Temperature Response of Photosynthesis in C3, C4, and CAM

Photosynth Res DOI 10.1007/s11120-013-9874-6 REVIEW Temperature response of photosynthesis in C3,C4, and CAM plants: temperature acclimation and temperature adaptation Wataru Yamori • Kouki Hikosaka • Danielle A. Way Received: 30 October 2012 / Accepted: 12 June 2013 Ó Springer Science+Business Media Dordrecht 2013 Abstract Most plants show considerable capacity to the published data to evaluate the extent of photosynthetic adjust their photosynthetic characteristics to their growth temperature acclimation in higher plants, and analyze temperatures (temperature acclimation). The most typical which plant groups (i.e., photosynthetic types and func- case is a shift in the optimum temperature for photosyn- tional types) have a greater inherent ability for photosynthesis, which can maximize the photosynthetic rate at the thetic acclimation to temperature than others, since there growth temperature. These plastic adjustments can allow have been reported interspecific variations in this ability. plants to photosynthesize more efficiently at their new We found that the inherent ability for temperature accli- growth temperatures. In this review article, we summarize mation of photosynthesis was different: (1) among C3,C4, the basic differences in photosynthetic reactions in C3,C4, and CAM species; and (2) among functional types within and CAM plants. We review the current understanding of C3 plants. C3 plants generally had a greater ability for the temperature responses of C3,C4, and CAM photosyn- temperature acclimation of photosynthesis across a broad thesis, and then discuss the underlying physiological and temperature range, CAM plants acclimated day and night biochemical mechanisms for temperature acclimation of photosynthetic process differentially to temperature, and photosynthesis in each photosynthetic type. Finally, we use C4 plants was adapted to warm environments. Moreover, within C3 species, evergreen woody plants and perennial herbaceous plants showed greater temperature homeostasis Electronic supplementary material The online version of this of photosynthesis (i.e., the photosynthetic rate at high- article (doi:10.1007/s11120-013-9874-6) contains supplementary material, which is available to authorized users. growth temperature divided by that at low-growth temperature was close to 1.0) than deciduous woody plants and W. Yamori (&) annual herbaceous plants, indicating that photosynthetic Center for Environment, Health and Field Sciences, acclimation would be particularly important in perennial, Chiba University, Kashiwa-no-ha 6-2-1, Kashiwa, Chiba 277-0882, Japan long-lived species that would experience a rise in growing e-mail: [email protected] season temperatures over their lifespan. Interestingly, across growth temperatures, the extent of temperature K. Hikosaka homeostasis of photosynthesis was maintained irrespective Graduate School of Life Sciences, Tohoku University, Aoba, Sendai 980-8578, Japan of the extent of the change in the optimum temperature for photosynthesis (Topt), indicating that some plants achieve K. Hikosaka greater photosynthesis at the growth temperature by shift- CREST, JST, Tokyo, Japan ing Topt, whereas others can also achieve greater photo- D. A. Way synthesis at the growth temperature by changing the shape Department of Biology, University of Western Ontario, of the photosynthesis–temperature curve without shifting London, ON, Canada Topt. It is considered that these differences in the inherent stability of temperature acclimation of photosynthesis D. A. Way Nicholas School of the Environment, Duke University, would be reflected by differences in the limiting steps of Durham, NC, USA photosynthetic rate. 123 Photosynth Res Keywords C3 photosynthesis Á C4 photosynthesis Á Read 1990; Cunningham and Read 2002), between cold CAM photosynthesis Á Phenotypic plasticity Á sensitive species and cold tolerant species (Yamori et al. Temperature acclimation Á Temperature adaptation 2010b), and even among ecotypes of the same species, depending on their original habitats (Bjo¨rkman et al. 1975; Pearcy 1977; Slatyer 1977). However, Campbell et al. (2007) found no difference in the level of temperature Introduction acclimation of photosynthesis among grasses, forbs, and woody plants. Thus, there is a discrepancy between studies Global climate change is resulting in increases in the daily, in the inherent ability for photosynthetic temperature seasonal, and annual mean temperatures experienced by acclimation between groups, and we need to understand plants. Moreover, climate change will increase the inten- this phenomenon to predict how changing temperatures sity, frequency, and duration of abnormally low and high will alter plant photosynthetic responses. temperatures (Wagner 1996; Tebaldi et al. 2006; Chris- In this review article, we first summarize the basic dif- tensen et al. 2007). Temperature limits plant growth and is ferences in photosynthetic reactions in C3,C4, and CAM also a major determining factor in the distribution of plants plants. Second, we show a typical, classic temperature across different environments (Mittler 2006). Since plants acclimation response of photosynthesis with the proposed cannot move from unfavorable to favorable temperature mechanisms underlying it. It is now possible to analyze conditions, the ability to withstand and/or acclimate to what process limits photosynthesis at various environ- environmental temperature variation is essential for plant mental conditions, based on well-tested models of photo- survival. Since photosynthesis has long been recognized as synthesis (Farquhar et al. 1980; von Caemmerer 2000). one of the most temperature-sensitive processes in plants, Moreover, developments of molecular biology and trans- understanding the physiological processes that underlie the genic technology have provided a set of powerful tools to temperature response of photosynthesis and its acclimation identify and then modify the limitations imposed on pho- is important to both agriculture and the environment. tosynthesis by the environment. Thus, we then consider the The temperature response of photosynthesis can be underlying physiological and biochemical mechanisms for described with a parabolic curve having an optimum tem- temperature acclimation of photosynthesis and discuss perature, and thus photosynthesis is inhibited at both low what process would be the limiting step of photosynthetic and high temperatures (Berry and Bjo¨rkman 1980). Most rate at various temperatures. Less research on photosyn- plants show considerable capacity to adjust their photo- thetic temperature responses has been done on CAM plants synthetic characteristics to their growth temperatures. The than C3 and C4 plants and differences in the temperature most typical phenomenon is a shift in the optimum tem- response of photosynthesis between day and night have not perature of photosynthesis as the growth temperature been clarified in CAM plants with diurnal photosynthetic changes or with seasonal temperature shifts, which allows patterns, although day and night temperatures vary con- the plant to increase photosynthetic efficiency at their new siderably in deserts where many CAM plants are found. growth temperature (Berry and Bjo¨rkman 1980; Yamori We therefore discuss the differences in temperature et al. 2005, 2006a, 2008, 2010b). From the desert to the responses of CO2 fixation rates at night and chloroplast arctic, plants also demonstrate extensive physiological and electron transport rates in the day in two CAM species biochemical adaptation to the large environmental range in grown at two different temperature regimes. Finally, we temperature. The inherent ability for temperature accli- evaluate the extent of photosynthetic temperature acclimation of photosynthesis can thus be expected to be dif- mation in higher plants from the pool of published data, ferent among plants utilizing differing photosynthetic and describe which plant types (i.e., photosynthetic types pathways [e.g., among C3,C4, and crassulacean acid and functional types) have the greatest inherent ability for metabolism (CAM) plants]. C4 plants are often associated photosynthetic acclimation to temperature. with relatively arid regions with high temperatures, such that C4 plants may have a greater ability for photosynthetic acclimation to high temperature than C3 plants (e.g., Photosynthetic reactions in C3,C4, and CAM plants Oberhuber and Edwards 1993; Kubien and Sage 2004; Osborne et al. 2008). Interestingly, even within C3 plants, C3 species represent approximately 85 % of all higher interspecific differences in temperature acclimation of plant species, C4 species account for about 5 %, and CAM photosynthesis have been observed. For example, the species make up the remaining 10 %. C4 plants are thought inherent ability for temperature acclimation of photosyn- to have originated in relatively arid regions, where high thesis appears to differ between temperate evergreen temperatures occur in combination with water stress, species and tropical evergreen species (Hill et al. 1988; whereas desert CAM plants are adapted to drought in arid 123 Photosynth Res regions, where day and night temperatures can show drastic high in C3 plants (Price et al. 1994). In the chloroplast, swings (although some CAM species occur in tropical Rubisco catalyzes the carboxylation of ribulose-1,5-bis- rainforests as epiphytes). Because of adaptation to their phosphate (RuBP) by CO2 and produces 3-phosphoglyceric respective growth conditions

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