C₄photosynthesis and climate through the lens of optimality

Abstract

1 CO 2 , temperature, water availability and light intensity were all potential selective pressures to 2 propel the initial evolution and global expansion of C 4 photosynthesis over the last 30 million 3 years. To tease apart how the primary selective pressures varied along this evolutionary 4 trajectory, we coupled photosynthesis and hydraulics models while optimizing photosynthesis 5 over stomatal resistance and leaf/fine-root allocation. We further examined the importance of 6 resource (e.g. nitrogen) reallocation from the dark to the light reactions during and after the 7 initial formation of C 4 syndrome. We show here that the primary selective pressures-all acting 8 upon photorespiration in C 3 progenitors-changed through the course of C 4 evolution. The 9higher stomatal resistance and leaf-to-root allocation ratio enabled by the C 4 10 carbon-concentrating mechanism led to a C 4 advantage without any change in hydraulic 11properties, but selection on nitrogen reallocation varied. Water limitation was the primary driver 12 for the initial evolution of C 4 25-32 million years ago, and could positively select for C 4 13 evolution with atmospheric CO 2 as high as 600 ppm. Under these high CO 2 conditions, nitrogen 14 reallocation was necessary. Low CO 2 and light intensity, but not nitrogen reallocation, were the 15 primary drivers during the global radiation of C 4 5-10 MYA. Finally, our results suggest that 16 identifying the predominate selective pressures at the time C 4 first evolved within a lineage 17 should help explain current biogeographical distributions. 18

The legacy of C4evolution in the hydraulics of C3and C4grasses

“…CO2 generally decreased through this period. Water limitation drove the earliest origin of C4 30 MYA (Christin et al 2008, Zhou et al 2018) and there was a more intense selective pressure for water transport safety, which led to higher decrease of Kleaf in older lineages; however, the role played by water limitation was weakened and replaced by low CO2 and high light as the CO2 decreased with the multiple C4 origins around 5-8 MYA (Zhou et al 2018).…”

“…We used our mechanism-based physiological model from Zhou et al (2018) to consider how the evolution of higher Kleaf would affect the optimal gs and photosynthesis in C3 and C4 plants. An increase in Kleaf in the C3 ancestor selects for higher gs and increases the steady-state leaf water potential to a limited extent ( Fig.…”

“…Furthermore, we used physiological models that couples the photosynthesis systems and hydraulic systems to predict the effect of changing Kleaf on assimilation rate (Zhou et al, 2018). The change of Kleaf was assumed to change the plant hydraulic conductance (Kplant) proportionally in the modeling process.…”

Optimal coordination and reorganization of photosynthetic properties in C4grasses

“…Although Jmax/Vcmax has been empirically measured in numerous C3 species (Wullschleger, 1993) and optimal Jmax/Vcmax has been modeled for C3 (Walker et al, 2014;Kromdijk and Long, 2016;Quebbeman and Ramirez, 2016), there have been few measurements in C4, and we are not aware of any theoretical optimality predictions. For C4 species, the assimilation rate would be mostly limited by the light reactions (Baker and Long, 1988;Pearcy and Ehleringer, 1984;Collatz et al, 2992) and there would be a redundancy in RuBP carboxylation if a C3-like Jmax/Vcmax was maintained (Zhou et al, 2018). Furthermore, Zhou et al (2018) showed that if nitrogen is reallocated from the CB cycle to the light reactions, which results in a higher Jmax/Vcmax, C4 assimilation rates will increase significantly in almost all environmental conditions.…”

“…For C4 species, the assimilation rate would be mostly limited by the light reactions (Baker and Long, 1988;Pearcy and Ehleringer, 1984;Collatz et al, 2992) and there would be a redundancy in RuBP carboxylation if a C3-like Jmax/Vcmax was maintained (Zhou et al, 2018). Furthermore, Zhou et al (2018) showed that if nitrogen is reallocated from the CB cycle to the light reactions, which results in a higher Jmax/Vcmax, C4 assimilation rates will increase significantly in almost all environmental conditions. In C3 plants, Jmax/Vcmax should vary along with different environmental factors (temperature, CO2, light, and water availability; Onoda et al, 2005;Rodriguez-Calcerrada et al, 2008;Kromdijk and Long, 2016;, and we expect the same for C4.…”