A maize wall-associated kinase confers quantitative resistance to head smut

Abstract

Head smut is a systemic disease in maize caused by the soil-borne fungus Sporisorium reilianum that poses a grave threat to maize production worldwide. A major head smut quantitative resistance locus, qHSR1, has been detected on maize chromosome bin2.09. Here we report the map-based cloning of qHSR1 and the molecular mechanism of qHSR1-mediated resistance. Sequential fine mapping and transgenic complementation demonstrated that ZmWAK is the gene within qHSR1 conferring quantitative resistance to maize head smut. ZmWAK spans the plasma membrane, potentially serving as a receptor-like kinase to perceive and transduce extracellular signals. ZmWAK was highly expressed in the mesocotyl of seedlings where it arrested biotrophic growth of the endophytic S. reilianum. Impaired expression in the mesocotyl compromised ZmWAK-mediated resistance. Deletion of the ZmWAK locus appears to have occurred after domestication and spread among maize germplasm, and the ZmWAK kinase domain underwent functional constraints during maize evolution.

Unraveling the molecules hidden in the gray shadows of quantitative disease resistance to pathogens

“…For example, the recently cloned QDR gene, ZmWAK, exhibits alleles differing in seven substitutions and a deletion between the resistant and susceptible maize lines. Although, in this case, polymorphisms affecting protein function were not found (Zuo et al, 2015), these polymorphisms could affect the interaction with other molecules or could prevent protein complexes formation. A similar situation was observed for the RKS1 gene, which, even if it is present in both resistant and susceptible accessions, has several SNPs that have been found to be associated with both phenotypes.…”

“…The maize ZmWAK gene is induced after pathogen inoculation. This gene is highly expressed in the mesocotyl and, at a lesser extent in the coleoptile of resistant lines, and the expression level of ZmWAKcan be associated with the degree of pathogen growth restriction in mesocotyl and coleoptiles (Zuo et al, 2015). Likewise, the RKS1 gene expression is correlated with the resistance level indifferent Arabidopsis accessions to Xanthomonas campestris pv.…”

“…In addition, the RKS1 gene,which encodes for an atypical kinase identified in the model plant Arabidopsis thaliana, confers resistance to most Xanthomonas campestris races, and to the pathovars raphani, incanae or armoraciae (Huard-Chauveau et al, 2013). Finally, the receptor-like protein coded by the ZmWAK gene of maize that confers resistance to Sphacelotheca reiliana was cloned recently (Zuo et al, 2015). Considering these discoveries and the gaps in QDR knowledge, different explanations of how it works are plausible.…”

“…in the ZmWAK gene; however, no association with function or phenotype has been studied for these variations (Zuo et al, 2015). Additional studies are required to reveal if there is an association between such polymorphisms and QDR.…”

“…RKS1 from Arabidopsis (Huard-Chauveau et al, 2013) is a typical kinase, ZmWAK from maize contains a kinase domain (Zuo et al, 2015) and Yr36 from wheat has a kinase domain similar to Arabidopsis WAK-like kinases (Fu et al, 2009). In addition, through eQTLs in barley, a gene that encodes for a "putative histidin-kinase" was identified as an important component of the resistance to Puccinia graminisf.…”