Cooperative Regulatory Functions of miR858 and MYB83 during Cyst Nematode Parasitism

Abstract

ORCID IDs: 0000-0003-4046-1672 (J.H.R.); 0000-0001-5256-8878 (T.H.).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 Heterodera cyst nematode parasitism of Arabidopsis (Arabidopsis thaliana). Gene expression analyses and promoter-GUS fusion assays documented a role of miR858 in posttranscriptional regulation of MYB83 in the Heterodera schachtii-induced feeding sites, the syncytia. Constitutive overexpression of miR858 interfered with H. schachtii parasitism of Arabidopsis, leading to reduced susceptibility, while reduced miR858 abundance enhanced plant susceptibility. Similarly, MYB83 expression increases were conducive to nematode infection because overexpression of a noncleavable coding sequence of MYB83 significantly increased plant susceptibility, whereas a myb83 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 MYB83 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 H. schachtii-induced syncytium. Together, our results suggest a role of the miR858-MYB83 regulatory system in finely balancing gene expression patterns during H. schachtii parasitism of Arabidopsis to ensure optimal cellular function.

The novel cyst nematode effector protein 30D08 targets host nuclear functions to alter gene expression in feeding sites

“…We observed significant similarities among several cellular processes differentially regulated in 30D08 transgenic lines and cyst nematode‐induced syncytia (Szakasits et al ., ), including cell cycle, hormone metabolism and cell wall modification. In addition, we identified a significant enrichment in the differential regulation of genes encoding several members of transcription factor families in Arabidopsis, including those known to participate in feeding site formation (Szakasits et al ., ; Jin et al ., ; Guo et al ., ; Piya et al ., ). Several biotic stress genes involved in jasmonic acid, salicylic acid, and glucosinolate biosynthesis were also upregulated in the 30D08 transgenic lines.…”

Small RNAs, emerging regulators critical for the development of horticultural traits

“…As this pathway of miR828/miR858 targeting MYB genes is in Gymnosperm 18 , how this pathway is evolved with anthocyanin biogenesis thereafter is interesting to study. Conceivably, the miR8282/miR858 pathway is evolved with broader function with the expansion of MYB genes, as evidenced by their roles in fiber development 84 and cyst nematode parasitism 85 .…”

Transcriptional activity of transposable elements may contribute to gene expression changes in the syncytium formed by cyst nematode in arabidopsis roots

“…Syncytium formation involves changes in the expression of a large number of genes, which are genetically and epigenetically controlled. [8][9][10][11] Recently, we found that infection of Arabidopsis plants with H. schachtii triggers widespread hypomethylation in TEs, particularly those adjacent to protein-coding genes, 6 providing strong evidence that the transcriptional activity of TEs possibly impacts expression of nearby genes during plant-nematode interactions.…”