PIF4 negatively modulates cold tolerance in tomato anthers via temperature-dependent regulation of tapetal cell death

Extreme temperature conditions seriously impair male reproductive development in plants; however, the molecular mechanisms underlying the response of anthers to extreme temperatures remain poorly described. The transcription factor phytochrome-interacting factor4 (PIF4) acts as a hub that integrates multiple signaling pathways to regulate thermosensory growth and architectural adaptation in plants. Here, we report that SIPIF4 in tomato (Solanum lycopersicum) plays a pivotal role in regulating cold tolerance in anthers. CRISPR (clustered regularly interspaced short palindromic repeats)-associated nuclease Cas9-generated SIPIF4 knockout mutants showed enhanced cold tolerance in pollen due to reduced temperature sensitivity of the tapetum, while overexpressing SIPIF4 conferred pollen abortion by delaying tapetal programmed cell death (PCD). SIPIF4 directly interacts with SIDYT1, a direct upstream regulator of SITDF1, both of which (SIDYT1 and SITDF1) play important roles in regulating tapetum development and tapetal PCD. Moderately low temperature (MLT) promotes the transcriptional activation of SITDF1 by the SIPIF4-SIDYT1 complex, resulting in pollen abortion, while knocking out SIPIF4 blocked the MLT-induced activation of SITDF1. Furthermore, SIPIF4 directly binds to the canonical E-box sequence in the SIDYT1 promoter. Collectively, these findings suggest that SIPIF4 negatively regulates cold tolerance in anthers by directly interacting with the tapetal regulatory module in a temperature-dependent manner. Our results shed light on the molecular mechanisms underlying the adaptation of anthers to low temperatures.

Automated summary

SIPIF4 plays a crucial role in regulating cold tolerance in tomato anthers by interacting with SIDYT1 and SITDF1, and directly binding to the promoter of SIDYT1. These findings reveal the molecular mechanisms of SIPIF4 in regulating anther adaptation to low temperatures.