Transcriptome analysis of poplar rust telia reveals overwintering adaptation and tightly coordinated karyogamy and meiosis processes

Abstract

Most rust fungi have a complex life cycle involving up to five different spore-producing stages. The telial stage that produces melanized overwintering teliospores is one of these and plays a fundamental role for generating genetic diversity as karyogamy and meiosis occur at that stage. Despite the importance of telia for the rust life cycle, almost nothing is known about the fungal genetic programs that are activated in this overwintering structure. In the present study, the transcriptome of telia produced by the poplar rust fungus Melampsora larici-populina has been investigated using whole genome exon oligoarrays and RT-qPCR. Comparative expression profiling at the telial and uredinial stages identifies genes specifically expressed or up-regulated in telia including osmotins/thaumatin-like proteins (TLPs) and aquaporins that may reflect specific adaptation to overwintering as well numerous lytic enzymes acting on plant cell wall, reflecting extensive cell wall remodeling at that stage. The temporal dynamics of karyogamy was followed using combined RT-qPCR and DAPI-staining approaches. This reveals that fusion of nuclei and induction of karyogamy-related genes occur simultaneously between the 25 and 39 days post inoculation time frame. Transcript profiling of conserved meiosis genes indicates a preferential induction right after karyogamy and corroborates that meiosis begins prior to overwintering and is interrupted in Meiosis I (prophase I, diplonema stage) until teliospore germination in early spring.

Symptom development and latent period of Austropuccinia psidii (myrtle rust) in relation to host species, temperature, and ontogenic resistance

“…The possible role of teliospores in high temperature survival of A. psidii is worthy of investigation. The telial stage does not appear to be involved in overwintering for A. psidii , as is the case for many rust species (e.g., Desprez‐Loustau et al , ; Hacquard et al , ), and teliospores were not observed during the overwintering studies in New Zealand. Determining if teliospores play an ecological role at high temperatures would help to understand when the greatest likelihood of genetic recombination within A. psidii occurs (McTaggart et al , ).…”

Half-reserve Mitosis of Sibling Nuclei in Gymnosporangium asiaticum

“…However, the genetic factors controlling the mitotic pathway and whether or not the newborn nuclei are homogenous are still unknown. Hacquard et al (2013) believe nuclei fusion genes Kar5 and Kar9, meiosis genes Rec8、Mre11、Rad50、Rad51、Spo11、Mnd1 are highly expressed before diploid telia formed, and behavior of nuclear is regulated by a kind of mating gene (Shimomura et al, 2012). However, two nuclei in telia did not undergo fusion till germination, and directly develop 4 basidiospores, which infests this short of urediospore fungi are diploid in most life time，including telial stage.…”

Advancing Knowledge on Biology of Rust Fungi Through Genomics

“…Among the most highly regulated genes reported in telia are several with functions possibly related to spore survival, that is, overwintering, such as those encoding thaumatin-like proteins and aquaporins that may help to prevent osmotic damage due to desiccation. Also, several meiotic-related transcripts were overexpressed in teliospores and showed temporal patterns of expression during karyogamy, an important biological process occurring in teliospores (Hacquard, Delaruelle, et al, 2013). These studies demonstrate that the use of common custom oligoarrays is an efficient approach to realize transcriptomic comparisons to gain a better understanding of the biology of the rust fungus at different life cycle stages.…”

“…The rust 191 Advances in Rust Genomics fungus expressed very different genetic programs in these two plant compartments and the most highly expressed fungal genes in the palisade compared to the spongy mesophyll coded for candidate effectors, suggesting that these might play a role in the maintenance of infection structures in planta during the later stages of biotrophy (Hacquard et al, 2010). These gene expression profiles were compared with those obtained from telia of M. larici-populina harvested early in autumn, allowing a direct comparison of expression profiles in another spore-forming structure in the poplar leaf (Hacquard, Delaruelle, et al, 2013). A larger number of genes specifically expressed in telia were found, most of which encode unknown functions.…”