Cleavage of β-carotene as the first step in sexual hormone synthesis in zygomycetes is mediated by a trisporic acid regulated β-carotene oxygenase

Burmester, Anke; Richter, Mareike; Schultze, Kornelia; Voelz, Kerstin; Schachtschabel, Doreen; Boland, Wilhelm; Wöstemeyer, Johannes; Schimek, Christine

doi:10.1016/j.fgb.2007.07.008

Cited by 48 publications

(29 citation statements)

References 63 publications

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“…Here, more attention has been given to the molecular biology of partner recognition that is mediated by trisporoid pheromones, synthesized by degradation of carotene. Some of the genes as well as the corresponding gene products necessary for synthesizing trisporic acid are known in detail (Czempinski et al, 1996;Wetzel et al, 2009;Burmester et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

“…As a general principle, sexual communication in the orders Mucorales and Mortierellales is triggered by trisporic acid and its precursors at different levels of sexual development (Schimek & Wöstemeyer, 2010). Trisporoids originate from b-carotene which is cleaved via different intermediates, studied at the chemical level in P. blakesleeanus (Polaino et al, 2010) and at the enzymic level in B. trispora (Burmester et al, 2007). The intermediate, common to both mating types, is 4-dihydrotrisporin.…”

Section: Introductionmentioning

confidence: 99%

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The mating-related loci sexM and sexP of the zygomycetous fungus Mucor mucedo and their transcriptional regulation by trisporoid pheromones

et al. 2012

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The putative mating type locus of mucoralean fungi consists of a single high mobility group (HMG)-domain transcription factor gene, sexM or sexP, flanked by genes for an RNA helicase and a triosephosphate transporter. We used degenerate primers derived from the amino acid sequence of the RNA helicase to sequence a fragment of this gene from Mucor mucedo. This fragment was extended by inverse PCR to obtain the complete sequences of the sex loci from both mating types of M. mucedo. The sex loci in M. mucedo reflect the general picture obtained previously for Phycomyces blakesleeanus, presenting a single HMG-domain transcription factor gene, sexM and sexP in the minus and plus mating types, respectively. These are located next to a gene for RNA helicase. Transcriptional analysis by quantitative real-time PCR showed that only transcription of sexM is considerably stimulated by adding trisporoid pheromones, thus mimicking sexual stimulation, whereas sexP is only slightly affected. These differences in regulation between sexM and sexP are supported by the observation that the promoter sequences controlling these genes show no similarities. The protein structures themselves are considerably different. The SexM, but not the SexP protein harbours a nuclear localization sequence. The SexM protein is indeed transported to nuclei. This was shown by means of a GFP fusion construct that was used to study the localization of SexM in the yeast Saccharomyces cerevisiae. The fusion protein is highly enriched in nuclei.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The mating-related loci sexM and sexP of the zygomycetous fungus Mucor mucedo and their transcriptional regulation by trisporoid pheromones

et al. 2012

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“…Unlike M. mucedo, B. trispora produces 1,000 times more trisporic acids, and a putative nonheme carotenoid cleavage oxygenase (TSP3) was reported as the first enzyme involved in sex hormone synthesis (16). Hence, we performed transcript analysis in B. trispora for carRA, tsp3, and tsp1, genes involved in three different stages of carotenoid metabolism, and to identify how the developmental phases induce temporal trends in gene expression.…”

Section: Resultsmentioning

confidence: 99%

“…CarS mutants in Phycomyces fail to produce those apocarotenoids present in the wild type (15). No functional characterization has been reported for the CarS homologue in Blakeslea trispora, designated TSP3 (16). All of the C 18 apocarotenoids ( Fig.…”

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confidence: 99%

Early and Late Trisporoids Differentially Regulate β-Carotene Production and Gene Transcript Levels in the Mucoralean Fungi Blakeslea trispora and Mucor mucedo

Sahadevan

Richter-Fecken

Kaerger

et al. 2013

Appl Environ Microbiol

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Blakeslea trispora displayed a very high transcript turnover in the gene for carotenoid cleavage dioxygenase, tsp3, during the sexual phase. An in vivo enzyme assay and chromatographic analysis led to the identification of ␤-apo-12=-carotenal as the first apocarotenoid involved in trisporic acid biosynthesis in B. trispora. Supplementation of C 18 trisporoids, namely D'orenone, methyl trisporate C, and trisporin C, increased tsp3 transcripts in the plus compared to minus partners. Interestingly, the tsp1 gene, which is involved in trisporic acid biosynthesis, was downregulated compared to tsp3 irrespective of asexual or sexual phase. Only the minus partners of both B. trispora and Mucor mucedo had enhanced ␤-carotene production after treatment with C 20 apocarotenoids, 15 different trisporoids, and their analogues. We conclude that the apocarotenoids and trisporoids influence gene transcription and metabolite production, depending upon the fungal strain, corresponding genus, and developmental phase, representing a "chemical dialect" during sexual communication. Mucorales fungi belonging to the subphylum incertae sedis Mucoromycotina (formerly classified in the class Zygomycetes) comprise 9 families, 51 genera, and around 205 species (1). These basal fungi are fast-growing soil saprotrophs that feed on dead and decaying organic matter. The asexual phase predominates their life cycle, with multinucleated haploid sporangiospores that germinate to mycelia of either the plus or minus mating type in heterothallic strains. Adversities, like environmental stresses or nutrient depletion, especially of nitrogen and phosphorus (2), lead to the sexual phase, in which complementary mating partners in close proximity exchange metabolites and form special aerial hyphae known as zygophores. The fusion of zygophores results in thousands of nuclei from both parents in the morphologically modified structure known as the progametangia. During further structural modifications and dormancy, which may extend from months to a year, most of the nuclei undergo degradation. Finally, gametangia bearing two nuclei from opposite partners fuse to form a thick-walled dikaryotic sexual spore known as the zygospore. Mitosis followed by meiosis results in four haploid products in a sporangium that develops from the zygospore (3). One Mucorales species in particular, Blakeslea trispora, has been commercially exploited for its potential to produce an excess of carotenoids, like ␤-carotene and lycopene, during its sexual phase of the life cycle (4, 5). According to a new report by Global Industrial Analysts, Inc., the worldwide market for carotenoids is projected to reach $1.3 billion by 2017. Hence, microbial carotenoids have been in the limelight as an ecofriendly sustainable alternative source for synthetics. Mucoralean carotenoids are not only under investigation for their biotechnological applications but also to help in understanding how they influence the sexual phase in those fungi.Apocarotenoids are the unsaturated nonpolar isoprenoids form...

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“…An advantage of cDNA-AFLP is that it does not depend on pre-existing genomic sequence information. The very few Blakeslea genes that have been sequenced include those for the two dedicated enzymes for carotene biosynthesis (Rodríguez-Sáiz et al 2004), a regulator of responses to light, including carotene biosynthesis (Quiles-Rosillo et al 2005), and a carotene oxygenase probably involved in trisporoid biosynthesis (Burmester et al 2007).…”

Section: Introductionmentioning

confidence: 99%

Genes involved in carotene synthesis and mating in Blakeslea trispora

et al. 2008

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Mating of Blakeslea trispora and other molds of the order Mucorales requires the interaction of mycelia of opposite sex, (+) and (¡), leading to the development of specialized structures and to an enhanced accumulation of -carotene. Industry obtains -carotene by co-cultivating appropriate strains of Blakeslea ("mated cultures"). Gene transcription in single and mated cultures was assayed by cDNA-AFLP, a technique to observe the diVerential expression of subsets of mRNA fragments. Overexpression in mated cultures is about ten times more frequent than underexpression. We obtained and sequenced fragments of 97 candidate genes that appeared to be overexpressed during mating and conWrmed four of them by reverse transcription and real-time PCR. Comparisons with gene sequences from other organisms suggest functions in carotene biosynthesis (4 genes), energy metabolism (8), cell wall synthesis (1), transfer of acetyl groups (1), and regulatory processes (10). Sodium acetate inhibited sexual overexpression in about two-thirds of the candidate genes and acted as a signal with broad eVects on the metabolism and the morphology of mated cultures. Our work oVers new materials for the study of carotene biosynthesis and its regulation and for the improvement of carotene production with Mucorales.

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Cleavage of β-carotene as the first step in sexual hormone synthesis in zygomycetes is mediated by a trisporic acid regulated β-carotene oxygenase

Cited by 48 publications

References 63 publications

The mating-related loci sexM and sexP of the zygomycetous fungus Mucor mucedo and their transcriptional regulation by trisporoid pheromones

The mating-related loci sexM and sexP of the zygomycetous fungus Mucor mucedo and their transcriptional regulation by trisporoid pheromones

Early and Late Trisporoids Differentially Regulate β-Carotene Production and Gene Transcript Levels in the Mucoralean Fungi Blakeslea trispora and Mucor mucedo

Genes involved in carotene synthesis and mating in Blakeslea trispora

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