Chromosome-level assembly of the Phytophthora agathidicida genome reveals adaptation in effector gene families

Authors: COX, MURRAY - Massey University; GUO, YANAN - Massey University; WINTER, DAVID - Institute Of Environmental Science And Research; SEN, DIYA - Scion; CAULDRON, NICHOLAS - Oregon State University; SHILLER, JASON - Scion; BRADLEY, ELLIE - Massey University; GANLEY, AUSTEN - University Of Auckland; GERTH, MONICA - Victoria University Of Wellington; LACEY, RANDY - Victoria University Of Wellington; MCDOUGAL, REBECCA - Scion; PANDA, PREETI - Plant And Food Research; WILLIAMS, NARI - Plant And Food Research; Grunwald, Niklaus - Nik; MESARICH, CARL - Massey University; BRADSHAW, ROSIE - Massey University

Submitted to: Frontiers in Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/11/2022
Publication Date: 12/2/2022
Citation: Cox, M.P., Guo, Y., Winter, D.J., Sen, D., Cauldron, N.C., Shiller, J., Bradley, E.L., Ganley, A.R., Gerth, M.L., Lacey, R.F., McDougal, R.L., Panda, P., Williams, N.M., Grunwald, N.J., Mesarich, C.H., Bradshaw, R.E. 2022. Chromosome-level assembly of the Phytophthora agathidicida genome reveals adaptation in effector gene families. Frontiers in Microbiology. 13. Article 1038444. https://doi.org/10.3389/fmicb.2022.1038444.
DOI: https://doi.org/10.3389/fmicb.2022.1038444

Interpretive Summary: Phytophthora species are notorious plant pathogens, with some causing devastating tree diseases that threaten the survival of their host species. One such example is Phytophthora agathidicida, the causal agent of kauri dieback – a root and trunk rot disease that kills the ancient, iconic and culturally significant tree species, Agathis australis native to New Zealand. A deeper understanding of how Phytophthora pathogens infect their hosts and cause disease is critical for the development of effective treatments. Such an understanding can be gained by interrogating pathogen genomes for genes, which are involved in causing disease. We sequenced and assembled the P. agathidicida genome. This is the first Phytophthora genome assembled to chromosome level. The novel P. agathidicida genome will help decipher how Phytophthora pathogens have evolved to cause disease on kauri tree. Ultimately, the analysis of this genome will inform new methods of disease control.

Technical Abstract: Phytophthora species are notorious plant pathogens, with some causing devastating tree diseases that threaten the survival of their host species. One such example is Phytophthora agathidicida, the causal agent of kauri dieback – a root and trunk rot disease that kills the ancient, iconic and culturally significant tree species, Agathis australis (New Zealand kauri). A deeper understanding of how Phytophthora pathogens infect their hosts and cause disease is critical for the development of effective treatments. Such an understanding can be gained by interrogating pathogen genomes for effector genes, which are involved in virulence or pathogenicity. Although genome sequencing has become more affordable, the complete assembly of Phytophthora genomes has been problematic, particularly for those with a high abundance of repetitive sequences. In such cases, effector genes located in repetitive regions could be truncated or missed in a fragmented genome assembly. Using a combination of long-read PacBio sequences, chromatin conformation capture (Hi-C) and Illumina short reads, we assembled the P. agathidicida genome into ten complete chromosomes, with a genome size of 57 Mb including 34% repeats. This is the first Phytophthora genome assembled to chromosome level and it reveals a high level of syntenic conservation with the complete genome of Peronospora effusa, the only other complete genome of an oomycete. All P. agathidicida chromosomes have clearly defined centromeres and contain candidate effector genes such as RXLRs and CRNs, but in different proportions, reflecting the presence of gene family clusters. Candidate effector genes were predominantly found in gene-poor, repeat-rich regions of the genome, and in some cases showed a high degree of duplication. Analysis of candidate RXLR effector genes indicated that half of the multicopy gene families were not expressed in planta. Candidate CRN effector gene families showed evidence of recombination leading to new combinations of protein domains, both within and between chromosomes, predicted to be caused by both RNA and DNA transposable elements nearby. The P. agathidicida genome assembly will help decipher how Phytophthora pathogens have evolved to shape their effector repertoires and how they might adapt in the future. Ultimately, the analysis of this complete genome assembly will inform new methods of disease control against P. agathidicida and other Phytophthora species.