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Title: Divergent and convergent modes of interaction between wheat and Puccinia graminis f. sp. tritici isolates revealed by the comparative gene co-expression network and genome analyses

Author
item Rutter, William
item SALCEDO, ANDRES - Kansas State University
item AKHUNOVA, ALLINA - Kansas State University
item WANG, SICHEN - Texas A&M University
item HANQUAN, LIANG - Sun Yat-Sen University
item Bowden, Robert
item AKHUNOVA, EDUARD - Kansas State University

Submitted to: BMC Genomics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/3/2017
Publication Date: 4/12/2017
Publication URL: http://handle.nal.usda.gov/10113/5678134
Citation: Rutter, W.B., Salcedo, A., Akhunova, A., Wang, S., Hanquan, L., Bowden, R.L., Akhunova, E. 2017. Divergent and convergent modes of interaction between wheat and Puccinia graminis f. sp. tritici isolates revealed by the comparative gene co-expression network and genome analyses. Biomed Central (BMC) Genomics. 18:291. doi:10.1186/s12864-017-3678-6.

Interpretive Summary: Stem rust is a historically important disease of wheat that was largely overcome through improved host resistance. Unfortunately, new highly virulent races have recently emerged in Africa that threaten existing resistant cultivars around the world. The causal fungus of stem rust, Puccinia graminis, is thought to inject small protein molecules known as effectors into plant cells in order to dampen plant defense response networks. Despite their importance, little is known about the effectors and their host targets. Using infected leaf tissue, we studied the gene co-expression networks of wheat genes and pathogen effectors from two different races of the stem rust fungus. Many different effectors appeared to target the same limited set of host defense networks in the plant, which suggests a degree of functional redundancy of the pathogen effectors. Understanding the whole set of effectors and their targets may be useful in designing more durable resistance to wheat stem rust by directly targeting the redundancy.

Technical Abstract: Two opposing evolutionary constraints exert pressure on pathogens: one to diversify virulence factors in order to evade host defenses, and the other to retain virulence factors critical for maintaining a compatible interaction. To better understand how the diversified arsenals of fungal genes promote interaction with the same compatible wheat host, we performed a comparative genomic analysis of two North American isolates of Puccinia graminis f. sp. tritici (Pgt). The patterns of inter-isolate divergence in the secreted candidate effector genes were compared with the levels of conservation and divergence of host-pathogen gene co-expression networks (GCN) developed for each isolate. Gene Ontology (GO) analyses of the conserved and unique parts of the isolate-specific GCNs identified a number of conserved host pathways targeted by both isolates. Interestingly, the degree of inter-isolate sub-network conservation varied widely for the different host pathways and was positively associated with the proportion of conserved effector candidates associated with each sub-network. While different Pgt isolates tended to exploit similar wheat pathways for infection, the mode of host-pathogen interaction varied for different pathways with some pathways being associated with the conserved set of effectors and others being linked with the diverged or isolate-specific effectors. These findings suggest that pathogen populations can maintain diversified sets of effector genes capable of targeting the same host’s biological pathways, thereby creating the basis for diverse virulence strategies that can be utilized by a pathogen to establish compatible interaction with its host.