Austropuccinia psidii, causing myrtle rust, has a gigabase-sized genome shaped by transposable elements.

Peri A Tobias,Zhenyan Lou,Karanjeet Sandhu,Robert F Park,Ashley Jones,Cecilia H Deng,Benjamin Schwessinger,Jana Sperschneider,David Chagné,Josquin Tibbits,Grant R Smith,Chen Wu,Peng Zhang,Chongmei Dong,J Berman

doi:10.1093/g3journal/jkaa015

Abstract

Austropuccinia psidii, originating in South America, is a globally invasive fungal plant pathogen that causes rust disease on Myrtaceae. Several biotypes are recognized, with the most widely distributed pandemic biotype spreading throughout the Asia-Pacific and Oceania regions over the last decade. Austropuccinia psidii has a broad host range with more than 480 myrtaceous species. Since first detected in Australia in 2010, the pathogen has caused the near extinction of at least three species and negatively affected commercial production of several Myrtaceae. To enable molecular and evolutionary studies into A. psidii pathogenicity, we assembled a highly contiguous genome for the pandemic biotype. With an estimated haploid genome size of just over 1 Gb (gigabases), it is the largest assembled fungal genome to date. The genome has undergone massive expansion via distinct transposable element (TE) bursts. Over 90% of the genome is covered by TEs predominantly belonging to the Gypsy superfamily. These TE bursts have likely been followed by deamination events of methylated cytosines to silence the repetitive elements. This in turn led to the depletion of CpG sites in TEs and a very low overall GC content of 33.8%. Compared to other Pucciniales, the intergenic distances are increased by an order of magnitude indicating a general insertion of TEs between genes. Overall, we show how TEs shaped the genome evolution of A. psidii and provide a greatly needed resource for strategic approaches to combat disease spread.

Highlights

The globally invasive fungal plant pathogen, Austropuccinia psidii
The major peak largely overlaps with the GC content profile of transposable element (TE), while the second peak overlaps with the GC content of genes in the A. psidii genome. We investigated if these AT-rich regions are specific to A. psidii or if they are present in other rust fungi
We identified that 47% and 40% of predicted effectors are localized to the apoplast in the primary and secondary A. psidii assemblies respectively, indicating a potential non-cytoplasmic role in host manipulation

Summary

Introduction

The globally invasive fungal plant pathogen, Austropuccinia psidii (G. Winter) Beenken (Beenken 2017), was first reported in South America (Winter 1884) on guava (Psidium guajava) and named Puccinia psidii. The disease represents a relatively recent arrival in these geographic regions with first detection in Hawaii in 2005, China in 2009, Australia in 2010, New Caledonia in 2013, and New Zealand in 2017 (Carnegie & Pegg 2018). It appears that A. psidii is spreading rapidly and causing devastating impacts to natural vegetation communities (Soewarto et al 2018; Carnegie et al 2015). The pathogen causes disease symptoms on the new foliage, stems and buds (Tobias et al 2015; Carnegie et al 2015) of a wide range of perennial plants with over 480 known host species globally (Soewarto et al 2019). There is little understanding of how this pathogen overcomes defense mechanisms and infects its diverse range of host plants, and even less understanding of why widespread, but very variable, within host resistance is observed

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