Balancing trade-offs: Enhanced carbon assimilation and productivity with reduced nutritional value in a well-watered C4 pasture under a warmer CO2-enriched atmosphere.

The concentration of atmospheric CO2 and temperature are pivotal components of ecosystem productivity, carbon balance, and food security. In this study, we investigated the impacts of a warmer climate (+2 °C above ambient temperature) and an atmosphere enriched with CO2 (600 ppm) on gas exchange, antioxidant enzymatic system, growth, nutritive value, and digestibility of a well-watered, managed pasture of Megathyrsus maximus, a tropical C4 forage grass, under field conditions. Elevated [CO2] (eC) improved photosynthesis and reduced stomatal conductance, resulting in increased water use efficiency and plant C content. Under eC, stem biomass production increased without a corresponding increase in leaf biomass, leading to a smaller leaf/stem ratio. Additionally, eC had negative impacts on forage nutritive value and digestibility. Elevated temperature (eT) increased photosynthetic gains, as well as stem and leaf biomass production. However, it reduced P and K concentration, forage nutritive value, and digestibility. Under the combined conditions of eC and eT (eCeT), eT completely offset the effects of eC on the leaf/stem ratio. However, eT intensified the effects of eC on photosynthesis, leaf C concentration, biomass accumulation, and nutritive value. This resulted in a forage with 12% more acid detergent fiber content and 28% more lignin. Additionally, there was a decrease of 19% in crude protein leading to a 15% decrease in forage digestibility. These changes could potentially affect animal feeding efficiency and feedback climate change, as ruminants may experience an amplification in methane emissions. Our results highlight the critical significance of conducting multifactorial field studies when evaluating plant responses to climate change variables.

Adjustments in photosynthetic pigments, PS II photochemistry and photoprotection in a tropical C4 forage plant exposed to warming and elevated [CO2].

Global climate change will impact crops and grasslands, affecting growth and yield. However, is not clear how the combination of warming and increased atmospheric carbon dioxide concentrations ([CO2]) will affect the photosystem II (PSII) photochemistry and the photosynthetic tissue photoinhibition and photoprotection on tropical forages. Here, we evaluated the effects of elevated [CO2] (∼600 µmol mol-1) and warming (+2 °C increase temperature) on the photochemistry of photosystem II and the photoprotection strategies of a tropical C4 forage Panicum maximum Jacq. grown in a Trop-T-FACE facility under well-watered conditions without nutrient limitation. Analysis of the maximum photochemical efficiency of PSII (Fv/Fm), the effective PSII quantum yield Y(II), the quantum yield of regulated energy dissipation Y(NPQ), the quantum yield of non-regulated energy dissipation Y(NO), and the malondialdehyde (MDA) contents in leaves revealed that the photosynthetic apparatus of plants did not suffer photoinhibitory damage, and plants did not increase lipid peroxidation in response to warming and [CO2] enrichment. Plants under warming treatment showed a 12% higher chlorophyll contents and a 58% decrease in α-tocopherol contents. In contrast, carotenoid composition (zeaxanthin and ß-carotene) and ascorbate levels were not altered by elevated [CO2] and warming. The elevated temperature increased both net photosynthesis rate and aboveground biomass but elevated [CO2] increased only net photosynthesis. Adjustments in chlorophyll, de-epoxidation state of the xanthophylls cycle, and tocopherol contents suggest leaves of P. maximum can acclimate to 2 °C warmer temperature and elevated [CO2] when plants are grown with enough water and nutrients during tropical autumn-winter season.

Warming offsets the benefits of elevated CO2 in water relations while amplifies elevated CO2-induced reduction in forage nutritional value in the C4 grass Megathyrsus maximus.

Tropical grasslands are very important to global carbon and water cycles. C4 plants have increased heat tolerance and a CO2 concentrating mechanism that often reduces responses to elevated concentrations of CO2 ([CO2]). Despite the importance of tropical grasslands, there is a scarcity of studies that elucidate how managed tropical grasslands will be affected by elevated [CO2] and warming. In our study, we used a combination of a temperature-free air-controlled enhancement (T-FACE) and a free-air carbon dioxide enrichment (FACE) systems to increase canopy temperature and [CO2] under field conditions, respectively. We warmed a field-grown pasture dominated by the C4 tropical forage grass Megathyrsus maximus by 2°C above ambient under two levels of [CO2] (ambient (aC) and elevated (eC - 600 ppm) to investigate how these two factors isolated or combined regulate water relations through stomatal regulation, and how this combination affects PSII functioning, biochemistry, forage nutritive value, and digestibility. We demonstrated that the effects of warming negated the effects of eC in plant transpiration, water potential, proline content, and soil moisture conservation, resulting in warming canceling the eCO2-induced improvement in these parameters. Furthermore, there were additive effects between eC and warming for chlorophyll fluorescence parameters and aboveground nutritive value. Warming sharply intensified the eCO2-induced decrease in crude protein content and increases in forage fibrous fraction and lignin, resulting in a smaller forage digestibility under a warmer CO2-enriched atmosphere. Our results highlight the importance of multifactorial studies when investigating global change impacts on managed ecosystems and the potential consequences for the global carbon cycle like amplification in methane emissions by ruminants and feeding a positive climate feedback system.

Future warming will change the chemical composition and leaf blade structure of tropical C3 and C4 forage species depending on soil moisture levels.

Temperature and soil moisture strongly affect the nutritional value and digestibility of forage plants through changes in leaf chemical composition or the proportion of leaf blade tissues. In this study, we aimed to evaluate leaf blade anatomical modifications of two tropical forage species, Stylosanthes capitata (C3) and Megathyrsus maximus (C4) under warmed conditions (+2 °C) at well-watered and rainfed conditions and investigate the interactions between leaf anatomical alterations, leaf chemical composition, and leaf digestibility. Experiments were conducted under field conditions using a Temperature-free air-controlled enhancement (T-FACE) system. We observed that plants under elevated temperature produced leaves with smaller stomata and thinner mesophyll tissue and reduced total leaf thickness, potentially impacting gas exchange. On the other hand, reduced soil moisture increased stomatal density and thickness of the adaxial epidermis. In both species, leaf fibrous fractions concentration increased under warmed and non-irrigated conditions, while crude protein concentration and digestibility decreased. However, leaf digestibility was associated with leaf chemical composition rather than the proportion of different leaf blade tissues. We concluded that although both species developed leaf anatomical modifications to acclimate under future warming conditions, leaf nutritional value and digestibility will be reduced, potentially impacting future livestock production and methane emissions by ruminants.

Morpho-physiological performance of Mikania glomerata Spreng. and Mikania laevigata Sch. Bip ex Baker plants under different light conditions / Desempenho morfo-fisiológico de Mikania glomerata Spreng. e Mikania laevigata Sch. Bip ex Baker sob diferentes condições de luminosidade

In tropical and subtropical zones, lianas play important roles in the process of ecological succession. This study aims to evaluate the photosynthetic and morpho-physiological performance between two lianas species from Mikania genus in response to different levels of radiation: full sun (I0), 25% (I25), 50% (I50), and 75% (I75) retention of solar radiation flux. Plants grown under I75 showed a reduced net photosynthetic rate (A). We observed dynamic photoinhibition at I0 during hours of high irradiation and temperature. The highest and lowest leaf chlorophyll content occurred at I75 and I0, respectively, while carotenoids/total chlorophyll and leaf thickness increased under I0. Total dry mass was higher in plants grown at I0 and I25. However, A values and biomass production of Mikania laevigata were higher at I25, while for Mikania glomerata greater biomass accumulation was observed between I0-I50. Therefore, we concluded that M. laevigata and M. glomerata have different morpho-physiological performances under same the radiation conditions.

Em regiões tropical e subtropical, lianas desempenham um papel importante no processo de sucessão ecológica. O objetivo deste estudo foi avaliar as respostas fotossintéticas e morfo-fisiológicas entre duas espécies de Mikania em diferentes níveis de radiação: sol pleno (I0), 25% (I25), 50% (I50) e 75% (I75) de retenção do fluxo da radiação solar. Plantas crescidas sob I75 mostraram reduzida taxa fotossintética (A). Nós observamos fotoinibição dinâmica em plantas crescidas sob I0 durante as horas de alta irradiação e temperatura. O maior e menor conteúdo de clorofila ocorreu em plantas sob I75 e I0, respectivamente; enquanto carotenoides/clorofila total e espessuras da epiderme e mesofilo aumentaram sob I0. A massa seca total foi maior em plantas crescidas sob I0 e I25. No entanto, os valores de A e a produção de biomassa de M. laevigata foram maiores sob I25; enquanto para M. glomerata, maior acúmulo de biomassa foi observado entre I0-I50. Portanto, nós concluímos que M. laevigata e M. glomerata apresentaram diferentes respostas morfo-fisiológicas sob mesma condição de radiação.

Correction: Increasing atmospheric CO2 and canopy temperature induces anatomical and physiological changes in leaves of the C4 forage species Panicum maximum.

[This corrects the article DOI: 10.1371/journal.pone.0212506.].

Stomatal Development and Conductance of a Tropical Forage Legume Are Regulated by Elevated [CO2] Under Moderate Warming.

The opening and closing of stomata are controlled by the integration of environmental and endogenous signals. Here, we show the effects of combining elevated atmospheric carbon dioxide concentration (eCO 2; 600 µmol mol-1) and warming (+2°C) on stomatal properties and their consequence to plant function in a Stylosanthes capitata Vogel (C3) tropical pasture. The eCO 2 treatment alone reduced stomatal density, stomatal index, and stomatal conductance (gs ), resulting in reduced transpiration, increased leaf temperature, and leading to maintenance of soil moisture during the growing season. Increased CO2 concentration inside leaves stimulated photosynthesis, starch content levels, water use efficiency, and PSII photochemistry. Under warming, plants developed leaves with smaller stomata on both leaf surfaces; however, we did not see effects of warming on stomatal conductance, transpiration, or leaf water status. Warming alone enhanced PSII photochemistry and photosynthesis, and likely starch exports from chloroplasts. Under the combination of warming and eCO 2, leaf temperature was higher than that of leaves from the warming or eCO 2 treatments. Thus, warming counterbalanced the effects of CO2 on transpiration and soil water content but not on stomatal functioning, which was independent of temperature treatment. Under warming, and in combination with eCO 2, leaves also produced more carotenoids and a more efficient heat and fluorescence dissipation. Our combined results suggest that control on stomatal opening under eCO 2 was not changed by a warmer environment; however, their combination significantly improved whole-plant functioning.

Increasing atmospheric CO2 and canopy temperature induces anatomical and physiological changes in leaves of the C4 forage species Panicum maximum.

Changes in leaf anatomy and ultrastructure are associated with physiological performance in the context of plant adaptations to climate change. In this study, we investigated the isolated and combined effects of elevated atmospheric CO2 concentration ([CO2]) up to 600 µmol mol-1 (eC) and elevated temperature (eT) to 2°C more than the ambient canopy temperature on the ultrastructure, leaf anatomy, and physiology of Panicum maximum Jacq. grown under field conditions using combined free-air carbon dioxide enrichment (FACE) and temperature free-air controlled enhancement (T-FACE) systems. Plants grown under eC showed reduced stomatal density, stomatal index, stomatal conductance (gs), and leaf transpiration rate (E), increased soil-water content (SWC) conservation and adaxial epidermis thickness were also observed. The net photosynthesis rate (A) and intrinsic water-use efficiency (iWUE) were enhanced by 25% and 71%, respectively, with a concomitant increase in the size of starch grains in bundle sheath cells. Under air warming, we observed an increase in the thickness of the adaxial cuticle and a decrease in the leaf thickness, size of vascular bundles and bulliform cells, and starch content. Under eCeT, air warming offset the eC effects on SWC and E, and no interactions between [CO2] and temperature for leaf anatomy were observed. Elevated [CO2] exerted more effects on external characteristics, such as the epidermis anatomy and leaf gas exchange, while air warming affected mainly the leaf structure. We conclude that differential anatomical and physiological adjustments contributed to the acclimation of P. maximum growing under elevated [CO2] and air warming, improving the leaf biomass production under these conditions.

Warming and water deficit impact leaf photosynthesis and decrease forage quality and digestibility of a C4 tropical grass.

Global warming is predicted to cause more intense extreme events such as heat waves, flooding and severe droughts, producing significant effects on agriculture. In tropics, climate change will severely impact livestock production affecting water availability, forage quality and food for cattle. We investigated the isolated and combined effects of soil water deficit (wS) and + 2°C increase in canopy temperature (eT) on leaf gas exchange, chlorophyll fluorescence, carbohydrate content, forage quality and in vitro dry matter digestibility (IVDMD) of a field-grown C4 tropical forage grass Panicum maximum Jacq. using a temperature-free air-controlled enhancement (T-FACE) system. The wS and eT treatments showed no effects on photosystem II photochemistry. However, wS under ambient temperature decreased net photosynthesis rate (A), stomatal conductance (gs ) and maximum rate of carboxylation of Rubisco (Vcmax ), leading to a reduced starch content in leaves. A 16% reduction in leaf dry mass (LDM) and reduction in forage quality by increasing fibers, reducing crude protein (CP) and decreasing the IVDMD was also observed by effect of wS. Warming under adequate soil moisture (eT) significantly increased LDM by 25% but reduced the forage quality, increasing the lignin content and reducing starch, CP and digestibility. The combined wSeT treatment reduced A, gs , Vcmax and the forage quality. When compared to control, the lignin content in leaves increased by 43, 28 and 17% in wS, eT and wSeT, respectively, causing a significant reduction in IVDMD. We concluded that despite physiological mechanisms to acclimate to warming, both warming and water deficit will impair the quality and digestibility of C4 tropical pastures.