Hydraulic architecture traits influence the co-optimization of efficiency and safety in cycads

As a present-day relict lineage, cycads possess key anatomical traits for understanding the evolution of plant hydraulics; however, how their hydraulic architecture influences the co-optimization of hydraulic safety and efficiency under drought remains unclear. We examined rachis cross-sectional anatomy traits in 20 cycad species and analyzed correlations between hydraulic construction design, tissue fractions, tissue connectivity, and hydraulic function. Additionally, we quantified the distance of cycads from the global hydraulic safety-efficiency trade-off boundary line (LBD) and assessed anatomical contributions to this distance. We found that cycad rachises resembled fern rhizomes, in that most histological and architectural traits did not correlate with embolism vulnerability, except that greater architectural dissection increased vulnerability at the water potential corresponding to 88% embolism. Cycads with higher conduit lumen fractions (Flx) and conduit-phloem connectivity (Ccphl), and lower conduit-parenchyma connectivity (Ccpar), exhibited greater embolism resistance. Notably, cycads showed a longer LBD compared with ferns, noncycad gymnosperms, and angiosperms, and this distance was shortened by larger pit membrane area and fraction and by higher phloem fraction and Flx. Species in Cycadaceae and Zamiaceae exhibited distinct hydraulic architectures. Cycadaceae species, which typically occupy wetter habitats, showed higher Flx and Ccphl, whereas Zamiaceae species from more arid habitats exhibited greater architectural dissection, higher conduit wall fractions (Fwx) and higher Ccpar. These differences reflect contrasting ecological strategies underlying cycad adaptation to divergent environments. Our findings demonstrate that xylem tissue fraction and connectivity play a central role in maintaining hydraulic function under drought, providing insight into water-stress regulation in ancient plant lineages.