Photosynthetic response of Cannabis sativa L., an important medicinal plant, to elevated levels of CO2

Abstract

Introduction

Increasing atmospheric CO₂ concentration and global warming are of major environmental concern around the world. The concentration of CO₂ in the atmosphere has increased by more than 30 %, from about 280 μmol mol⁻¹ in the eighteenth century to the present level of 390 μmol mol⁻¹ (Mauna Loa Observatory-MLO, Hawaii), and is projected to reach as high as 700 μmol mol⁻¹ by the end of the twenty first century (Houghton et al. 1996). Thus, the future environment will be characterized by elevated CO₂, higher temperature and drier climate in certain parts of the globe. The increase in CO₂ concentration may have considerable direct and indirect effects on various life forms. Particular effects are related to the distribution, abundance and productivity of vegetation (Pounds and Puschendorf 2004). Therefore, understanding the effects of the increasing atmospheric CO₂ concentration on plants and vegetation has become an important issue. A large number of studies have shown enhancement in growth of the plants subjected to both short and long-term CO₂ exposure (Kimball 1983; Cure and Acock 1986) by affecting a number of basic physiological processes, particularly photosynthesis and other gas exchange parameters (Ceulemans et al. 1995). A close correlation between net photosynthesis (P_N) and crop yield has been reported since more than 90 % of the dry matter of live plants is derived from photosynthetic CO₂assimilation (Zelitch 1975). However, the magnitude of the enhancement in photosynthesis and growth of the plants appear to be species and genotype/variety specific (Minorsky 2002). Doubling in CO₂concentration has been reported to increase the yield by 30 % or more in many crops (Poorter 1993). On the other hand, inhibition of photosynthesis with increasing CO₂ concentration has also been reported in many plant species (Bazzaz and Garbutt 1988; Juurola 2003).

Cannabis sativa L. (Cannabaceae) is a widely distributed plant around the world. It has a long history of medicinal use as far back as the 6th century B.C. Cannabis sativa is the natural source of the cannabinoids, a unique group of terpeno-phenolic compounds that accumulate in the glandular trichomes of the plant. Δ⁹-Tetrahydrocannabinolic acid (Δ⁹-THCA) is the major cannabinoid which upon decarboxylation with age or heating gives rise to Δ⁹-THC, the primary psychoactive agent (Pertwee 2006). The pharmacologic and therapeutic potency of Cannabis preparations and Δ⁹-THC have been extensively reviewed (Grinspoon and Bakalar 1993; Mattes et al. 1994 and Brenneisen et al. 1996). Despite of its medicinal importance and widespread occurrence, to the best of our knowledge, no information (except a previous note by our group on—one Cannabis variety, Chandra et al. 2008) is available on the consequences of rising atmospheric CO₂ concentration on its photosynthesis and growth performance. This study describes the short term effect of elevated CO₂ on photosynthetic characteristics and stomatal response in four different high Δ⁹-THC yielding varieties of Cannabis sativa.

Materials and methods

Result and discussion

There is a growing concern that human-induced climatic change will affect the eco-physiological processes of plant species, and hence their productivity and distribution (Sanz-Elorza et al. 2003). Further, the responsiveness of the species to recent and past climate changes also suggests that climate change could act as a major cause of extinction of some plant species in the near future (Thomas et al. 1994). The ability of plant species to grow and to survive in a particular environment depends on their photosynthetic capacity (Berry and Downton 1982, Joshi et al. 2007). It has been reported that plants with high rates of photosynthesis and WUE have the potential to grow faster and yield more than the species with low photosynthesis rate and WUE under fluctuating environmental conditions (Jones 1992; Zhang et al. 1996). Elevated atmospheric CO₂ concentration in the environment has also been reported to enhance the photosynthesis and growth of many plant species (Kimball 1983, Cure and Acock 1986). It is also generally suspected that the studies on short term exposure of elevated CO₂ overestimate the relative enhancements in CO₂ assimilation rates in plants as compared to those under the long term exposures (Sage et al. 1989). Nonetheless, short term studies serve a key role in providing first approximation and indication of plants behavior under future environmental conditions (Joshi 2006). Figure 1a shows the effect of ambient and elevated CO₂ concentrations on net photosynthesis of different varieties of C. sativa. In all the varieties, a slight but statistically insignificant (p < 0.05) increase in P_N was observed when measurements were made at 545 μmol mol⁻¹ CO₂ concentration as compared to ambient (390 μmol mol⁻¹) CO₂, whereas, a significant increase (p < 0.05) of about 48 %, 45 %, 44 % and 38 % in P_N was observed when the measurements were made at 700 μmol mol⁻¹ CO₂ concentration as compared to ambient level in HPM, K2, MX and W1 varieties, respectively. The increase in P_N due to the short term increase in CO₂ concentration is reported to be primarily because of an increase in carboxylation efficiency and secondarily, due to the reduction in photorespiration (Minorsky 2002). However, the magnitude of enhancement was reported to be species and genotype/variety specific. It has also been reported that doubling of ambient CO₂ concentration increases P_N in the plant species whose photosynthesis is not saturated by the present ambient CO₂ level (Joshi 2006). Since photosynthesis of C3 plant species is not saturated at the present ambient CO₂ concentration, these plants are thus reported to benefit more than C4 plants (Bowes 1993; Joshi 2006). Average increase of about 33 % in the rate of photosynthesis and productivity of C3 plants has been reported with doubling of atmospheric CO₂ concentration (Kimball 1983; Bazzaz and Garbutt 1988; Cure and Acock 1986, Joshi 2006). In the present investigation, under elevated CO₂ concentration (700 μmol mol⁻¹) the photosynthetic rate of Cannabis sativa was ~ 44 % higher relative to that under ambient CO₂ (390 μmol mol⁻¹).

Fig. 1

Effect of different CO₂ concentrations (390, 545 and 700 μmol mol⁻¹) on net photosynthesis (a), stomatal conductance (b), transpirational water loss (c), intercellular CO₂ concentration (d) and water use efficiency (e) of Cannabis …

Increasing CO₂ concentration decreased the stomatal conductance (Fig. 1b) and subsequently, the transpiration rate (Fig. 1c), thereby increasing the water use efficiency (Fig. 1e) of C. sativa. Under elevated CO₂ (545 μmol mol⁻¹), about 22 %, 12 %, 19 % and 13 % decrease in g_s, 19 %, 27 %, 29 % and 32 % decrease in E and, 36 %, 63 %, 62 % and 78 % increase in WUE was observed in HPM, K2, MX and W1 varieties, respectively, as compared to those under ambient CO₂ (390 μmol mol⁻¹); whereas, under 700 μmol mol⁻¹ CO₂ concentration, about 44 %, 43 %, 30 % and 23 % decrease in g_s, 45 %, 44 %, 50 % and 51 % decrease in E and, 177 %, 157 %, 191 % and 182 % increase in WUE was observed in HPM, K2, MX and W1 respectively, as compared to those under ambient CO₂ level. It is important to mention that compared to the report presented earlier by Chandra et al. (2008), in the present study differences were observed in P_N and WUE of HPM variety under the ambient CO₂ concentration. These differences could be attributed to the growth stages of plants at the time of observations recorded. However, the effect of doubling of CO₂ on these parameters was found comparable in both the studies. In the present study, the observed decrease in stomatal conductance and the reduction in the transpirational water loss under elevated CO₂ concentration has been previously reported in many plant species (Eamus et al. 1993; Thomas et al. 1994). Elevated CO₂ has also been reported to improve the water use efficiency of plants (Morison 1993; Joshi 2006; Chandra et al. 2008). The increase in C_i (Fig. 1d), ratio for C_i and g_s (C_i/g_s) which reflects the mesophyll efficiency of plants and no change in C_i/C_a ratio (Table 1) in response to the elevated CO₂ levels were observed in Cannabis sativa. Constant C_i/C_a values under the different environmental conditions represent a stress free state and a close coordination between stomatal and mesophyll functions regulating CO₂ uptake and water loss in plants (Jarvis et al. 1999). A similar result has been reported for many C3 and C4 plant species exposed to elevated CO₂ levels (Morison 1993).

Table 1

Effect of different CO₂ concentrations on C_i/C_a and C_i/g_s ratios in Cannabis sativa varieties. Values within a parameter (C_i/C_a or C_i/g_s) followed by the same letter are not significantly different at p < 0.05. C_i—intercellular …

In conclusion, the effects of elevated CO₂ concentrations on Cannabis sativa varieties were significant, leading to an increase in P_N and WUE of this species. However, the magnitude of the increase was ‘variety-specific’. The decreases in g_s and E, and a constant C_i/C_a ratio under the elevated CO₂concentrations are the indicators of survival potential of this species under the climatic changes leading to drought conditions in the future.

Acknowledgements

Abbreviations

References