982) Photosynthetic variation in the Crassulaceae. In: Ting IP, Gibbs M (eds) Crassulacean acid metabolism. American Society of Plant Physiologists, Rockville, pp 244–259

    Google Scholar 

  • Thomas JC, DeArmond RL, Bohnert HJ (1992a) The influence of NaCl on growth, proline and phosphoenolpyruvate carboxylase levels in Mesembryanthemum crystallinum suspension cultures. Plant Physiol 98: 626–631

    Article  PubMed  CAS  Google Scholar 

  • Thomas JC, McElwain EF, Bohnert HJ (1992b) Convergent induction of osmotic stress-responses. Abscisic acid, cytokinin, and the effects of NaCl. Plant Physiol 100: 416–423

    Article  PubMed  CAS  Google Scholar 

  • Ting IP (1985) Crassulacean acid metabolism. Annu Rev Plant Physiol 36: 595–622

    Article  CAS  Google Scholar 

  • Ting IP, Hanscom Z (1977) Induction of acid metabolism in Portulacaria afra. Plant Physiol 59: 511–514

    Article  PubMed  CAS  Google Scholar 

  • Treichel S (1986) The influence of NaCl on pyrroline-5-carboxylate reductase in proline-accumulating cell suspension cultures of Mesembryanthemum nodiflorum and other halophytes. Physiol Plant 67: 173–181

    Article  CAS  Google Scholar 

  • Vernon DM, Bohnert HJ (1992a) A novel methyl transferase induced by osmotic stress in the facultative halophyte Mesembryanthemum crystallinum. EMBO J 11: 2077–2085

    PubMed  CAS  Google Scholar 

  • Vernon DM, Bohnert HJ (1992b) Increased expression of a myo-inositol methyl transferase in Mesembryanthemum crystallinum is part of a stress response distinct from crassulacean acid metabolism induction. Plant Physiol 99: 1695–1698

    Article  PubMed  CAS  Google Scholar 

  • Vernon DM, Ostrem JA, Bohnert HJ (1993a) Stress perception and response in a facultative halophyte: the regulation of salinity-induced genes in Mesembryanthemum crystallinum. Plant Cell Environ 16: 437–444

    Article  CAS  Google Scholar 

  • Vernon DM, Tarczynski MC, Jensen RG, Bohnert HJ (1993b) Cyclitol production in transgenic tobacco: analysis of the biochemical pathway from myo-inositol to pinitol. Plant J 4: 199–205

    Article  CAS  Google Scholar 

  • Winter K (1985) Crassulacean acid metabolism. In: Barber J, Baker NR (eds) Photosynthetic mechanisms and the environment. Elsevier, Amsterdam, pp 329–387

    Google Scholar 

  • Winter K, Gademann R (1991) Daily changes in CO2 and water vapor exchange, chlorophyll fluorescence, and leaf water relations in the halophyte Mesembryanthemum crystallinum during the induction of crassulacean acid metabolism in response to high salinity. Plant Physiol 95: 768–776

    Article  PubMed  CAS  Google Scholar 

  • Winter K, von Willert DJ (1972) NaCl-induzierter Crassulaceensäurestoffwechsel bei Mesembryanthemum crystallinum. Z Pflanzenphysiol 67:166–170

    CAS  Google Scholar 

  • Winter K, Ziegler H (1992) Induction of crassulacean acid metabolism in Mesembryanthemum crystallinum increases reproductive success under conditions of drought and salinity stress. Oecologia 92: 475–479

    Article  Google Scholar 

  • 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 Physiol 68: 300–307

    Article  Google Scholar 

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Cushman, J.C., Bohnert, H.J. (1996). Transcriptional Activation of CAM Genes During Development and Environmental Stress. In: Winter, K., Smith, J.A.C. (eds) Crassulacean Acid Metabolism. Ecological Studies, vol 114. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-79060-7_10

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  • DOI: https://doi.org/10.1007/978-3-642-79060-7_10

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