Plant lncRNAs are enriched in and move systemically through the phloem in response to phosphate deficiency

Abstract In response to phosphate (Pi) deficiency, it has been shown that micro‐RNAs (miRNAs) and mRNAs are transported through the phloem for delivery to sink tissues. Growing evidence also indicates that long non‐coding RNAs (lncRNAs) are critical regulators of Pi homeostasis in plants. However, whether lncRNAs are present in and move through the phloem, in response to Pi deficiency, remains to be established. Here, using cucumber as a model plant, we show that lncRNAs are enriched in the phloem translocation stream and respond, systemically, to an imposed Pi‐stress. A well‐known lncRNA, IPS1, the target mimic (TM) of miRNA399, accumulates to a high level in the phloem, but is not responsive to early Pi deficiency. An additional 24 miRNA TMs were also detected in the phloem translocation stream; among them miRNA171 TMs and miR166 TMs were induced in response to an imposed Pi stress. Grafting studies identified 22 lncRNAs which move systemically into developing leaves and root tips. A CU‐rich PTB motif was further identified in these mobile lncRNAs. Our findings revealed that lncRNAs respond to Pi deficiency, non‐cell‐autonomously, and may act as systemic signaling agents to coordinate early Pi deficiency signaling, at the whole‐plant level.