miR164-targeted TaPSK5 encodes a phytosulfokine precursor that regulates root growth and yield traits in common wheat (Triticum aestivum L.).

KEY MESSAGE: TaPSK5 is a less conserved target of miR164 in wheat encoding a positive regulator of root growth and yield traits that could be used for crop improvement. MicroRNAs (miRNAs) play key roles in regulating plant growth and development by targeting the mRNAs of conserved genes. However, little is known about the roles of less conserved miRNA-targeted genes in plants. In the current study, we identified TaPSK5, encoding a phytosulfokine precursor, as a novel target of miR164. Compared with miR164-targeted NAC transcription factor genes, TaPSK5 is less conserved between monocots and dicots. Expression analysis indicated that TaPSK5 homoeologs were constitutively expressed in wheat tissues, especially young spikes. Overexpression of TaPSK5-D and miR164-resistant TaPSK5-D (r-TaPSK5-D) led to increased primary root growth and grain yield in rice, with the latter having more significant effects. Comparison of the transcriptome between wild-type and r-TaPSK5-D overexpression plants revealed multiple differentially expressed genes involved in hormone signaling, transcription regulation, and reactive oxygen species (ROS) homeostasis. Moreover, we identified three TaPSK5-A haplotypes (TaPSK5-A-Hap1/2/3) and two TaPSK5-B haplotypes (TaPSK5-B-Hap1/2) in core collections of Chinese wheat. Both TaPSK5-A-Hap1 and TaPSK5-B-Hap2 are favorable haplotypes associated with superior yield traits that were under positive selection during wheat breeding. Together, our findings identify miR164-targeted TaPSK5 as a regulator of root growth and yield traits in common wheat with potential applications for the genetic improvement of crops.