Ovary Abortion Induced by Combined Waterlogging and Shading Stress at the Flowering Stage Involves Amino Acids and Flavonoid Metabolism in Maize

Abstract

Maize (Zea mays L.) crops on the North China Plain are often subject to continuous overcast rain at the flowering stage. This causes waterlogging and shading stresses simultaneously and leads to huge yield losses, but the causes of these yield losses remain largely unknown. To explore the factors contributing to yield loss caused by combined waterlogging and shading stress at the flowering stage, we performed phenotypic, physiological, and quasi-targeted metabolomics analyses of maize plants subjected to waterlogging, shading, and combined waterlogging and shading (WS) treatments. Analyses of phenotypic and physiological indexes showed that, compared with waterlogging or shading alone, WS resulted in lower source strength, more severe inhibition of ovary and silk growth at the ear tip, a reduced number of emerged silks, and a higher rate of ovary abortion. Changes in carbon content and enzyme activity could not explain the ovary abortion in our study. Metabolomic analyses showed that the events occurred in ovaries and silks were closely related to abortion, WS forced the ovary to allocate more resources to the synthesis of amino acids involved in the stress response, inhibited the energy metabolism, glutathione metabolism and methionine salvage pathway, and overaccumulation of H2O2. In silks, WS led to lower accumulation levels of specific flavonoid metabolites with antioxidant capacity, and to over accumulation of H2O2. Thus, compared with each single stress, WS more seriously disrupted the normal metabolic process, and resulted more serious oxidative stress in ovaries and silks. Amino acids involved in the stress response in ovaries and specific flavonoid metabolites with antioxidant capacity in silks play important roles during ovary abortion. These results identify novel traits for selection in breeding programs and targets for genome editing to increase maize yield under WS stress.