A Rice cis-Natural Antisense RNA Acts as a Translational Enhancer for Its Cognate mRNA and Contributes to Phosphate Homeostasis and Plant Fitness

• Published in: The Plant cell Vol. 25; no. 10; pp. 4166 - 4182
• Main Authors: Jabnoune, Mehdi, Secco, David, Lecampion, Cécile, Robaglia, Christophe, Shu, Qingyao, Poirier, Yves
• Format: Journal Article
• Language: English
• Published: United States American Society of Plant Biologists 01.10.2013
• Subjects: Enhancer Elements, Genetic; Gene Expression Regulation, Plant; Genes; Genomes; Homeostasis; Messenger RNA; Molecular Sequence Data; Oryza - genetics; Oryza - metabolism; Oryza sativa; Phosphates; Phosphates - metabolism; Plant roots; Plants; Plants, Genetically Modified - genetics; Plants, Genetically Modified - metabolism; Promoter Regions, Genetic; Protein Biosynthesis; Reverse transcriptase polymerase chain reaction; Rice; RNA; RNA, Antisense - genetics; RNA, Messenger - genetics; RNA, Plant - genetics; Transgenic plants; Xylem - metabolism
• ISSN: 1040-4651; 1532-298X
• DOI: 10.1105/tpc.113.116251

cis-natural antisense transcripts (cis-NATs) are widespread in plants and are often associated with downregulation of their associated sense genes. We found that a cis-NAT positively regulates the level of a protein critical for phosphate homeostasis in rice (Oryza sativa). PHOSPHATE1;2 (PHO1;2), a gene involved in phosphate loading into the xylem in rice, and its associated cis-NAT PHO1;2 are both controlled by promoters active in the vascular cylinder of roots and leaves. While the PHO1;2 promoter is unresponsive to the plant phosphate status, the cis-NAT PHO1;2 promoter is strongly upregulated under phosphate deficiency. Expression of both cis-NAT PHO1;2 and the PHO1;2 protein increased in phosphate-deficient plants, while the PHO1;2 mRNA level remained stable. Downregulation of cis-NAT PHO1;2 expression by RNA interference resulted in a decrease in PHO1;2 protein, impaired the transfer of phosphate from root to shoot, and decreased seed yield. Constitutive overexpression of NAT PHO1;2 in trans led to a strong increase of PHO1;2, even under phosphate-sufficient conditions. Under all conditions, no changes occurred in the level of expression, sequence, or nuclear export of PHO1;2 mRNA. However, expression of cis-NATPHO1;2 was associated with a shift of both PHO1;2 and cis-NAT PHO1;2 toward the polysomes. These findings reveal an unexpected role for cis-NAT PHO1;2 in promoting PHO1;2 translation and affecting phosphate homeostasis and plant fitness.