Abstract
MicroRNAs (miRNAs) play crucial regulatory roles in plant growth and development by interacting with RNA molecules, including messenger RNAs (mRNAs) and long non-coding RNAs (lncRNAs); however, the genetic networks of miRNAs and their targets influencing the phenotypes of perennial trees remain to be investigated. Here, we integrated expression profiling and association analysis of underlying physiology and expression traits to dissect the allelic variations and genetic interactions of Pto-MIR167a and its targets, sponge lncRNA ARFRL, and Pto-ARF8, in 435 unrelated individuals of Populus tomentosa. Tissue-specific expression analysis in eight tissues, including stem, leaf, root, and shoot apex, revealed negative correlations between Pto-MIR167a and lncRNA ARFRL and Pto-ARF8 (r = −0.60 and −0.61, respectively, P < 0.01), and a positive correlation between sponge lncRNA ARFRL and Pto-ARF8 (r = 0.90, P < 0.01), indicating their potential regulatory roles in tree growth and wood formation. Single nucleotide polymorphism (SNP)-based association studies detected 53 significant associations (P < 0.01, Q < 0.1) representing 41 unique SNPs from the three genes and six traits, suggesting their potential roles in wood formation. Epistasis uncovered 88 pairwise interactions for 10 traits, which provided substantial evidence for genetic interactions among Pto-MIR167a, lncRNA ARFRL, and Pto-ARF8. Using gene expression-based association mapping, we also examined SNPs within the three genes that influence phenotypes by regulating the expression of Pto-ARF8. Interestingly, SNPs in the precursor region of Pto-MIR167a altered its secondary structure stability and transcription, thereby affecting the expression of its targets. In summary, we elucidated the genetic interactions between Pto-MIR167a and its targets, sponge lncRNA ARFRL, and Pto-ARF8, in tree growth and wood formation, and provide a feasible method for further investigation of multi-factor genetic networks influencing phenotypic variation in the population genetics of trees.
Highlights
MicroRNAs are a class of non-coding RNAs that are derived from hairpin precursors and loaded into the RNA-induced silencing complex to post-transcriptionally regulate gene expression via cleavage or inhibitory mechanisms (Ramachandran and Chen, 2008; Voinnet, 2009)
Our study provides a better understating of the genetic networks of Pto-MIR167a and its targets, long non-coding RNAs (lncRNAs) auxin response factors-related lncRNA (ARFRL), and Pto-ARF8, in tree growth and wood formation, and the association analysis of underlying physiology and expression traits proposed an alternative method for dissecting the genetic networks of ncRNAs and messenger RNAs (mRNAs) in the population genetics of trees
Using the lncRNA database of cambium, developing xylem, and mature xylem of P. tomentosa, we identified lncRNA ARFRL as a potential target of Pto-miR167a-d, whose mature sequences were conserved in the Pto-miR167 family (Figure 1A)
Summary
MicroRNAs (miRNAs) are a class of non-coding RNAs (ncRNAs) that are derived from hairpin precursors and loaded into the RNA-induced silencing complex to post-transcriptionally regulate gene expression via cleavage or inhibitory mechanisms (Ramachandran and Chen, 2008; Voinnet, 2009). MiR167 was found to be involved in significant biological processes by interacting with its target genes, auxin response factors (ARFs). Nitrogen treatment increases the expression of ARF8 by reducing miR167 levels in the pericycle and root cap, initiating lateral root formation in Arabidopsis (Gifford et al, 2008). The detailed regulatory mechanisms and how the interactions between miR167 and ARFs contribute to tree growth and development, remain largely unknown
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