Grafting Reveals Organ-Autonomous and Feedback Roles of Root Phloem Development in Source-Sink Dynamics

Carbon fixed in source leaves is partitioned between local use and long-distance transport through the phloem to heterotrophic sinks like roots. Here, we investigated how mild defects in sink phloem differentiation influence whole-plant growth using two Arabidopsis mutants: ops, which exhibits short roots with protophloem differentiation defects, and ops opl2, which displays even shorter roots with combined proto- and metaphloem differentiation defects. Carbon partitioning and phloem transport velocity were compromised in both mutants, with ops opl2 exhibiting stronger effects. Root growth responses to exogenous sucrose highlighted functional differences: only ops opl2 root growth was partially rescued, indicating additional limitations from compromised metaphloem function. Reciprocal grafting confirmed that root growth defects in both mutants are root-autonomous. In contrast, source-limited starch mutants with short roots were rescued by sucrose supplementation or by grafting wild-type scions, highlighting that the growth limitation in the phloem mutants’ roots is not solely due to carbon shortage. Impaired root phloem also restricted wild-type scion growth, revealing feedback from sink phloem integrity on source activity. Together, these findings show that sink phloem development supports sink function and mediates systemic feedback shaping whole-plant growth. Targeted modulation of sink phloem development could help optimize source-sink relations and improve crop performance.