The soybean rust pathogen Phakopsora pachyrhizi displays transposable element proliferation that correlates with broad host-range adaptation on legumes

Abstract

Asian soybean rust, caused by Phakopsora pachyrhizi, is one of the world's most economically damaging agricultural diseases. Despite P. pachyrhizi's impact, the exceptional size and complexity of its genome prevented generation of an accurate genome assembly. We simultaneously sequenced three P. pachyrhizi genomes uncovering a genome up to 1.25 Gb comprising two haplotypes with a transposable element (TE) content of ~93%. The proliferation of TEs within the genome occurred in several bursts and correlates with the radiation and speciation of the legumes. We present data of clear de-repression of TEs that mirrors expression of virulence-related candidate effectors. We can see a unique expansion in amino acid metabolism for this fungus. Our data shows that TEs play a dominant role in P. pachyrhizi's genome and have a key impact on various processes such as host range adaptation, stress responses and genetic plasticity of the genome.

Long‐term and rapid evolution in powdery mildew fungi

“…In eukaryotes, TEs can occupy large proportions of the genome. One extreme example is the Asian soybean rust fungus Phakopsora pachyrhizi , with around 93% of its genome being inhabited by TEs (Gupta et al, 2022). In response, eukaryotic organisms evolved means to mitigate or suppress TE activity, such as RNA interference (RNAi), RNAi‐directed DNA methylation, and epigenetic silencing of repetitive elements (Gladyshev, 2017).…”

An Improved 1.5-Gigabase Draft Assembly of Massospora cicadina (Zoopagomycota), an Obligate Fungal Parasite of 13- and 17-Year Cicadas

“…The genome of M. cicadina strain MCPNR19 is a significant improvement over the previously sequenced strain MICH 231384 ( 5 ). Similarly to the 1.018-Gbp myrtle rust genome ( 43 ) and the 1.25-Gbp soybean rust genome ( 44 ), 92% (1.369 Gbp) of the MCPNR19 genome consists of TEs, 73% of which are LTR Ty3 retrotransposons. The low predicted protein-coding gene count likely reflects gene undercalling in the absence of transcriptome sequencing (RNA-seq) data and efforts to avoid overpredicting TEs as genes ( Table 1 ).…”

A decade after the first Pucciniales genomes: A bibliometric snapshot of (post) genomics studies in three model rust fungi

“…Only recently, sequencing and assembly of larger rust genomes (of hundreds of Megabases to over a Gigabase) was made possible by including high amounts of long molecule sequencing, for instance by using the PacBio HiFi technology ( Wu et al, 2020 ; Tobias et al, 2021 ; Henningsen et al, 2022 ; Liang et al, 2022 ). Notably, the recent genome analysis of three isolates of the Asian soybean rust fungus Phakopsora pachyrhizi revealed extremely high (>90%) content of transposable elements and a drastic expansion of gene families related to amino acid metabolism ( Gupta et al, 2022 ). Finally, for a handful of rust species, such as P. pachyrhizi , Hemileia vastatrix (the coffee rust fungus), or Puccinia triticina (the wheat leaf rust fungus), coordinated studies involving genomics, transcriptomics, and gene family analyses have revealed candidate effectors; some of which have been already functionally investigated ( Kunjeti et al, 2016 ; Qi et al, 2016 , 2018 ; Segovia et al, 2016 ; Maia et al, 2017 ).…”