Genetic interactions among Pto-miR319 family members and their targets influence growth and wood properties in Populus tomentosa

Abstract

MicroRNAs (miRNAs) play crucial roles in all aspects of plant growth and development, but the genetic interactions of miRNAs and their target genes in woody plants are largely unknown. Here, we integrated association genetics and expression profiling to decipher the allelic variations and interactions of the Pto-MIR319 family of miRNAs and 12 putative Pto-miR319 target genes related to wood formation in 435 unrelated individuals of Populus tomentosa Carrière (Chinese white poplar). Expression pattern analysis showed that among all pairings between expressions of pre-miRNA of Pto-MIR319 members and targets, 70.0% showed negative correlation of expression levels (r = - 0.944 to 0.674, P < 0.01) in eight tissues and organs of poplar, suggesting that Pto-miR319 may participate in the regulatory network of wood formation. Single SNP-based association studies identified 137 significant associations (P < 0.01, Q < 0.1), representing 126 unique SNPs from Pto-MIR319 members and their targets, with 10 tree growth traits, revealing that these genetic factors have common roles related to wood formation. Epistasis analysis uncovered 105 significant SNP-SNP associations (P < 0.01) influencing the 10 traits, demonstrating the close genetic interactions between Pto-MIR319 family members and the 12 Pto-miR319 target genes. Notably, one common SNP, in the precursor region of Pto-MIR319e, affected the stability of Pto-MIR319e's secondary structure by altering the stem-loop structure and minimum free energy, contributing to variations in the expression of Pto-MIR319e and Pto-miR319e target genes. This study enriches the understanding of the functions of miR319 family miRNAs in poplar and exemplifies a feasible approach to exploring the genetic effects underlying miRNA-mRNA interactions related to complex traits in trees.