A wheat NAC interacts with an orphan protein and enhances resistance to Fusarium head blight disease.

Alexandre Perochon,Jianguang Jia,Emma Wallington,Melanie Craze,Amal Kahla,Fiona M Doohan,Monika Vranić,Keshav B Malla

doi:10.1111/pbi.13105

Alexandre Perochon, Jianguang Jia + Show 6 more

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https://doi.org/10.1111/pbi.13105

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Abstract

SummaryTaxonomically‐restricted orphan genes play an important role in environmental adaptation, as recently demonstrated by the fact that the Pooideae‐specific orphan TaFROG (Triticum aestivum Fusarium Resistance Orphan Gene) enhanced wheat resistance to the economically devastating Fusarium head blight (FHB) disease. Like most orphan genes, little is known about the cellular function of the encoded protein TaFROG, other than it interacts with the central stress regulator TaSnRK1α. Here, we functionally characterized a wheat (T. aestivum) NAC–like transcription factor TaNACL‐D1 that interacts with TaFROG and investigated its’ role in FHB using studies to assess motif analyses, yeast transactivation, protein‐protein interaction, gene expression and the disease response of wheat lines overexpressing TaNACL‐D1. TaNACL‐D1 is a Poaceae‐divergent NAC transcription factor that encodes a Triticeae‐specific protein C‐terminal region with transcriptional activity and a nuclear localisation signal. The TaNACL‐D1/TaFROG interaction was detected in yeast and confirmed in planta, within the nucleus. Analysis of multi‐protein interactions indicated that TaFROG could form simultaneously distinct protein complexes with TaNACL‐D1 and TaSnRK1α in planta. TaNACL‐D1 and TaFROG are co‐expressed as an early response to both the causal fungal agent of FHB, Fusarium graminearum and its virulence factor deoxynivalenol (DON). Wheat lines overexpressing TaNACL‐D1 were more resistant to FHB disease than wild type plants. Thus, we conclude that the orphan protein TaFROG interacts with TaNACL‐D1, a NAC transcription factor that forms part of the disease response evolved within the Triticeae.

Highlights

Advances in genome sequencing technologies over the last decade have exponentially increased the availability of whole genomes in all different kingdoms, including plants and animals
Recent studies revealed that orphan genes are important players in key agronomic traits, including Ms2 that confers male sterility in wheat (Ni et al, 2017), QQS (Qua-Quine Starch) that regulates carbon and nitrogen partitioning across species (Li et al, 2015) and TaFROG (Triticum aestivum Fusarium Resistance Orphan Gene) that enhances wheat resistance to disease (Perochon et al, 2015)
We found that TaFROG is an intrinsically disordered proteins (IDPs) that can interact with the Sucrose NonFermenting1-Related Kinase1 (SnRK1); SnRK1 is a key signaling protein, and is the orthologue of the yeast Sucrose NonFermenting1 (SNF1) and the mammalian AMP-activated protein kinase (AMPK) (Perochon et al, 2015)

Summary

Introduction

Advances in genome sequencing technologies over the last decade have exponentially increased the availability of whole genomes in all different kingdoms, including plants and animals. This revealed that a significant portion of eukaryotic genomes encodes orphan genes (or taxonomically restricted genes). These genes are phylogenetically restricted and do not encode any previously identified protein domains (Khalturin et al, 2009). Despite the fact that orphan genes can represent about 10–20% of the genes encoded by eukaryotic genomes (Khalturin et al, 2009), their functions remain largely unknown (Arendsee et al, 2014). Recent studies revealed that orphan genes are important players in key agronomic traits, including Ms2 that confers male sterility in wheat (Ni et al, 2017), QQS (Qua-Quine Starch) that regulates carbon and nitrogen partitioning across species (Li et al, 2015) and TaFROG (Triticum aestivum Fusarium Resistance Orphan Gene) that enhances wheat resistance to disease (Perochon et al, 2015)

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