Degree Type

Dissertation

Date of Award

2016

Degree Name

Doctor of Philosophy

Department

Plant Pathology and Microbiology

Major

Genetics and Genomics

First Advisor

Thomas J. Baum

Abstract

Plant-parasitic nematodes (PPN) are among the most devastating plant pathogens. However, our understanding of how nematodes adapted to plant parasitism, and the molecular mechanisms that PPN use during infection is limited. Among the most important genomic changes that occurred in the free-living nematode ancestors of PPN were multiple horizontal gene transfer (HGT) events from bacteria. Though it is clear that HGT helped shape the genomes of many PPN, how this process occurred is unknown. Also, it is evident that successful parasitism occurs from the delivery of proteinaceous effectors into plant roots to hijack and modify host cellular processes.

The research included in this dissertation aims at addressing several important questions regarding HGT in PPN, and investigates important molecular, cellular and developmental processes that are determined critical for successful parasitism. Of particular emphasis throughout this dissertation is the soybean cyst nematode, Heterodera glycines, due to a highly specialized and agronomically important interaction with its soybean host.

Major findings for HGT in PPN include the identification of eighteen new H. glycines effectors, three of which are determined to have been part of more ancient HGT events from rhizosphere bacteria. Additionally, homologs of two of the three HGT genes are shown to have been transferred numerous different times from bacteria to diverse eukaryotes and archaea. The latter findings indicate the likely evolutionary advantages that these genes provided not just to PPN, but many different taxa. Intriguingly, we reveal that a group of retroviruses specific to distal nematode clades is genomically associated with HGT genes in PPN genomes. These retroviruses potentially have all of the elements that would be necessary for HGT to occur in PPN. Thus, we propose the tempting hypothesis that this specific group of retroviruses might have contributed to HGT in these nematodes.

We also reveal several novelties for plant-nematode interactions. Major findings include the discovery of a strongly expressed H. glycines effector that is essential for virulence and efficiently targets plant cell nucleoli for suppression of innate immune responses. Also, this H. glycines effector contains marginal, but significant sequence similarity with an immunosuppressive effector found only in Plasmodium spp., the malaria parasites. Extensive database searches, phylogenetic analyses, and functional complementation experiments conclude that the similarities are best explained by sequence convergence due to similar immunosuppressive functions. Furthermore, we determine that a specific microRNA network in soybean that is essential for plant development delineates the formation of the H. glycines feeding site, and interfering with this network renders soybean roots much less susceptible to infection.

In conclusion, the major findings included in this dissertation reveal novel insights into how nematodes adapted to plant parasitism, and for how PPN manipulate their host plants during infection to establish compatible interactions. Moreover, these findings will undoubtedly provide foundations for developing novel control measures against these important plant pathogens.

Copyright Owner

Jason Brett Noon

Language

en

File Format

application/pdf

File Size

290 pages

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