Long noncoding RNAs emerge from transposon-derived antisense sequences and may contribute to infection stage-specific transposon regulation in a fungal phytopathogen

bioRxiv (Cold Spring Harbor Laboratory)

Abstract

Abstract The genome of the obligate biotrophic phytopathogenic barley powdery mildew fungus Blumeria hordei is inflated due to highly abundant and possibly active transposable elements (TEs). In the absence of the otherwise common repeat-induced point mutation transposon defense mechanism, noncoding RNAs could be key for regulating the activity of TEs and coding genes during the pathogenic life cycle. We performed time-course whole-transcriptome shotgun sequencing (RNA-seq) of total RNA derived from infected barley leaf epidermis at various stages of fungal pathogenesis and observed significant transcript accumulation and time point-dependent regulation of TEs in B. hordei . Using a manually curated consensus database of 344 TEs, we discovered phased small RNAs mapping to 104 consensus transposons, suggesting that RNA interference contributes significantly to their regulation. Further, we identified 5,127 long noncoding RNAs (lncRNAs) genome-wide in B. hordei , of which 823 originated from the antisense strand of a TE. Co-expression network analysis of lncRNAs, TEs, and coding genes throughout the asexual life cycle of B. hordei points at extensive positive and negative co-regulation of lncRNAs, subsets of TEs and coding genes. Our work suggests that similar to mammals and plants, fungal lncRNAs support the dynamic modulation of transcript levels, including TEs, during pivotal stages of host infection. The lncRNAs may support transcriptional diversity and plasticity amid loss of coding genes in powdery mildew fungi and may give rise to novel regulatory elements and virulence peptides, thus representing key drivers of rapid evolutionary adaptation to promote pathogenicity and overcome host defense.

Authors 6

1. Jiangzhao Qian Aachen Unit of Plant Molecular Cell Biology Institute for Biology I

   RWTH Aachen University

   Affiliation as printed

   RWTH Aachen University;

   Unit of Plant Molecular Cell Biology, Institute for Biology I, RWTH Aachen University, Worringerweg 1, D-52056 Aachen, Germany

   RWTH Aachen University

2. Heba M. M. Ibrahim

   KU Leuven

   Affiliation as printed

   Division of Plant Biotechnics, Department of Biosystems, Faculty of Bioscience Engineering, Katholieke Universiteit Leuven, 3001 Leuven, Belgium

   KU Leuven;

   KU Leuven

3. Myriam Erz Aachen Unit of Plant Molecular Cell Biology Institute for Biology I

   RWTH Aachen University

   Affiliation as printed

   RWTH Aachen University;

   Unit of Plant Molecular Cell Biology, Institute for Biology I, RWTH Aachen University, Worringerweg 1, D-52056 Aachen, Germany

   RWTH Aachen University

4. Florian Kümmel

   Max Planck Institute for Plant Breeding Research

   Affiliation as printed

   Department of Plant-Microbe Interactions, Max Planck Institute for Plant Breeding Research, Carl-von-Linné-Weg 10, Cologne D-50829, Germany

   Max Planck Institute for Plant Breeding Research

5. Ralph Panstruga Aachen Unit of Plant Molecular Cell Biology Institute for Biology I

   RWTH Aachen University

   Affiliation as printed

   RWTH Aachen University;

   Unit of Plant Molecular Cell Biology, Institute for Biology I, RWTH Aachen University, Worringerweg 1, D-52056 Aachen, Germany

   RWTH Aachen University

6. Stefan Kusch corresponding Aachen Unit of Plant Molecular Cell Biology Institute for Biology I

   Forschungszentrum Jülich · RWTH Aachen University

   Affiliation as printed

   Institute of Bio- and Geosciences IBG-4, Forschungszentrum Jülich, D-52425 Jülich, Germany

   RWTH Aachen University;

   Unit of Plant Molecular Cell Biology, Institute for Biology I, RWTH Aachen University, Worringerweg 1, D-52056 Aachen, Germany

   RWTH Aachen University