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 such as 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 roots of phloem mutants 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.