C₄ savanna grasses fail to maintain assimilation in drying soil under low CO₂ compared with C₃ trees despite lower leaf water demand

Abstract

C4 photosynthesis evolved when grasses migrated out of contracting forests under a declining atmospheric CO2 concentration ([CO2]a) and drying climate around 30 million years ago. C4 grasses are hypothesised to benefit from improved plant–water relations in open habitats such as savannas, giving advantages over C3 plants under low [CO2]a. But experimental evidence in a low CO2 environment is limited, and comparisons with C3 trees are needed to understand savanna vegetation patterns. To test whether stomatal conductance (gS) and CO2 assimilation (A) are maintained in drier soil for C4 grasses than C3 trees, particularly under low [CO2]a, we investigated photosynthesis and plant–water relations of three C3 tree and three C4 grass species grown at 800, 400 or 200 ppm [CO2]a over moderate wetting–drying cycles. C4 grasses had a lower soil‐to‐leaf water potential gradient than C3 trees, especially at 200 ppm [CO2]a, indicating reduced leaf water demand relative to supply. Yet the dependence of gS and A on predawn leaf water potential (a measure of soil water availability) was greater for the C4 grasses than trees, particularly under low [CO2]a. Our findings establish that gS and A are not maintained in drier soil for C4 grasses compared with C3 trees, suggesting that this mechanism was not prevailing in the expansion of C4‐dominated grasslands under low [CO2]a. This inherent susceptibility to sudden decreases in soil water availability justifies why C4 grasses have not evolved a resistant xylem allowing operation under drought, but instead shut down below a water potential threshold and rapidly recover. We point to this capacity to respond to transient water availability as a key overlooked driver of C4 grass success under low [CO2]a. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13240/suppinfo is available for this article.

Response of photosynthesis, growth and water relations of a savannah-adapted tree and grass grown across high to low CO2

“…4B). We have recently shown that decreasing soil water availability impinges on assimilation relatively more for C 4 grasses than for C 3 trees (Quirk et al, 2018). However, in monoculture stands like our pots, higher WUE for C 4 grasses confers soil water savings, allowing stomata to remain open and extending the duration of assimilation.…”

“…Moreover, grass stomata respond faster than tree stomata (Franks and Farquhar, 2007;McAusland et al, 2016) and many grasses, including Eragrostis, can further regulate transpiration through leaf rolling (Kipchirchir et al, 2015). Fast-closing stomata and leaf rolling are important competitive attributes in the persistence of grass cover through their effects on soil water savings where water is periodically limiting (Quirk et al, 2018). Yet, as these advantages are related to grass leaf architecture and hydraulic traits, and are independent of photosynthetic type, C 3 grasses may become increasingly competitive under future [CO 2 ] a , particularly if rainfall is limiting and thicker woody canopies create increasingly shaded habitats unfavourable for C 4 grasses (Polley et al, 1993(Polley et al, , 2002Ibrahim et al, 2008).…”

“…When atmospheric CO 2 concentration ([CO 2 ] a ) is low, leaf temperatures are above 25-30 °C and water is limiting, photorespiration can completely offset carbon fixation, impairing growth and making C 3 plants increasingly reliant on stored carbon to fuel basic metabolism (Walker et al, 2016). Demand for stored carbon is greatest under low [CO 2 ] a and when stomata close to reduce water losses, thereby reducing CO 2 assimilation (A) (Hartmann et al, 2013;Mitchell et al, 2013;Quirk et al, 2013Quirk et al, , 2018.…”

A leaf‐level biochemical model simulating the introduction of C2 and C4 photosynthesis in C3 rice: gains, losses and metabolite fluxes

“…There were striking differences in stomatal conductance, which was c. 40% less in C 4 than in C 3 under a PPFD of 1500 μmol m −2 s −1 and a C a of 400 μmol mol −1 (Fig. c), indicating that the same amount of A was achieved with lower transpiration and higher water‐use efficiency (WUE), in line with differences between extant C 3 and C 4 species (Bellasio et al ., ; Quirk et al ., ) although in the field there is some negative feedback on the effect on WUE because of temperature changes. The same differences were maintained in the simulated A/C i curves (Fig.…”

“…There is a growing body of data gained under controlled conditions (e.g. Bellasio et al, 2018;Quirk et al, 2018) and in free air experiments (e.g. Bishop et al, 2015), yet responses are species-specific and, currently, evidence is not sufficient to generalize the acclimation responses of C 4 and C 3 plants.…”