Transcriptional programs controlling sporulation in Phytophthora respond to nutrition, humidity, and cryptochrome-mediated light signals.

Many filamentous pathogens employ environmental signals to regulate sporulation, maximizing the likelihood that their spores survive to colonize a new host. In the oomycete Phytophthora, little is known of the transcriptional program that underlies sporangia formation and how it is influenced by environmental inputs such as light, humidity, and nutrients. By studying time courses of the potato blight pathogen P. infestans on artificial media and tomato leaves, we identified over 4000 genes up-regulated during sporulation. These are associated with signal transduction, cell structure, vesicle trafficking, metabolism, flagellar assembly, and other processes required for sporangium formation and germination. Most of their mRNAs remain abundant in mature sporangia. Media manipulation and metabolomic studies indicated that sporulation is triggered by nitrogen limitation, with asparagine and possibly other amino acids playing the main role. Light, which delays sporulation in P. infestans, apparently influences a later regulatory step since while many sporulation-induced transcripts oscillate with a day/night cycle, others are light-neutral. Both blue and red wavelengths result in the light response, which is likely mediated by a cryptochrome. One cryptochrome was shown to be required for sporulation based on gene silencing experiments. Humidity appears to regulate a late checkpoint, since while spore development requires high humidity, low humidity has only limited effects on sporulation-associated transcription. Comparative studies with P. capsici, which unlike P. infestans requires light for sporulation, yielded evidence of substantial rewiring of the transcriptional program between the species. The contrasting light responses within the genus correlate with whether species are primarily leaf colonizers such as P. infestans or root colonizers such as P. capsici.