The smut fungus Ustilago esculenta has a bipolar mating system with three idiomorphs larger than 500 kb

Liang, Syun Wun; Huang, Yen Hua; Chiu, Jian Ying; Tseng, Hsin Wan; Huang, Jin Hsing; Shen, Wei

doi:10.1016/j.fgb.2019.02.007

Cited by 10 publications

(11 citation statements)

References 39 publications

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“…Indeed, with linked HD and PR loci, a given diploid individual produces only two New Phytologist (2021) 229: 2470-2491 Ó 2020 The Authors New Phytologist Ó 2020 New Phytologist Foundation www.newphytologist.com mating types among its progeny, instead of four as occurs with unlinked mating-type loci; a given gamete is therefore compatible with half of other gametes instead of one quarter of them. The linkage of the two mating-type loci thus is beneficial under selfing, and has occurred repeatedly in several basidiomycete genera, such as the Microbotryum anther-smuts (Branco et al, 2017), the Cryptococcus human pathogen (Fraser & Heitman, 2005), the Malassezia human pathogens (Xu et al, 2007;Gioti et al, 2013), and the Sporisorium and Ustilago cereal smuts (Bakkeren & Kronstad, 1994;Que et al, 2014;Taniguti et al, 2015;Rabe et al, 2016;Liang et al, 2019). The region of suppressed recombination linking HD and PR loci can span from c. 100 kb and 20 genes in C. neoformans to 600 genes and megabases of DNA in Microbotryum fungi (Fraser & Heitman, 2005;Branco et al, 2017), trapping in-between many genes with no functions in mating.…”

Section: Uniparental Mitochondrion Inheritance or Selfing Mating Systems Can Trigger Beneficial Recombination Suppression Around Fungal Mmentioning

confidence: 99%

“…Beyond the advantage of reproductive assurance, selfing also can be selected for due to the automatic fitness advantage of transmitting twice as many of gene copies (Busch & Delph, 2012). In at least three genera or families – Microbotryum , Ustilago, Cryptococcus – multiple independent events of HD–PR linkage even occurred within clades (Bakkeren & Kronstad, 1994; Rabe et al ., 2016; Branco et al ., 2018; Liang et al ., 2019; Sun et al ., 2019), revealing frequent evolutionarily convergent events within each of these genera.…”

Section: Uniparental Mitochondrion Inheritance or Selfing Mating Syst...mentioning

confidence: 99%

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Recombination suppression and evolutionary strata around mating‐type loci in fungi: documenting patterns and understanding evolutionary and mechanistic causes

et al. 2020

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Summary Genomic regions determining sexual compatibility often display recombination suppression, as occurs in sex chromosomes, plant self‐incompatibility loci and fungal mating‐type loci. Regions lacking recombination can extend beyond the genes determining sexes or mating types, by several successive steps of recombination suppression. Here we review the evidence for recombination suppression around mating‐type loci in fungi, sometimes encompassing vast regions of the mating‐type chromosomes. The suppression of recombination at mating‐type loci in fungi has long been recognized and maintains the multiallelic combinations required for correct compatibility determination. We review more recent evidence for expansions of recombination suppression beyond mating‐type genes in fungi (‘evolutionary strata’), which have been little studied and may be more pervasive than commonly thought. We discuss testable hypotheses for the ultimate (evolutionary) and proximate (mechanistic) causes for such expansions of recombination suppression, including (1) antagonistic selection, (2) association of additional functions to mating‐type, such as uniparental mitochondria inheritance, (3) accumulation in the margin of nonrecombining regions of various factors, including deleterious mutations or transposable elements resulting from relaxed selection, or neutral rearrangements resulting from genetic drift. The study of recombination suppression in fungi could thus contribute to our understanding of recombination suppression expansion across a broader range of organisms.

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Section: Uniparental Mitochondrion Inheritance or Selfing Mating Systems Can Trigger Beneficial Recombination Suppression Around Fungal Mmentioning

confidence: 99%

Section: Uniparental Mitochondrion Inheritance or Selfing Mating Syst...mentioning

confidence: 99%

Recombination suppression and evolutionary strata around mating‐type loci in fungi: documenting patterns and understanding evolutionary and mechanistic causes

et al. 2020

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“…The interaction between the host and pathogen is also very important in the early stage of disease occurrence when the mycelium began to invade the plant cells, such as in rice and blast fungus and maize and U. maydis interactions [29,36]. Previous studies have characterized some genes related to stem enlargement in Z. latifolia and U. esculenta separately [10,37,38], but the analyses were not sufficiently systematic or comprehensive. RNA-seq has been successfully used to study the patterns of global gene expression in both plants and pathogenic fungi during plant-pathogen interactions [28,29,31].…”

Section: Discussionmentioning

confidence: 99%

Mixed Transcriptome Analysis Revealed the Possible Interaction Mechanisms between Zizania latifolia and Ustilago esculenta Inducing Jiaobai Stem-Gall Formation

Zhang

Song

Liu

et al. 2021

IJMS

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The smut fungus Ustilago esculenta infects Zizania latifolia and induces stem expansion to form a unique vegetable named Jiaobai. Although previous studies have demonstrated that hormonal control is essential for triggering stem swelling, the role of hormones synthesized by Z. latifolia and U. esculenta and the underlying molecular mechanism are not yet clear. To study the mechanism that triggers swollen stem formation, we analyzed the gene expression pattern of both interacting organisms during the initial trigger of culm gall formation, at which time the infective hyphae also propagated extensively and penetrated host stem cells. Transcriptional analysis indicated that abundant genes involving fungal pathogenicity and plant resistance were reprogrammed to maintain the subtle balance between the parasite and host. In addition, the expression of genes involved in auxin biosynthesis of U. esculenta obviously decreased during stem swelling, while a large number of genes related to the synthesis, metabolism and signal transduction of hormones of the host plant were stimulated and showed specific expression patterns, particularly, the expression of ZlYUCCA9 (a flavin monooxygenase, the key enzyme in indole-3-acetic acid (IAA) biosynthesis pathway) increased significantly. Simultaneously, the content of IAA increased significantly, while the contents of cytokinin and gibberellin showed the opposite trend. We speculated that auxin produced by the host plant, rather than the fungus, triggers stem swelling. Furthermore, from the differently expressed genes, two candidate Cys2-His2 (C2H2) zinc finger proteins, GME3058_g and GME5963_g, were identified from U. esculenta, which may conduct fungus growth and infection at the initial stage of stem-gall formation.

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“…Dimorphism conversion from saprophytic haploid to parasitic dikaryotic mycelium is critical for the colonization of U. esculenta and other smut fungi [ 15 , 16 , 17 ]. It is regulated by mating loci a and b .…”

Section: Introductionmentioning

confidence: 99%

Transcriptome Comparison between Two Strains of Ustilago esculenta during the Mating

Wang

Gao

Yin

et al. 2022

JoF

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Ustilago esculenta is a smut fungus that obligately infects Zizania latifolia and stimulates tissue swelling to form galls. Unlike T-type, MT-type U. esculenta can only proliferate within plant tissues and infect the offspring of their host. Production of telispores, haploid life, and plant cuticle penetration are not essential for it, which may lead to the degeneration in these processes. Transcriptome changes during the mating of T- and MT-type U. esculenta were studied. The functions of several secreted proteins were further confirmed by knock-out mutants. Our results showed that MT-type U. esculenta can receive environmental signals in mating and circumstance sensing as T-type does. However, MT-type U. esculenta takes a longer time for conjunction tube formation and cytoplasmic fusion. A large number of genes encoding secreted proteins are enriched in the purple co-expression module. They are significantly up-regulated in the late stage of mating in T-type U. esculenta, indicating their relationship with infecting. The knock-out of g6161 (xylanase) resulted in an attenuated symptom. The knock-out of g943 or g4344 (function unidentified) completely blocked the infection at an early stage. This study provides a comprehensive comparison between T- and MT-type during mating and identifies two candidate effectors for further study.

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The smut fungus Ustilago esculenta has a bipolar mating system with three idiomorphs larger than 500 kb

Cited by 10 publications

References 39 publications

Recombination suppression and evolutionary strata around mating‐type loci in fungi: documenting patterns and understanding evolutionary and mechanistic causes

Recombination suppression and evolutionary strata around mating‐type loci in fungi: documenting patterns and understanding evolutionary and mechanistic causes

Mixed Transcriptome Analysis Revealed the Possible Interaction Mechanisms between Zizania latifolia and Ustilago esculenta Inducing Jiaobai Stem-Gall Formation

Transcriptome Comparison between Two Strains of Ustilago esculenta during the Mating

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The smut fungus Ustilago esculenta has a bipolar mating system with three idiomorphs larger than 500 kb

Cited by 10 publications

References 39 publications

Recombination suppression and evolutionary strata around mating‐type loci in fungi: documenting patterns and understanding evolutionary and mechanistic causes

Recombination suppression and evolutionary strata around mating‐type loci in fungi: documenting patterns and understanding evolutionary and mechanistic causes

Mixed Transcriptome Analysis Revealed the Possible Interaction Mechanisms between Zizania latifolia and Ustilago esculenta Inducing Jiaobai Stem-Gall Formation

Transcriptome Comparison between Two Strains of Ustilago esculenta during the Mating

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The smut fungus Ustilago esculenta has a bipolar mating system with three idiomorphs larger than 500 kb