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.

Keywords: Defense-yield trade-off; Genome editing; MicroRNA; Plant immunity; Rice.

Fig. 1

Summary of known miRNA-mediated defense mechanisms against pathogens and herbivores in rice. The left panel indicates an overview of the miRNAs responsive to fungal pathogens and insects. The right panel shows the miRNAs involved in resistance to bacterial and viral diseases. The miRNAs written in blue and red represent the positively and negatively regulated miRNAs, respectively. Xoo- Xanthomonas oryzae pv. oryzae; D. zeae- Dickey Zeae, RSV- Rice stripe virus; RRSV- Rice ragged stunt virus

Fig. 2

Functionally characterized miRNAs associated with the immune response against bacterial, fungal, and viral pathogens, as well as insect herbivores. Pathogen-derived effector molecules elicit the expression of MIR genes by RNA polymerase II via mitogen-activated protein (MAP) kinase signaling. The long hairpin transcript is processed by Dicer-like protein (DCL). The miR162 targets the DCL and produces ROS. Various miRNAs such as miR162, miR164, miR169, miR398, and miR439 also participate in the immune response mechanism via ROS. On the other hand, a tug of war between AGO1 and AGO18 for binding to miR528 and miR168 facilitates the expression of strong resistance against the invading viral pathogen through the production of reactive oxygen species (ROS). The miR156, miR396, and miR159 confer resistance to pathogens and insect pests by targeting transcription factors through a mechanism modulated by phytohormones

Fig. 3

Model depicting the possible roles of miRNAs and phased secondary siRNAs (phasiRNA) in the regulation of R-genes. A Under normal conditions, when the host plant is not challenged, constitutive and unregulated expression of R-genes results in high fitness costs; B In the direct targeting pathway of R-genes by miRNA, the MIR loci produce miRNA transcripts that are processed to mature miRNAs. Subsequently, mature miRNA is complexed with AGO1/7 and directly binds to R-gene transcript followed by cleavage, resulting in basal resistance response and concomitant effects on fitness cost (box with dashed line). In the indirect targeting pathway of R-genes by miRNAs, the mature miRNA is produced from MIR loci and interacts with AGO1. The AGO1-miRNA complex binds to PHAS transcripts produced from the coding region of PHAS loci and cleaves the PHAS transcripts in a sequence-specific manner. SGS3 and RDR6 convert the single-stranded RNA to long double-stranded RNA which is processed by DCL4 to phased siRNA (phasiRNA). AGO1/7-phasiRNA complex cleaves R- gene transcripts and maintain the basal level of R-gene expression to achieve optimized and well-balanced resource usage for defense and maintenance of plant fitness by robust growth and development. R genes-resistance genes; AGO1-ARGONAUTE 1; SGS3-SUPPRESSOR OF GENE SILENCING 3; RDR6- RNA-DEPENDENT RNA POLYMERASE 6; DCL4- DICER-LIKE 4