The Hemibiotroph Colletotrichum graminicola Locally Induces Photosynthetically Active Green Islands but Globally Accelerates Senescence on Aging Maize Leaves

Abstract

Typically, pathogenesis of the hemibiotroph Colletotrichum graminicola and defense responses of its host, Zea mays, are studied on young leaves. Equivalent studies have not been performed with leaves undergoing senescence, a situation that is relevant in the field. We discovered that, in contrast to anthracnose symptoms formed on young and mature leaves, green islands reminiscent of those known from obligate biotrophs were formed on senescing leaves. Microscopy revealed that the fungus grew in both symptoms from the epidermis towards the bundle sheath. In green islands, tissues remained intact for an extended time period. Imaging PAM (pulse-amplitude-modulation) fluorescence analyses revealed that photosynthesis is transiently maintained at green islands but declined in tissue surrounding the infection. In younger leaves however, photosynthesis was reduced only at infection sites. Support for the local modification of host physiology came from quantitative reverse transcription-polymerase chain reaction analyzing gene expression at high spatial resolution. Decreased transcript levels of the senescence markers see1 and ccp1 corroborated a pathogen-induced delay of senescence. Expression of several genes encoding proteins involved in photosynthesis was strongly reduced by infection. In contrast, transcript levels of incw1, encoding a cell-wall invertase, were increased 70-fold at green islands, suggesting that C. graminicola induced carbon sinks in senescing tissue.