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

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.