Abstract
MicroRNAs (miRNAs) contribute to plant defense responses by increasing the overall genetic diversity; however, their origins and functional importance in plant defense remain unclear. Here, we employed Illumina sequencing technology to assess how miRNA and messenger RNA (mRNA) populations vary in the Chinese white poplar (Populus tomentosa) during a leaf black spot fungus (Marssonina brunnea) infection. We sampled RNAs from infective leaves at conidia germinated stage [12 h post-inoculation (hpi)], infective vesicles stage (24 hpi), and intercellular infective hyphae stage (48 hpi), three essential stages associated with plant colonization and biotrophic growth in M. brunnea fungi. In total, 8,938 conserved miRNA-target gene pairs and 3,901 Populus-specific miRNA-target gene pairs were detected. The result showed that Populus-specific miRNAs (66%) were more involved in the regulation of the disease resistance genes. By contrast, conserved miRNAs (>80%) target more whole-genome duplication (WGD)-derived transcription factors (TFs). Among the 1,023 WGD-derived TF pairs, 44.9% TF pairs had only one paralog being targeted by a miRNA that could be due to either gain or loss of a miRNA binding site after the WGD. A conserved hierarchical regulatory network combining promoter analyses and hierarchical clustering approach uncovered a miR164–NAM, ATAF, and CUC (NAC) transcription factor–mRNA regulatory module that has potential in Marssonina defense responses. Furthermore, analyses of the locations of miRNA precursor sequences reveal that pseudogenes and transposon contributed a certain proportion (∼30%) of the miRNA origin. Together, these observations provide evolutionary insights into the origin and potential roles of miRNAs in plant defense and functional innovation.
Highlights
MicroRNAs are ∼21 to 24-nucleotide non-coding endogenous small RNAs that can regulate gene expression, maintain genome integrity and chromatin structure, and influence plant development and stress response (Carrington and Ambros, 2003; Jones-Rhoades et al, 2006; Voinnet, 2009; Sunkar et al, 2012; Meyers and Axtell, 2019)
To study the posttranscriptional regulation associated with poplar defense to Marssonina, we inoculated the leaves of P. tomentosa LM50 clones with M. brunnea f. sp
To elucidate the underlying mechanism of emergence of miRNAs, we examined the locations of miRNA precursor sequences (MIRs) in the regions of P. trichocarpa genome, including intragenic regions and intergenic regions (Supplementary Data 7)
Summary
MicroRNAs (miRNAs) are ∼21 to 24-nucleotide (nt) non-coding endogenous small RNAs that can regulate gene expression, maintain genome integrity and chromatin structure, and influence plant development and stress response (Carrington and Ambros, 2003; Jones-Rhoades et al, 2006; Voinnet, 2009; Sunkar et al, 2012; Meyers and Axtell, 2019). Many lines of evidence have confirmed that miRNAs contribute to plant defenses against pathogens (Li et al, 2012; Pumplin and Voinnet, 2013; Thiebaut et al, 2015; Yang and Huang, 2015). MiRNAs– transcription factor (TFs) regulation module was proposed to be ubiquitous in plant defense and plays key roles in regulation networks controlling many biological processes, including responses to biotic and abiotic stresses (Seo et al, 2015; Thiebaut et al, 2015)
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