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Published on October 23, 2009; 10.1104/pp.109.147280

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Received September 9, 2009
Accepted October 21, 2009

Uncovering small RNA-mediated responses to phosphate-deficiency in Arabidopsis by deep sequencing

Li-Ching Hsieh , Shu-I Lin , Arthur Chun-Chieh Shih , June-Wei Chen , Wei-Yi Lin , Ching-Ying Tseng , Wen-Hsiung Li , and Tzyy-Jen Chiou *

Genomics Research Center, Academia Sinica, Taipei 115, Taiwan; Agricultural Biotechnology Research Center, Academia Sinica, Taipei 115, Taiwan; Graduate Institute of Life Sciences, National Defense Medical Center, Taipei 114, Taiwan; Institute of Information Science, Academia Sinica, Taipei 115, Taiwan; Molecular and Biological Agricultural Sciences Program, Taiwan International Graduate Program, Academia Sinica, Taipei 115, Taiwan; Graduate Institute of Biotechnology, National Chung-Hsing University, Taichung 402, Taiwan; Biodiversity Research Center, Academia Sinica, Taipei 115, Taiwan; Department of Ecology and Evolution, University of Chicago, Chicago, IL 60637; Department of Life Sciences, National Chung-Hsing University, Taichung 402, Taiwan

* Corresponding author; email: tjchiou{at}gate.sinica.edu.tw.

Recent studies have demonstrated the important role of plant miRNAs under nutrient deficiencies. In this study, deep sequencing of Arabidopsis thaliana small RNAs was conducted to reveal microRNAs (miRNAs) and other small RNAs that were differentially expressed in response to phosphate (Pi) deficiency. About 3.5 million sequence reads corresponding to 0.6-1.2 million unique sequence tags from each Pi-sufficient or -deficient root or shoot sample were mapped to the Arabidopsis genome. We showed that upon Pi deprivation, the expression of miR156, miR399, miR778, miR827 and miR2111 was induced, whereas the expression of miR169, miR395 and miR398 was repressed. We found crosstalks coordinated by these miRNAs under different nutrient deficiencies. In addition to miRNAs, we identified one Pi starvation-induced DCL1-dependent small RNA derived from the long terminal repeat of a retrotransposon and a group of 19-nucleotide small RNAs corresponding to the 5‘ end of tRNA and expressed at a high level in Pi-starved roots. Importantly, we observed an increased abundance of TAS4-derived trans-acting siRNAs (ta-siRNAs) in Pi-deficient shoots and uncovered an autoregulatory mechanism of PAP1/MYB75 via miR828 and TAS4-siR81(-) that regulates the biosynthesis of anthocyanin. This finding sheds light on the regulatory network between miRNA/ta-siRNA and its target gene. Of note, a substantial amount of miR399* accumulated under Pi deficiency. Like miR399, miR399* can move across the graft junction, implying a potential biological role for miR399*. This study represents a comprehensive expression profiling of Pi-responsive small RNAs and advances our understanding of the regulation of Pi homeostasis mediated by small RNAs.






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