Cross-species analysis between the maize smut fungiUstilago maydisandSporisorium reilianumhighlights the role of transcriptional plasticity of effector orthologs for virulence and disease

Abstract

The constitution and regulation of effector repertoires determines and shapes the outcome of the interaction with the host. Ustilago maydis and Sporisorium reilianum are two closely related smut fungi, which both infect maize, but cause distinct disease symptoms. Understanding how effector orthologs are regulated in these two pathogens can therefore provide insights to pathogen evolution and host adaption. We tracked the infection progress of U. maydis and S. reilianum in maize leaves, characterized two distinct infection stages for cross species RNA-sequencing analysis and identified 207 out of 335 one-to-one effector orthologs being differentially regulated during host colonization, while transcriptional plasticity of the effector orthologs correlated with the distinct disease development strategies. By using CRISPR-Cas9 mediated gene conversion, we identified two differentially expressed effector orthologs with conserved function between two pathogens. Thus, differential expression of functionally conserved genes contributes to species specific adaptation and symptom development. Interestingly, another differentially expressed orthogroup (UMAG_05318/sr1007) showed diverged protein function during speciation, providing a possible case for neofunctionalization. Together, we showed the diversification of effector genes in related pathogens can be caused both by plasticity on the transcriptional level, as well as through neofunctionalization of the encoded effector proteins.

Effectors with Different Gears: Divergence of Ustilago maydis Effector Genes Is Associated with Their Temporal Expression Pattern during Plant Infection

“…The expression of tin2 shows a wave-like fashion which gradually increases during infection and peaks at 6 days post infection (dpi) to then drop again at 8 dpi. In contrast to U. maydis , transcriptome analysis has not been studied throughout the disease cycle of S. reilianum as hitherto only RNA libraries of early seedling infection stages have been sequenced [ 22 , 23 ].…”