Network Analysis Reveals a Common Host–Pathogen Interaction Pattern in Arabidopsis Immune Responses

Abstract

Many plant pathogens secrete virulence effectors into host cells to target important proteins in host cellular network. However, the dynamic interactions between effectors and host cellular network have not been fully understood. Here, an integrative network analysis was conducted by combining Arabidopsis thaliana protein–protein interaction network, known targets of Pseudomonas syringae and Hyaloperonospora arabidopsidis effectors, and gene expression profiles in the immune response. In particular, we focused on the characteristic network topology of the effector targets and differentially expressed genes (DEGs). We found that effectors tended to manipulate key network positions with higher betweenness centrality. The effector targets, especially those that are common targets of an individual effector, tended to be clustered together in the network. Moreover, the distances between the effector targets and DEGs increased over time during infection. In line with this observation, pathogen-susceptible mutants tended to have more DEGs surrounding the effector targets compared with resistant mutants. Our results suggest a common plant–pathogen interaction pattern at the cellular network level, where pathogens employ potent local impact mode to interfere with key positions in the host network, and plant organizes an in-depth defense by sequentially activating genes distal to the effector targets.

EffectorK, a comprehensive resource to mine for pathogen effector targets in the Arabidopsis proteome

“…We have reinforced previously described intra- and interspecific convergence of effector targeting with effectors from two new species [11, 12], and showed at the same time that most effector targets are pathogen specific (Fig 2 and S2). Our analyses also supported the previously described tendency of effectors to interact with plant proteins better connected and central in the network [43, 45], and showed that this tendency is even stronger among effector hubs, multi-pathogen targets and bacterial core T3E targets (Table 2 and Fig S5).…”

“…In this work, by compiling our experimental interactomic data on Xcc and Rps and the literature-curated interactions from a wide variety of other pathogen effectors, we extended the notion that effectors tend to privilege interactions with host proteins with higher Ath degree and betweenness centrality [43, 45]. Furthermore, we showed that this tendency is stronger among effector hubs compared to single targets and among multi-pathogen effector targets compared to pathogen-specific targets.…”

“…The betweenness centrality of a protein is the fraction of all shortest paths connecting two proteins from the network that pass through it. There are two main types of key proteins in a network [43]: 1) proteins important for local network organization, typically showing high degree, and 2) proteins important for the global diffusion of the information through the network, characterized by high betweenness centrality. It had been previously reported in more limited networks that effectors tend to target host proteins with high degree and centrality [43–45].…”

Integrative network analyses of wilt transcriptome in chickpea reveal genotype dependent regulatory hubs in immunity and susceptibility

“…Consequently, network-based protein-protein interaction (PPI) characterize intricate and interwoven relationships that govern cellular functions. Thus, integrating PPI and gene-expression profile provides novel insights into functional interactions amongst deregulated genes 21 – 25 . This combined approach can provide insights into regulation of cellular processes and identify the interaction architecture and the underlying gene regulatory networks 26 .…”

Integrated analysis of full-length transcriptome and secondary metabolism reveals novel regulation in Paulownia fortunei infected with phytoplasma

“…Flavonoids and other substances are used mainly as antioxidants to eliminate reactive oxygen species produced by plants in response to biological stress[ 42]. In P. fortunei, the flavonoids may be used as antioxidants to eliminate the damage caused by excess reactive oxygen, which may play a role in balancing plant defense responses.Pfwus responded to PaWB to regulate morphological variations When invaded by a pathogen, host plants initiate pathogen-associated molecular pattern-triggered immunity and effector-triggered immunity responses, and gene expression patterns of the host plant change[ 43]. Previous studies showed that squamosa promoter binding protein-like 9 SPL9 is the major target of miR156b, and SPL9 by physically interacting with the WUS may regulate axillary bud formation and branching[ 26].…”