Internal recycling of respired CO₂ may be important for plant functioning under changing climate regimes

Abstract

Recent studies have provided evidence of a large flux of root-respired CO₂ in the transpiration stream of trees. In our study, we investigated the potential impact of this internal CO₂ transport on aboveground carbon assimilation and CO₂ efflux. To trace the transport of root-respired CO₂, we infused a ¹³C label at the stem base of field-grown Populus deltoides Bartr. ex. Marsh trees. The ¹³C label was transported to the top of the stem and throughout the crown via the transpiration stream. Up to 17% of the ¹³C label was assimilated by chlorophyll-containing tissues. Our results provide evidence of a mechanism for recycling respired CO₂ within trees. Such a mechanism may have important implications for how plants cope with predicted increases in intensity and frequency of droughts. Here, we speculate on the potential significance of this recycling mechanism within the context of plant responses to climate change and plants currently inhabiting arid environments.

In forest ecosystems, soil CO₂ efflux is the second-largest carbon flux after photosynthesis.^1,2,3 Thirty to 88% of ecosystem CO₂ efflux diffuses from the soil surface into the atmosphere and is a combination of CO₂ from respiring autotrophic (roots and associated microorganisms) and heterotrophic (decomposition of soil organic matter) sources. Conventional measurements use soil CO₂ efflux as a proxy for belowground respiration in forests according to the long-standing paradigm that all root-respired CO₂ diffuses radially from roots into the soil environment and then from the soil to the atmosphere.^4,5,6,7 Recently, Aubrey and Teskey⁹ showed that efflux-based measurements of soil respiration underestimated the contribution of belowground autotrophic respiration. Based on simultaneous measurements of CO₂ efflux from the soil and the upward transport of respired CO₂ in xylem, they found that half of the root-respired CO₂ remained within the root system of Populus deltoides Bartr. ex. Marsh. trees and was transported upwards with the transpiration stream.⁹ High CO₂ concentrations ([CO₂]) in the xylem (range < 1 to over 26%) and transport of respired CO₂ in the transpiration stream were previously reported.⁸ However, Aubrey and Teskey⁷ were the first to demonstrate experimentally that a substantial amount of this internal CO₂ was derived belowground, indicating that standard soil efflux-based estimates of root respiration are inadequate.

Our study was designed to investigate the fate of root-respired CO₂ that is transported upwards with the transpiration stream.⁹ We infused a dissolved ¹³C label at 2 concentrations into the stem base of field-grown 7-y-old Populus deltoides Bartr. ex. Marsh. trees to trace the path of root-respired CO₂ entering the above-ground portion of the tree. We originally intended to label the roots directly, but there were few roots near the soil surface, and when we supplied these with the ¹³CO₂ label it was insufficient to provide the stem with the quantity of label needed to trace the movement of CO₂ throughout the aboveground portion of the tree. After label infusion, trees were harvested for isotope analysis of stem, branch, and leaf tissues. Our findings showed that CO₂ infused at the base of the stem was transported upward throughout the tree, where a portion (17%) was assimilated in both woody (stem and branch) and leaf tissues. However, most of the CO₂ (83%) diffused out of the stem and branches. The highest enrichment levels in the woody organs were found in the inner bark, whereas petioles were the most enriched part of the leaves. When scaled for biomass, the largest quantity of infused ¹³C was assimilated in the living tissues of the xylem and in the mesophyll of the leaves. Previous studies have demonstrated that leaves and chlorophyll-containing woody tissues have the capacity to assimilate xylem-transported CO₂.^10,11,12 Our results suggest that assimilation of xylem-transported CO₂ might substantially reduce the respiratory carbon loss. Moreover, these assimilates might be loaded into the phloem stream and distributed to other parts of the tree, where they could serve as substrate for tissue synthesis or new respiratory processes.

We speculate that under predicted future climate conditions, with increased atmospheric [CO₂] as well as increased intensity and frequency of drought, the internal mechanism for recycling respired CO₂ in plants may become more important. At higher atmospheric [CO₂], a larger quantity of carbon will be allocated belowground,^13,14,15 thereby increasing root proliferation and the overall respiratory release of CO₂ in the root system. Thus, a larger amount of root-respired CO₂ is likely to be available for internal transport, potentially leading to a higher rate of internal recycling by woody and leaf tissues.

Other factors affect the amount of root-respired CO₂ that is transported into the stem and subsequently available as substrate for internal recycling, including the structure of the root network, tree species,^16,17 and environmental conditions that affect rates of sap flow and respiration and the solubility of CO₂. For example, it is likely that the portion of root-respired CO₂ that was internally transported into the stem in Populus deltoides observed by Aubrey and Teskey⁷ (50%) may be a high estimate relative to other species, as this species is characterized by high transpiration rates and high xylem sap pH, which induces a larger amount of respired CO₂ to dissolve in the transpiration stream.¹⁸

In leaves, stomatal closure is among the earliest responses to drought, impacting leaf photosynthesis¹⁹ by limiting the uptake of atmospheric CO₂. In addition, under severe drought, CO₂ assimilation becomes biochemically limited.¹⁹ In contrast, woody tissue photosynthesis can be supplied with CO₂ endogenously by respiration^20,21 with no associated water loss. Therefore, woody tissue photosynthesis is expected to be less sensitive to water deficit than leaf photosynthesis²² and thus it may function as means of improving carbon balance and intrinsic water use efficiency (i.e., ratio of net photosynthetic assimilation to transpiration). Under severe drought, trees will often shed their leaves long before the branches and stem reach irreversible dehydration. In such circumstances, woody tissues can still assimilate carbon. Although reduced sap flow resulting from stomatal closure or leaf shed will limit the amount of root-respired CO₂ that is transported upward in the stem, CO₂ substrate will be available for woody tissue photosynthesis as long as the branches and stem continue to respire, even if prolonged drought reduces maintenance respiration.²³ Thus, internal recycling of xylem-transported CO₂ can be considered a component of plant adaptations to cope with drought. Assimilation of CO₂ in xylary chloroplasts of woody tissues might also be important for maintaining xylem hydraulic conductivity in plants during periods of drought stress, as observed recently for mangrove species.²⁴ Sugars synthesized by these chloroplasts potentially supply the necessary energy for vessel refilling²⁵ or are used as a trigger for a biological response to xylem embolism.²⁶

The internal transport and re-assimilation of root-respired CO₂ is likely an integral part of maintaining the carbon balance of plants growing in arid environments. Compared with temperate species, these plants have limited leaf area, which increases the potential importance of woody tissue photosynthesis. Moreover, due to the minimal leaf canopy of these plants, light incidence is higher on the branches and stems, further enhancing the capacity for woody tissue photosynthesis. In CAM plants, the temporal separation between CO₂ uptake and fixation in small vestigial leaves and succulent stems is a well-known adaptation to desert climatic conditions.²² In plants that have persisted in arid environments but lack CAM photosynthesis, internal recycling of respired CO₂ might serve a similar function as an important mechanism to maintain a positive carbon balance.

In conclusion, assimilation of respired CO₂ by woody and leaf tissues might improve the overall carbon budget of plants, especially under changing climate regimes that favor belowground carbon allocation and increased root respiration (e.g., increased atmospheric [CO₂]) or reduce water availability and gas exchange (e.g., increased intensity and frequency of droughts). Under current climate conditions, non-temperate drought-adapted desert species already depend on the re-assimilation of respired CO₂ in woody tissues for a considerable fraction of their carbon supply,^22,27,28 and this source of carbon could become increasingly important for non-drought-adapted species as well under future conditions. However, we still lack a detailed picture of the role of assimilation of internally derived CO₂ for plant functioning, particularly during periods of environmental stress. Hence, assimilation of respired CO₂ in plants should be included in the array of ecophysiological measurements to improve our understanding of plant responses to changing climate regimes.

Bloemen J, McGuire MA, Aubrey DP, Teskey RO, Steppe K. Transport of root-respired CO₂ via the transpiration stream affects aboveground carbon assimilation and CO₂ efflux in trees. New Phytol. 2013;197:555–65. doi: 10.1111/j.1469-8137.2012.04366.x.