Photosynthetic responses to altitude: an explanation based on optimality principles

Forum Letter Photosynthetic responses to altitude: an explanation based on optimality principles Introduction Ecophysiologists have long been fascinated by the photosynthetic behaviour of alpine plants, which often have to withstand extreme environmental pressures (Gale, 1972; Friend & Woodward, 1990; K€ orner, 2003, 2007; Shi et al., 2006). About 8% of the world’s land surface is above 1500 m altitude (K€ orner, 2007). High altitudes can be climatically unusual, often with (for example) low temperatures, strong winds, and now high rates of warming (K€ orner, 2003; Pepin & Lundquist, 2008; Rangwala & Miller, 2012). Moreover, the low atmospheric pressure provides a set of environmental conditions unique on Earth (Table 1). There has been extensive speculation about altitudinal effects on photosynthesis and, in particular, how to account for the puzzling – but consistently observed – tendencies towards higher carbon dioxide (CO 2 ) drawdown (low ratio of leaf- internal to ambient CO 2 partial pressures (c i :c a ; hereafter, v), resulting in low carbon isotope discrimination) and higher carboxylation capacity (V cmax ) with increasing altitude (Gale, 1972; K€ orner & Diemer, 1987; Friend et al., 1989; Terashima et al., 1995; Bresson et al., 2009; Zhu et al., 2010). At first glance, it might be expected that CO 2 assimilation rates would be reduced at high altitudes due to the low partial pressure of CO 2 (Friend & Woodward, 1990). However, actual measured photosynthetic rates are usually as high as, or even higher than, those at low altitudes (M€ achler & N€ osberger, 1977; K€ orner & Diemer, 1987; Cordell et al., 1999; Shi et al., 2006). One group of hypotheses that attempt to explain the effects of altitude on photosynthetic physiology focuses on the effects of low temperature. It has been argued that alpine plants possess thick leaves as an adaptation to low temperatures, and thus higher leaf nitrogen on an area basis (N area ). Higher N area is taken to imply higher V cmax , in turn leading to higher CO 2 drawdown due to higher photosynthetic rates (Woodward, 1979; K€ orner & Diemer, 1987; Friend et al., 1989; Sparks & Ehleringer, 1997). This reasoning assumes that higher N area in thicker leaves would be associated with higher V cmax , but this is not necessarily so, as a substantial fraction of leaf nitrogen (N) in thick leaves (with low specific leaf area) is located in cell walls rather than in chloroplasts (Onoda et al., 2004). An alternative argument, from the perspec- tive of carbon isotope discrimination, suggests that increased leaf thickness could lengthen the diffusional pathway for CO 2 from the atmosphere to the site of carboxylation, and therefore potentially O 2016 The Authors New Phytologist O 2016 New Phytologist Trust decrease v (Vitousek et al., 1990). However, low air pressure would be expected to counteract this effect, by allowing CO 2 to diffuse more readily through the stomata (Table 1). In any case, no hypothesis based on temperature effects can account for the difference in plant responses to altitudinal and latitudinal gradients, i.e. why the same adaptations in photosyn- thetic capacity observed on high mountains are not observed in polar regions where growing-season temperatures are also low (Billings et al., 1961; Mooney & Billings, 1961; Billings & Mooney, 1968; Chabot et al., 1972; Zhu et al., 2010). It is moreover worth noting that although low temperatures can depress photosynthesis, measured growing-season leaf temperatures and optimal temperatures for photosynthesis in both alpine and arctic plants are typically only reduced by a few degrees, in contrast with a much larger decline in air temperature with altitude or latitude (K€ orner & Diemer, 1987; K€ orner, 2007). The dense canopy structure and crowded leaf arrangement on stems of cushion and prostrate alpine plants create a low boundary-layer conductance and thus allow the maintenance of large differences between the temperatures of leaves and air (Gauslaa, 1984; K€ orner, 2003; Michaletz et al., 2015). The effect of such morphological adapta- tions is superimposed on the universal tendency, rooted in the fundamentals of leaf energy balance, for leaf temperatures to be maintained in a narrower range than air temperatures (Campbell & Norman, 1998; Michaletz et al., 2015). A further group of hypotheses suggests that low atmospheric pressure might influence photosynthesis through more direct physiological influences, independently of temperature (Decker, 1959; Billings et al., 1961; Mooney & Billings, 1961). However, despite much previous speculation, and the fact that many biophysical quantities relevant to gas exchange are known to change with air pressure and leaf temperature in a predictable manner (Table 1), effects of those biophysical quantities on plant physiology have not been fully explored. Misconceptions abound in the literature. For example, alpine plants were predicted to be more sensitive to the decreased CO 2 concentration (molar mixing ratio) in the Quaternary glacial periods simply because the CO 2 partial pressure at high altitudes is low (Street-Perrott et al., 1997). This is incorrect, however, because the partial pressure of O 2 is also reduced at high altitudes – implying a reduced photorespiratory burden which counteracts the effect of CO 2 concentration on photosynthesis, as previously noted for example by K€ orner et al. (1991) and Terashima et al. (1995). ‘First-principles’ hypotheses on photosynthetic behaviour Natural selection implies that plants optimize ecophysiological traits by regulating the allocation of resources to different functions. This principle leads to the least-cost hypothesis and the coordination New Phytologist (2016) 1 www.newphytologist.com