The Plant-Dependent Life Cycle of Thecaphora thlaspeos: A Smut Fungus Adapted to Brassicaceae

Abstract

Smut fungi are globally distributed plant pathogens that infect agriculturally important crop plants such as maize or potato. To date, molecular studies on plant responses to smut fungi are challenging due to the genetic complexity of their host plants. Therefore, we set out to investigate the known smut fungus of Brassicaceae hosts, Thecaphora thlaspeos. T. thlaspeos infects different Brassicaceae plant species throughout Europe, including the perennial model plant Arabis alpina. In contrast to characterized smut fungi, mature and dry T. thlaspeos teliospores germinated only in the presence of a plant signal. An infectious filament emerges from the teliospore, which can proliferate as haploid filamentous cultures. Haploid filaments from opposite mating types mate, similar to sporidia of the model smut fungus Ustilago maydis. Consistently, the a and b mating locus genes are conserved. Infectious filaments can penetrate roots and aerial tissues of host plants, causing systemic colonization along the vasculature. Notably, we could show that T. thlaspeos also infects Arabidopsis thaliana. Exploiting the genetic resources of A. thaliana and Arabis alpina will allow us to characterize plant responses to smut infection in a comparative manner and, thereby, characterize factors for endophytic growth as well as smut fungi virulence in dicot plants.

Smut infection of perennial hosts: the genome and the transcriptome of the Brassicaceae smut fungus Thecaphora thlaspeos reveal functionally conserved and novel effectors

“…We previously described the presence of a mating system in T. thlaspeos (Frantzeskakis et al ., ). Now, the mating type loci a1 and a2 of LF1 and LF2 are assembled revealing massive rearrangements between T. thlaspeos (Fig.…”

“…To assemble the reference genome for T. thlaspeos , gDNA from the haploid strain LF1 of the mating type a1b1 (Frantzeskakis et al ., ) was sequenced using both long‐read ( PacBio , c . 40× coverage) and short‐read (Illumina MiSeq, c .…”

“…S2) and downstream signaling components of mating, such as the transcription factor prf1 and genes involved in signaling via the cAMP pathway and the MAPK cascade, are conserved in T. thlaspeos (Table S10) (Feldbrügge et al ., ). Hence, the mating process of T. thlaspeos (Frantzeskakis et al ., ) appears to rely on the same molecular processes that are conserved in smut fungi.…”

“…The Thecaphora thlaspeos-Brassicaceae pathosystem is a remarkable example of a sustained systemic plantÀmicrobe interaction. T. thlaspeos establishes an infection of the entire plant, which can be maintained over several years (Vanky et al, 2008;Frantzeskakis et al, 2017). After penetration, intercellular hyphae of T. thlaspeos proliferate along the vasculature throughout the entire plant without visible impact on plant development.…”

“…T. thlaspeos is a relative of the well studied grass smut Ustilago maydis, which is adapted to Brassicaceae hosts (Vanky et al, 2008;Frantzeskakis et al, 2017). Closely related sister species of T. thlaspeos comprise devastating crop pathogens such as T. solani on potato (up to 85% losses, Andrade et al, 2004) or T. frezii on peanut (Andrade et al, 2004;Conforto et al, 2013).…”