The Rust Fungus Melampsora larici-populina Expresses a Conserved Genetic Program and Distinct Sets of Secreted Protein Genes During Infection of Its Two Host Plants, Larch and Poplar

Abstract

Mechanisms required for broad-spectrum or specific host colonization of plant parasites are poorly understood. As a perfect illustration, heteroecious rust fungi require two alternate host plants to complete their life cycles. Melampsora larici-populina infects two taxonomically unrelated plants, larch, on which sexual reproduction is achieved, and poplar, on which clonal multiplication occurs, leading to severe epidemics in plantations. We applied deep RNA sequencing to three key developmental stages of M. larici-populina infection on larch: basidia, pycnia, and aecia, and we performed comparative transcriptomics of infection on poplar and larch hosts, using available expression data. Secreted protein was the only significantly overrepresented category among differentially expressed M. larici-populina genes between the basidial, the pycnial, and the aecial stages, highlighting their probable involvement in the infection process. Comparison of fungal transcriptomes in larch and poplar revealed a majority of rust genes were commonly expressed on the two hosts and a fraction exhibited host-specific expression. More particularly, gene families encoding small secreted proteins presented striking expression profiles that highlight probable candidate effectors specialized on each host. Our results bring valuable new information about the biological cycle of rust fungi and identify genes that may contribute to host specificity.

Fusarium virguliforme Transcriptional Plasticity Is Revealed by Host Colonization of Maize versus Soybean

“…Indeed, while the vast majority of the transcriptome was expressed during fungal colonization of both maize and soybean, the induction of genes underlying distinct, often divergent, biological processes were temporally distinct. This observation agrees with previous studies which identified temporal changes of gene expression during colonization of hosts by the same fungus exhibiting different lifestyles (Lahrmann et al, 2013;Lorrain et al, 2018), and this may suggest a reduction in a shift to necrotrophy on maize.…”

An evolutionary framework for host shifts – jumping ships for survival

“…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. By switching hosts concomitantly, the possibility of variation beyond optimal interaction is provided – sub‐optimal performance on one of the two hosts may be outweighed by more successful performance on the other.…”

Advances in understanding obligate biotrophy in rust fungi

“…Very little information is available about infection mechanisms of alternate hosts and sexual stages. To date, only a handful of studies have considered gene expression on the alternate host and they have revealed concomitant expression of sets of candidate effectors in both hosts as well as in each host individually (Xu et al ., ; Liu et al ., ; Cuomo et al ., ; Lorrain et al ., ). This type of approach is particularly helpful for narrowing down the list of effectors related to the main host where disease causes the most significant damage.…”