The largest terrestrial organic carbon pool, carbon in soils, is regulated by an intricate connection between plant carbon inputs, microbial activity, and the soil matrix. This is manifested by how microorganisms, the key players in transforming plant-derived carbon into soil organic carbon, are controlled by the physical arrangement of organic and inorganic soil particles. Here we conduct an incubation of isotopically labelled litter to study effects of soil structure on the fate of litter-derived organic matter. While microbial activity and fungal growth is enhanced in the coarser-textured soil, we show that occlusion of organic matter into aggregates and formation of organo-mineral associations occur concurrently on fresh litter surfaces regardless of soil structure. These two mechanisms—the two most prominent processes contributing to the persistence of organic matter—occur directly at plant–soil interfaces, where surfaces of litter constitute a nucleus in the build-up of soil carbon persistence. We extend the notion of plant litter, i.e., particulate organic matter, from solely an easily available and labile carbon substrate, to a functional component at which persistence of soil carbon is directly determined.

Plant roots are major transmitters of atmospheric carbon into soil. The rhizosphere, the soil volume around living roots influenced by root activities, represents hotspots for organic carbon (OC) inputs, microbial activity, and carbon turnover. Rhizosphere processes remain poorly understood and the observation of key mechanisms for carbon transfer and protection in intact rhizosphere microenvironments are challenging. We deciphered the fate of photosynthesis-derived OC in intact wheat rhizosphere, combining stable isotope labeling at field scale with high-resolution 3D-imaging. We used nano-scale secondary ion mass spectrometry and focus ion beam-scanning electron microscopy to generate insights into rhizosphere processes at nanometer scale. In immature wheat roots, the carbon circulated through the apoplastic pathway, via cell walls, from the stele to the cortex. The carbon was transferred to substantial microbial communuties, mainly represented by bacteria surrounding peripheral root cells. Iron oxides formed bridges between roots and bigger mineral particles, such as quartz, and surrounded bacteria in microaggregates close to the root surface. Some microaggregates were also intimately associated with the fungal hyphae surface. Based on these results, we propose a conceptual model depicting the fate of carbon at biogeochemical interfaces in the rhizosphere, at the forefront of growing roots. We observed complex interplays between vectors (roots, fungi, bacteria), transferring plant-derived OC into root-free soil and stabilizing agents (iron oxides, root and microorganism products), potentially protecting plant-derived OC within microaggregates in the rhizosphere.

Earthworms play a major role in litter decomposition, in processing soil organic matter and driving soil structure formation. Earthworm casts represent hot spots for carbon turnover and formation of biogeochemical interfaces in soils. Due to the complex microscale architecture of casts, understanding the mechanisms of cast formation and development at a process relevant scale, i.e., within microaggregates and at the interface between plant residues, microorganisms and mineral particles, remains challenging. We used stable isotope enrichment to trace the fate of shoot and root litter in intact earthworm cast samples. Surface casts produced by epi-anecic earthworms (Lumbricus terrestris) were collected after 8 and 54 weeks of soil incubation in mesocosms, in the presence of ¹³C-labeled Ryegrass shoot or root litter deposited onto the soil surface. To study the alteration in the chemical composition from initial litter to particulate organic matter (POM) and mineral-associated organic matter (MOM) in cast samples, we used solid-state ¹³C Nuclear Magnetic Resonance spectroscopy (¹³C-CPMAS-NMR) and isotopic ratio mass spectrometry (EA-IRMS). We used spectromicroscopic approach to identify plant tissues and microorganisms involved in plant decomposition within casts. A combination of transmission electron microscopy (TEM) and nano-scale secondary ion mass spectrometry (NanoSIMS) was used to obtain the distribution of organic carbon and δ¹³C within intact cast sample structures. We clearly demonstrate a different fate of shoot- and root-derived organic carbon in earthworm casts, with a higher abundance of less degraded root residues recovered as particulate organic matter on the short-term (8 weeks) (73 mg·g⁻¹ in Cast-Root vs. 44 mg·g⁻¹ in Cast-Shoot). At the early stages of litter decomposition, the chemical composition of the initial litter was the main factor controlling the composition and distribution of soil organic matter within casts. At later stages, we can demonstrate a clear reduction of structural and chemical differences in root and shoot-derived organic products. After 1 year, MOM clearly dominated the casts (more than 85% of the total OC in the MOM fraction). We were able to highlight the shift from a system dominated by free plant residues to a system dominated by MOM during cast formation and development.

Summary: Biophysicochemical rhizosheath properties play a vital role in plant drought adaptation. However, their integration into the framework of plant drought response is hampered by incomplete mechanistic understanding of their drought responsiveness and unknown linkage to intraspecific plant–soil drought reactions. Thirty‐eight Zea mays varieties were grown under well‐watered and drought conditions to assess the drought responsiveness of rhizosheath properties, such as soil aggregation, rhizosheath mass, net‐rhizodeposition, and soil organic carbon distribution. Additionally, explanatory traits, including functional plant trait adaptations and changes in soil enzyme activities, were measured. Drought restricted soil structure formation in the rhizosheath and shifted plant–carbon from litter‐derived organic matter in macroaggregates to microbially processed compounds in microaggregates. Variety‐specific functional trait modifications determined variations in rhizosheath drought responsiveness. Drought responses of the plant–soil system ranged among varieties from maintaining plant–microbial interactions in the rhizosheath through accumulation of rhizodeposits, to preserving rhizosheath soil structure while increasing soil exploration through enhanced root elongation. Drought‐induced alterations at the root–soil interface may hold crucial implications for ecosystem resilience in a changing climate. Our findings highlight that rhizosheath soil properties are an intrinsic component of plant drought response, emphasizing the need for a holistic concept of plant–soil systems in future research on plant drought adaptation.

A holistic understanding of plant strategies to acquire soil resources is pivotal in achieving sustainable food security. However, we lack knowledge about variety‐specific root and rhizosphere traits for resource acquisition, their plasticity and adaptation to drought. We conducted a greenhouse experiment to phenotype root and rhizosphere traits (mean root diameter [Root D], specific root length [SRL], root tissue density, root nitrogen content, specific rhizosheath mass [SRM], arbuscular mycorrhizal fungi [AMF] colonization) of 16 landraces and 22 modern cultivars of temperate maize (Zea mays L.). Our results demonstrate that landraces and modern cultivars diverge in their root and rhizosphere traits. Although landraces follow a ‘do‐it‐yourself’ strategy with high SRLs, modern cultivars exhibit an ‘outsourcing’ strategy with increased mean Root Ds and a tendency towards increased root colonization by AMF. We further identified that SRM indicates an ‘outsourcing’ strategy. Additionally, landraces were more drought‐responsive compared to modern cultivars based on multitrait response indices. We suggest that breeding leads to distinct resource acquisition strategies between temperate maize varieties. Future breeding efforts should increasingly target root and rhizosphere economics, with SRM serving as a valuable proxy for identifying varieties employing an outsourcing resource acquisition strategy.