REVIEW: Time lag between photosynthesis and carbon dioxide efflux from soil: a review of mechanisms and controls

CO2 efflux from soil depends on the availability of organic substances respired by roots and microorganisms. Therefore, photosynthetic activity supplying carbohydrates from leaves to roots and rhizosphere is a key driver of soil CO2. This fact has been overlooked in most soil CO2 studies because temperature variations are highly correlated with solar radiation and mask the direct effect of photosynthesis on substrate availability in soil. This review highlights the importance of photosynthesis for rhizosphere processes and evaluates the time lag between carbon (C) assimilation and CO2 release from soil. Mechanisms and processes contributing to the lag were evaluated. We compared the advantages and shortcomings of four main approaches used to estimate this time lag: (1) interruption of assimilate flow from leaves into the roots and rhizosphere, and analysis of the decrease of CO2 efflux from soil, (2) time series analysis (TSA) of CO2 fluxes from soil and photosynthesis proxies, (3) analysis of natural delta 13C variation in CO2 with photosynthesis-related parameters or delta 13C in the phloem and leaves, and (4) pulse labeling of plants in artificial 14CO(2) or 13CO(2) atmosphere with subsequent tracing of 14C or 13C in CO2 efflux from soil. We concluded that pulse labeling is the most advantageous approach. It allows clear evaluation not only of the time lag, but also of the label dynamics in soil CO2, and helps estimate the mean residence time of recently assimilated C in various above- and belowground C pools. The impossibility of tracing the phloem pressure-concentration waves by labeling approach may be overcome by its combination with approaches based on TSA of CO2 fluxes and its delta 13C with photosynthesis proxies. Numerous studies showed that the time lag for grasses is about 12.5 +/- 7.5 (SD) h. The time lag for mature trees was much longer (similar to 4-5 days). Tree height slightly affected the lag, with increasing delay of 0.1 day m-1. By evaluating bottle-neck processes responsible for the time lag, we conclude that, for trees, the transport of assimilates in phloem is the rate-limiting step. However, it was not possible to predict the lag based on the phloem transport rates reported in the literature. We conclude that studies of CO2 fluxes from soil, especially in ecosystems with a high contribution of root-derived CO2, should consider photosynthesis as one of the main drivers of C fluxes. This calls for incorporating photosynthesis in soil C turnover models.