Deconstructing the evolutionary complexity between rust fungi (Pucciniales) and their plant hosts

Abstract

The rust fungi (Pucciniales) are the most speciose natural group of plant pathogens, members of which possess the most complex lifecycles in Fungi. How natural selection works on the Pucciniales has been the subject of several hypotheses in mycology. This study uses molecular age estimation using sequence data from multiple loci, and cophylogeny reconciliation analyses to test hypotheses regarding how the aecial and telial stages in the lifecycle of rust fungi may have differentially impacted their diversification. Molecular age estimates show that the timing of diversification in the Pucciniales correlates with the diversification of their gymnosperm and angiosperm hosts. Host reconciliation analyses suggest that systematic relationships of hosts from the aecial stage of the Pucciniales lifecycle better reflect the systematic relationships among the Pucciniales. The results demonstrate the relative importance of this stage on the overall evolution of the Pucciniales and supports hypotheses made by Leppik over half a century ago. This study represents the first evaluation of how different life stages in the Pucciniales shape the evolution of these fungi.

An evolutionary framework for host shifts – jumping ships for survival

“…An example for (4) is the anther‐smut genus Microbotryum , in which it is still apparent that the ancestral host family was the Polygonaceae, but several subsequent host jumps to a number of families, including Dipsacaceae, Asteraceae and Caryophyllaceae have resulted in a considerable expansion of the genus (Kemler et al ., ). Finally (5), there are genera such as Peronospora (Voglmayr, ), Plasmopara (Voglmayr et al ., ), and Puccina (Aime et al ., ) for which the original host group is no longer obvious and cannot be ascertained based on currently available data.…”

“…A special situation is present in the rust fungi of the class Pucciniomycetes, many of which perform an obligate host switch during their life cycle, so specific stages occur on a specific host. In the case of the rust fungi of the class Pucciniales, the hosts often belong to phylogenetically distant groups, such as angiosperms and gymnosperms or monocots and dicots (Aime et al ., ). The host switching within the life cycle in these cases is likely enabled by a strong separation of gene regulation in monokaryotic and dikaryotic hyphae (Lorrain et al ., ), which might be enabled by stage‐specific transcription factors that can only be activated or deactivated in the presence or absence of a second nucleus in a hyphal compartment.…”

“…While there is no selection towards jumping to a new hostthis happens by chancethere will be selection pressure to maintain the possibility of jumping if the boundary conditions are met, as otherwise pathogens would likely eventually face extinction over the course of evolution. A result of this is the plethora of host jump events that have been identified in various successful (in terms of species diversity and abundance) pathogen groups (Voglmayr, 2003;V agi et al, 2007;Thines & Kummer, 2013;Thines, 2014;Aime et al, 2018;Kruse et al, 2018a).…”

“…Puccina ( Aime et al, 2018) for which the original host group is no longer obvious and cannot be ascertained based on currently available data.…”

Puccinia modiolae in North America: distribution and natural host range

“…DNA was extracted and the 5’ end of the nuclear 28S rDNA, amplified with rust-specific primers and sequenced following previous published protocols (Aime 2006, Aime et al 2018). Sequences were edited using Sequencher 5.2.3 (Gene Codes Corp., Ann Arbor, MI) and aligned using the MUSCLE algorithm in Geneious 9.1.5 (Biomatters Ltd., Newark, NJ).…”