Cooperative Regulatory Functions of miR858 and MYB83 during Cyst Nematode Parasitism

Abstract

MicroRNAs (miRNAs) recently have been established as key regulators of transcriptome reprogramming that define cell function and identity. Nevertheless, the molecular functions of the greatest number of miRNA genes remain to be determined. Here, we report cooperative regulatory functions of miR858 and its MYB83 transcription factor target gene in transcriptome reprogramming during <i>Heterodera</i> cyst nematode parasitism of Arabidopsis (<i>Arabidopsis thaliana</i>). Gene expression analyses and promoter-GUS fusion assays documented a role of miR858 in posttranscriptional regulation of <i>MYB83</i> in the <i>Heterodera schachtii-</i>induced feeding sites, the syncytia. Constitutive overexpression of miR858 interfered with <i>H. schachtii</i> parasitism of Arabidopsis, leading to reduced susceptibility, while reduced miR858 abundance enhanced plant susceptibility. Similarly, <i>MYB83</i> expression increases were conducive to nematode infection because overexpression of a noncleavable coding sequence of <i>MYB83</i> significantly increased plant susceptibility, whereas a <i>myb83</i> mutation rendered the plants less susceptible. In addition, RNA-seq analysis revealed that genes involved in hormone signaling pathways, defense response, glucosinolate biosynthesis, cell wall modification, sugar transport, and transcriptional control are the key etiological factors by which MYB83 facilitates nematode parasitism of Arabidopsis. Furthermore, we discovered that miR858-mediated silencing of <i>MYB83</i> is tightly regulated through a feedback loop that might contribute to fine-tuning the expression of more than a thousand of MYB83-regulated genes in the <i>H. schachtii</i>-induced syncytium. Together, our results suggest a role of the miR858-MYB83 regulatory system in finely balancing gene expression patterns during <i>H. schachtii</i> parasitism of Arabidopsis to ensure optimal cellular function.