Photosynthetic responses to temperature of phosphoenolpyruvate carboxykinase type C<sub>4</sub> species differing in cold sensitivity

Peixoto

Sugarcane: Physiology, Biochemistry, and Functional Biology

2013

Sugarcane and related species utilize the NADP malic enzyme type of C 4 photosynthesis, which confers superior radiation-, nitrogen-, and wateruse efficiencies relative to C 3 plants in the warm environments where sugarcane thrives. By being able to concentrate CO 2 around Rubisco, sugarcane avoids limitations due to photorespiration and exhibits superior photosynthesis over C 3 plants at low CO 2 levels and warm temperatures (> 30 • C). At current atmospheric CO 2 levels, reported photosynthetic capacities of sugarcane are often low relative to other cultivated C 4 species and frequently are equivalent to photosynthesis rates in C 3 crops such as wheat and rice. These reduced photosynthetic capacities are present in older sugarcane plants because leaf nitrogen values become depleted as cumulatively more tissues are produced, and high carbohydrate levels may downregulate photosynthesis. This is particularly apparent when growers limit late nitrogen applications to boost sugar production. When photosynthesis is measured in young plants with cumulatively low leaf area, or in plants where leaf nitrogen is maintained by regular or heavy nitrogen applications, then sugarcane photosynthetic capacities are typical of C 4 plants and higher than observed in most C 3 species at current CO 2 levels. In leaves with reduced N, photosynthesis in sugarcane could become less efficient, because an imbalance between the C 3 and C 4 metabolic cycles may promote leakage of bundle sheath CO 2 out of the leaf. These observations indicate that photosynthesis in sugarcane could be improved by creating new varieties that either maintain high leaf nitrogen or enhance photosynthetic nitrogen-use efficiency to match that of productive C 4 crops such as maize.

Section: Chilling Effects On Amentioning

confidence: 99%

Photosynthesis in Sugarcane

Peixoto

Sugarcane: Physiology, Biochemistry, and Functional Biology

2013

“…Furthermore, an analysis of transgenic F. bidentis with antisense PPDK gene constructs showed that PPDK shares control of C 4 photosynthetic rate with Rubisco under ambient CO 2 and high light (Furbank et al, 1997). A key role for PPDK in low temperature tolerance is also inferred in two chilling-tolerant PEP carboxykinase type C 4 species, which apparently maintain photosynthetic rates at low temperature by bypassing PPDK in PEP synthesis, via PEP carboxykinase (Smith and Woolhouse, 1983;Matsuba et al, 1997). Although analysis of the cDNA sequences for PPDK in M. 3 giganteus and maize have failed to reveal any differences in putative amino acids sequences that could confer cold tolerance, the amount of PPDK was reported to increase significantly in M. 3 giganteus when grown at low temperature.…”

mentioning

confidence: 98%

Cool C4 Photosynthesis: Pyruvate Pi Dikinase Expression and Activity Corresponds to the Exceptional Cold Tolerance of Carbon Assimilation inMiscanthus×giganteus

et al. 2008

The bioenergy feedstock grass Miscanthus 3 giganteus is exceptional among C 4 species for its high productivity in cold climates. It can maintain photosynthetically active leaves at temperatures 6°C below the minimum for maize (Zea mays), which allows it a longer growing season in cool climates. Understanding the basis for this difference between these two closely related plants may be critical in adapting maize to colder weather. When M. 3 giganteus and maize grown at 25°C were transferred to 14°C, light-saturated CO 2 assimilation and quantum yield of photosystem II declined by 30% and 40%, respectively, in the first 48 h in these two species. The decline continued in maize but arrested and then recovered partially in M. 3 giganteus. Within 24 h of the temperature transition, the pyruvate phosphate dikinase (PPDK) protein content per leaf area transiently declined in M. 3 giganteus but then steadily increased, such that after 7 d the enzyme content was significantly higher than in leaves growing in 25°C. By contrast it declined throughout the chilling period in maize leaves. Rubisco levels remained constant in M. 3 giganteus but declined in maize. Consistent with increased PPDK protein content, the extractable PPDK activity per unit leaf area (V max,ppdk ) in cold-grown M. 3 giganteus leaves was higher than in warm-grown leaves, while V max,ppdk was lower in coldgrown than in warm-grown maize. The rate of light activation of PPDK was also slower in cold-grown maize than M. 3 giganteus. The energy of activation (E a ) of extracted PPDK was lower in cold-grown than warm-grown M. 3 giganteus but not in maize. The specific activities and E a of purified recombinant PPDK from M. 3 giganteus and maize cloned into Escherichia coli were similar. The increase in PPDK protein in the M. 3 giganteus leaves corresponded to an increase in PPDK mRNA level. These results indicate that of the two enzymes known to limit C 4 photosynthesis, increase of PPDK, not Rubisco content, corresponds to the recovery and maintenance of photosynthetic capacity. Functionally, increased enzyme concentration is shown to increase stability of M. 3 giganteus PPDK at low temperature. The results suggest that increases in either PPDK RNA transcription and/or the stability of this RNA are important for the increase in PPDK protein content and activity in M. 3 giganteus under chilling conditions relative to maize.

“…Pyruvate orthophosphate dikinase (PPDK, EC 2.7.9.1) and phosphoenolpyruvate (PEP) carboxylase (PEPCase, EC 4.1.1.31) can both dissociate below 8°C to 12°C in vitro (Sugiyama and Boku, 1976;Edwards et al, 1985;Krall and Edwards, 1993). However, considerable species and ecotypic variability has been noted, and these steps are not fundamentally prone to failure at low temperatures in vivo (Leegood and Edwards, 1996;Matsuba et al, 1997).The possibility that the bundle sheath reactions may limit C 4 photosynthesis at suboptimal temperatures has received less attention. Bjö rkman and Pearcy (1971) found that the activation energy (Ea) of photosynthesis was similar to that of Rubisco (EC 4.1.1.39) in several warm-climate C 3 and C 4 species.…”

mentioning

confidence: 99%

C4 Photosynthesis at Low Temperature. A Study Using Transgenic Plants with Reduced Amounts of Rubisco

Kubien

Caemmerer²,

Furbank³

et al. 2003

Plant Physiology

143

137

C 4 plants are rare in the cool climates characteristic of high latitudes and elevations, but the reasons for this are unclear. We tested the hypothesis that CO 2 fixation by Rubisco is the rate-limiting step during C 4 photosynthesis at cool temperatures. We measured photosynthesis and chlorophyll fluorescence from 6°C to 40°C, and in vitro Rubisco and phosphoenolpyruvate carboxylase activity from 0°C to 42°C, in Flaveria bidentis modified by an antisense construct (targeted to the nuclear-encoded small subunit of Rubisco, anti-RbcS) to have 49% and 32% of the wild-type Rubisco content. Photosynthesis was reduced at all temperatures in the anti-Rbcs plants, but the thermal optimum for photosynthesis (35°C) did not differ. The in vitro turnover rate (kcat) of fully carbamylated Rubisco was 3.8 mol mol 1 s 1 at 24°C, regardless of genotype. The in vitro kcat (Rubisco Vcmax per catalytic site) and in vivo kcat (gross photosynthesis per Rubisco catalytic site) were the same below 20°C, but at warmer temperatures, the in vitro capacity of the enzyme exceeded the realized rate of photosynthesis. The quantum requirement of CO 2 assimilation increased below 25°C in all genotypes, suggesting greater leakage of CO 2 from the bundle sheath. The Rubisco flux control coefficient was 0.68 at the thermal optimum and increased to 0.99 at 6°C. Our results thus demonstrate that Rubisco capacity is a principle control over the rate of C 4 photosynthesis at low temperatures. On the basis of these results, we propose that the lack of C 4 success in cool climates reflects a constraint imposed by having less Rubisco than their C 3 competitors.