Ploidy alters root anatomy and shapes the evolution of wheat polyploids

Abstract

Polyploidization played a crucial role in crop domestication and modern agriculture. While increased cell size in polyploids is known to enhance plant biomass and vigor, its impact on soil exploration remains poorly understood. Using wheat as a model, we identify a ploidy-induced belowground domestication syndrome, characterized by (a) increased root cortical cell size reducing root respiration, nitrogen content, and phosphorus content; (b) enlarged metaxylem vessels, increasing axial hydraulic conductance; and (c) blunter root tips, limiting penetration ability in compacted soils. Our empirical and in silico experiments show that reduced root respiration and reduced cellular nutrient content in wheat polyploids improved nutrient use and acquisition efficiency under suboptimal nitrogen and phosphorus availability. These adaptations would have been advantageous in nutrient-depleted agroecosystems of the Pre-Pottery Neolithic B (PPNB) Fertile Crescent, where continuous cultivation depleted soil fertility over time. Functional-structural modeling indicates that larger cortical cells in wheat polyploids increase vacuolar occupancy, reducing root metabolic costs. Enhanced axial hydraulic conducta nce may have improved water transport, an advantage in irrigated PPNB agroecosystems. However, polyploids have blunter root tips, which reduces their penetration ability in compacted soils, making them less suited for native soils with greater mechanical impedance. We propose that root anatomical changes driven by ploidy played an important role in adaptations of wheat domesticates to PPNB agriculture. One-Sentence SummaryPolyploidy induced changes in root anatomy may have improved adaptation of wheat to Neolithic agroecosystems.