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Genome-Wide Analysis of Coding and Non-coding RNA Reveals a Conserved miR164-NAC-mRNA Regulatory Pathway for Disease Defense in Populus.

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.

SUBMITTER: Chen S

PROVIDER: S-EPMC8195341 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundNAC (NAM, ATAF1/2 and CUC2) domain proteins are plant-specific transcriptional factors known to play diverse roles in various plant developmental processes. NAC transcription factors comprise of a large gene family represented by more than 100 members in Arabidopsis, rice and soybean etc. Recently, a preliminary phylogenetic analysis was reported for NAC gene family from 11 plant species. However, no comprehensive study incorporating phylogeny, chromosomal location, gene structure, conserved motifs, and expression profiling analysis has been presented thus far for the model tree species Populus.ResultsIn the present study, a comprehensive analysis of NAC gene family in Populus was performed. A total of 163 full-length NAC genes were identified in Populus, and they were phylogenetically clustered into 18 distinct subfamilies. The gene structure and motif compositions were considerably conserved among the subfamilies. The distributions of 120 Populus NAC genes were non-random across the 19 linkage groups (LGs), and 87 genes (73%) were preferentially retained duplicates that located in both duplicated regions. The majority of NACs showed specific temporal and spatial expression patterns based on EST frequency and microarray data analyses. However, the expression patterns of a majority of duplicate genes were partially redundant, suggesting the occurrence of subfunctionalization during subsequent evolutionary process. Furthermore, quantitative real-time RT-PCR (RT-qPCR) was performed to confirm the tissue-specific expression patterns of 25 NAC genes.ConclusionBased on the genomic organizations, we can conclude that segmental duplications contribute significantly to the expansion of Populus NAC gene family. The comprehensive expression profiles analysis provides first insights into the functional divergence among members in NAC gene family. In addition, the high divergence rate of expression patterns after segmental duplications indicates that NAC genes in Populus are likewise to have been retained by substantial subfunctionalization. Taken together, our results presented here would be helpful in laying the foundation for functional characterization of NAC gene family and further gaining an understanding of the structure-function relationship between these family members.

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Genome-Wide Analysis of Coding and Non-coding RNA Reveals a Conserved miR164-NAC-mRNA Regulatory Pathway for Disease Defense in Populus.

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