Decoupling of stomatal and mesophyll recovery drives photosynthetic resilience to water deficit in sugar beet: evidence from multiscale structural and functional traits

Water deficit severely constrains sugar beet productivity by impairing photosynthetic capacity. However, the underlying structure-function mechanisms conferring photosynthetic resilience remain poorly characterised. This study investigates the temporal dynamics of photosynthetic limitations and structural adaptations in sugar beet during water deficit and subsequent rehydration. We found that water deficit significantly reduced the maximum net CO2 assimilation rate (ANmax) and the Rubisco carboxylation rate (Vcmax) by impairing CO2 diffusion and biochemical processes. The reduction in photosynthetic capacity is primarily and stably attributed to mesophyll limitation, while contributions from stomatal and biochemical limitations flexibly change with deficit degree and rehydration. Severe water deficit caused irreversible structural damage that hinders recovery even after rehydration, while moderate water deficit allows partial restoration of leaf and chloroplast function. Partial least squares structural equation modelling (PLS-SEM) demonstrated that CO2 diffusion was governed by the volume fraction of intercellular air space (fias, β = 0.28) and surface areas of the chloroplasts exposed to leaf intercellular air spaces (Sc/S, β = 0.35), with Sc/S indirectly influencing mesophyll conductance (gm) through fias mediation (β = 0.53). Severe water deficit caused irreversible fias reduction and chloroplast interface damage (59% cell volume loss). These findings establish that resilience to water deficit in sugar beet depends on mesophyll structural integrity, with fias and Sc/S as key modulators of gm recovery. The study advances understanding of stress recovery mechanisms in sugar beet and provides a framework for multiscale crop improvement in the context of climate change.