Transcriptomic Insights into Innate Immunity Responding to Red Rot Disease in Red Alga Pyropia yezoensis

Abstract

Pyropia yezoensis, one of the most economically important marine algae, suffers from the biotic stress of the oomycete necrotrophic pathogen Pythium porphyrae. However, little is known about the molecular defensive mechanisms employed by Pyr. yezoensis during the infection process. In the present study, we defined three stages of red rot disease based on histopathological features and photosynthetic physiology. Transcriptomic analysis was carried out at different stages of infection to identify the genes related to the innate immune system in Pyr. yezoensis. In total, 2139 up-regulated genes and 1672 down-regulated genes were identified from all the infected groups. Pathogen receptor genes, including three lectin genes (pattern recognition receptors (PRRs)) and five genes encoding typical plant R protein domains (leucine rich repeat (LRR), nucleotide binding site (NBS), or Toll/interleukin-1 receptor (TIR)), were found to be up-regulated after infection. Several defense mechanisms that were typically regarded as PAMP-triggered immunity (PTI) in plants were induced during the infection. These included defensive and protective enzymes, heat shock proteins, secondary metabolites, cellulase, and protease inhibitors. As a part of the effector-triggered immunity (ETI), the expression of genes related to the ubiquitin-proteasome system (UPS) and hypersensitive cell death response (HR) increased significantly during the infection. The current study suggests that, similar to plants, Pyr. yezoensis possesses a conserved innate immune system that counters the invasion of necrotrophic pathogen Pyt. porphyrae. However, the innate immunity genes of Pyr. yezoensis appear to be more ancient in origin compared to those in higher plants.

Physiological and Dual Transcriptional Analysis of Microalga Graesiella emersonii–Amoeboaphelidium protococcarum Pathosystem Uncovers Conserved Defense Response and Robust Pathogenicity

“…In 2019, Im et al identified the genes involved in the interaction of the red alga Pyropia tenera and three pathogens using microarray analysis and histochemical methods [ 13 ]. Tang et al identified the genes associated with the defense response of the red alga Pyropia yezoensis against the necrotrophic pathogen Pythium porphyrae using transcriptomic analysis [ 14 ]. However, microalgal responses and defense reactions to pathogen infection at the molecular level have never been investigated.…”

Role and Evolution of the Extracellular Matrix in the Acquisition of Complex Multicellularity in Eukaryotes: A Macroalgal Perspective

“…Pattern Recognition Receptors, including three lectin genes and a Toll/interleukin-1 receptor, were upregulated after infection. Expression of genes related to the ubiquitin-proteasome system and hypersensitive cell death, again reminiscent of plant effector-triggered immunity, increased significantly during the infection [ 153 ].…”

“…A family of potential microbe-sensing domains, specific of the Bangiophytes, was also identified, including C-lectins with Von Willebrand factor type A [ 7 ]. Several of these proteins were upregulated in Pyropia cultures infected by oomycetes [ 152 , 153 ]. Altogether, innate immunity in marine macroalgae consists of general constitutive defenses and genetic toolkits against specific pathogens [ 152 , 161 ].…”

Enzymatic Functions for Toll/Interleukin-1 Receptor Domain Proteins in the Plant Immune System

“…Two pine TNL loci, TNL1 and TNL2, are correlated with blister rust resistance (Liu and Ekramoddoullah, 2011). TIR-domainencoding genes were more recently reported in the agriculturally important red algae, Pyropia yezoensis, which is used for nori production (Tang et al, 2019). At least one TIR-domain encoding gene, along with several NBS genes of Pyropia are upregulated by challenge with the oomycete pathogen, Pythium (Tang et al, 2019).…”

“…TIR-domainencoding genes were more recently reported in the agriculturally important red algae, Pyropia yezoensis, which is used for nori production (Tang et al, 2019). At least one TIR-domain encoding gene, along with several NBS genes of Pyropia are upregulated by challenge with the oomycete pathogen, Pythium (Tang et al, 2019). Genes with TIR immune receptor-like domain combinations have been found in the genomes of green algae.…”