Colin P. Osborne

Rising atmospheric CO ₂ concentrations are impacting the global terrestrial biosphere through indirect climate effects and direct effects on plant performance ^1–3 . In tropical forests, long-term monitoring indicates a substantial CO ₂ -driven carbon sink ⁴ . C ₄ -grass-dominated tropical and subtropical savannas contribute approximately 30% of terrestrial net primary production ⁵ , and yet equivalent long-term analyses of CO ₂ responses are lacking. Here we show a clear and consistent result across a meta-analysis of 70 CO ₂ -addition experiments and 32 years of in situ field observations from southern Africa: CO ₂ fertilization of wild C ₄ grasses is widespread in dry conditions. In experiments, grasses reduced stomatal conductance under higher levels of CO ₂ , limiting water loss while increasing carbon gain. In the field, improved water use efficiency translated into increased C ₄ grass biomass production across three decades of observations. Finally, simulations via the Community Land Model ⁶ suggest that CO ₂ fertilization of C ₄ grass aboveground productivity may continue to increase under future conditions. Together, these results challenge the view that C ₄ grasses are unresponsive to increasing levels of CO ₂ , demonstrating instead that annual aboveground production of grasses in the field in southern Africa has increased by 28% over three decades (a CO ₂ -driven increase of 75.1 g m ⁻² (95% confidence interval of 74.5–75.8 g m ⁻² ) or 0.37 tons C ha ⁻¹ of annual production). Although the fate of this carbon is uncertain (depending on feedbacks with fire, herbivory and woody vegetation), effects on the global carbon cycle may be profound.

Rising atmospheric CO ₂ is expected to have limited direct effects on C ₄ photosynthesis because the carbon‐concentrating mechanism maintains near‐saturating CO ₂ at Rubisco. Consequently, growth responses of C ₄ plants to elevated CO ₂ (eCO ₂ ) are generally attributed to indirect improvements in plant water relations. However, it remains unclear whether sustained exposure to eCO ₂ also induces changes in photosynthetic capacity that contribute directly to carbon gain. We examined the interactive effects of CO ₂ concentration and soil water availability on photosynthesis, biochemical capacity, and growth in three African C ₄ grasses grown under ambient (400 ppm) and elevated (550 ppm) CO ₂ . Elevated CO ₂ increased net photosynthesis across species, with stronger responses under drought. Intrinsic water‐use efficiency increased primarily through enhanced assimilation, while stomatal responses were contingent on water availability rather than driven directly by elevated CO ₂ . Importantly, eCO ₂ induced species‐ and context‐dependent increases in apparent photosynthetic capacity after prolonged treatment exposure. Megathyrsus maximus showed strong V _cmax increases under both water treatments and J _max upregulation under well‐watered conditions, Heteropogon contortus exhibited biochemical upregulation primarily under drought, and Themeda triandra showed little evidence of acclimation. Growth responses closely mirrored these physiological patterns, occurring only in species exhibiting coordinated biochemical adjustment. These results indicate that C ₄ responses to eCO ₂ cannot be explained solely by stomatal water saving and provide evidence that species‐specific changes in apparent photosynthetic capacity may contribute to sustained carbon gain, particularly under water limitation.

Afforestation schemes in savannas are increasingly promoted as a carbon storage strategy despite threats to biodiversity. We also lack a clear understanding of how trees and grasses differentially contribute to the major carbon store in savannas, that is, soil organic carbon (SOC) and its fractions. Because SOC fractions vary in their persistence, saturation potential, and vulnerability to loss, it is crucial to understand how shifts in tree cover and biomass will influence both the amount and stability of SOC, particularly under disturbance regimes and future climate scenarios such as rising atmospheric CO ₂ . Using an Open‐Top Chamber system, we examined the responses of five C ₃ leguminous savanna tree species and the C ₄ grass species Themeda triandra to grass‐tree competition under ambient (400 ppm) or elevated (550 ppm) atmospheric CO ₂ . We hypothesised that SOC increases will mostly depend on plant biomass rather than plant life form; and that CO ₂ fertilisation will benefit C ₃ savanna trees more than C ₄ grasses, leading to a loss in labile grass root exudates and thus the mineral‐associated organic carbon (MAOC) that depends on these exudates. We found that grasses, not trees, were associated with increased SOC in savanna soil to a depth of 0.3 m due to their relatively large biomass, regardless of CO ₂ concentration. Soil planted with both grass and trees had 10% more carbon and 8% more nitrogen compared to trees only. End‐member mixing models indicated that 50% to more than 90% of this carbon was grass‐derived. Savanna SOC accumulation occurred primarily through below‐ground and indirectly through aboveground biomass, which drove the formation of the occluded particulate organic carbon fraction (oPOC) according to a structural equation model. Similar results were observed for soil nitrogen. The responsiveness of oPOC (and not MAOC) in this savanna soil is different to temperate grassland soils, emphasising the need to understand savanna SOC dynamics. While recognising the limitations of pot culture, our results provide a clear message for policymakers and land managers: Conservation of grassy biomes such as savannas, and not afforestation, aligns with both climate and biodiversity goals. Read the free Plain Language Summary for this article on the Journal blog.

Summary: The evolution of C ₄ photosynthesis requires biochemical innovations to be coordinated with anatomical modifications. In many C ₄ species, CO ₂ is concentrated and fixed within leaf bundle sheath tissues, which are enlarged relative to other leaf tissues via cell expansion and the insertion of additional minor veins. In this study, we tested the hypothesis that anatomical adaptations for C ₄ photosynthetic carbon assimilation also improve plant–water relations. We measured leaf hydraulics and water retention characteristics in photosynthetically diverse populations of the grass Alloteropsis semialata . C ₄ individuals of Alloteropsis semialata had higher values of leaf capacitance and leaf hydraulic conductance than non‐C ₄ plants. Greater minor vein density contributed to higher values of leaf hydraulic conductance and less negative leaf water potential. Moreover, a greater ratio of bundle sheath area : leaf width and thicker leaves were associated with higher values of leaf capacitance and more negative turgor loss points in C ₄ plants. Further diversification of leaf water relations traits was related to secondary adaptations to climate and polyploid formation. These findings are consistent with the hypothesis that anatomical adaptations for C ₄ photosynthesis also improve plant–water relations in grasses and explain how C ₄ photosynthesis expanded the hydrological niche in this species.

Plants with amphitropical distributions have closely related populations in both Northern and Southern Hemispheres, but are absent from the intervening tropics. They provide a unique opportunity to study the constraints shaping the distribution of temperate lineages through time. Using grasses from the ecologically diverse supertribe Melicodae, an emerging study system with species distributed throughout the temperate regions, we test the hypothesis that geography and/or environmental niche constrain which lineages successfully cross the tropics to establish in the opposite hemisphere. Biogeographic and evolutionary modelling was conducted on well resolved plastid and nuclear phylogenies constructed from whole-genome sequencing of 178 accessions of 103 Melicodae species. Results show that species from cold regions are much less likely to successfully cross the tropics, with successful lineages all sharing warmer niches that evolved prior to their establishment in the opposite hemisphere. Evidence suggests that this result is explained both by the greater distances that high-latitude, cold-origin lineages must disperse to cross the tropics, and inherent limitations associated with colder thermal niches. In particular, our results suggest that traits allowing species to cope with cold winters, rather than an inability to cope with warm summers, limit their ability to establish in the opposite hemisphere, hinting at important trade-offs between cold-tolerance and biogeographic potential. These results provide insight into the drivers of the distribution and diversity of plants, and the challenges facing cold-origin lineages in a rapidly warming world. If cold-origin species occupy a smaller proportion of their potential range, and are unlikely to establish in new areas with suitable climates, their ability to track preferred habitat as climates warm may be worse than currently expected.

Societal Impact Statement: Understanding how plants evolve more efficient photosynthesis is important in a warming world where improving crop productivity and resilience is a global priority. By generating the first reference genomes for an early‐diverging group of grasses called the Aristidoideae, we were able to reconstruct the genetic makeup of the last common ancestor of all grasses that use C ₄ photosynthesis that is more efficient in hot climates. We show that early genetic changes in this lineage may have laid the groundwork for the later evolution of C ₄ photosynthesis. These findings help explain how complex biological innovations can repeatedly arise yet often remain restricted to particular evolutionary lineages. Summary: In grasses, almost all species belong to two evenly sized clades: BOP (Bambusoideae, Oryzoideae and Pooideae) and PACMAD (Panicoideae, Arundinoideae, Chloridoideae, Micrairoideae, Aristidoideae and Danthonioideae). Yet the >20 independent origins of C ₄ photosynthesis are confined to the PACMAD lineage. This pattern suggests that PACMAD grasses may harbour genetic features that primed them for the repeated evolution of this trait. To investigate this possibility, we examine gene turnover to identify genetic components that potentially facilitated the repeated evolution of C ₄ photosynthesis and were present at the base of the PACMAD clade, representing the last common ancestor of all C ₄ grasses. We generated the first reference genomes for Aristidoideae species ( Aristida adscensionis and Stipagrostis hirtigluma ), the sister lineage of all other PACMAD grasses. In combination with 34 other Poales genomes, we identify genes gained at the base of the PACMAD clade and genes lost in the sister BOP lineage. Gene expansion at the base of the PACMAD lineage includes one with a known C ₄ function (β‐carbonic anhydrase), as well as genes involved in amino acid and nitrate transport, carbon metabolism, oxidative stress management and transcription regulation. Gene turnover in the PACMAD stem lineage generated novel variation in the last common ancestor of all C ₄ grasses. Although this predates the emergence of C ₄ photosynthesis itself, these changes may have generated the genetic substrate and requirements for the repeated emergence of C ₄ photosynthesis in this clade.

Summary: As global temperatures and the severity of droughts continue to increase, food crops will more frequently experience high vapour pressure deficit (VPD) during heatwave events. However, the interactive effects of rising atmospheric CO ₂ and high‐VPD heatwaves on crop water fluxes and yields are currently unknown. We investigate stomatal, photosynthetic and productivity changes in wheat during simulated future high‐VPD heatwaves, under ambient (450 ppm) or elevated (720 ppm) CO ₂ concentrations, across four N‐fertiliser treatments. We measured the physiological response of abaxial and adaxial leaf surfaces to elevated CO ₂ concentration and/or high‐VPD heatwave exposure, and quantified drought responses, seasonal water usage and ear weight. Transpiration ( E ) and stomatal conductance ( g _sw ) increased during high‐VPD heatwaves (irrespective of CO ₂ concentration or N‐fertiliser), largely due to increased water fluxes from abaxial leaf surfaces. Higher E and water usage increased wheat vulnerability to drought and led to reduced total ear weight. High‐VPD heatwaves also hindered stomatal responses to light, with g _sw only reducing by 37–38% after 1 h of dark treatment. Our results show that wheat stomata are inhibited from closing under future high CO ₂ , high‐VPD heatwave conditions. This has considerable implications for future wheat water requirements, which in‐turn could significantly impact drought susceptibility and yield potential.