Complexity of miRNA-dependent regulation in root symbiosis

Abstract

The development of root systems may be strongly affected by the symbiotic interactions that plants establish with soil organisms. Legumes are able to develop symbiotic relationships with both rhizobial bacteria and arbuscular mycorrhizal fungi leading to the formation of nitrogen-fixing nodules and mycorrhizal arbuscules, respectively. Both of these symbiotic interactions involve complex cellular reprogramming and profound morphological and physiological changes in specific root cells. In addition, the repression of pathogenic defence responses seems to be required for successful symbiotic interactions. Apart from typical regulatory genes, such as transcription factors, microRNAs (miRNAs) are emerging as riboregulators that control gene networks in eukaryotic cells through interactions with specific target mRNAs. In recent years, the availability of deep-sequencing technologies and the development of in silico approaches have allowed for the identification of large sets of miRNAs and their targets in legumes. A number of conserved and legume-specific miRNAs were found to be associated with symbiotic interactions as shown by their expression patterns or actions on symbiosis-related targets. In this review, we combine data from recent literature and genomic and deep-sequencing data on miRNAs controlling nodule development or restricting defence reactions to address the diversity and specificity of miRNA-dependent regulation in legume root symbiosis. Phylogenetic analysis of miRNA isoforms and their potential targets suggests a role for miRNAs in the repression of plant defence during symbiosis and revealed the evolution of miRNA-dependent regulation in legumes to allow for the modification of root cell specification, such as the formation of mycorrhized roots and nitrogen-fixing nodules.

Soybean miR172c Targets the Repressive AP2 Transcription Factor NNC1 to Activate ENOD40 Expression and Regulate Nodule Initiation

“…] legume partners are to determine how the association arises, how nodule organogenesis and thus nodule number are regulated, and how nitrogen fixation is controlled. Recently, there has been a great deal of interest in understanding the roles of miRNAs during nodulation in legumes Bazin et al, 2012;Bustos-Sanmamed et al, 2013;Turner et al, 2013). Our analysis here identified miR172c-NNC1 as a critical regulatory module of nodulation that targets early nodulin ENOD40 genes and is essential for nodule initiation and nodule organogenesis in soybean.…”

“…Deep sequencing studies have identified a number of miRNAs that are upregulated during nodulation, and ecotopic expression has demonstrated that some are involved in early nodule organogenesis. For example, a specific isoform of miR171 represses critical NODULATION SIGNALING PATHWAY2 (NSP2) expression in M. truncatula and L. japonicus (Devers et al, 2011;Bazin et al, 2012;De Luis et al, 2012). In soybean, numerous miRNAs are differentially expressed during nodule organogenesis (Subramanian et al, 2008;Wang et al, 2009;Dong et al, 2013).…”

A Significant Fraction of 21-Nucleotide Small RNA Originates from Phased Degradation of Resistance Genes in Several Perennial Species

“…Recent data from legumes suggest that the repression of NBS-LRR genes by specific miRNAs may have evolved to avoid plant defense responses during symbiotic interactions (Bazin et al, 2012). Such a mechanism could potentially explain the high incidence of miRNA-guided siRNA-mediated degradation of NBS-LRR genes observed in Medicago spp.…”

MicroRNA167-Directed Regulation of the Auxin Response Factors GmARF8a and GmARF8b Is Required for Soybean Nodulation and Lateral Root Development

“…Several profiling studies have revealed that miRNAs are involved in rhizobial infection, nodule formation, and nodule functioning (Subramanian et al, 2008;Lelandais-Brière et al, 2009;Wang et al, 2009;Bazin et al, 2012;De Luis et al, 2012;Dong et al, 2013; for review, see Formey et al, 2014). Indeed, functional analyses have demonstrated an altered number of nodules following miRNA overexpression or knockdown (Combier et al, 2006;Li et al, 2010;De Luis et al, 2012;Turner et al, 2013;Yan et al, 2013;Wang et al, 2014).…”