The Timing of Soil Hydraulic Constraints Shapes Plant Drought Responses

As soils dry, soil hydraulic conductivity (Ks) declines nonlinearly and can become a dominant bottleneck to root water uptake, constraining plant gas exchange. Although drought regulation involves both physiological and structural mechanisms, it remains unclear how these mechanisms differ between plants exposed to drought during early development versus at later developmental stage, and how soil texture and its hydraulic behavior shape regulation of soil–plant water relations. The objective of this study was to resolve how the timing of drought exposure reorganizes regulation of the soil–plant–atmosphere continuum (SPAC). Specifically, we aimed to (i) compare drought imposed from early vs at late developmental stage in terms of their reliance on physiological versus structural mechanisms of water-use regulation, and (ii) assess how soil texture and hydraulic trajectories condition these mechanisms.

We addressed these objectives using a controlled phenotyping experiment with six maize genotypes (three landraces and three hybrids) grown in contrasting soil textures (sandy loam and silt loam). Drought was imposed either continuously from the onset of growth or at later stage of plant development. Whole-plant transpiration, plant and soil water potentials, and above- and belowground structural traits were quantified to resolve SPAC regulation under contrasting drought timings.

Across soils and genotypes, transpiration declined to comparable fractions of its maximum within a narrow range of Ks, despite large differences in soil water content (θ) and matric potential (Ψsoil) between sandy loam and silt loam, this identifies Ks rather than θ or Ψsoil as the dominant physical control governing transpiration downregulation. Additionally, SPAC regulation differed strongly with drought timing. Under drought, imposed from early development, plants primarily reduced whole-plant water use through structural downscaling, characterized by reduced shoot area and increased root-to-shoot ratios, while maintaining relatively high transpiration rates per unit leaf area. In contrast, plants exposed to drought at later stage retained larger shoot area but reduced transpiration predominantly through strong stomatal regulation, resulting in lower transpiration rates per unit leaf area at comparable Ks and xylem water potential.

Belowground responses mirrored these contrasting strategies. Drought from onset promoted coordinated structural adjustment, including higher total root length, finer mean root diameters, and enhanced rhizosheath formation relative to late drought. These traits increased effective uptake surface area and were associated with higher soil–plant hydraulic conductance under low Ks. Across soils, high-performing plants converged on a common belowground trait syndrome, characterized by high total root length, fine roots, and enhanced rhizosheath formation, although the genotypes expressing this syndrome differed between soil textures.

Overall, our findings show that drought responsiveness emerges from the interaction between the soil’s hydraulic limit and its timing during development. Accounting for the temporal dynamics of hydraulic constraint, rather than treating drought as a static stress, providing a mechanistic framework to link soil texture, plant traits, and genotypic performance, with implications for targeted breeding and improved crop resilience under increasing climate extremes.