Crassulacean acid metabolism photosynthesis: ‘working the night shift’

Abstract

Crassulacean acid metabolism (CAM) can be traced from Roman times through persons who noted a morning acid taste of some common house plants. From India in 1815, Benjamin-Heyne described a ‘daily acid taste cycle’ with some succulent garden plants. Recent work has shown that the nocturnally formed acid is decarboxylated during the day to become the CO2 for photosynthesis. Thus, CAM photosynthesis extends over a 24-hour day using several daily interlocking cycles. To understand CAM photosynthesis, several landmark discoveries were made at the following times: daily reciprocal acid and carbohydrate cycles were found during 1870 to 1887; their precise identification, as malic acid and starch, and accurate quantification occurred from 1940 to 1954; diffusive gas resistance methods were introduced in the early 1960s that led to understanding the powerful stomatal control of daily gas exchanges; C4 photosynthesis in two different types of cells was discovered from 1965 to ∼1974 and the resultant information was used to elucidate the day and night portions of CAM photosynthesis in one cell; and exceptionally high internal green tissue CO2 levels, 0.2 to 2.5%, upon the daytime decarboxylation of malic acid, were discovered in 1979. These discoveries then were combined with related information from C3 and C4 photosynthesis, carbon biochemistry, cellular anatomy, and ecological physiology. Therefore by ∼1980, CAM photosynthesis finally was rigorously outlined. In a nutshell, 24-hour CAM occurs by phosphoenol pyruvate (PEP) carboxylase fixing CO2(HCO3 −) over the night to form malic acid that is stored in plant cell vacuoles. While stomata are tightly closed the following day, malic acid is decarboxylated releasing CO2 for C3 photosynthesis via ribulose bisphosphate carboxylase oxygenase (Rubisco). The CO2 acceptor, PEP, is formed via glycolysis at night from starch or other stored carbohydrates and after decarboxylation the three carbons are restored each day. In mid to late afternoon the stomata can open and mostly C3 photosynthesis occurs until darkness. CAM photosynthesis can be both inducible and constitutive and is known in 33 families with an estimated 15 to 20 000 species. CAM plants express the most plastic and tenacious photosynthesis known in that they can switch photosynthesis pathways and they can live and conduct photosynthesis for years even in the virtual absence of external H2O and CO2, i.e., CAM tenaciously protects its photosynthesis from both H2O and CO2 stresses.Key wordsBill BradbeerBryophyllumCAMcarbohydratesNancy CarnalCO2 fixationBill CockburnCrassulacean acid metabolismdaily cycleCharles Darwindiffusive gas resistancefructose 2,6-bisphosphateglucansNeimiah GrewBenjamin HeyneKalanchoeManfred KlugeMac Laetschmalic acidOpuntiapyrophosphateOrlando QueirozStanley Ransonrespiratory quotientstarchstomataSedumMeirion ThomasIrwin TingHubert VickeryDavid WalkerKlaus Winter