Up to half of the photosynthate produced by plants may be transported to belowground organs (Högberg and Högberg 2002; Pausch and Kuzyakov 2018), depending on environmental conditions. Much of it is used for root growth and maintenance or is stored, but 10-44% of photosynthetically fixed carbon is excreted by roots or transferred to mycorrhizal fungi (Bais et al. 2006; Pausch & Kuzyakov 2018). The C exuded from roots or from associated mycorrhizal fungi supports a large component of the soil biota, including invertebrates as well as micro-organisms (Pollierer et al. 2007; Drigo et al. 2008, Yarwood et al. 2009). Half or more of the soil activity in forests may be driven by photosynthate that is transported to mycorrhizal fungi and root-associated microbes within a few days of being fixed (Högberg et al. 2008). Why do trees export so much photosynthate to the belowground ecosystem?
The amount and proportion of fixed C transported belowground is related to the relative availabilities of C versus growth-limiting resources (N, P or water). In forests with high nutrient availability, a greater proportion of the photosynthates produced annually is used for plant biomass production, compared with forests with low nutrient availability (58% vs 42% in a synthesis of 49 forests; Vicca et al. 2012). In the loblolly pine stand at the Duke free-air CO2 enrichment (FACE) experiment, elevated CO2 conditions led to increases in total belowground C flux, root production, biomass and respiration, exudation and fungal allocation, microbial biomass, heterotrophic respiration and soil CO2 efflux (Drake et al. 2011). Belowground C flux in both ambient and elevated CO2 plots was much lower where soil N availability was increased through N fertilization (Drake et al. 2011). Other FACE experiments have reported that in forests where growth is nutrient-limited, elevated CO2 increases photosynthesis rates, but not tree growth, and the additional fixed C is respired and released back to the atmosphere, primarily from belowground organs (Körner et al. 2005; Reich et al. 2014; Ellsworth et al. 2017; Jiang et al. 2020).
In boreal pine forests, aboveground productivity is strongly limited by N and about 50% of tree photosynthate is transferred belowground and respired from the soil (Högberg and Högberg 2002). Nitrogen additions to a boreal pine forest reduced the flux of tree photosynthate to roots and soil biota, including ectomycorrhizal (ECM) fungi, by as much as 60% (Högberg et al. 2010). Belowground C flux returned to pre-fertilization levels after N additions ceased, coincident with increased abundance of mycorrhizal fungi (Högberg et al. 2011). Belowground C flux (as a proportion of gross primary productivity, GPP) also increases under conditions of high light (Smith and Reynolds 2015), elevated CO2 (Jackson et al. 2009; Drake et al. 2011) or reduced availability of P (Keith et al. 1997) or water (Stape et al. 2008; Preece & Peñuelas 2016; Hasibeder et al. 2015; Ledo et al. 2018). These observations are consistent with the amount of plant C transported belowground being strongly influenced by the need to remove surplus fixed C from plant leaves. Indeed, the rapid (1-day) link between GPP and respiration from roots and mycorrhizal fungi in forests prompted Heinemeyer et al. (2007) to propose that the mycorrhizal CO2 flux component represents an overflow ‘CO2 tap’ through which surplus plant carbon can be returned directly to the atmosphere.
A strong seasonal pattern of photosynthate fluxes in boreal pine forests was also noted by Högberg et al. (2010). Belowground flux of photosynthate in August was 500% greater than that in June. They attributed this to developing leaves being a sink for fixed C early in the growing season (Horwath et al. 1994; Kagawa et al. 2006). Once leaves had fully expanded, much of the fixed C was translocated belowground, much of it to mycorrhizal fungi. Sporocarp production of ECM fungi was totally dependent on allocation of recent photosynthate in the late season. This late-summer flux of surplus photosynthate may underly the autumn peak in sporocarp production in boreal forests. Sporocarp production by mycorrhizal fungi may therefore function as an alternate sink for surplus carbohydrates once leaf expansion is complete.
Living stumps and carbon sharing among living trees
Leafless tree stumps, which are nevertheless ‘alive’ in the sense that they respire, have been observed in many forests. These stumps have a living root system, which is connected to that of other trees through root grafts and/or mycorrhizal fungal hyphae. These connections give them access to carbohydrates from the root systems of living trees, which sustains the remaining tissues of the leafless tree (Bader & Leuzinger 2019). Evolutionary rationales for the living plants investing carbohydrates in non-photosynthesizing neighbors are challenging, but it has been suggested that the stumps provide an extended root system for mechanical stability and uptake of water and nutrients (Bormann 1966, Keeley 1988, but see Loehl and Jones 1990). Alternatively, living stumps may result from surplus carbohydrates from living trees traveling to them through the phloem of connected roots, driven by the difference in hydrostatic pressure provided by phloem unloading and respiration in the surviving tissues of the stump tree.
Transfer of carbohydrates among living trees through root grafts (Fraser et al. 2006) or mycorrhizal fungi (Simard et al. 1997; Klein et al. 2016) have received considerable attention. Carbon fluxes have been traced from source trees growing in full light to sink trees growing in low light conditions (Fraser et al. 2006; Teste et al. 2009). The adaptive ‘purpose’ of the transfers through common mycorrhizal networks has been explained through kin selection processes, as neighboring trees have a high probability of being related (Gorzelak et al. 2015). Alternatively, these fluxes may represent the movement of plant surplus carbohydrates along pressure gradients through roots and fungal hyphae driven by phloem loading in source trees and phloem unloading in sink trees. The source plant benefits from the removal of surplus photo-assimilates and prevention of consequent physiological dysfunction, regardless of the relatedness of the sink plant.
Roots of plants growing under conditions of low P availability often exude more carboxylates, especially organic anions such as citrate and malate (Lambers et al. 2013; 2011). In the rhizosphere, carboxylates compete with inorganic and organic P for binding sites which increases the availability of P for plant uptake (Lambers et al. 2011). Release of carboxylates is therefore widely considered to be part of a P-acquisition strategy that allows plants to survive in low-P environments (Lambers et al. 2006, 2010). However, several observations are inconsistent with this interpretation, such as increased carboxylate exudation at low N availability (Zhu et al. 2016) and inconsistent relationships between rates of carboxylate release and both P uptake and plant growth (Huang et al. 2017; He et al. 2021; Wang and Lambers 2020). Carboxylate exudation by roots of alfalfa (Medicago sativa) growing in an alkaline soil low in both N and P was studied by He et al. (2020, 2021). Root exudation of carboxylates (particularly tartrate) decreased with increasing P availability but also increased exponentially with increasing shoot N concentration. The closer association of root carboxylate release with N than with P concentration prompted He et al. (2021) to suggest that N addition resulted in increased production of photosynthates, which could not be used for primary metabolism and growth due to the lack of P, and so were discharged as carboxylates.
Metabolite profiling of root exudates (as well as of shoots and roots) of P-deficient and P-sufficient plants also supports the hypothesis that root exudates can be a means of removing surplus metabolites. Relative to P-sufficient soybean plants, root exudates of P-deficient plants had higher concentrations of TCA cycle intermediates and amino acids, and lower concentrations of phosphate esters (Tawaraya et al. 2014). Shoot and root extracts of P-deficient plants also had low levels of P-containing metabolites such as adenosine 5’-monophosphate and glycerol 3-phosphate and elevated concentrations of adenine, cytosine and adenosine, reflecting inhibition of nucleotide synthesis induced by P starvation. Remobilization of P from phosphate esters is common in P-deficient plants (Tawaraya et al. 2014). The higher concentrations of TCA cycle intermediates such as organic acids in root exudates from P-deficient plants may be a consequence of their accumulation in root cells as surplus metabolites. Plants exposed to very low P supply have very low concentrations of Pi and ADP which restricts the cytochrome pathway and causes TCA-cycle intermediates such as organic acids – especially citrate – to accumulate (Selinski et al. 2018). Increased carbon supply for organic acid synthesis in the TCA cycle in P-deficient roots has been demonstrated through transcriptome (Wasaki et al. 2003; Li et al. 2010) and proteome (Fukuda et al. 2007) analysis; this would lead to higher concentrations of organic acids in P-deficient roots (Tawaraya et al. 2014). Therefore, a primary function of organic acid exudation may be the disposal of surplus metabolites. Particular morphological and physiological traits such as releasing carboxylates in exudative bursts from specialized structures such as cluster roots or dauciform roots are more probably adaptations for P acquisition (Lambers et al. 2006).