1932

Abstract

Crassulacean acid metabolism (CAM) has evolved from a C ground state to increase water use efficiency of photosynthesis. During CAM evolution, selective pressures altered the abundance and expression patterns of C genes and their regulators to enable the trait. The circadian pattern of CO fixation and the stomatal opening pattern observed in CAM can be explained largely with a regulatory architecture already present in C plants. The metabolic CAM cycle relies on enzymes and transporters that exist in C plants and requires tight regulatory control to avoid futile cycles between carboxylation and decarboxylation. Ecological observations and modeling point to mesophyll conductance as a major factor during CAM evolution. The present state of knowledge enables suggestions for genes for a minimal CAM cycle for proof-of-concept engineering, assuming altered regulation of starch synthesis and degradation are not critical elements of CAM photosynthesis and sufficient malic acid export from the vacuole is possible.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-071720-104814
2021-06-17
2024-04-13
Loading full text...

Full text loading...

/deliver/fulltext/arplant/72/1/annurev-arplant-071720-104814.html?itemId=/content/journals/10.1146/annurev-arplant-071720-104814&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Abraham PE, Hurtado Castano N, Cowan-Turner D, Barnes J, Poudel S et al. 2020. Peeling back the layers of crassulacean acid metabolism: functional differentiation between Kalanchoë fedtschenkoi epidermis and mesophyll proteomes. Plant J 103:869–88
    [Google Scholar]
  2. 2. 
    Abraham PE, Yin H, Borland AM, Weighill D, Lim SD et al. 2016. Transcript, protein and metabolite temporal dynamics in the CAM plant Agave. Nat. Plants 2:16178Demonstrates that not all CAM proteins show diurnal rhythms.
    [Google Scholar]
  3. 3. 
    Alabadí D, Oyama T, Yanovsky MJ, Harmon FG, Más P, Kay SA. 2001. Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science 293:880–83
    [Google Scholar]
  4. 4. 
    Aldous SH, Weise SE, Sharkey TD, Waldera-Lupa DM, Stühler K et al. 2014. Evolution of the phosphoenolpyruvate carboxylase protein kinase family in C3 and C4Flaveria spp. Plant Physiol 165:1076–91
    [Google Scholar]
  5. 5. 
    Allaway W, Austin B, Slatyer R 1974. Carbon dioxide and water vapour exchange parameters of photosynthesis in a crassulacean plant, Kalanchoe daigremontiana. Funct. Plant Biol. 1:397–405
    [Google Scholar]
  6. 6. 
    Alvarez CE, Detarsio E, Moreno S, Andreo CS, Drincovich MF. 2012. Functional characterization of residues involved in redox modulation of maize photosynthetic NADP-malic enzyme activity. Plant Cell Physiol 53:1144–53
    [Google Scholar]
  7. 7. 
    Antony E, Taybi T, Courbot M, Mugford ST, Smith JAC, Borland AM 2008. Cloning, localization and expression analysis of vacuolar sugar transporters in the CAM plant Ananas comosus (pineapple). J. Exp. Bot. 59:1895–908
    [Google Scholar]
  8. 8. 
    Assmann SM, Simoncini L, Schroeder JI. 1985. Blue light activates electrogenic ion pumping in guard-cell protoplasts of Vicia faba. Nature 318:285–87
    [Google Scholar]
  9. 9. 
    Astley HM, Parsley K, Aubry S, Chastain CJ, Burnell JN et al. 2011. The pyruvate, orthophosphate dikinase regulatory proteins of Arabidopsis are both bifunctional and interact with the catalytic and nucleotide-binding domains of pyruvate, orthophosphate dikinase. Plant J 68:1070–80
    [Google Scholar]
  10. 10. 
    Baerenfaller K, Massonnet C, Walsh S, Baginsky S, Bühlmann P et al. 2012. Systems-based analysis of Arabidopsis leaf growth reveals adaptation to water deficit. Mol. Syst. Biol. 8:18
    [Google Scholar]
  11. 11. 
    Bagge P, Larsson C. 1986. Biosynthesis of aromatic amino acids by highly purified spinach chloroplasts– compartmentation and regulation of the reactions. Physiol. Plant. 68:641–47
    [Google Scholar]
  12. 12. 
    Bennet-Clark TA. 1933. The role of the organic acids in plant metabolism. New Phytol 32:37–71
    [Google Scholar]
  13. 13. 
    Bhardwaj V, Meier S, Petersen LN, Ingle RA, Roden LC. 2011. Defence responses of Arabidopsis thaliana to infection by Pseudomonas syringae are regulated by the circadian clock. PLOS ONE 6:e26968
    [Google Scholar]
  14. 14. 
    Bläsing OE, Gibon Y, Günther M, Höhne M, Morcuende R et al. 2005. Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis. Plant Cell 17:3257–81
    [Google Scholar]
  15. 15. 
    Borland AM, Hartwell J, Weston DJ, Schlauch KA, Tschaplinski TJ et al. 2014. Engineering crassulacean acid metabolism to improve water-use efficiency. Trends Plant Sci 19:327–38
    [Google Scholar]
  16. 16. 
    Boston HL, Adams MS. 1983. Evidence of crassulacean acid metabolism in two North American isoetids. Aquat. Bot. 15:381–86
    [Google Scholar]
  17. 17. 
    Boxall SF, Dever LV, Kneřová J, Gould PD, Hartwell J. 2017. Phosphorylation of phosphoenolpyruvate carboxylase is essential for maximal and sustained dark CO2 fixation and core circadian clock operation in the obligate crassulacean acid metabolism species Kalanchoë fedtschenkoi. Plant Cell 29:2519–36Shows that genetic perturbations are a critical tool for understanding CAM.
    [Google Scholar]
  18. 18. 
    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 137:969–82
    [Google Scholar]
  19. 19. 
    Boxall SF, Kadu N, Dever LV, Kneřová J, Waller JL et al. 2020. Kalanchoë PPC1 is essential for crassulacean acid metabolism and the regulation of core circadian clock and guard cell signaling genes. Plant Cell 32:41136–60
    [Google Scholar]
  20. 20. 
    Bräutigam A, Gowik U. 2016. Photorespiration connects C3 and C4 photosynthesis. J. Exp. Bot. 67:2953–62
    [Google Scholar]
  21. 21. 
    Bräutigam A, Schliesky S, Külahoglu C, Osborne CP, Weber APM. 2014. Towards an integrative model of C4 photosynthetic subtypes: insights from comparative transcriptome analysis of NAD-ME, NADP-ME, and PEP-CK C4 species. J. Exp. Bot. 65:3579–93
    [Google Scholar]
  22. 22. 
    Bräutigam A, Schlüter U, Eisenhut M, Gowik U. 2017. On the evolutionary origin of CAM photosynthesis. Plant Physiol 174:473–77
    [Google Scholar]
  23. 23. 
    Bremberger C, Haschke HP, Lüttge U. 1988. Separation and purification of the tonoplast ATPase and the pyrophosphatase from plants with constitutive and inducible crassulacean acid metabolism. Planta 175:465–70
    [Google Scholar]
  24. 24. 
    Brilhaus D, Bräutigam A, Mettler-Altmann T, Winter K, Weber APM. 2016. Reversible burst of transcriptional changes during induction of crassulacean acid metabolism in Talinum triangulare. Plant Physiol 170:102–22
    [Google Scholar]
  25. 25. 
    Burnell JN, Hatch MD. 1985. Light dark modulation of leaf pyruvate, Pi dikinase. Trends Biochem. Sci. 10:288–91
    [Google Scholar]
  26. 26. 
    Cai J, Liu X, Vanneste K, Proost S, Tsai W-C et al. 2015. The genome sequence of the orchid Phalaenopsis equestris. Nat. Genet. 47: 65–72. Erratum. 2015. Nat. Genet 47:3304
    [Google Scholar]
  27. 27. 
    Carter PJ, Nimmo HG, Fewson CA, Wilkins MB. 1991. Circadian rhythms in the activity of a plant protein kinase. EMBO J 10:2063–68
    [Google Scholar]
  28. 28. 
    Cheung CYM, Poolman MG, Fell DA, Ratcliffe RG, Sweetlove LJ. 2014. A diel flux balance model captures interactions between light and dark metabolism during day-night cycles in C3 and crassulacean acid metabolism leaves. Plant Physiol 165:917–29
    [Google Scholar]
  29. 29. 
    Choi HI, Hong JH, Ha JO, Kang JY, Kim SY. 2000. ABFs, a family of ABA-responsive element binding factors. J. Biol. Chem. 275:1723–30
    [Google Scholar]
  30. 30. 
    Choudhary MK, Nomura Y, Wang L, Nakagami H, Somers DE. 2015. Quantitative circadian phosphoproteomic analysis of Arabidopsis reveals extensive clock control of key components in physiological, metabolic, and signaling pathways. Mol. Cell. Proteom. 14:2243–60
    [Google Scholar]
  31. 31. 
    Christin P-A, Salamin N, Savolainen V, Duvall MR, Besnard G. 2007. C4 photosynthesis evolved in grasses via parallel adaptive genetic changes. Curr. Biol. 17:1241–47
    [Google Scholar]
  32. 32. 
    Christopher JT, Holtum JAM. 1996. Patterns of carbon partitioning in leaves of crassulacean acid metabolism species during deacidification. Plant Physiol 112:393–99
    [Google Scholar]
  33. 33. 
    Chu C, Dai ZY, Ku MSB, Edwards GE. 1990. Induction of crassulacean acid metabolism in the facultative halophyte Mesembryanthemum crystallinum by abscisic acid. Plant Physiol 93:1253–60
    [Google Scholar]
  34. 34. 
    Crayn DM, Winter K, Schulte K, Smith JAC. 2015. Photosynthetic pathways in Bromeliaceae: phylogenetic and ecological significance of CAM and C3 based on carbon isotope ratios for 1,893 species. Bot. J. Linn. Soc. 178:169–221
    [Google Scholar]
  35. 35. 
    Crayn DM, Winter K, Smith JAC 2004. Multiple origins of crassulacean acid metabolism and the epiphytic habit in the Neotropical family Bromeliaceae. PNAS 101:3703–8
    [Google Scholar]
  36. 36. 
    Crumpton-Taylor M, Grandison S, Png KMY, Bushby AJ, Smith AM. 2012. Control of starch granule numbers in Arabidopsis chloroplasts. Plant Physiol 158:905–16
    [Google Scholar]
  37. 37. 
    Cruz ER, Nguyen H, Nguyen T, Wallace IS. 2019. Functional analysis tools for post-translational modification: a post-translational modification database for analysis of proteins and metabolic pathways. Plant J 99:1003–13
    [Google Scholar]
  38. 38. 
    Cushman JC, Agarie S, Albion RL, Elliot SM, Taybi T, Borland AM. 2008. Isolation and characterization of mutants of common ice plant deficient in crassulacean acid metabolism. Plant Physiol 147:228–38
    [Google Scholar]
  39. 39. 
    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. 59:1875–94
    [Google Scholar]
  40. 40. 
    De Angeli A, Zhang JB, Meyer S, Martinoia E. 2013. AtALMT9 is a malate-activated vacuolar chloride channel required for stomatal opening in Arabidopsis. Nat. Commun. 4:1804
    [Google Scholar]
  41. 41. 
    Dever LV, Blackwell RD, Fullwood NJ, Lacuesta M, Leegood RC et al. 1995. The isolation and characterization of mutants of the C-4 photosynthetic pathway. J. Exp. Bot. 46:1363–76
    [Google Scholar]
  42. 42. 
    Dever LV, Boxall SF, Kneřová J, Hartwell J. 2015. Transgenic perturbation of the decarboxylation phase of crassulacean acid metabolism alters physiology and metabolism but has only a small effect on growth. Plant Physiol 167:44–59Shows that genetic perturbations are a critical tool for understanding CAM.
    [Google Scholar]
  43. 43. 
    Dittrich P. 1976. Nicotinamide adenine dinucleotide-specific “malic” enzyme in Kalanchoë daigremontiana and other plants exhibiting crassulacean metabolism. Plant Physiol 57:310–14
    [Google Scholar]
  44. 44. 
    Dittrich P, Campbell WH, Black CC. 1973. Phosphoenolpyruvate carboxykinase in plants exhibiting crassulacean acid metabolism. Plant Physiol 52:357–61
    [Google Scholar]
  45. 45. 
    Dodd AN, Salathia N, Hall A, Kévei E, Tóth R et al. 2005. Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309:630–33
    [Google Scholar]
  46. 46. 
    Drincovich MF, Andreo CS. 1994. Redox regulation of maize NADP-malic enzyme by thiol-disulfide interchange: effect of reduced thioredoxin on activity. Biochim. Biophys. Acta Protein Struct. Mol. Enzymol. 1206:10–16
    [Google Scholar]
  47. 47. 
    Eastmond PJ, Astley HM, Parsley K, Aubry S, Williams BP et al. 2015. Arabidopsis uses two gluconeogenic gateways for organic acids to fuel seedling establishment. Nat. Commun. 6:6659
    [Google Scholar]
  48. 48. 
    Emmerlich V, Linka N, Reinhold T, Hurth MA, Traub M et al. 2003. The plant homolog to the human sodium/dicarboxylic cotransporter is the vacuolar malate carrier. PNAS 100:11122–26
    [Google Scholar]
  49. 49. 
    Fahnenstich H, Saigo M, Niessen M, Zanor MI, Andreo CS et al. 2007. Alteration of organic acid metabolism in Arabidopsis overexpressing the maize C4 NADP-malic enzyme causes accelerated senescence during extended darkness. Plant Physiol 145:640–52
    [Google Scholar]
  50. 50. 
    Fowler SG, Cook D, Thomashow ME. 2005. Low temperature induction of Arabidopsis CBF1, 2, and 3 is gated by the circadian clock. Plant Physiol 137:961–68
    [Google Scholar]
  51. 51. 
    Franco AC, Ball E, Lüttge U. 1990. Patterns of gas-exchange and organic acid oscillations in tropical trees of the genus Clusia. Oecologia 85:108–14
    [Google Scholar]
  52. 52. 
    Frank A, Matiolli CC, Viana AJC, Hearn TJ, Kusakina J et al. 2018. Circadian entrainment in Arabidopsis by the sugar-responsive transcription factor bZIP63. Curr. Biol. 28:2597–606
    [Google Scholar]
  53. 53. 
    Furumoto T, Yamaguchi T, Ohshima-Ichie Y, Nakamura M, Tsuchida-Iwata Y et al. 2011. A plastidial sodium-dependent pyruvate transporter. Nature 476:472–75
    [Google Scholar]
  54. 54. 
    Gauthier PPG, Bligny R, Gout E, Mahé A, Nogues S et al. 2010. In folio isotopic tracing demonstrates that nitrogen assimilation into glutamate is mostly independent from current CO2 assimilation in illuminated leaves of Brassica napus. New Phytol 185:988–99
    [Google Scholar]
  55. 55. 
    Goodspeed D, Chehab EW, Min-Venditti A, Braam J, Covington MF 2012. Arabidopsis synchronizes jasmonate-mediated defense with insect circadian behavior. PNAS 109:4674–77
    [Google Scholar]
  56. 56. 
    Grabov A, Leung J, Giraudat J, Blatt MR. 1997. Alteration of anion channel kinetics in wild-type and abi1-1 transgenic Nicotiana benthamiana guard cells by abscisic acid. Plant J 12:203–13
    [Google Scholar]
  57. 57. 
    Graf A, Schlereth A, Stitt M, Smith AM 2010. Circadian control of carbohydrate availability for growth in Arabidopsis plants at night. PNAS 107:9458–63
    [Google Scholar]
  58. 58. 
    Gregory AL, Hurley BA, Tran HT, Valentine AJ, She Y-M et al. 2009. In vivo regulatory phosphorylation of the phosphoenolpyruvate carboxylase AtPPC1 in phosphate-starved Arabidopsis thaliana. Biochem. J. 420:57–65
    [Google Scholar]
  59. 59. 
    Griffiths H. 1989. Carbon dioxide concentrating mechanisms and the evolution of CAM in vascular epiphytes. Vascular Plants as Epiphytes: Evolution and Ecophysiology U Lüttge 42–86 Berlin: Springer-Verlag
    [Google Scholar]
  60. 60. 
    Grinevich DO, Desai JS, Stroup KP, Duan JQ, Slabaugh E, Doherty CJ. 2019. Novel transcriptional responses to heat revealed by turning up the heat at night. Plant Mol. Biol. 101:1–19
    [Google Scholar]
  61. 61. 
    Gross P, Aprees T. 1986. Alkaline inorganic pyrophosphatase and starch synthesis in amyloplasts. Planta 167:140–45
    [Google Scholar]
  62. 62. 
    Hafke JB, Hafke Y, Smith JAC, Lüttge U, Thiel G. 2003. Vacuolar malate uptake is mediated by an anion-selective inward rectifier. Plant J 35:116–28
    [Google Scholar]
  63. 63. 
    Harmer SL, Kay SA. 2005. Positive and negative factors confer phase-specific circadian regulation of transcription in Arabidopsis. Plant Cell 17:1926–40
    [Google Scholar]
  64. 64. 
    Hartwell J. 2018. The circadian clock in CAM plants. Annual Plant Reviews, Vol. 21: Endogenous Plant Rhythms AJW Hall, H McWatters 211–36 Hoboken, NJ: Wiley
    [Google Scholar]
  65. 65. 
    Hartwell J, Gill A, Nimmo GA, Wilkins MB, Jenkins GL, Nimmo HG 1999. Phosphoenolpyruvate carboxylase kinase is a novel protein kinase regulated at the level of expression. Plant J 20:333–42Seminal paper reports the molecular identification of the PEPC kinase.
    [Google Scholar]
  66. 66. 
    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. 8:391–97
    [Google Scholar]
  67. 67. 
    Häusler RE, Kleines M, Uhrig H, Hirsch H-J, Smets H. 1999. Overexpression of phosphoenolpyruvate carboxylase from Corynebacterium glutamicum lowers the CO2 compensation point (Γ*) and enhances dark and light respiration in transgenic potato. J. Exp. Bot. 50:1231–42
    [Google Scholar]
  68. 68. 
    Haydon MJ, Mielczarek O, Robertson FC, Hubbard KE, Webb AAR. 2013. Photosynthetic entrainment of the Arabidopsis thaliana circadian clock. Nature 502:689–92
    [Google Scholar]
  69. 69. 
    Hedrich R, Kurkdjian A, Guern J, Flügge UI. 1989. Comparative studies on the electrical properties of the H+ translocating ATPase and pyrophosphatase of the vacuolar-lysosomal compartment. EMBO J 8:2835–41
    [Google Scholar]
  70. 70. 
    Hedrich R, Sauer N, Neuhaus HE. 2015. Sugar transport across the plant vacuolar membrane: nature and regulation of carrier proteins. Curr. Opin. Plant Biol. 25:63–70
    [Google Scholar]
  71. 71. 
    Herrera A. 2009. Crassulacean acid metabolism and fitness under water deficit stress: If not for carbon gain, what is facultative CAM good for?. Ann. Bot. 103:645–53
    [Google Scholar]
  72. 72. 
    Herrera A, Ballestrini C, Montes E. 2015. What is the potential for dark CO2 fixation in the facultative crassulacean acid metabolism species Talinum triangulare?. J. Plant Physiol. 174:55–61
    [Google Scholar]
  73. 73. 
    Holtum JAM, Smith JAC, Neuhaus HE. 2005. Intracellular transport and pathways of carbon flow in plants with crassulacean acid metabolism. Funct. Plant Biol. 32:429–49
    [Google Scholar]
  74. 74. 
    Hong-Hermesdorf A, Brux A, Gruber A, Gruber G, Schumacher K. 2006. A WNK kinase binds and phosphorylates V-ATPase subunit C. FEBS Lett 580:932–39
    [Google Scholar]
  75. 75. 
    Hu HH, Boisson-Dernier A, Israelsson-Nordström M, Böhmer M, Xue SW et al. 2010. Carbonic anhydrases are upstream regulators of CO2-controlled stomatal movements in guard cells. Nat. Cell Biol. 12:87–93
    [Google Scholar]
  76. 76. 
    Hu JL, Huang XH, Chen LC, Sun XW, Lu CM et al. 2015. Site-specific nitrosoproteomic identification of endogenously S-nitrosylated proteins in Arabidopsis. Plant Physiol 167:1731–46
    [Google Scholar]
  77. 77. 
    Hudson ME, Quail PH. 2003. Identification of promoter motifs involved in the network of phytochrome A-regulated gene expression by combined analysis of genomic sequence and microarray data. Plant Physiol 133:1605–16
    [Google Scholar]
  78. 78. 
    Izui K, Matsumura H, Furumoto T, Kai Y 2004. Phosphoenolpyruvate carboxylase: a new era of structural biology. Annu. Rev. Plant Biol. 55:69–84
    [Google Scholar]
  79. 79. 
    Jewer PC, Incoll LD, Howarth GL. 1981. Stomatal responses in isolated epidermis of the crassulacean acid metabolism plant Kalanchoe daigremontiana Hamet et Perr. Planta 153:238–45
    [Google Scholar]
  80. 80. 
    Jones MB. 1975. Effect of leaf age on the leaf resistance and CO2 exchange of CAM plant Bryophyllum fedtschenkoi. Planta 123:91–96
    [Google Scholar]
  81. 81. 
    Kandoi D, Mohanty S, Govindjee, Tripathy BC 2016. Towards efficient photosynthesis: overexpression of Zea mays phosphoenolpyruvate carboxylase in Arabidopsis thaliana. Photosyn. Res. 130:47–72
    [Google Scholar]
  82. 82. 
    Kenyon WH, Severson RF, Black CC. 1985. Maintenance carbon cycle in crassulacean acid metabolism plant leaves: source and compartmentation of carbon for nocturnal malate synthesis. Plant Physiol 77:183–89
    [Google Scholar]
  83. 83. 
    Kim TH, Böhmer M, Hu HH, Nishimura N, Schroeder JI. 2010. Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annu. Rev. Plant Biol. 61:561–91
    [Google Scholar]
  84. 84. 
    Kinoshita T, Doi M, Suetsugu N, Kagawa T, Wada M, Shimazaki K. 2001. phot1 and phot2 mediate blue light regulation of stomatal opening. Nature 414:656–60
    [Google Scholar]
  85. 85. 
    Kinoshita T, Shimazaki K. 1999. Blue light activates the plasma membrane H+-ATPase by phosphorylation of the C-terminus in stomatal guard cells. EMBO J 18:5548–58
    [Google Scholar]
  86. 86. 
    Klepikova AV, Kasianov AS, Gerasimov ES, Logacheva MD, Penin AA. 2016. A high resolution map of the Arabidopsis thaliana developmental transcriptome based on RNA-seq profiling. Plant J 88:1058–70
    [Google Scholar]
  87. 87. 
    Knappe S, Löttgert T, Schneider A, Voll L, Flügge U-I, Fischer K. 2003. Characterization of two functional phosphoenolpyruvate/phosphate translocator (PPT) genes in Arabidopsis–AtPPT1 may be involved in the provision of signals for correct mesophyll development. Plant J 36:411–20
    [Google Scholar]
  88. 88. 
    Kötting O, Santelia D, Edner C, Eicke S, Marthaler T et al. 2009. STARCH-EXCESS4 is a laforin-like phosphoglucan phosphatase required for starch degradation in Arabidopsis thaliana. Plant Cell 21:334–46
    [Google Scholar]
  89. 89. 
    Kovermann P, Meyer S, Hörtensteiner S, Picco C, Scholz-Starke J et al. 2007. The Arabidopsis vacuolar malate channel is a member of the ALMT family. Plant J 52:1169–80
    [Google Scholar]
  90. 90. 
    Kwak JM, Murata Y, Baizabal-Aguirre VM, Merrill J, Wang M et al. 2001. Dominant negative guard cell K+ channel mutants reduce inward-rectifying K+ currents and light-induced stomatal opening in Arabidopsis. Plant Physiol 127:473–85
    [Google Scholar]
  91. 91. 
    Latorre-Muro P, Baeza J, Armstrong EA, Hurtado-Guerrero R, Corzana F et al. 2018. Dynamic acetylation of phosphoenolpyruvate carboxykinase toggles enzyme activity between gluconeogenic and anaplerotic reactions. Mol. Cell 71:718–32.e9
    [Google Scholar]
  92. 92. 
    Lawson T, Matthews J. 2020. Guard cell metabolism and stomatal function. Annu. Rev. Plant Biol. 71:273–302
    [Google Scholar]
  93. 93. 
    Li L, Nelson CJ, Trosch J, Castleden I, Huang SB, Millar AH. 2017. Protein degradation rate in Arabidopsis thaliana leaf growth and development. Plant Cell 29:207–28
    [Google Scholar]
  94. 94. 
    Lim SD, Mayer JA, Yim WC, Cushman JC. 2020. Plant tissue succulence engineering improves water-use efficiency, water-deficit stress attenuation and salinity tolerance in Arabidopsis. Plant J 103:31049–72
    [Google Scholar]
  95. 95. 
    Liu SC, Yu FC, Yang Z, Wang TL, Xiong HR et al. 2018. Establishment of dimethyl labeling-based quantitative acetylproteomics in Arabidopsis. Mol. Cell. Proteom. 17:1010–27
    [Google Scholar]
  96. 96. 
    Lundgren MR, Mathers A, Baillie AL, Dunn J, Wilson MJ et al. 2019. Mesophyll porosity is modulated by the presence of functional stomata. Nat. Commun. 10:2825
    [Google Scholar]
  97. 97. 
    Lüttge U. 1988. Day-night changes of citric acid levels in crassulacean acid metabolism: phenomenon and ecophysiological significance. Plant Cell Environ 11:445–51
    [Google Scholar]
  98. 98. 
    Lüttge U. 2007. Clusia: A Woody Neotropical Genus of Remarkable Plasticity and Diversity Berlin: Springer-Verlag
  99. 99. 
    Lüttge U, Nobel PS. 1984. Day-night variations in malate concentration, osmotic pressure, and hydrostatic pressure in Cereus validus. Plant Physiol 75:804–7
    [Google Scholar]
  100. 100. 
    Lüttge U, Smith JAC. 1984. Mechanisms of passive malic acid efflux from vacuoles of the CAM plant Kalanchoe daigremontiana. J. Membr. Biol. 81:149–58
    [Google Scholar]
  101. 101. 
    Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y et al. 2009. Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324:1064–68
    [Google Scholar]
  102. 102. 
    Maleckova E, Brilhaus D, Wrobel TJ, Weber APM. 2019. Transcript and metabolite changes during the early phase of abscisic acid-mediated induction of crassulacean acid metabolism in Talinum triangulare. J. Exp. Bot. 70:6581–96
    [Google Scholar]
  103. 103. 
    Males J. 2017. Secrets of succulence. J. Exp. Bot. 68:2121–34
    [Google Scholar]
  104. 104. 
    Males J. 2018. Concerted anatomical change associated with crassulacean acid metabolism in the Bromeliaceae. Funct. Plant Biol. 45:681–95
    [Google Scholar]
  105. 105. 
    Marquardt G, Lüttge U. 1987. Proton transporting enzymes at the tonoplast of leaf cells of the CAM plant Kalanchoë daigremontiana. II. The pyrophosphatase. J. Plant Physiol. 129:269–86
    [Google Scholar]
  106. 106. 
    Martinoia E, Maeshima M, Neuhaus HE. 2007. Vacuolar transporters and their essential role in plant metabolism. J. Exp. Bot. 58:83–102
    [Google Scholar]
  107. 107. 
    McClung CR. 2006. Plant circadian rhythms. Plant Cell 18:792–803
    [Google Scholar]
  108. 108. 
    McWatters HG, Bastow RM, Hall A, Millar AJ. 2000. The ELF3 zeitnehmer regulates light signalling to the circadian clock. Nature 408:716–20
    [Google Scholar]
  109. 109. 
    Michael TP, McClung CR. 2002. Phase-specific circadian clock regulatory elements in Arabidopsis. Plant Physiol 130:627–38
    [Google Scholar]
  110. 110. 
    Michael TP, McClung CR. 2003. Enhancer trapping reveals widespread circadian clock transcriptional control in Arabidopsis. Plant Physiol 132:629–39
    [Google Scholar]
  111. 111. 
    Ming R, VanBuren R, Wai CM, Tang HB, Schatz MC et al. 2015. The pineapple genome and the evolution of CAM photosynthesis. Nat. Genet. 47:1435–42
    [Google Scholar]
  112. 112. 
    Müller ML, Taiz L. 2002. Regulation of the lemon-fruit V-ATPase by variable stoichiometry and organic acids. J. Membr. Biol. 185:209–20
    [Google Scholar]
  113. 113. 
    Murata Y, Pei Z-M, Mori IC, Schroeder J. 2001. Abscisic acid activation of plasma membrane Ca2+ channels in guard cells requires cytosolic NAD(P)H and is differentially disrupted upstream and downstream of reactive oxygen species production in abi1-1 and abi2-1 protein phosphatase 2C mutants. Plant Cell 13:2513–23
    [Google Scholar]
  114. 114. 
    Mustilli AC, Merlot S, Vavasseur A, Fenzi F, Giraudat J. 2002. Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell 14:3089–99
    [Google Scholar]
  115. 115. 
    Nakagami H, Sugiyama N, Mochida K, Daudi A, Yoshida Y et al. 2010. Large-scale comparative phosphoproteomics identifies conserved phosphorylation sites in plants. Plant Physiol 153:1161–74
    [Google Scholar]
  116. 116. 
    Neales T. 1973. The effect of night temperature on CO2 assimilation, transpiration, and water use efficiency in Agave americana L. Aust. J. Biol. Sci. 26:705–14
    [Google Scholar]
  117. 117. 
    Nelson CJ, Alexova R, Jacoby RP, Millar AH. 2014. Proteins with high turnover rate in barley leaves estimated by proteome analysis combined with in planta isotope labeling. Plant Physiol 166:91–108
    [Google Scholar]
  118. 118. 
    Nelson EA, Sage RF. 2008. Functional constraints of CAM leaf anatomy: Tight cell packing is associated with increased CAM function across a gradient of CAM expression. J. Exp. Bot. 59:1841–50
    [Google Scholar]
  119. 119. 
    Nelson EA, Sage TL, Sage RF. 2005. Functional leaf anatomy of plants with crassulacean acid metabolism. Funct. Plant Biol. 32:409–19
    [Google Scholar]
  120. 120. 
    Neuhaus HE, Schulte N. 1996. Starch degradation in chloroplasts isolated from C3 or CAM (crassulacean acid metabolism)-induced Mesembryanthemum crystallinum L. Biochem. J. 318:945–53
    [Google Scholar]
  121. 121. 
    Niechayev NA, Pereira PN, Cushman JC. 2019. Understanding trait diversity associated with crassulacean acid metabolism (CAM). Curr. Opin. Plant Biol. 49:74–85
    [Google Scholar]
  122. 122. 
    Nobel PS. 1976. Water relations and photosynthesis of a desert CAM plant, Agave deserti. Plant Physiol 58:576–82
    [Google Scholar]
  123. 123. 
    Park S-Y, Fung P, Nishimura N, Jensen DR, Fujii H et al. 2009. Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324:1068–71
    [Google Scholar]
  124. 124. 
    Pei ZM, Kuchitsu K, Ward JM, Schwarz M, Schroeder JI. 1997. Differential abscisic acid regulation of guard cell slow anion channels in Arabidopsis wild-type and abi1 and abi2 mutants. Plant Cell 9:409–23
    [Google Scholar]
  125. 125. 
    Pfister B, Zeeman SC. 2016. Formation of starch in plant cells. Cell. Mol. Life Sci. 73:2781–807
    [Google Scholar]
  126. 126. 
    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.. J. Biol. Chem. 277:24204–11
    [Google Scholar]
  127. 127. 
    Plaxton WC. 1990. Glycolysis. Methods in Plant Biochemistry PJ Lea pp. 145–73 London: Academic
    [Google Scholar]
  128. 128. 
    Ranson SL, Thomas M. 1960. Crassulacean acid metabolism. Annu. Rev. Plant Physiol. 11:81–110
    [Google Scholar]
  129. 129. 
    Rentsch D, Martinoia E. 1991. Citrate transport into barley mesophyll vacuoles—comparison with malate-uptake activity. Planta 184:532–37
    [Google Scholar]
  130. 130. 
    Ritte G, Lloyd JR, Eckermann N, Rottmann A, Kossmann J, Steup M 2002. The starch-related R1 protein is an α-glucan, water dikinase. PNAS 99:7166–71
    [Google Scholar]
  131. 131. 
    Roelfsema MRG, Hanstein S, Felle HH, Hedrich R. 2002. CO2 provides an intermediate link in the red light response of guard cells. Plant J 32:65–75
    [Google Scholar]
  132. 132. 
    Roelfsema MRG, Hedrich R. 2005. In the light of stomatal opening: new insights into ‘the Watergate. ’. New Phytol 167:665–91
    [Google Scholar]
  133. 133. 
    Roitinger E, Hofer M, Köcher T, Pichler P, Novatchkova M et al. 2015. Quantitative phosphoproteomics of the ataxia telangiectasia-mutated (ATM) and ataxia telangiectasia-mutated and Rad3-related (ATR) dependent DNA damage response in Arabidopsis thaliana. Mol. Cell. Proteom. 14:556–71
    [Google Scholar]
  134. 134. 
    Sayed OH. 2001. Crassulacean acid metabolism 1975–2000, a check list. Photosynthetica 39:339–52Provides a list of nearly 400 CAM species in 26 families.
    [Google Scholar]
  135. 135. 
    Schaffer R, Landgraf J, Accerbi M, Simon V, Larson M, Wisman E. 2001. Microarray analysis of diurnal and circadian-regulated genes in Arabidopsis. Plant Cell 13:113–23
    [Google Scholar]
  136. 136. 
    Scheidig A, Fröhlich A, Schulze S, Lloyd JR, Kossmann J. 2002. Downregulation of a chloroplast-targeted β-amylase leads to a starch-excess phenotype in leaves. Plant J 30:581–91
    [Google Scholar]
  137. 137. 
    Schneider A, Häusler RE, Kolukisaoglu U, Kunze R, van der Graaff E et al. 2002. An Arabidopsis thaliana knock-out mutant of the chloroplast triose phosphate/phosphate translocator is severely compromised only when starch synthesis, but not starch mobilisation is abolished. Plant J 32:685–99
    [Google Scholar]
  138. 138. 
    Schroeder JI, Hagiwara S. 1989. Cytosolic calcium regulates ion channels in plasma membrane of Vicia faba guard cells. Nature 338:427–30
    [Google Scholar]
  139. 139. 
    Shameer S, Baghalian K, Cheung CYM, Ratcliffe RG, Sweetlove LJ. 2018. Computational analysis of the productivity potential of CAM. Nat. Plants 4:165–71
    [Google Scholar]
  140. 140. 
    Shi JH, Yi KK, Liu Y, Xie L, Zhou ZJ et al. 2015. Phosphoenolpyruvate carboxylase in Arabidopsis leaves plays a crucial role in carbon and nitrogen metabolism. Plant Physiol 167:671–81
    [Google Scholar]
  141. 141. 
    Shimada T, Nakano R, Shulaev V, Sadka A, Blumwald E. 2006. Vacuolar citrate/H+ symporter of citrus juice cells. Planta 224:472–80
    [Google Scholar]
  142. 142. 
    Shimazaki K, Iino M, Zeiger E. 1986. Blue light-dependent proton extrusion by guard cell protoplasts of Vicia faba. Nature 319:324–26
    [Google Scholar]
  143. 143. 
    Silvera K, Neubig KM, Whitten WM, Williams NH, Winter K, Cushman JC. 2010. Evolution along the crassulacean acid metabolism continuum. Funct. Plant Biol. 37:995–1010
    [Google Scholar]
  144. 144. 
    Silvera K, Santiago LS, Cushman JC, Winter K. 2009. Crassulacean acid metabolism and epiphytism linked to adaptive radiations in the Orchidaceae.. Plant Physiol 149:1838–47
    [Google Scholar]
  145. 145. 
    Silvera K, Santiago LS, Winter K. 2005. Distribution of crassulacean acid metabolism in orchids of Panama: evidence of selection for weak and strong modes. Funct. Plant Biol. 32:397–407
    [Google Scholar]
  146. 146. 
    Sowokinos JR, Preiss J. 1982. Pyrophosphorylases in Solanum tuberosum III. Purification, physical, and catalytic properties of ADP-glucose pyrophosphorylase in potatoes. Plant Physiol 69:1459–66
    [Google Scholar]
  147. 147. 
    Steudle E, Smith JAC, Lüttge U. 1980. Water-relation parameters of individual mesophyll cells of the crassulacean acid metabolism plant Kalanchoë daigremontiana. Plant Physiol 66:1155–63
    [Google Scholar]
  148. 148. 
    Stitt M, Aprees T. 1979. Capacities of pea chloroplasts to catalyze the oxidative pentose-pathway and glycolysis. Phytochemistry 18:1905–11
    [Google Scholar]
  149. 149. 
    Stitt M, Zeeman SC. 2012. Starch turnover: pathways, regulation and role in growth.. Curr. Opin. Plant Biol. 15:282–92
    [Google Scholar]
  150. 150. 
    Streb S, Eicke S, Zeeman SC. 2012. The simultaneous abolition of three starch hydrolases blocks transient starch breakdown in Arabidopsis. J. Biol. Chem. 287:41745–56
    [Google Scholar]
  151. 151. 
    Szecowka M, Heise R, Tohge T, Nunes-Nesi A, Vosloh D et al. 2013. Metabolic fluxes in an illuminated Arabidopsis rosette. Plant Cell 25:694–714
    [Google Scholar]
  152. 152. 
    Tallman G, Zhu JX, Mawson BT, Amodeo G, Nouhi Z et al. 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 38:236–42
    [Google Scholar]
  153. 153. 
    Tavakoli N, Kluge C, Golldack D, Mimura T, Dietz KJ. 2001. Reversible redox control of plant vacuolar H+-ATPase activity is related to disulfide bridge formation in subunit E as well as subunit A. Plant J 28:51–59
    [Google Scholar]
  154. 154. 
    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 Physiol 123:1471–81
    [Google Scholar]
  155. 155. 
    Tcherkez G, Cornic G, Bligny R, Gout E, Ghashghaie J. 2005. In vivo respiratory metabolism of illuminated leaves. Plant Physiol 138:1596–606
    [Google Scholar]
  156. 156. 
    Tcherkez G, Mahé A, Gauthier P, Mauve C, Gout E et al. 2009. In folio respiratory fluxomics revealed by 13C isotopic labeling and H/D isotope effects highlight the noncyclic nature of the tricarboxylic acid “cycle” in illuminated leaves. Plant Physiol 151:620–30
    [Google Scholar]
  157. 157. 
    Thalmann M, Pazmino D, Seung D, Horrer D, Nigro A et al. 2016. Regulation of leaf starch degradation by abscisic acid is important for osmotic stress tolerance in plants. Plant Cell 28:1860–78
    [Google Scholar]
  158. 158. 
    Tiessen A, Hendriks JHM, Stitt M, Branscheid A, Gibon Y et al. 2002. Starch synthesis in potato tubers is regulated by post-translational redox modification of ADP-glucose pyrophosphorylase: a novel regulatory mechanism linking starch synthesis to the sucrose supply. Plant Cell 14:2191–213
    [Google Scholar]
  159. 159. 
    Töpfer N, Braam T, Shameer S, Ratcliffe RG, Sweetlove LJ. 2020. Alternative crassulacean acid metabolism modes provide environment-specific water-saving benefits in a leaf metabolic model. Plant Cell 32:123689–705
    [Google Scholar]
  160. 160. 
    Tronconi MA, Fahnenstich H, Weehler MCG, Andreo CS, Flügge UI et al. 2008. Arabidopsis NAD-malic enzyme functions as a homodimer and heterodimer and has a major impact on nocturnal metabolism. Plant Physiol 146:1540–52
    [Google Scholar]
  161. 161. 
    Umezawa T, Sugiyama N, Takahashi F, Anderson JC, Ishihama Y et al. 2013. Genetics and phosphoproteomics reveal a protein phosphorylation network in the abscisic acid signaling pathway in Arabidopsis thaliana. Sci. Signal. 6:rs8
    [Google Scholar]
  162. 162. 
    Vahisalu T, Kollist H, Wang Y-F, Nishimura N, Chan W-Y et al. 2008. SLAC1 is required for plant guard cell S-type anion channel function in stomatal signalling. Nature 452:487–91
    [Google Scholar]
  163. 163. 
    Voll LM, Häusler RE, Hecker R, Weber APM, Weissenböck G et al. 2003. The phenotype of the Arabidopsis cue1 mutant is not simply caused by a general restriction of the shikimate pathway. Plant J 36:301–17
    [Google Scholar]
  164. 164. 
    Von Caemmerer S, Griffiths H. 2009. Stomatal responses to CO2 during a diel crassulacean acid metabolism cycle in Kalanchoe daigremontiana and Kalanchoe pinnata. Plant Cell Environ 32:567–76
    [Google Scholar]
  165. 165. 
    von Willert DJ, Armbrüster N, Drees T, Zaborowski M. 2005. Welwitschia mirabilis: CAM or not CAM – what is the answer?. Funct. Plant Biol. 32:389–95
    [Google Scholar]
  166. 166. 
    Walker RP, Chen Z-H, Acheson RM, Leegood RC. 2002. Effects of phosphorylation on phosphoenolpyruvate carboxykinase from the C4 plant Guinea grass. Plant Physiol 128:165–72
    [Google Scholar]
  167. 167. 
    Walker RP, Leegood RC. 1995. Purification, and phosphorylation in vivo and in vitro of phosphoenolpyruvate carboxykinase from cucumber cotyledons. FEBS Lett 362:70–74
    [Google Scholar]
  168. 168. 
    Walker RP, Leegood RC. 1996. Phosphorylation of phosphoenolpyruvate carboxykinase in plants. Studies in plants with C4 photosynthesis and crassulacean acid metabolism and in germinating seeds. Biochem. J. 317:653–58
    [Google Scholar]
  169. 169. 
    Wang N, Nobel PS. 1998. Phloem transport of fructans in the crassulacean acid metabolism species Agave deserti. Plant Physiol 116:709–14
    [Google Scholar]
  170. 170. 
    Weise SE, Schrader SM, Kleinbeck KR, Sharkey TD. 2006. Carbon balance and circadian regulation of hydrolytic and phosphorolytic breakdown of transitory starch. Plant Physiol 141:879–86
    [Google Scholar]
  171. 171. 
    Weise SE, van Wijk KJ, Sharkey TD. 2011. The role of transitory starch in C3, CAM, and C4 metabolism and opportunities for engineering leaf starch accumulation. J. Exp. Bot. 62:3109–18
    [Google Scholar]
  172. 172. 
    Weissmann S, Ma F, Furuyama K, Gierse J, Berg H et al. 2016. Interactions of C4 subtype metabolic activities and transport in maize are revealed through the characterization of DCT2 mutants. Plant Cell 28:466–84
    [Google Scholar]
  173. 173. 
    Wheeler MCG, Tronconi MA, Drincovich MF, Andreo CS, Flügge U-I, Maurino VG. 2005. A comprehensive analysis of the NADP-malic enzyme gene family of Arabidopsis. Plant Physiol 139:39–51
    [Google Scholar]
  174. 174. 
    Wilkins MB. 1959. An endogenous rhythm in the rate of carbon dioxide output of Bryophyllum. I. Some preliminary experiments. J. Exp. Bot. 10:377–90
    [Google Scholar]
  175. 175. 
    Winter H, Robinson DG, Heldt HW. 1993. Subcellular volumes and metabolite concentrations in barley leaves. Planta 191:180–90
    [Google Scholar]
  176. 176. 
    Winter K, Aranda J, Holtum JAM. 2005. Carbon isotope composition and water-use efficiency in plants with crassulacean acid metabolism. Funct. Plant Biol. 32:381–88
    [Google Scholar]
  177. 177. 
    Winter K, Holtum JAM. 2014. Facultative crassulacean acid metabolism (CAM) plants: powerful tools for unravelling the functional elements of CAM photosynthesis. J. Exp. Bot. 65:3425–41
    [Google Scholar]
  178. 178. 
    Winter K, Holtum JAM, Smith JAC. 2015. Crassulacean acid metabolism: a continuous or discrete trait?. New Phytol 208:73–78
    [Google Scholar]
  179. 179. 
    Winter K, von Willert DJ 1972. NaCl-induzierter crassulacean-Säurestoffwechsel bei Mesembryanthemum crystallinum. Z. Pflanzenphysiol. 67:166–70
    [Google Scholar]
  180. 180. 
    Winter K, Wallace BJ, Stocker GC, Roksandic Z. 1983. Crassulacean acid metabolism in Australian vascular epiphytes and some related species. Oecologia 57:129–41
    [Google Scholar]
  181. 181. 
    Wong SC, Hew CS. 1976. Diffusive resistance, titratable acidity, and CO2 fixation in two tropical epiphytic ferns. Am. Fern J. 66:121–24
    [Google Scholar]
  182. 182. 
    Wyka TP, Duarte HM, Lüttge UE. 2005. Redundancy of stomatal control for the circadian photosynthetic rhythm in Kalanchoë daigremontiana Hamet et Perrier. Plant Biol 7:176–81
    [Google Scholar]
  183. 183. 
    Yang XH, Hu RB, Yin HF, Jenkins J, Shu SQ et al. 2017. The Kalanchoë genome provides insights into convergent evolution and building blocks of crassulacean acid metabolism. Nat. Commun. 8:1899
    [Google Scholar]
  184. 184. 
    Zambrano VAB, Lawson T, Olmos E, Fernández-García N, Borland AM. 2014. Leaf anatomical traits which accommodate the facultative engagement of crassulacean acid metabolism in tropical trees of the genus Clusia. J. Exp. Bot. 65:3513–23
    [Google Scholar]
  185. 185. 
    Zeeman SC, Thorneycroft D, Schupp N, Chapple A, Weck M et al. 2004. Plastidial α-glucan phosphorylase is not required for starch degradation in Arabidopsis leaves but has a role in the tolerance of abiotic stress. Plant Physiol 135:849–58
    [Google Scholar]
  186. 186. 
    Zhang HT, Zhou HJ, Berke L, Heck AJR, Mohammed S et al. 2013. Quantitative phosphoproteomics after auxin-stimulated lateral root induction identifies an SNX1 protein phosphorylation site required for growth. Mol. Cell. Proteom. 12:1158–69
    [Google Scholar]
  187. 187. 
    Zhang JB, Martinoia E, De Angeli A. 2014. Cytosolic nucleotides block and regulate the Arabidopsis vacuolar anion channel AtALMT9. J. Biol. Chem. 289:25581–89
    [Google Scholar]
/content/journals/10.1146/annurev-arplant-071720-104814
Loading
/content/journals/10.1146/annurev-arplant-071720-104814
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error