Abstract
Although it is generally accepted that Crassulacean Acid Metabolism (CAM) originated from C3 ancestors through a co-option process, this is rarely discussed in terms of specific characteristics and putative mechanisms behind this event. Here we discuss the available data concerning the biochemical and stomatal traits that are present in C3 plants and could have been enrolled in the CAM cycle. In summary, the biochemical machinery of CAM seems to have originated from a potential stress-driven recruitment of key non-photosynthetic enzymes of the C3 background which have entrained circadian rhythm. CAM stomatal behavior could be either a direct consequence of an upregulation of the biochemical machinery or it might require additional changes in the signaling/perception pathways controlling stomatal aperture. Considering that CAM has multiple origins, it is likely that each plant group developed it through different combinations of biochemical/stomatal changes, resulting in various degrees of plasticity of this photosynthetic pathway.
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References
Araújo WL, Fernie AR, Nunes-Nesi A (2011) Control of stomatal aperture, a renaissance of the old guard. Plant Signal Behav 6:1305–1311
Ashraf M, Harris PJC (2013) Photosynthesis under stressful environments: an overview. Photosynthetica 51:163–190
Aubry S, Brown NJ, Hibberd JM (2011) The role of proteins in C3 plants prior to their recruitment into the C4 pathway. J Exp Bot 62:3049–3059
Berry JO, Yerramsetty P, Zielinski AM, Mure CM (2013) Photosynthetic gene expression in higher plants. Photosynth Res 117:91–120
Böcher M, Kluge M (1978) The C4-pathway of C-fixation in Spinacea olearacea II. Pulse chase experiments with suspended leaf slices. Zeitschriftfür Pflanzenphysiologie 86:405–421
Borland AM, Griffiths H (1997) A comparative study on the regulation of C3 and C4 carboxylation processes in the constitutive crassulacean acid metabolism (CAM) plant Kalanchoe daigremontiana and the C3-CAM intermediate Clusia minor. Planta 201:368–378
Borland A, Taybi T (2004) Synchronization of metabolic processes in plants with crassulacean acid metabolism. J Exp Bot 55:1255–1265
Borland AM, Hartwell J, Jenkins GI, Wilkins MB, Nimmo HG (1999) Metabolite control overrides circadian regulation of phosphoenolpyruvate carboxylase kinase and CO2 fixation in crassulacean acid metabolism. Plant Physiol 121:889–896
Borland AM, Griffiths H, Hartwell J, Smith JAC (2009) Exploiting the potential of plants with crassulacean acid metabolism for bioenergy production on marginal lands. J Exp Bot 60:2879–2896
Borland AM, Zambrano VAB, Ceusters J, Shorrock K (2011) The photosynthetic plasticity of crassulacean acid metabolism: an evolutionary innovation for sustainable productivity in a changing world. New Phytol 191:619–633
Borland AM, Hartwell J, Weston DJ, Schlauch KA, Tschaplinski TJ, Tuskan GA, Yang X, Cushman JC (2014) Engineering crassulacean acid metabolism to improve water-use efficiency. Trends Plant Sci 19:327–338
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 Physiol 137:969–982
Brodribb TJ, Feild TS (2010) Leaf hydraulic evolution led a surge in leaf photosynthetic capacity during early angiosperm diversification. Ecol Lett 13:175–183
Caird MA, Richards JH, Donovan LA (2007) Nighttime stomatal conductance and transpiration in C3 and C4 plants. Plant Physiol 143:4–10
Chen C, Xiao Y-G, Li X, Ni M (2012) Light-regulated stomatal aperture in Arabidopsis. Mol Plant 5:566–572
Cominelli E, Galbiati M, Vavasseur A, Conti L, Sala T, Vuylsteke M, Leonhardt N, Dellaporta SL, Tonelli C (2005) A guard-cell-specific MYB transcription factor regulates stomatal movements and plant drought tolerance. Curr Biol 15:1196–1200
Covington MF, Panda S, Liu XL, Strayer CA, Wagner DR, Kay SA (2001) ELF3 modulates resetting of the circadian clock in Arabidopsis. Plant Cell 13:1305–1315
Cowling SA (2013) Did early land plants use carbon concentrating mechanisms? Trends Plant Sci 18:120–124
Crayn MC, Winter K, Smith JAC (2004) Multiple origins of Crassulacean acid metabolism and the epiphytic habit in the Neotropical family Bromeliaceae. Proc Natl Acad Sci U S A 101:3703–3708
Cushman JC, Bohnert HJ (1999) Crassulacean acid metabolism: molecular genetics. Annu Rev Plant Physiol Plant Mol Biol 50:305–332
Cushman JC, Tillett RL, Wood JA, Branco JM, Schlauch KA (2008) Large-scale mRNA expression profiling in the common ice plant, Mesembryanthemum crystallinum, performing C3 photosynthesis and Crassulacean acid metabolism (CAM). J Exp Bot 59:1875–1894
Dodd AN, Borland AM, Haslam RP, Griffiths H, Maxwell K (2002) Crassulacean acid metabolism: plastic, fantastic. J Exp Bot 53:569–580
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
Doubnerová V, Ryslavá H (2011) What can enzymes of C4 photosynthesis do for C3 plants under stress? Plant Sci 180:575–583
Drennan PM, Nobel PS (2000) Responses of CAM species to increase atmospheric CO2 concentrations. Plant Cell Environ 23:767–781
Edwards EJ, Ogburn RM (2012) Angiosperm responses to a low-CO2 world: CAM and C4 photosynthesis as parallel evolutionary trajectories. Int J Plant Sci 173:724–733
Ehleringer JR, Monson JK (1993) Evolutionary and ecological aspects of photosynthetic pathway variation. Annu Rev Ecol Syst 24:411–439
Ehleringer JR, Sage RF, Flanagan LB, Pearcy RW (1991) Climate change and the evolution of C4 photosynthesis. Trends Ecol Evol 6:95–99
Flexas J, Ribas-Carbó M, Diaz-Espejo A, Galmés J, Medrano H (2008) Mesophyll conductance to CO2: current knowledge and future prospects. Plant Cell Environ 31:602–621
Gennidakis S, Rao S, Greenham K, Winter K, Uhrig RG, O’Leary B, Snedden WA, Lu C, Plaxton WC (2007) Bacterial- and plant-type phosphoenolpyruvate carboxylase polypeptides interact in the hetero-oligomeric Class-2 PEPC complex of developing castor oil seeds. Plant J 52:839–849
Gonzalez MC, Sanchez R, Cejudo FJ (2003) Abiotic stresses affecting water balance induce phosphoenolpyruvate carboxylase expression in roots of wheat seedlings. Planta 216:985–992
Gousset-Dupont A, Lebouteiller B, Monreal J, Echevarria C, Pierre JN, Hodges M, Vidal J (2005) Metabolite and post-translational control of phosphoenolpyruvate carboxylase from leaves and mesophyll cell protoplasts of Arabidopsis thaliana. Plant Sci 169:1096–1101
Hartwell J, Nimmo G, Wilkins M, Jenkins G, Nimmo H (1999) Phosphoenolpyruvate carboxylase kinase is a novel protein kinase regulated at the level of gene expression. Plant J 20:333–342
Hartwell J, Nimmo GA, Wilkins MB, Jenkins GI, Nimmo HG (2002) Probing the circadian control of phosphoenolpyruvate carboxylase kinase expression in Kalanchoë fedtschenkoi. Funct Plant Biol 29:663–668
Hashimoto M, Negi J, Young J, Israelsson M, Schroeder JI, Iba K (2006) Arabidopsis HT1 kinase controls stomatal movements in response to CO2. Nat Cell Biol 8:391–397
Hibberd JM, Covshoff S (2010) The regulation of gene expression required for C4 photosynthesis. Annu Rev Plant Biol 61:181–207
Hicks KA, Millar AJ, Carré IA, Somers DE, Straume M, Meeks-Wagner DR, Kay SA (1996) Conditional circadian dysfunction of the Arabidopsis early-flowering 3 mutant. Science 274:790–792
Holthe PA, Sternberg LSL, Ting IP (1987) Developmental control of CAM in Peperomia scandens. Plant Physiol 84:743–747
Hubbard KE, Webb AAR (2011) Circadian rhythms: FLOWERING LOCUS T extends opening hours. Curr Biol 21:636–638
Keeley JE (1985) The role of CAM in the carbon economy of the submerged-aquatic Isoetes howellii. Verhandlungen des Internationalen Verein Limnologie 22:2909–2911
Keeley JE, Rundel PW (2003) Evolution of CAM and C4 carbon-concentrating mechanisms. Int J Plant Sci 164:55–77
Kim T-H, Böhmer M, Hu H, Nishimura N, Schroeder JI (2010) Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ Signaling. Annu Rev Plant Biol 61:561–591
KinoshitaT ON, HayashiY MS, Nakamura S, Soda M, Kato Y, Ohnishi M, Nakano T, Inoue S, Shimazaki K (2011) FLOWERING LOCUS T regulates stomatal opening. Curr Biol 21:1232–1238
Kluge M (1968) Untersuchungenüber den Gaswechsel von Bryophyllum während der Lichtperiode. Planta 80:359–377
Kluge M (2008) Ecophysiology: migrations between different levels of scaling. Prog Bot 69:5–34
Klüsener B, Young JJ, Murata Y, Allen GJ, Mori IC, Hugouvieux V, Schroeder JI (2002) Convergence of calcium signaling pathways of pathogenic elicitors and abscisic acid in Arabidopsis guard cells. Plant Physiol 130:2152–2163
Langdale JA (2011) C4 cycles: past, present, and future research on C4 photosynthesis. Plant Cell 23:3879–3892
Lee DM, Assmann SM (1992) Stomatal responses to light in the facultative crassulacean acid metabolism species, Portulacaria afra. Physiol Plant 85:35–42
Liang YK, Dubos C, Dodd IC, Holroyd GH, Hetherington AM, Campbell MM (2005) AtMYB61, an R2R3-MYB transcription factor controlling stomatal aperture in Arabidopsis thaliana. Curr Biol 15:1201–1206
Liu XL, Covington MF, Fankhauser C, Chory J, Wagner DR (2001) ELF3 encodes a circadian clock–regulated nuclear protein that functions in an Arabidopsis PHYB signal transduction pathway. Plant Cell 13:1293–1304
Lüttge U (2002) CO2-concentrating: consequences in crassulacean acid metabolism. J Exp Bot 53:2131–2142
Lüttge U (2004) Ecophysiology of crassulacean acid metabolism (CAM). Ann Bot 93:629–652
Lüttge U (2008) Clusia: Holy Grail and enigma. J Exp Bot 59:1503–1514
Lüttge U, Beck F (1992) Endogenous rhythms and chaos in crassulacean acid metabolism. Planta 188:28–38
Masumoto C, Miyazawa SI, Ohkawa H, Fukuda T, Taniguchi Y, Murayama S, KusanoM SK, Fukayama H, Miyao M (2010) Phosphoenolpyruvate carboxylase intrinsically located in the chloroplast of rice plays a crucial role in ammonium assimilation. Proc Natl Acad Sci U S A 107:5226–5231
Matiz A, Mioto PT, Mayorga AY, Freschi L, Mercier H (2013) CAM photosynthesis in bromeliads and agaves: what can we learn from these plants? In: Dubinsky Z (ed) Photosynthesis. Intech, Rijeka, Croatia, pp 91–134
Matthews PGD, Seymour R (2013) Stomata actively regulate internal aeration of the sacred lotus Nelumbo nucifera. Plant Cell Environ 37:402–413
Merilo E, Laanemets K, Hu H, Xue S, Jakobson L, Tulva I, Gonzalez-Guzman M, Rodruiguez PL, Schroeder JI, Broschè M, Kollist H (2013) PYR/RCAR receptors contribute to ozone-, reduced air humidity-, darkness-, and CO2-induced stomatal regulation. Plant Physiol 162:1652–1668
Mott KA, Sibbernsen ED, Shope JC (2008) The role of the mesophyll in stomatal responses to light and CO2. Plant Cell Environ 31:1299–1306
Nimmo HG (2000) The regulation of phosphoenolpyruvate carboxylase in CAM plants. Trends Plant Sci 5:75–80
Nimmo HG (2003) Control of the phosphorylation of phosphoenolpyruvate carboxylase in higher plants. Arch Biochem Biophys 414:189–196
O’Leary B, Park J, Plaxton WC (2011) The remarkable diversity of plant PEPC (phosphoenolpyruvate carboxylase): recent insights into the physiological functions and post-translational controls of non-photosynthetic PEPCs. Biochem J 436:15–34
Onai K, Okamoto K, Nishimoto H, Morioka C, Hirano M, Kami-ike N, Ishiura M (2004) Large-scale screening of Arabidopsis circadian clock mutants by a high-throughput real-time bioluminescence monitoring system. Plant J 40:1–11
Osmond CB (1978) Crassulacean acid metabolism: a curiosity in context. Annu Rev Plant Physiol 29:379–414
Owen NA, Griffiths H (2013) A system dynamics model integrating physiology and biochemical regulation predicts extent of crassulacean acid metabolism (CAM) phases. New Phytol 200:1116–1131
Ranson SL, Thomas M (1960) Crassulacean acid metabolism. Annu Rev Plant Physiol 11:81–110
Raven JA, Spicer RA (1996) The evolution of crassulacean acid metabolism. In: Winter K, Smith JAC (eds) Crassulacean acid metabolism. Biochemistry, ecophysiology and evolution. Springer, Berlin, pp 360–385
Rodrigues MA, Matiz A, Cruz AB, Matsumura AT, Takahashi CA, Hamachi L, Félix LM, Pereira PN, Latansio-Aidar SP, Aidar MPM, Demarco D, Freschi L, Mercier H, Kerbauy GB (2013) Spatial patterns of photosynthesis in thin- and thick-leaved epiphytic orchids: unravelling C3-CAM plasticity in an organ-compartmented way. Ann Bot 112:17–29
Rodrigues MA, Freschi L, Pereira PN, Mercier H (2014) Interactions between nutrients and crassulacean acid metabolism. Prog Bot 75:167–186
Rogiers SY, Clarke SJ (2013) Nocturnal and daytime stomatal conductance respond to root-zone temperature in ‘Shiraz’ grapevines. Ann Bot 111:433–444
Shane MW, Fedosejevs ET, Plaxton WC (2013) Reciprocal control of anaplerotic phosphoenolpyruvate carboxylase by in vivo monoubiquitination and phosphorylation in developing proteoid roots of phosphate-deficient. Plant Physiol 161:1634–1644
Shenton M, Fontaine V, Hartwell J, Marsh JT, Jenkins GI, Nimmo HG (2006) Distinct patterns of control and expression amongst members of the PEP carboxylase kinase gene family in C4 plants. Plant J 48:45–53
Silvera K, Neubig KM, Whitten M, Williams NH, Winter K, Cushman JC (2010) Evolution along the crassulacean acid metabolism continuum. Funct Plant Biol 37:995–1010
Sriram G, Fulton DB, Shanks JV (2007) Flux quantification in central carbon metabolism of Catharanthus roseus hairy roots by C-13 labeling and comprehensive bondomer balancing. Phytochemistry 68:2243–2257
Tallman G, Zhu J, Mawson BT, Amodeo G, Nouhi Z, Levy K, Zeiger E (1997) Induction of CAM in Mesembryanthemum crystallinum abolishes the stomatal response to blue light and light-dependent zeaxanthin formation in guard cell chloroplasts. Plant Cell Physiol 38:236–242
Taybi T, Nimmo HG, Borland AM (2004) Expression of phosphoenolpyruvate carboxylase and phosphoenolpyruvate carboxylase kinase genes. Implications for genotypic capacity and phenotypic plasticity in the expression of Crassulacean acid metabolism. Plant Physiol 135:587–598
Thomas M, Beevers H (1949) Physiological studies on acid metabolism in green plants. II. Evidence of CO2 fixation in Bryophyllum and the study of diurnal variation of acidity in this genus. New Phytol 48:421–447
Ting IP (1985) Crassulacean acid metabolism. Annu Rev Plant Physiol 36:595–622
Vahisalu T, Kollist H, Wang YF, Nishimura N, Chan WY, Valerio G, Lamminmäki A, Brosché M, Moldau H, Desikan R, Schroeder JI, Kangasjärvi J (2008) SLAC1 is required for plant guard cell S-type anion channel function in stomatal signaling. Nature 452:487–491
Von Caemmerer S, Griffiths H (2009) Stomatal responses to CO2 during a dielcrassulacean acid metabolism cycle in Kalanchoë daigremontiana and Kalanchoë pinnata. Plant Cell Environ 32:567–576
West-Eberhard MJ, Smith JAC, Winter K (2011) Photosynthesis, reorganized. Science 332:311–312
Wilkins MB (1984) A rapid circadian rhythm of carbon-dioxide metabolism in Bryophyllum fedtschenkoi. Planta 161:381–384
Williams BP, Aubry S, Hicks JM (2012) Molecular evolution of genes recruited into C4 photosynthesis. Trends Plant Sci 17:213–220
Winter K, Holtum JAM (2007) Environment or development? Lifetime net CO2 exchange and control of the expression of Crassulacean acid metabolism in Mesembryanthemum crystallinum. Plant Physiol 143:98–107
Winter K, Holtum JAM (2014) Facultative crassulacean acid metabolism (CAM) plants: powerful tools for unravelling the functional elements of CAM photosynthesis. J Exp Bot. doi:10.1093/jxb/eru063
Winter K, Smith JAC (1996) Crassulacean acid metabolism. Current status and perspectives. In: Winter K, Smith JAC (eds) Crassulacean acid metabolism. Biochemistry, ecophysiology and evolution. Springer, Berlin, pp 389–426
Winter K, Garcia M, Holtum JAM (2008) On the nature of facultative and constitutive CAM: environmental and developmental control of CAM expression during early growth of Clusia, Kalanchoë, and Opuntia. J Exp Bot 59:1829–1840
Wyka TP, Lüttge U (2003) Contribution of C3 carboxylation to the circadian rhythm of carbon dioxide uptake in a Crassulacean acid metabolism plant Kalanchoë daigremontiana. J Exp Bot 54:1471–1479
Wyka TP, Bohn A, Duarte HM, Kaiser F, Lüttge U (2004) Perturbations of malate accumulation and the endogenous rhythms of gas exchange in the crassulacean acid metabolism plant Kalanchoë daigremontiana: testing the tonoplast-as-oscillator model. Planta 219:705–713
Zeppel M, Logan B, Lewis JD, Phillips N, Tissue D (2013) Why lose water at night? Disentangling the mystery of nocturnal sap flow, transpiration and stomatal conductance – when, where, who? Acta Hortic 991:307–312
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The authors would like to thank Dr. Luciano Freschi for valuable discussions on the topic of this review.
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Mioto, P.T., Rodrigues, M.A., Matiz, A., Mercier, H. (2015). CAM-Like Traits in C3 Plants: Biochemistry and Stomatal Behavior. In: Lüttge, U., Beyschlag, W. (eds) Progress in Botany. Progress in Botany, vol 76. Springer, Cham. https://doi.org/10.1007/978-3-319-08807-5_8
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