MicroRNAs fine-tune immunity and yield trade-offs
Developing high yielding varieties with resistance to biotic stress is one of the current major goals of plant breeding (Eichmann & Schäfer 2015). While this is paramount to sustainable crop production, it is also well known that strong defence response against pathogens often comes with unexpected trade-offs in terms of significant losses of yield (Ning et al. 2017). Modern plant breeding approaches such as marker-assisted selection, transgenics, and genome-editing are being applied to breed resistant cultivars with minimal penalty to yield. In the past few decades, many R-genes in rice have been tagged with tightly linked molecular markers. However, a limited set of genes are deployed in crop improvement programs due to the fact that many of them exhibit pleiotropic effects, unwanted linkage drags that undermine agronomic traits, and low heritability (Tang & Chu 2017). Furthermore, because of the rapid breakdown of the R-genes and associated fitness cost, miRNAs controlling rice immunity has attracted more attention as a means to develop resistant cultivars while minimizing the negative trade-offs to plant growth and yield.
Recent reports have shown that many miRNAs facilitate the maintenance of fitness and resistance without compromising yield in rice. For instance, the Osa-miR156 , Osa-miR162 , Osa-miR396 , andOsa-miR1873 have been found to regulate defense-yield trade-off in rice (Chandran et al., 2019; Zhou et al., 2019b; Li et al., 2020; Zhang et al., 2020b). The Osa-miR156 negatively regulates immunity against the rice blast, bacterial blight, and BPH by targeting the IPA1 (Ideal Plant Architecture 1) , OsSPLs (SQUAMOSA Promoter-binding protein-Like transcription factors) and several OsWRKY genes. Sequestering Osa-miR156 by target mimicry method exhibited enhanced resistance to blast, BB and BPH through accumulation of target genes and defence-related genes (Geet al. 2018; Liu et al. 2019; Zhang et al. 2020b). However, downregulation of Osa-miR156 proved to cause significant reduction in plant height, tiller number, and delayed seed germination.
Inducible expression of IPA1 gene under control of bacterial effector-induced promoter displayed enhanced resistance to BB, with concomitant improvement in grain size, plant architecture and grain yield (Liu et al. 2019). The Osa-miR162 synergizes the mechanisms involved in resistance to blast with the genetic potential for yield through the OsDCL1 that causes the accumulation of intracellular H2O2. Nevertheless, overexpression of Osa-miR162 showed significantly narrower grains, lower seed weight and poor seed set, leading to negative effects on grain yield. Silencing of Osa-miR162 showed positive effects on yield by increasing the number of grains per panicle during M. oryzae infection (Li et al. 2020).
Suppression of Osa-miR396 induces multiple growth regulating factors (GRF) genes that leads to the enhancement of blast and BPH resistance (Chandran et al. 2019; Dai et al.2019) 2019). The Osa-miR396 also regulates grain size, grain yield, inflorescence development, panicle branching, salinity, and alkali tolerance (Duan et al. 2015; Gao et al. 2015; Zhanget al. 2020a). The Osa-miR1873 has been shown to balance blast resistance and plant growth in rice. Overexpression ofOsa-miR1873 compromises resistance and negatively impacts yield potential by lowering seed-set and by reducing the filled grain per panicle. In contrast, sequestering Osa-miR1873 was shown to cause no significant effects in yield (Zhou et al. 2019b). Apart from these miRNA, Osa-miR159 , Osa-miR160 , Osa-miR164 ,Osa-miR167 , and Osa-miR398 have been shown to affect yield and component traits, independently. However, further studies might reveal the modulation of yield and component traits by immune-responsive miRNAs in response to pathogen and herbivore attack.