Contributions to the smut fungi of Africa. 7. First records of Tilletia brachypodii-ramosi and Ustilago constantineanui

Two poorly known smut fungi are recorded for the first time from Africa: Tilletia brachypodii-ramosi on Brachypodium retusum (from Morocco) and Ustilago constantineanui on Sporobolus schoenoides (from Algeria). Descriptions and illustrations are provided for these taxa.

Onset and stepwise extensions of recombination suppression are common in mating-type chromosomes of Microbotryum anther-smut fungi

Sex chromosomes and mating-type chromosomes can display large genomic regions without recombination. Recombination suppression often extended stepwise with time away from the sex- or mating-type-determining genes, generating evolutionary strata of differentiation between alternative sex or mating-type chromosomes. In anther-smut fungi of the Microbotryum genus, recombination suppression evolved repeatedly, linking the two mating-type loci and extended multiple times in regions distal to the mating-type genes. Here, we obtained high-quality genome assemblies of alternative mating types for four Microbotryum fungi. We found an additional event of independent chromosomal rearrangements bringing the two mating-type loci on the same chromosome followed by recombination suppression linking them. We also found, in a new clade analysed here, that recombination suppression between the two mating-type loci occurred in several steps, with first an ancestral recombination suppression between one of the mating-type locus and its centromere; later, completion of recombination suppression up to the second mating-type locus occurred independently in three species. The estimated dates of recombination suppression between the mating-type loci ranged from 0.15 to 3.58 million years ago. In total, this makes at least nine independent events of linkage between the mating-type loci across the Microbotryum genus. Several mating-type locus linkage events occurred through the same types of chromosomal rearrangements, where similar chromosome fissions at centromeres represent convergence in the genomic changes leading to the phenotypic convergence. These findings further highlight Microbotryum fungi as excellent models to study the evolution of recombination suppression.

Fungal Pathogen Emergence: Investigations with an Ustilago maydis × Sporisorium reilianum Hybrid

The emergence of new fungal pathogens threatens sustainable crop production worldwide. One mechanism by which new pathogens may arise is hybridization. To investigate hybridization, the related smut fungi, Ustilago maydis and Sporisorium reilianum, were selected because they both infect Zea mays, can hybridize, and tools are available for their analysis. The hybrid dikaryons of these fungi grew as filaments on plates but their colonization and virulence in Z. mays were reduced compared to the parental dikaryons. The anthocyanin induction caused by the hybrid dikaryon infections was distinct, suggesting its interaction with the host was different from that of the parental dikaryons. Selected virulence genes previously characterized in U. maydis and their predicted S. reilianum orthologs had altered transcript levels during hybrid infection of Z. mays. The downregulated U. maydis effectors, tin2, pit2, and cce1, and transcription factors, rbf1, hdp2, and nlt1, were constitutively expressed in the hybrid. Little impact was observed with increased effector expression; however, increased expression of rbf1 and hdp2, which regulate early pathogenic development by U. maydis, increased the hybrid’s capacity to induce symptoms including the rare induction of small leaf tumors. These results establish a base for investigating molecular aspects of smut fungal hybrid pathogen emergence.

Smuts to the Power of Three: Biotechnology, Biotrophy, and Basic Biology

Smut fungi are a large group of mainly biotrophic plant pathogens, many of which cause disease on cereal crops [...]

SCREENING OF COLLECTION SAMPLES OF OATS BY RESISTANCE TO DAMAGE OF A DUST SMUT IN THE CONDITIONS OF THE MIDDLE VOLGA

Studies to identify the sources of resistance to dust smut among the collection samples of oats of various ecological and geographical origin, and varieties and breeding lines created in Ulyanovsk Research Institute of Agriculture, were performed on an artificial infectious background of Ulyanovsk Research Institute of Agriculture in the Middle Volga region in 2016-2018. 36 samples were studied that showed varying degrees of resistance-susceptibility to the harmful pathogen, including five varieties with identified resistance genes to diseases caused by smut fungi Ustilago avenae (Pers.) Rostr. and Ustilago kolleri Wille. Allur variety susceptible to dust smut was used as a universal indicator. The indicator variety over the years of research on average was affected by-44.4 %, with the lowest value in 2018 - 25.6 % and the maximum in 2017-58.1 %, when the conditions for the development of the disease were the best. Most of the oat samples studied showed varying degrees of resistance to Ulyanovsk dust smut population: 9 samples were immune, 14 were practically resistant. A significant proportion of stable genotypes were collected samples whose country of origin is the United States (52.2 %) and varieties of local selection (12.7 %). Of particular interest are the stable naked forms of oats, including the new variety of oat Griva. It has shown a high degree of stability over all the years of testing. Weak and medium susceptibility was characterized by 8 and 3 samples, respectively. Severe dust smut damage, over 50 %, was observed in two samples

Microbotryum bardanense and M. polygoni-alati —new records from Nepal

Two smut fungi, Microbotryum bardanense and M. polygoni-alati, are reported for the first time from Nepal. Descriptions, illustrations, and taxonomic notes are provided for these taxa.

A Novel Core Effector Vp1 Promotes Fungal Colonization and Virulence of Ustilago maydis

The biotrophic fungus Ustilago maydis secretes a plethora of uncharacterized effector proteins and causes smut disease in maize. Among the effector genes that are up-regulated during the biotrophic growth in maize, we identified vp1 (virulence promoting 1), which has an expression that was up-regulated and maintained at a high level throughout the life cycle of the fungus. We characterized Vp1 by applying in silico analysis, reverse genetics, phenotypic assessment, microscopy, and protein localization and provided a fundamental understanding of the Vp1 protein in U. maydis. The reduction in fungal virulence and colonization in the vp1 mutant suggests the virulence-promoting function of Vp1. The deletion studies on the NLS (nuclear localization signal) sequence and the protein localization study revealed that the C-terminus of Vp1 is processed after secretion in plant apoplast and could localize to the plant nucleus. The Ustilago hordei ortholog UhVp1 lacks NLS localized in the plant cytoplasm, suggesting that the orthologs might have a distinct subcellular localization. Further complementation studies of the Vp1 orthologs in related smut fungi revealed that none of them could complement the virulence function of U. maydis Vp1, suggesting that UmVp1 could acquire a specialized function via sequence divergence.

Tempo of degeneration across independently evolved non-recombining regions

Recombination is beneficial over the long term, allowing more effective selection. Despite long-term advantages of recombination, local recombination suppression is known to evolve and lead to genomic degeneration, in particular on sex and mating-type chromosomes, sometimes linked to severe genetic diseases. Here, we investigated the tempo of degeneration in non-recombining regions, i.e., the function curve for the accumulation of deleterious mutations over time, taking advantage of 17 independent events of large recombination suppression identified on mating-type chromosomes of anther-smut fungi, including five newly identified in the present study. Using high-quality genomes assemblies of alternative mating types of 13 Microbotryum species, we estimated the degeneration levels in terms of accumulation of non-optimal codons and non-synonymous substitutions in non-recombining regions. We found a reduced frequency of optimal codons in the non-recombining regions on mating-type chromosomes compared to autosomes. We showed that the lower frequency of optimal codons in non-recombining regions was not due to less frequent GC-biased gene conversion or lower ancestral expression levels compared to recombining regions. We estimated that the frequency of optimal codon usage decreased linearly at a rate of 0.989 per My. The non-synonymous over synonymous substitution rate (dN/dS) increased rapidly after recombination suppression and then reached a plateau. To our knowledge this is the first study to disentangle effects of reduced selection efficacy from GC-biased gene conversion in the evolution of optimal codon usage to quantify the tempo of degeneration in non-recombining regions, leveraging on multiple independent recombination suppression events. Understanding the tempo of degeneration is important for our knowledge on genomic evolution, on the origin of genetic diseases and on the maintenance of regions without recombination.

Additions to the smut fungi of the Iberian Peninsula

After examination of specimens, mainly from the herbarium (MA) and the mycological collection (MA-Fungi) of the Royal Botanic Garden of Madrid, we report several novelties on smut fungi within Europe. Two species of smut fungi, Sporisorium egyptiacum and Tilletia viennotii, are reported for the first time from Europe. A finding of Sphacelotheca polygoni-serrulati represents a second record for Europe. Six species of smut fungi, Moreaua kochiana, Schizonella elynae, Sporisorium egyptiacum, Thecaphora thlaspeos, Tilletia viennotii, and Ustanciosporium majus, are recorded for the first time from the Iberian Peninsula. Five species of smut fungi, Moreaua kochiana, Schizonella elynae, Sporisorium egyptiacum, Thecaphora thlaspeos, and Ustanciosporium majus, are newly recorded from Spain. Three species, Moreaua kochiana, Sphacelotheca polygoni-serrulati, and Tilletia viennotii, are new for Portugal. A specimen of Moreaua kochiana represents a new record for France. Arabis serpillifolia is reported as a new host of Thecaphora thlaspeos. New distribution records from the Iberian Peninsula are given for Anthracoidea arenariae, Microbotryum minuartiae, M. silenes-saxifragae, and Tranzscheliella sparti. We also include a phylogenetic analysis of DNA sequences of Moreaua kochiana, generated in this study, to understand this species’ relationships within its genus.