Stem juice production of the C₄ sugarcane (Saccharum officinarum) is enhanced by growth at double-ambient CO₂ and high temperature

Summary

Two cultivars of sugarcane (Saccharum officinarum cv. CP73-1547 and CP88-1508) were grown for 3 months in paired-companion, temperature-gradient, sunlit greenhouses under daytime [CO₂] of 360 (ambient) and 720 (double ambient) μmol mol⁻¹ and at temperatures of 1.5 °C (near ambient) and 6.0 °C higher than outside ambient temperature. Leaf area and biomass, stem biomass and juice and CO₂ exchange rate (CER) and activities of ribulose bisphosphate carboxylase-oxygenase (Rubisco) and phosphoenolpyruvate carboxylase (PEPC) of fully developed leaves were measured at harvest. On a main stem basis, leaf area, leaf dry weight, stem dry weight and stem juice volume were increased by growth at doubled [CO₂] or high temperature. Such increases were even greater under combination of doubled [CO₂]/high temperature. Plants grown at doubled [CO₂]/high temperature combination averaged 50%, 26%, 84% and 124% greater in leaf area, leaf dry weight, stem dry weight and stem juice volume, respectively, compared with plants grown at ambient [CO₂]/near-ambient temperature combination. In addition, plants grown at doubled [CO₂]/high temperature combination were 2–3-fold higher in stem soluble solids than those at ambient [CO₂]/near-ambient temperature combination. Although midday CER of fully developed leaves was not affected by doubled [CO₂] or high temperature, plants grown at doubled [CO₂] were 41–43% less in leaf stomatal conductance and 69–79% greater in leaf water-use efficiency, compared with plants grown at ambient [CO₂]. Activity of PEPC was down-regulated 23–32% at doubled [CO₂], while high temperature did not have a significant impact on this enzyme. Activity of Rubisco was not affected by growth at doubled [CO₂], but was reduced 15–28% at high temperature. The increases in stem juice production and stem juice soluble solids concentration for sugarcane grown at doubled [CO₂] or high temperature, or at doubled [CO₂]/high temperature combination, were partially the outcome of an increase in whole plant leaf area. Such increase would enhance the ongoing and cumulative photosynthetic capability of the whole plant. The results indicate that a doubling of [CO₂] would benefit sugarcane production more than the anticipated 10–15% increase for a C₄ species.

Introduction

The photosynthetic performance of many terrestrial plants is below their potential capability at current atmospheric CO₂ and O₂ levels. A rise in atmospheric CO₂ concentration ([CO₂]) by itself could stimulate photosynthesis and enhance productivity of important agricultural crops (Bowes, 1993; Kimball, 1993; Drake et al., 1997; Long et al., 2004). In C₃ photosynthesis, the CO₂ exchange rate (CER) in the leaf is a direct result of the activity of ribulose bisphosphate carboxylase-oxygenase (Rubisco), which is not saturated at current atmospheric [CO₂]. An increase in air [CO₂] availability results in increased leaf CER, because elevated [CO₂] inhibits the Rubisco oxygenase reaction and the subsequent loss of CO₂ through photorespiration (Bowes, 1996). In addition to atmospheric [CO₂], CER of C₃ plants is affected by air temperature, and this effect is also primarily exerted through Rubisco (Long, 1991). An increase in ambient temperature reduces the activation state of Rubisco (Kobza and Edwards, 1987; Holaday et al., 1992) and decreases both the specificity for CO₂ and the solubility of CO₂, relative to O₂ (Long, 1991). As growth temperature increases, the CO₂/O₂ ratio in solution is reduced and results in a decline in the Rubisco carboxylation/oxygenation ratio and an enhancement in photorespiration (Jordan and Ogren, 1984; Long, 1991; Bowes, 1993). Since the balance between the carboxylation and oxygenation reaction depends on the relative concentrations of CO₂ and O₂ at the Rubisco site, an increase in atmospheric [CO₂], and the concomitant inhibition of the Rubisco oxygenase reaction, should moderate the adverse impacts of high air temperature on C₃ photosynthesis (Long, 1991). It has been projected that atmospheric [CO₂], currently at about 385 μmol mol⁻¹, may surpass 700 μmol mol⁻¹ before the end of this century (Solomon et al., 2007). A rise in atmospheric [CO₂] and other greenhouse gases would cause an increase in the mean global air temperature by as much as 6 °C (Schneider, 2001; Solomon et al., 2007), and undoubtedly have a significant impact on photosynthesis and productivity of many plants. As a result, research on rising atmospheric [CO₂], and elevated [CO₂] interacting with high temperature or soil water deficit, has focused extensively in the last 30 years on C₃ plants, which represent more than 90% of terrestrial plant species (Bowes, 1993).

Plants of the C₄ photosynthetic category have evolved specific mechanisms to overcome the limitations of low atmospheric [CO₂], improve their photosynthetic efficiency and conserve their water use under hostile environmental conditions. By using the C₄ photosynthetic cycle to concentrate [CO₂] at the Rubisco site to levels manyfold higher than ambient [CO₂], C₄ plants are able to achieve a greater photosynthetic capacity than C₃ plants at the current atmospheric [CO₂], particularly at high growth temperatures (Matsuoka et al., 2001). Because of this unique CO₂-concentrating mechanism capability, photosynthesis of C₄ plants is practically near saturation at current atmospheric [CO₂], and therefore C₄ plants would not show significant growth responses to a rise in ambient [CO₂] (Bowes, 1993). Nevertheless, a positive growth response to elevated growth [CO₂] has been reported for a variety of C₄ plants, although to a smaller extent compared with the C₃ species (Kimball, 1993; Poorter et al., 1996; Ghannoum et al., 2000; Long et al., 2004). In spite of the fact that recent research progress has been made in characterizing the mechanisms of a limited number of C₄ species to increases in air levels of [CO₂] and temperature and changes in soil moisture status (Leakey et al., 2006; Vu et al., 2006; De Souza et al. 2008; Vu and Allen, 2009), the responses of C₄ crops to future rising [CO₂] and climate changes are still very variable and uncertain (Leakey et al., 2006; De Souza et al., 2008). Such uncertainties would limit predictions of future global climate change impacts on C₄-dominated agricultural and ecological systems.

Although C₄ plants represent fewer than 4% of all angiosperm species, their ecological and economic significance is substantial (Brown et al., 2005). On a global basis, up to one-third of terrestrial productivity is provided by C₄ plants (Cerling et al., 1997; Ghannoum et al., 1997; Brown et al., 2005). In many tropical regions, the food source is primarily based on C₄ crops, among those maize, millet, sorghum and sugarcane are the most agriculturally important monocots in terms of production (Brown, 1999). Up to 75% of the world sugar production is provided by sugarcane (De Souza et al., 2008), with an estimation at about 150 million tonnes for the year 2005/06 (Glassop et al., 2007). In addition, the use of sugarcane as a source for biofuel production has been highly recognized (Goldenberg, 2007). Studies are therefore needed for advancing our understanding on growth and yield and the mechanisms underlying the photosynthesis and metabolism of this C₄ crop plant, as well as other economically important C₄ species, in response to the predicted changes in atmospheric [CO₂] and climate (Leakey et al., 2006).

In a previous study with sugarcane, we have demonstrated that elevated growth [CO₂] enhances leaf CER and up-regulates the capacity of certain key photosynthetic enzymes and sucrose metabolism in young developing leaves (Vu et al., 2006). In the present study, two cultivars of sugarcane with distinct characteristics in terms of soil water availability were grown for 3 months in sunlit greenhouses under ambient and double-ambient [CO₂] and at temperatures up to 6.0 °C above outdoors. Leaf area and biomass, biomass and juice production of the main stem and CER and activity of the two C₄ photosynthesis carboxylating enzymes of fully developed leaves were determined at harvest. Our objective was to characterize the photosynthesis and growth performance of sugarcane under double-ambient [CO₂] and high temperature, and to test if growth of this C₄ monocot at doubled [CO₂] and high temperature enhanced the production of stem juice. Sugarcane has the characteristics of simplicity for sugar storage, as sucrose is the sugar which is synthesized in the leaf, translocated in the phloem and stored in the stem as soluble solids or BRIX (Moore, 1995). As a result, juice of the mature stems of sugarcane contains a very high concentration of sucrose (Moore, 1995; Lingle, 1999; Rae et al., 2005), which is extracted and purified during commercial sugar production. Understanding growth as well as photosynthesis of economically important C₄ crops in response to rises in atmospheric [CO₂] and temperature and variations in soil moisture availability is essential for predictions of how agricultural C₄ populations would perform under a future CO₂- and climate-changed world.