First published online May 5, 2006; 10.1104/pp.106.079707
Plant Physiology 141:988-999 (2006)
© 2006 American Society of Plant Biologists
OPEN ACCESS ARTICLE
ENVIRONMENTAL STRESS AND ADAPTATION TO STRESS
PHO2, MicroRNA399, and PHR1 Define a Phosphate-Signaling Pathway in Plants1,[W],[OA]
Rajendra Bari2,
Bikram Datt Pant2,
Mark Stitt and
Wolf-Rüdiger Scheible*
Max Planck Institute for Molecular Plant Physiology, Science Park Golm, 14476 Potsdam, Germany
Inorganic phosphate (Pi)-signaling pathways in plants are still largely unknown. The Arabidopsis (Arabidopsis thaliana) pho2 mutant overaccumulates Pi in leaves in Pi-replete conditions. Micrografting revealed that a pho2 root genotype is sufficient to yield leaf Pi accumulation. In pho2 mutants, Pi does not repress a set of Pi starvation-induced genes, including AtIPS1, AT4, and Pi transporters Pht1;8 and Pht1;9. Map-based cloning identified PHO2 as At2g33770, an unusual E2 conjugase gene. It was recently shown that Pi deprivation induces mature microRNA (miRNA [miR399]) and that overexpression of miR399 in Pi-replete conditions represses E2 conjugase expression and leads to high leaf Pi concentrations, thus phenocopying pho2. We show here that miR399 primary transcripts are also strongly induced by low Pi and rapidly repressed after addition of Pi. PHO2 transcripts change reciprocally to miR399 transcripts in Pi-deprived plants and in miR399 overexpressers. However, responses after Pi readdition and in  -glucuronidase reporter lines suggest that PHO2 expression is also regulated by Pi in a manner unrelated to miR399-mediated transcript cleavage. Expression of miR399 was strongly reduced in Pi-deprived Arabidopsis phr1 mutants, and a subset of Pi-responsive genes repressed in Pi-deprived phr1 mutants was up-regulated in Pi-replete pho2 mutants. This places miR399 and PHO2 in a branch of the Pi-signaling network downstream of PHR1. Finally, putative PHO2 orthologs containing five miR399-binding sites in their 5'-untranslated regions were identified in other higher plants, and Pi-dependent miR399 expression was demonstrated in rice (Oryza sativa), suggesting a conserved regulatory mechanism.
1 This work was supported by the Max Planck Society and the German Federal Ministry of Education and Research.
2 These authors contributed equally to the paper.
The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Wolf-Rüdiger Scheible (scheible{at}mpimp-golm.mpg.de).
[W] The online version of this article contains Web-only data.
[OA] Open Access articles can be viewed online without a subscription.
Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.106.079707.
* Corresponding author; e-mail scheible{at}mpimp-golm.mpg.de; fax 49–331–5678136.
Received February 24, 2006;
returned for revision April 4, 2006;
accepted April 24, 2006.
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