Urediospores of Puccinia spp. and other rusts are warm-temperature ice nucleators and harbor ice nucleation active bacteria

Abstract

Various features of the biology of the rust fungi and of the epidemiology of the plant diseases they cause illustrate the important role of rainfall in their life history. Based on this insight we have characterized the ice nucle- ation activity (INA) of the aerially disseminated spores (ure- diospores) of this group of fungi. Urediospores of this ob- ligate plant parasite were collected from natural infections of 7 species of weeds in France, from coffee in Brazil and from field and greenhouse-grown wheat in France, the USA, Turkey and Syria. Immersion freezing was used to determine freezing onset temperatures and the abundance of ice nuclei in suspensions of washed spores. Microbiological analyses of spores from France, the USA and Brazil, and subsequent tests of the ice nucleation activity of the bacteria associated with spores were deployed to quantify the contribution of bacteria to the ice nucleation activity of the spores. All sam- ples of spores were ice nucleation active, having freezing on- set temperatures as high as−4 ◦C. Spores in most of the sam- ples carried cells of ice nucleation-active strains of the bac- terium Pseudomonas syringae (at rates of less than 1 bacte- rial cell per 100 urediospores), but bacterial INA accounted for only a small fraction of the INAobserved in spore suspen- sions. Changes in the INA of spore suspensions after treat- ment with lysozyme suggest that the INA of urediospores involves a polysaccharide. Based on data from the literature, we have estimated the concentrations of urediospores in air at cloud height and in rainfall. These quantities are very sim- ilar to those reported for other biological ice nucleators in these same substrates. However, at cloud level convective ac- tivity leads to widely varying concentrations of particles of surface origin, so that mean concentrations can underesti- mate their possible effects on clouds. We propose that spa- tial and temporal concentrations of biological ice nucleators active at temperatures >−10 ◦C and the specific conditions under which they can influence cloud glaciation need to be further evaluated so as to understand how evolutionary pro- cesses could have positively selected for INA