2.1.6 Crassulacean acid metabolism (CAM)
A further adaptation to high temperature and in particular arid conditions is crassulacean acid metabolism (CAM) photo-synthesis. Compared with the anatomical specialisation and spatial separation of biochemical function in C4 plants, CAM photosynthesis does not require anatomical differentiation but instead involves a temporal separation of an in situ biochemical function. CAM is essentially an adaptation to reduce water loss through stomata by reversing the diurnal rhythm of CO2 ﬁxation. Typically, CAM plants are equipped with fleshy assimilatory organs (commonly phyllodes or cladodes) and include the majority of cacti and orchids as well as many salt-tolerant succulents (such as the ice plant Mesembryanthemum crystallinum) and pineapple. Whereas C4 plants have a biochemical CO2 pump, CAM plants operate more like a biochemical storage battery. During the night-time when heat load is low and atmospheric water vapour pressure relatively high, stomata open, admitting CO2, which is ﬁxed by PEP carboxylase in much the same way as in C4 photosynthesis. The C4 product (usually malate) is stored in vacuolar compartments of these fleshy organs until the daytime. Malate is then decarboxylated to provide CO2 for Rubisco (reviewed by Winter 1985). This tight cycle of malic acid storage and breakdown, often called ‘acidiﬁcation’ and ‘deacidiﬁcation’, is shown schematically in Figure 2.7 along with a simpliﬁed version of the CAM pathway.
Historically, the discovery of CAM plants can be attributed to this cyclical acidiﬁcation/deacidiﬁcation. In a letter to the Linnean Society in 1813 Benjamin Heyne wrote ‘the leaves of the…plant called by Mr Salisbury Bryophyllum calycinum, which on the whole have an herbaceous taste, are in the morning as acid as sorrel, if not more so. As the day advances, they lose their acidity and are tasteless about noon…’ (a more detailed account appears in Walker 1992). B. calycinum is, of course, a CAM plant and the acid taste is due to the build up of malic acid at night. However, despite these early observations, it took another 150 years to unravel the complexities of the CAM pathway.
Because the primary steps of carbon ﬁxation by CAM plants occur in darkness, PEP synthesis and energy supply (in the form of ATP and reducing power) are closely linked to respiration plus breakdown of stored carbohydrates made during the previous photoperiod. Simpliﬁed in Figure 2.7, the CAM pathway relies on starch as a ‘storage battery’ of light-derived energy for subsequent PEP carboxylation in darkness. Malate stored in vacuolar compartments from night-time ﬁxation is a carbon store that yields CO2 in daytime.
Unlike C4 plants, which have some of the highest growth rates of all land plants (Hatch 1988), CAM plants achieve rather meagre rates of photosynthesis and suffer a yield penalty as a result. Moreover, their modiﬁed pathway of photosynthesis with temporal separation of photochemical and biochemcial functions incurs an energetic cost of between 5.5 and 6.5 ATP and two NADPH per CO2 ﬁxed (Walker 1992). Compare this with a requirement of only three ATP (and two NADPH) per CO2 ﬁxed during C3 photosynthesis in low O2.
Restrictions on inward diffusion of ambient CO2 via sparse stomata and slow progress between decarboxylation and ﬁxation sites through an extensive liquid phase of assimilatory tissue would place further constraints on carbon gain. Some relativities for C3, C4 and CAM gas exchange are summarised in Table 2.1. Potentially greater rates of assimilation by C4 plants put that group at an advantage in terms of biomass gain and water use efﬁciency in daytime. For a given stomatal conductance, transpiration by C3 and C4 would be comparable, but the greater CO2-scavenging capacity of C4 plants makes them more water efﬁcient (greater inward flux of CO2 for a given outward flux of H2O). At night, CAM plants achieve further improvement in water use efﬁciency because CO2 uptake is then combined with much reduced transpiration.
Table 2.1 emphasises adaptive features of C3, C4 and CAM photosynthesis. Light-saturated rates of photosynthesis in C4 plants can be up to twice those in C3, even though maximum stomatal conductance is commonly somewhat lower. By contrast, C4 plants achieve much higher mesophyll conductance (a consequence of their remarkable CO2-scavenging ability), and water use efﬁciency during photosynthesis is consequently enhanced (i.e. transpiration ratio is lower). Daytime assimilation by CAM plants can occur when moisture is abundant, and is analogous to C3 photosynthesis with maximal rates comparable to lower values of C3 plants. C3 engagement by CAM plants diminishes as moisture stress intensiﬁes, and in full CAM mode night-time assimilation assumes prominence. In that condition, PEP carboxylase is responsible for initial ﬁxation with mesophyll conductance comparable to that of a C4 plant. Water use efﬁciency is, however, much greater due to lower evaporative demand. Under extreme conditions, the night-time transpiration ratio in CAM plants can be an order of magnitude lower than in C4 plants (right-hand column, Table 2.1).
Notwithstanding stomatal restrictions on CO2 assimilation, frugal use of water rather than high rates of carbon gain would have been the primary driving variable for evolution of CAM plants. In this context, CAM photosynthesis is more of a ‘survival option’ where slow assimilation is an acceptable trade-off for a water-retentive physiology. The spectacular success of CAM photosynthesis in arid zones and dry habitats worldwide conﬁrms this principle.