MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis

• Published in: The Plant journal : for cell and molecular biology Vol. 53; no. 5; pp. 731 - 738
• Main Authors: Pant, Bikram Datt, Buhtz, Anja, Kehr, Julia, Scheible, Wolf-Rüdiger
• Format: Journal Article
• Language: English
• Published: Oxford, UK Oxford, UK : Blackwell Publishing Ltd 01.03.2008; Blackwell Publishing Ltd; Blackwell Science
• Subjects: Arabidopsis; Arabidopsis - genetics; Arabidopsis - metabolism; bioactive properties; Biological and medical sciences; biological control; Biological Transport, Active; Botany; Brassica; Brassica napus; Brassica napus - genetics; Brassica napus - metabolism; Cell physiology; chimerism; Cucurbita; Cucurbita - genetics; Cucurbita - metabolism; Flowers & plants; Fundamental and applied biological sciences. Psychology; gene expression regulation; Gene Expression Regulation, Plant; genetics; Homeostasis; long-distance signaling; metabolism; microRNA; MicroRNAs; MicroRNAs - genetics; MicroRNAs - metabolism; Molecular and cellular biology; Molecules; mutants; nutrient; nutrients; Original; phenotype; phloem; phosphate homeostasis; phosphates; Phosphates - metabolism; Plant Roots; Plant Roots - metabolism; Plant Shoots; Plant Shoots - metabolism; Plant species; pumpkins; rapeseed; Ribonucleic acid; RNA; RNA, Plant; RNA, Plant - metabolism; Roots; sap; Signal Transduction; phosphate homeostasis; nutrient; Root; Arabidopsis; Homeostasis; Gene expression; Biological activity; Brassica; Phloem; Cruciferae; Dicotyledones; Angiospermae; Above ground plant part; long-distance signaling; microRNA; Spermatophyta; Mutation
• ISSN: 0960-7412; 1365-313X; 1365-313X
• DOI: 10.1111/j.1365-313X.2007.03363.x

The presence of microRNA species in plant phloem sap suggests potential signaling roles by long-distance regulation of gene expression. Proof for such a role for a phloem-mobile microRNA is lacking. Here we show that phosphate (Pi) starvation-induced microRNA399 (miR399) is present in the phloem sap of two diverse plant species, rapeseed and pumpkin, and levels are strongly and specifically increased in phloem sap during Pi deprivation. By performing micro-grafting experiments using Arabidopsis, we further show that chimeric plants constitutively over-expressing miR399 in the shoot accumulate mature miR399 species to very high levels in their wild-type roots, while corresponding primary transcripts are virtually absent in roots, demonstrating shoot-to-root transport. The chimeric plants exhibit (i) down-regulation of the miR399 target transcript (PHO2), which encodes a critical component for maintenance of Pi homeostasis, in the wild-type root, and (ii) Pi accumulation in the shoot, which is the phenotype of pho2 mutants, miR399 over-expressers or chimeric plants with a genetic knock-out of PHO2 in the root. Hence the transported miR399 molecules retain biological activity. This is a demonstration of systemic control of a biological process, i.e. maintenance of plant Pi homeostasis, by a phloem-mobile microRNA.