ZmWAK, A Quantitative Resistance Gene To Head Smut In Maize, Improves Yield Performance By Reducing The Endophytic Pathogen Sporisorium Reiliana

Head smut is a soil-borne systemic maize disease caused by the causal pathogen Sporisorium reiliana. ZmWAK is the gene within the major QTL-qHSR1conferring resistance to head smut disease. ZmWAK from the completely resistant inbred line Ji1037has been transferred by marker-assisted backcrossing into elite inbred lines with high-yield potential but susceptible to head smut to produce converted inbred lines. The disease incidence of four inbred lines before and after introgression of resistance gene was determined in2012and2013. Four original hybrids with variable head smut resistance were selected, including highly susceptible Jidan209, susceptible Jidan535, moderately resistant Jidan536, and resistant Jidan522. Based on these four original hybrids, six converted hybrids were prepared by using one or two converted inbred lines as parental lines. The four original and six converted hybrids were grown in2012and2013to investigate yield per plot, and yield-related traits under natural and artificial inoculations.Under heavy diseased condition, the converted inbred lines displayed significantly lower disease incidence than their original inbred lines. Likewise, the converted hybrids, Jidan209R1, Jidan209R2, Jidan209R3and Jidan535R, showed significant increase in resistance to head smut, thus leading to effective reduction of yield loss. ZmWAK showed dose-independent resistance manner, the converted hybrids with one ZmWAK allele could enhance resistance as high as the converted hybrid carrying two ZmWAK alleles. However, the converted hybrid with two ZmWAK alleles displayed the lowest values in some yield-related traits. This is due to the overlapped ZmWAK-containing regions in two converted parental lines. In addition, ZmWAK could reduce the quantity of S. reiliana in symptomless plants of the converted hybrids, Jidan209R1, Jidan209R2, Jidan209R3, and Jidan535R. While the original hybrids, Jidan536and Jidan522, prepared from moderately resistant and resistant lines showed very low content of the pathogenic DNA. The amount of S. reiliana DNA in symptomless plants was negatively associated with yield-related traits, suggesting the infection of S. reiliana could also affect yield potential even though it does not show head smut symptom. The total sugar content in infected mesocoty1of Jidan209at seedling stage was significantly higher than its three converted hybrids, Jidan209R1, Jidan209R2and Jidan209R3with ZmWAK gene(s), suggesting the presence of possible intrinsic connection between sugar and resistance.Overall, the results suggest that ZmWAK-mediated resistance to maize head smut follows a dominant genetic model, and a single ZmWAK allele could achieve high disease resistance and reduce the amount of endophytic S. reiliana to prevent yield loss and improve most yield components. Thus far, ZmWAK is beneficial to head smut resistance, yield, and yield-related traits in maize.