MicroRNA-mediated host defense mechanisms against pathogens and herbivores in rice: balancing gains from genetic resistance with trade-offs to productivity potential

Abstract

Background Rice (Oryza sativa L.) is the major source of daily caloric intake for more than 30% of the human population. However, the sustained productivity of this staple food crop is continuously threatened by various pathogens and herbivores. Breeding has been successful in utilizing various mechanisms of defense by gene pyramiding in elite cultivars, but the continuous resurgence of highly resistant races of pathogens and herbivores often overcomes the inherent capacity of host plant immunity. MicroRNAs (miRNAs) are endogenous, short, single-stranded, non-coding RNA molecules that regulate gene expression by sequence-specific cleavage of target mRNA or suppressing target mRNA translation. While miRNAs function as upstream regulators of plant growth, development, and host immunity, their direct effects on growth and development in the context of balancing defenses with agronomic potential have not been extensively discussed and explored as a more viable strategy in breeding for disease and pest resistant cultivars of rice with optimal agronomic potentials. Results Using the available knowledge in rice and other model plants, this review examines the important roles of miRNAs in regulating host responses to various fungal, bacterial, and viral pathogens, and insect pests, in the context of gains and trade-offs to crop yield. Gains from R-gene-mediated resistance deployed in modern rice cultivars are often undermined by the rapid breakdown of resistance, negative pleiotropic effects, and linkage drags with undesirable traits. In stark contrast, several classes of miRNAs are known to efficiently balance the positive gains from host immunity without significant costs in terms of losses in agronomic potentials (i.e., yield penalty) in rice. Defense-related miRNAs such as Osa-miR156, Osa-miR159, Osa-miR162, Osa-miR396, Osa-530, Osa-miR1432, Osa-miR1871, and Osa-miR1873 are critical in fine-tuning and integrating immune responses with physiological processes that are necessary to the maintenance of grain yield. Recent research has shown that many defense-related miRNAs regulate complex and agronomically important traits. Conclusions Identification of novel immune-responsive miRNAs that orchestrate physiological processes critical to the full expression of agronomic potential will facilitate the stacking of optimal combinations of miRNA-encoding genes to develop high-yielding cultivars with durable resistance to disease and insect pests with minimal penalties to yield.

Novel genes and alleles of the BTB/POZ protein family in Oryza rufipogon

“…These findings suggest that OrBTB genes are involved in various signaling pathways relevant to stress-response mechanisms. Surveying for miRNA target sites can also provide another layer of crucial information for gene expression 98 , 99 . The specific pairing of miRNAs with OrBTB genes could change their expression dynamics through post-transcriptional gene silencing (PTGS).…”

Recent Developments in Rice Molecular Breeding for Tolerance to Heavy Metal Toxicity

“…In several investigations, high-throughput sequencing and miRNA microarray data have indicated the involvement of several miRNAs in the responses of various plant species to toxic HMs [62]. Overexpression of miRNAs or the development of miRNAresistant target genes have been widely utilized to demonstrate the role of metal-responsive miRNAs, and these miRNAs and their target genes are an essential component of a largescale regulatory network controlling different metabolic processes in response to metal stress [63,64]. Several regulatory networks involving miRNAs and their TFs have been studied [35].…”

Combined analysis of mRNA and miRNA transcriptomes reveals the regulatory mechanism of Xanthomonas arboricola pv pruni resistance in Prunus persica

“…Lü et al summarized the regulatory roles of miRNAs in plant‒pathogen and plant-probiotic interactions [ 37 ]. Using the available knowledge in rice and other model plants, the important roles of miRNAs in regulating host responses to various fungal, bacterial, and viral pathogens and insect pests in the context of gains and trade-offs to crop yield have been examined [ 38 ]. Yan et al studied WRKY genes to provide novel insights into their role against Ralstonia solanacearum infection in cultivated peanut ( Arachis hypogaea l.) [ 39 ].…”