Photosynthetic limitations in two Antarctic vascular plants: importance of leaf anatomical traits and Rubisco kinetic parameters

Abstract

Particular physiological traits allow the vascular plants Deschampsia antarctica Desv. and Colobanthus quitensis (Kunth) Bartl. to inhabit Antarctica. The photosynthetic performance of these species was evaluated in situ, focusing on diffusive and biochemical constraints to CO2 assimilation. Leaf gas exchange, Chl a fluorescence, leaf ultrastructure, and Rubisco catalytic properties were examined in plants growing on King George and Lagotellerie islands. In spite of the species- and population-specific effects of the measurement temperature on the main photosynthetic parameters, CO2 assimilation was highly limited by CO2 diffusion. In particular, the mesophyll conductance (gm)-estimated from both gas exchange and leaf chlorophyll fluorescence and modeled from leaf anatomy-was remarkably low, restricting CO2 diffusion and imposing the strongest constraint to CO2 acquisition. Rubisco presented a high specificity for CO2 as determined in vitro, suggesting a tight co-ordination between CO2 diffusion and leaf biochemistry that may be critical ultimately to optimize carbon balance in these species. Interestingly, both anatomical and biochemical traits resembled those described in plants from arid environments, providing a new insight into plant functional acclimation to extreme conditions. Understanding what actually limits photosynthesis in these species is important to anticipate their responses to the ongoing and predicted rapid warming in the Antarctic Peninsula.

Keywords: Antarctic plants; Rubisco; leaf traits; mesophyll conductance; photosynthesis; temperature.

Fig. 1.

The Antarctic continent (A), Antarctic Peninsula (B, inset from A), South Shetland Islands, and area of the Antarctic Peninsula (C, inset from B). Vascular plants from 62° to 67° South latitude, including the two study areas represented by an asterisk (*): King George Island (62°09'S, 58°28ʹW) and Lagotellerie Island (67°53ʹ20ʺS, 67°25ʹ30ʺW), Marguerite Bay (modified from Alberdi et al., 2002).

Fig. 2.

Diurnal course of photosynthetically active radiation (A), air temperature (B), and leaf temperature in D. antarctica (C) and C. quitensis (D) in King George (KGI) and Lagotellerie Island (LAG) between 17 and 22 January 17 2015. Values are means ± SE

Fig. 3.

The net photosynthetic CO₂ assimilation rate (A_N) and dark respiration (R_dark) of D. antarctica (A, C) and C. quitensis (B, D) in King George (KGI) and Lagotellerie Island (LAG), measured at 10 °C (white bars) or 15 °C (gray bars). Values are means ± SE (n=5–7). Different letters indicate statistically significant differences for each species between populations and measurement temperature according to Tukey (P<0.05).

Fig. 4.

The stomatal (A, B) and the leaf mesophyll (C, D) conductances, and the maximum rate of Rubisco carboxylation (E, F) of D. antarctica (left) and C. quitensis (right) in King George (KGI) and Lagotellerie Island (LAG), measured at 10 °C (white bars) or 15 °C (gray bars). Values are means ± SE (n=5–7). Different letters indicate statistically significant differences between populations for each species and measurement temperature according to Tukey (P<0.05).

Fig. 5.

The relationship of (A) the total leaf conductance (g_tot), (B) the leaf mesophyll conductance (g_m), and (C) the chloroplast CO₂ concentration (C_c) to the net photosynthetic CO₂ assimilation rate (A_N) of D. antarctica (open circles) and C. quitensis (filled circles) in King George (KGI) and Lagotellerie Island (LAG). Goodness of fit with a saturation model is shown for both species and considering all populations and measurement temperatures together. Values are means ± SE (n=5–7).

Fig. 6.

Correlations of the leaf mesophyll conductance modeled with anatomical parameters (g_m modeled) with the mesophyll (S_m/S) and chloroplast (S_c/S) surface area facing intercellular air spaces per leaf area in D. antarctica (left) and C. quitensis (right). The Pearson correlation coefficient and the significance of the relationship are shown for each species considering both populations together. Values are means ± SE (n=3–5).

Fig. 7.

The ratio of the electron transport rate and gross photosynthesis (ETR/A_G) for D. antarctica (A) and C. quitensis (B) in King George (KGI) and Lagotellerie Island (LAG), measured at 10 °C (white bars) or 15 °C (gray bars). Values are means ± SE (n=5–7). Different letters indicate statistically significant differences for each species between populations and measurement temperatures according to Tukey (P<0.05).