A membrane-bound ankyrin repeat protein confers race-specific leaf rust disease resistance in wheat

Abstract

Plasma membrane-associated and intracellular proteins and protein complexes play a pivotal role in pathogen recognition and disease resistance signaling in plants and animals. The two predominant protein families perceiving plant pathogens are receptor-like kinases and nucleotide binding-leucine-rich repeat receptors (NLR), which often confer race-specific resistance. Leaf rust is one of the most prevalent and most devastating wheat diseases. Here, we clone the race-specific leaf rust resistance gene Lr14a from hexaploid wheat. The cloning of Lr14a is aided by the recently published genome assembly of ArinaLrFor, an Lr14a-containing wheat line. Lr14a encodes a membrane-localized protein containing twelve ankyrin (ANK) repeats and structural similarities to Ca2+-permeable non-selective cation channels. Transcriptome analyses reveal an induction of genes associated with calcium ion binding in the presence of Lr14a. Haplotype analyses indicate that Lr14a-containing chromosome segments were introgressed multiple times into the bread wheat gene pool, but we find no variation in the Lr14a coding sequence itself. Our work demonstrates the involvement of an ANK-transmembrane (TM)-like type of gene family in race-specific disease resistance in wheat. This forms the basis to explore ANK-TM-like genes in disease resistance breeding.

Bioinformatic-Based Approaches for Disease-Resistance Gene Discovery in Plants

“…Neither the Pm4 nor a close homologue is present in the Chinese Spring wheat reference genome, demonstrating that MutChromSeq is a sequence-unbiased non-reference approach to finding R genes. Similarly, Kolodziej and collaborators [61] proved the involvement of an ankyrin (ANK)-transmembrane, another non-canonical domain, in race-specific leaf rust resistance in wheat. The ANK proteins are typically involved in protein-protein interactions and plant immunity [62].…”

Mapping of additive and epistatic QTLs linked to seed longevity in bread wheat (Triticum aestivum L.)

“…For standard germination, on chromosome 4A, ankyrin (ANK)-3-like isoform X1 and 60S ribosomal protein L10a and on chromosome 5A pentatricopeptide repeat-containing protein were identified. ANK proteins in plants play important roles in plant immunity, development and growth, and they are typically involved in protein-protein interactions (Kolodziej et al 2021), whereas members of the pentatricopeptide repeat (PPR) protein family are sequence specific RNA binding proteins that play crucial roles in organelle RNA metabolism (Yan et al 2019).…”

A recombined Sr26 and Sr61 disease resistance gene stack in wheat encodes unrelated NLR genes

“…Therefore, NLR proteins predominate in providing all-stage resistance to all three fungal rust species in wheat and its immediate ancestors. However, other proteins can also contribute, such as the recently reported membrane bound ankyrin repeat protein encoded by Lr14a 38 .…”