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.

Keywords: Basidiomycota; Biogenic radiation; Biological specialization; Hologenetic ladder hypothesis; Melampsorineae; Phytopathogenic fungi; Pucciniaceae; Pucciniomycotina; Uredinales.

Fig. 1

Alternation of generations, depicted in a species of Melampsora, illustrating stages of the Pucciniales life cycle that may reinforce host association via natural selection. In the outer circle, blue indicates aecial (gametophytic) stage and red indicates telial (sporophytic) stage. Illustration adapted from Merje Toome (2010) with permission.

Fig. 2

The Pucciniales. Letters identify the same nodes found in Fig. 3, Fig. 4. Numbers adjacent to nodes represent median ages in millions of years. Blue bars represent 95 % highest posterior density around the nodes. Taxa are labelled with their corresponding aecial (circles) and telial (squares) host families. The Host Reconciliation Analysis illustrates the steps involved in reconciling host and rust phylogenies. Each step is a different coevolutionary event (e.g. cospeciation, duplications, losses, etc.) that can involve different costs. In host reconciliation analysis, all evolutionary events are given a cost of 1, except: * = cospeciation is given a cost of 0; and ** = duplication and host switching is given a cost of 2. See text and Supplementary Information Table S5 for details.

Fig. 3

The Melampsorineae. Letters identify the same nodes found in Fig. 2, Fig. 4. All other details are the same as those described in the caption for Fig. 2.

Fig. 4

The Pucciniaceae. Letters identify the same nodes found in Fig. 2, Fig. 3. All other details are the same as those described in the caption for Fig. 2.