ZmWAK-mediated Head Smut Resistance

Head smut,caused by the fungal pathogen Sporisorium reilianum,poses grave threat to maize production worldwide.ZmWAK,a transmembrane protein with an extracellular receptor domain and an intercellular kinase domain,has been previously validated to confer the quantitative resistance to head smut disease.Here,a pair of near-isogenic lines,a susceptible line Huangzao4 and its ZmWAK-converted resistant line Huangzao4R,were used to decipher the molecular mechanism of ZmWAK-mediated head smut resistance.1.Huangzao4 and Huangzao4R were inoculated with S.reilianum in afield trial for two years.Huangzao4R gained nearly 20-40%higher percentage ofresistant plantsthan Huangzao4,suggesting ZmWAK confers a durable resistance to head smut.2.The growth of pathogen hyphae was severely arrested by hypersensitive response-likePCD in Huangzao4R while aggressive in Huangzao4.HR-like PCD in Huangzao4R enhanced head smut resistance by stopping S.relianum heading towards SAM,crucial step for S.relianum pathogenicity.3.Two NILs showed different modes of cell death upon S.reilianum attack.Infected cells exhibited apoptosis-like features in Huangzao4R to restrict hyphae within dead cells,while pathogen invasion caused autophagy in Huangzao4which failed in preventing hyphae from spreading.4.A jointed metabolomic and trancriptomic analysis indicated ZmWAK mediated growth and defense tradeoff,whereby ZmWAK promotes cell growth in the absence of pathogen and switches to defense response upon S.reilianum attack.5.The intracellular domain ZmWAKIN was used as a bait to screen the Ji1037 mesocotyl cDNA library,the donor of ZmWAK.A sucrose non-fermenting related protein kinase ZmSnRK1,key regulator in maintaining nutrient and energy homeostasis,was identified to interact with ZmWAKIN.ZmWAK orchestrate between cell growth and head smut resistance through coordination with ZmSnRKl.6.ZmSnRK1 encodes the a catalytic subunit of SnRK complex,sharing high identities to Arabidopsis AtSnRK1.1 and AtSnRK1.2.ZmWAK does not transcriptionally regulate ZmSnRK1.