Introduction

Plant-soil microbial carbon (C) “trade” at root and soil interface (i.e. rhizosphere) is incrementally receiving research attention within the disciplines of plant and soil sciences (Prescott et al., 2020; Wang et al., 2022). Reasons for this emerging hot topic lie in the fact that C allocation to rhizosphere is considered as the “currency” of trading for other resources but comes at the expense of reducing C for shoot growth (Hartmann et al., 2020). For instance, some estimates suggest that plants allocate nearly one-third of photosynthetic assimilates belowground with the proportion varying substantially among plant species and experimental/environmental conditions (Pausch & Kuzyakov, 2018). Therefore, rhizospheric C trading is a fundamental ecological process for plants optimizing belowground nutrient acquisition versus aboveground biomass yield, which is usually interpreted at the angles of plant C-nutrient economics or tradeoffs in C allocation between above- and belowground components (Kong & Fridley, 2019; Ledo et al., 2018).

Specifically, the traded C is mainly used to elongate plant roots, prime soil microorganisms, and maintain symbiosis between plants and soil mycorrhizas (Wang et al., 2022). Therefore, rhizosphere C-nutrient exchanges are plant strategies to upregulate nutrient-acquisition efficiencies, thereafter, adapting to nutrient-poor or resource-fluctuating environments (Raven et al., 2018). Rhizodeposit C, as an integral part of rhizospheric C trading, is mainly exudated in soils via fine roots after transporting photosynthates downwards (Villarino et al., 2021). Rhizodeposits fuel soil microbial turnover to destabilize soil organic matter and at the same time accelerate nutrient release for plant growth (Dijkstra et al., 2021). This underlies the current consensus of regarding rhizodeposit C as a pivot linking above- and belowground C cycling pathways. A substantial proportion of belowground allocated C (over 30%) is mineralized into CO₂ during short periods of time via pathways of root respiration, rhizodeposit decomposition, and mycorrhizal fungal respiration (Han et al., 2021; Pausch & Kuzyakov, 2018; Wang, Bicharanloo, et al., 2021). The rest of C remains in the ecosystem in relatively longer terms in the form of root biomass, rhizodeposits, and fungal biomass or necromass (Wang, Cavagnaro, et al., 2021). The above-mentioned rhizodeposit cycling processes are largely sketched in greenhouse studies with most of them being precisely controlled and viable for the collection and measurement of rhizodeposits (Hao et al., 2022; Semchenko et al., 2021; Wang, Bicharanloo, et al., 2021; Wang, Cavagnaro, et al., 2021). However, challenges are still formidable in upscaling the results from laboratory studies to ecosystems (Chen et al., 2023). Nevertheless, it remains largely elusive for both laboratory and field studies in terms of how newly incorporated soil C from rhizodeposits would be stabilized in the soil.

A Conceptual Framework of Rhizodeposit C Stabilization

In this review, we proposed a conceptual framework synthesizing the current knowledge to anticipate the possible stabilizing pathways of the belowground allocated C as rhizodeposits (Figure 1). Mounting evidence has proved that treating soil organic matter as a single and uniform entity would impede our broader scope and deeper understanding in C stabilization mechanisms (Lavallee et al., 2020). Therefore, this framework mostly emphasized key processes of C incorporation and stabilization in two fundamentally and differently conceptualized soil fractions, that is, formation of mineral-associated organic matter (MAOM) and C integration into microaggreagtes.

Figure 1.

Rhizodeposited carbon (C) is an essential plant investment strategy for taking up soil nutrients, because it can be used to prime soil microorganism, maintain plant-mycorrhizal symbionts, and elongate plant roots. Some of the rhizodeposited C can also remain in the soil in a short term via forming particulate organic matter (POM) and in a long term as mineral-associated organic matter (MAOM) or encapsulated in microaggregates. Vertical arrow represents the direction of carbon (downward and red) and nutrient flow (upward and blue).

Note. AMF = arbuscular mycorrhizal fungi.

As a complex of soil inorganics and organic matter, MAOM is resistant to microbial attack due to the strong chemical bond between organic matter and minerals or occlusion within micropores (Lavallee et al., 2020). Given the fact that MAOM averagely shows a lower C:nitrogen (N) ratio, it is primarily considered as an organic matter fraction of microbial origin from ex vivo modification and in vivo transformation of plant- and microbial-derived C (Bai & Cotrufo, 2022). Moreover, it is pervasively evidenced that rhizodeposits exhibit a high MAOM formation efficiency (46%, Villarino et al., 2021). This is because low-molecular-weight C compounds from rhizodeposition, such as sugars and amino acids, are more accessible to microbial in vivo transformations as compared to structural compounds from plant litter (Villarino et al., 2021). Currently, if the transformation efficiency of rhizodeposits is greater than that of plant residues still lacks a holistic evaluation across different ecosystem types with various environmental conditions.

Soil microaggregates are widely known to physically protect organic matter via limiting microbial proliferation and activity (Wang et al., 2020). Indeed, microaggregates are proved to possess smaller pore sizes and lower rates of water and oxygen diffusion (Totsche et al., 2018). Consequently, microbial activity and organic C turnover rates are strongly restricted in microaggregates. In this context, tracking the processes of photosynthetic C to be adsorbed by soil minerals and to be encapsulated within microaggregates are crucial for understanding the C flow from plant photosynthesis to soils and therefore evaluating soil potential of C sequestration. However, studies on this C flow from rhizodeposition to soil aggregates are conducted sporadically and thereby give a limited view of the C dynamics in soil microsites.

Exploring the Fate of Rhizodeposits With ¹³C Tracing Techniques

Stable carbon isotope (namely ¹³C) is a powerful tracer to depict the fate of photosynthates in plant and soil components (Chomel et al., 2022). Both continuous and pulse labeling using ¹³CO₂ are sensitive, precise, and practical approaches to achieve this C-tracing goal but in different ways (Figure 2; Liu et al., 2019). Continuous ¹³CO₂ labeling approach is capable of labeling plant materials homogenously by exposing plants in a ¹³CO₂-enriched condition for a long time from days to years (Pang et al., 2021). This approach can determine rhizodeposition rates approximately by quantifying how much photosynthetic C allocated to soils and respired as CO₂ during a given period (Pausch & Kuzyakov, 2018). However, pulse labeling feeds plants with ¹³CO₂ from minutes to hours via injecting the tracer gas in an air-tight chamber (Figure 2; Pang et al., 2021). This technique can only deliver the information of plant C allocation patterns, such as the proportions of photosynthates translocated to roots and soils or mineralized into CO₂ via root and soil respiration (Wang, Bicharanloo, et al., 2021). Therefore, studies using pulse labeling approach treated CO₂ efflux from rhizodeposition decomposition as a proxy for rhizodeposition rates (Bicharanloo et al., 2022; Wang, Bicharanloo, et al., 2021). Of course, this assumes that rhizodeposition rate is linearly proportional to its decomposition rates. Irrespective of labeling techniques, the way to separate different C sources is constrained to two-source isotopic mixing models. Moreover, the use of these quantifying methods requires to implement the measurements in a relatively short time scale from days to weeks. This principle is set to avoid any significant plant C inputs through root turnover or aboveground biomass abscission and decomposition (Wang, Cavagnaro, et al., 2021). Nevertheless, to outline the essential pathway of plant C flowing into soils via rhizodeposition, isotopic techniques of ¹³C tracing, either continuous or pulse labeling, as followed by the calculations with isotopic two-source mixing models (see Wang, Bicharanloo, et al., 2021) are vastly needed.

Figure 2.

Continuous or pulse ¹³CO₂ labeling of plants in an air-tight chamber (i.e. the box at the top). Plants photosynthesize ¹³CO₂ and allocate ¹³C-labeled carbohydrates belowground to roots (i.e. the box at the bottom). Respired rhizodeposit C can be roughly used to represent rhizodeposition rate. However, residual rhizodeposit C in the soil would form labile (e.g. particulate organic C) and recalcitrant C fractions, for example, encapsulated in mineral-associated organic matter (MAOM) or microaggreagtes.

After ¹³C-labeled photosynthate deposited into the soil, separation of MAOM from particulate organic matter and consecutive ¹³C measurements could help delineate the C flow and stabilization from plants to soils (Dijkstra et al., 2021). Similarly, quantifying the ¹³C recovery across aggregate size classes with isotopic mass balance equations (see Wang, Cavagnaro, et al., 2021) can illustrate integration of photosynthate C among soil particles with different capability of physical C protection (Wang et al., 2020). According to the soil aggregate hierarchy hypothesis (Totsche et al., 2018), the absolute amount and proportion of ¹³C distributed in microaggreagtes somewhat show the degree of physical protection of newly secreted C from roots. Particle size fractionation of the ¹³C-labeled soils can simply follow the widely-used standard protocols, which are fractionation by size (53 µm) after full soil dispersion for POM versus MAOM (sensu Cotrufo et al., 2019) and wet sieving for soil aggregates (Six et al., 2000). Overall, quantification of ¹³C allocation in MOAM and microaggregates are undoubtedly the central key to unlock how much C from this shoot-root-soil flow pathway will be stabilized.

Conclusion

Considerable efforts and progresses have already made toward understanding the role of rhizodeposit carbon in promoting plant nutrient acquisition. Currently, a major challenge is to probe the stabilization mechanisms of rhizodeposits in order to formulating management practices for sequestering and preserving plant-derived carbon in soils. By systematically synthesizing current knowns and unknowns, we proposed a conceptual framework on the fate of rhizodeposits in forming mineral-associated organic matter or encapsulating into microaggregates. We also underscored continuous or pulse ¹³CO₂ labeling techniques to be powerful approaches to tackle the unknowns in terms of the fate of rhizodeposits.