Spotlight: Antisense regulation of miRNA action during phosphate starvation

Phosphorus (P) is a vital nutrient for plant growth, acquired primarily in the form of inorganic phosphate (Pi). Pi deficiency limits plant growth and development and significantly constrains crop productivity worldwide. To face scarcity and maintain P homeostasis, plants have evolved different strategies to acquire this nutrient efficiently, where the regulation of gene expression plays a pivotal role, and several non-coding RNAs (ncRNAs) were shown to participate in this elaborate regulation. At the transcriptional level, responses to Pi deficiency are highly conserved between Arabidopsis thaliana and rice (Oryza sativa). For example, the MYB transcription factor At-PHR1 in Arabidopsis and its paralogs At-PHL1 and Os-PHR2 in rice play a pivotal role in the Pi starvation signaling pathway ( Rubio et al., 2001 Rubio V. Linhares F. Solano R. Martín A.C. Iglesias J. Leyva A. Paz-Ares J. A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes Dev. 2001; 15: 2122-2133 Crossref PubMed Scopus (964) Google Scholar ; Zhou et al., 2008 Zhou J. Jiao F. Wu Z. Li Y. Wang X. He X. Zhong W. Wu P. OsPHR2 is involved in phosphate-starvation signaling and excessive phosphate accumulation in shoots of plants. Plant Physiol. 2008; 146: 1673-1686 Crossref PubMed Scopus (467) Google Scholar ; Bustos et al., 2010 Bustos R. Castrillo G. Linhares F. Puga M.I. Rubio V. Pérez-Pérez J. Solano R. Leyva A. Paz-Ares J. A central regulatory system largely controls transcriptional activation and repression responses to phosphate starvation in Arabidopsis. PLoS Genet. 2010; 6e1001102 Crossref PubMed Scopus (494) Google Scholar ; Das et al., 2022 Das D. Paries M. Hobecker K. Gigl M. Dawid C. Lam H.M. Zhang J. Chen M. Gutjahr C. PHOSPHATE STARVATION RESPONSE transcription factors enable arbuscular mycorrhiza symbiosis. Nat. Commun. 2022; 13: 477 Crossref PubMed Scopus (43) Google Scholar ). Under Pi-limited conditions, At-PHR1 activates the expression of the microRNA399 (miR399), which targets and cleaves the E2 ubiquitin conjugase PHO2 mRNA. In Arabidopsis, PHO2 mediates the degradation of PHO1 (PHOSPHATE 1), which is responsible for transferring Pi from the epidermal and cortical root cells to the shoots, regulating Pi homeostasis ( Bari et al., 2006 Bari R. Datt Pant B. Stitt M. Scheible W.R. PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol. 2006; 141: 988-999 Crossref PubMed Scopus (897) Google Scholar ; Arpat et al., 2012 Arpat A.B. Magliano P. Wege S. Rouached H. Stefanovic A. Poirier Y. Functional expression of PHO1 to the Golgi and trans-Golgi network and its role in export of inorganic phosphate. Plant J. 2012; 71: 479-491 PubMed Google Scholar ; Liu et al., 2012 Liu T.Y. Huang T.K. Tseng C.Y. Lai Y.S. Lin S.I. Lin W.Y. Chen J.W. Chiou T.J. PHO2-dependent degradation of PHO1 modulates phosphate homeostasis in Arabidopsis. Plant Cell. 2012; 24: 2168-2183 Crossref PubMed Scopus (256) Google Scholar ). PHO2 also influences the expression levels of certain phosphate transporter genes (PHTs) ( Hu et al., 2011 Hu B. Zhu C. Li F. Tang J. Wang Y. Lin A. Liu L. Che R. Chu C. LEAF TIP NECROSIS1 plays a pivotal role in the regulation of multiple phosphate starvation responses in rice. Plant Physiol. 2011; 156: 1101-1115 Crossref PubMed Scopus (184) Google Scholar ), and the miR399-PHO2 module is crucial for Pi response and the control of Pi uptake and translocation in plants. Interestingly, several years ago, the long ncRNA transcript called INDUCED BY PHOSPHATE STARVATION1 (IPS1) in rice, or At4 in Arabidopsis, was shown to be strongly induced by Pi starvation, and its sequence contains a region complementary to miR399. Through elegant experiments, it was shown that IPS1 acts as a target mimic sequestrating and inhibiting the action of miR399 on PHO2, consequently affecting the regulation of Pi-related processes ( Franco-Zorrilla et al., 2007 Franco-Zorrilla J.M. Valli A. Todesco M. Mateos I. Puga M.I. Rubio-Somoza I. Leyva A. Weigel D. García J.A. Paz-Ares J. Target mimicry provides a new mechanism for regulation of microRNA activity. Nat. Genet. 2007; 39: 1033-1037 Crossref PubMed Scopus (1574) Google Scholar ) and further revealing the complex regulation of Pi-related gene expression. Another lncRNA, the natural antisense cis-NATPHO1;2 was shown to regulate polysomal recruitment of the PHO1;2 gene in rice, the functional ortholog of At-PHO1, and hence its translational level ( Jabnoune et al., 2013 Jabnoune M. Secco D. Lecampion C. Robaglia C. Shu Q. Poirier Y. A rice cis-natural antisense RNA acts as a translational enhancer for its cognate mRNA and contributes to phosphate homeostasis and plant fitness. Plant Cell. 2013; 25: 4166-4182 Crossref PubMed Scopus (177) Google Scholar ). In their recent paper, Wang et al., 2023 Wang Y. Wang Z. Du Q. Wang K. Zou C. Li W.X. The long noncoding RNA PILNCR2 increases low phosphate tolerance in maize by interfering with miRNA399-guided cleavage of ZmPHT1s. Mol. Plant. 2023; 16: 1146-1159 Abstract Full Text Full Text PDF PubMed Scopus (2) Google Scholar describe a new mechanism through which Pi-related processes are controlled in maize.