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A cis-natural antisense RNA regulates alternative polyadenylation of SlSPX5 under Pi starvation in tomato

Shenghong Ge, Jinkai Li, Hui Ma, María Sánchez-Bermúdez, Siqun Wu, Qiuyu Lv, Fengxiao Guo, Jinsong Dong, Guojie Ma, Qingshun Quinn Li (), Viswanathan Satheesh () and Mingguang Lei ()
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Shenghong Ge: Hangzhou Normal University
Jinkai Li: Chinese Academy of Sciences
Hui Ma: Xiamen University
María Sánchez-Bermúdez: Universidad Politécnica de Madrid (UPM)—Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria-CSIC (INIA/CSIC), Campus Montegancedo
Siqun Wu: Chinese Academy of Sciences
Qiuyu Lv: Hangzhou Normal University
Fengxiao Guo: Hangzhou Normal University
Jinsong Dong: Hangzhou Normal University
Guojie Ma: Hangzhou Normal University
Qingshun Quinn Li: Xiamen University
Viswanathan Satheesh: Iowa State University
Mingguang Lei: Hangzhou Normal University

Nature Communications, 2025, vol. 16, issue 1, 1-15

Abstract: Abstract Alternative polyadenylation (APA) generates transcript diversity by producing mRNA isoforms with distinct 3’ ends. Despite the critical roles that APA plays in various biological processes, the mechanisms regulating APA in response to stresses have remained poorly understood in plants. Here, we perform comprehensive analysis of APA in tomato, and focus on a phosphate (Pi)- regulated APA gene SlSPX5, encoding a putative Pi sensor protein. SlSPX5 interacts with and sequesters the transcription factor SlPHL1 in the cytosol, thereby inhibiting the expression of Pi starvation inducible genes. We discover that a cis-natural antisense RNA (cis-NAT) is activated from SlSPX5 to promote its proximal polyadenylation under Pi-depleted conditions. The transcription of this cis-NAT induces RNA Polymerase II pausing, generating Ser2 phosphorylation signals that recruit polyadenylation machinery to the 5’ end of SlSPX5. Our findings demonstrate that a cis-NAT regulates APA of its cognate gene in response to Pi starvation.

Date: 2025
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DOI: 10.1038/s41467-025-63406-1

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