Physcomitrium patens Infection by Colletotrichum gloeosporioides: Understanding the Fungal–Bryophyte Interaction by Microscopy, Phenomics and RNA Sequencing

Abstract

Anthracnose caused by the hemibiotroph fungus <i>Colletotrichum gloeosporioides</i> is a devastating plant disease with an extensive impact on plant productivity. The process of colonization and disease progression of <i>C. gloeosporioides</i> has been studied in a number of angiosperm crops. To better understand the evolution of the plant response to pathogens, the study of this complex interaction has been extended to bryophytes. The model moss <i>Physcomitrium patens</i> Hedw. B&S (former <i>Physcomitrella patens</i>) is sensitive to known bacterial and fungal phytopathogens, including <i>C. gloeosporioides</i>, which cause infection and cell death. <i>P. patens</i> responses to these microorganisms resemble that of the angiosperms. However, the molecular events during the interaction of <i>P. patens</i> and <i>C. gloeosporioides</i> have not been explored. In this work, we present a comprehensive approach using microscopy, phenomics and RNA-seq analysis to explore the defense response of <i>P. patens</i> to <i>C. gloeosporioides</i>. Microscopy analysis showed that appressoria are already formed at 24 h after inoculation (hai) and tissue colonization and cell death occur at 24 hai and is massive at 48 hai. Consequently, the phenomics analysis showed progressing browning of moss tissues and impaired photosynthesis from 24 to 48 hai. The transcriptomic analysis revealed that more than 1200 <i>P. patens</i> genes were differentially expressed in response to <i>Colletotrichum</i> infection. The analysis of differentially expressed gene function showed that the <i>C. gloeosporioides</i> infection led to a transcription reprogramming in <i>P. patens</i> that upregulated the genes related to pathogen recognition, secondary metabolism, cell wall reinforcement and regulation of gene expression. In accordance with the observed phenomics results, some photosynthesis and chloroplast-related genes were repressed, indicating that, under attack, <i>P. patens</i> changes its transcription from primary metabolism to defend itself from the pathogen.