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Transcriptome analysis and its application in identifying genes associated with fruiting body development in basidiomycete Hypsizygus marmoreus.

Zhang J, Ren A, Chen H, Zhao M, Shi L, Chen M, Wang H, Feng Z - PLoS ONE (2015)

Bottom Line: During the transition from H-V to H-P, stress signals associated with MAPK, cAMP and ROS signals might be the most important inducers.Our data suggested that nitrogen starvation might be one of the most important factors in promoting fruit body maturation, and nitrogen metabolism and mTOR signaling pathway were associated with this process.This study advances our understanding of the molecular mechanism of fruiting body development in H. marmoreus by identifying a wealth of new genes that may play important roles in mushroom morphogenesis.

View Article: PubMed Central - PubMed

Affiliation: College of Life Science, Nanjing Agricultural University, Key Laboratory of Microbiological Engineering of Agricultural Environment, Ministry of Agriculture, Nanjing, Jiangsu, China; National Research Center for Edible Fungi Biotechnology and Engineering, Key Laboratory of Applied Mycological Resources and Utilization, Ministry of Agriculture, the People's Republic of China, Shanghai Key Laboratory of Agricultural Genetics and Breeding, Institute of Edible Fungi, Shanghai Academy of Agricultural Sciences, Shanghai, China.

ABSTRACT
To elucidate the mechanisms of fruit body development in H. marmoreus, a total of 43609521 high-quality RNA-seq reads were obtained from four developmental stages, including the mycelial knot (H-M), mycelial pigmentation (H-V), primordium (H-P) and fruiting body (H-F) stages. These reads were assembled to obtain 40568 unigenes with an average length of 1074 bp. A total of 26800 (66.06%) unigenes were annotated and analyzed with the Kyoto Encyclopedia of Genes and Genomes (KEGG), Gene Ontology (GO), and Eukaryotic Orthologous Group (KOG) databases. Differentially expressed genes (DEGs) from the four transcriptomes were analyzed. The KEGG enrichment analysis revealed that the mycelium pigmentation stage was associated with the MAPK, cAMP, and blue light signal transduction pathways. In addition, expression of the two-component system members changed with the transition from H-M to H-V, suggesting that light affected the expression of genes related to fruit body initiation in H. marmoreus. During the transition from H-V to H-P, stress signals associated with MAPK, cAMP and ROS signals might be the most important inducers. Our data suggested that nitrogen starvation might be one of the most important factors in promoting fruit body maturation, and nitrogen metabolism and mTOR signaling pathway were associated with this process. In addition, 30 genes of interest were analyzed by quantitative real-time PCR to verify their expression profiles at the four developmental stages. This study advances our understanding of the molecular mechanism of fruiting body development in H. marmoreus by identifying a wealth of new genes that may play important roles in mushroom morphogenesis.

No MeSH data available.


Related in: MedlinePlus

Pathways and genes associated with the three transitions between the four developmental stages in H. marmoreus.Light may play a crucial role during the first transition as determined by the potential involvement of tyrosinase (Tyr), the blue light transduction signal pathway (WC), the MAPK signaling pathway (MAPK), the cAMP signaling pathway (PKC) and the two-component system pathway (HDK). In addition, the cytochrome P450 (P450s) and alcohol dehydrogenase (adh) genes were active in this process to facilitate mycelial growth. During the second transition, pathways related to stress reactions, such as the MAPK signaling (Mkk1_2 and PBS2) and cAMP signaling (PKA) pathways, were active, as were NADPH oxidase enzyme (Noxs) and the genes encoding glucosidase (gld) and laccase (lcc). These pathways and genes might be associated with primordium initiation. During the last transition, pathways related to nitrogen starvation, such as nitrogen metabolism (ats, nrd), mTOR signaling (mTOR) and Ca2+ signaling (Ca2+-ATPase), might be more important in fruit body maturation than in other stages. Genes encoding ribosomal protein (rbp), rho guanine nucleotide exchange factor scd1 (rho) and STE3-like pheromone receptor (ste3) had higher expression levels in fruit body maturation than in the other stages. The solid line indicates that the results were confirmed by transcriptomic analysis and RT-PCR; the dotted line indicates that the results were only confirmed by transcriptomic analysis.
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pone.0123025.g011: Pathways and genes associated with the three transitions between the four developmental stages in H. marmoreus.Light may play a crucial role during the first transition as determined by the potential involvement of tyrosinase (Tyr), the blue light transduction signal pathway (WC), the MAPK signaling pathway (MAPK), the cAMP signaling pathway (PKC) and the two-component system pathway (HDK). In addition, the cytochrome P450 (P450s) and alcohol dehydrogenase (adh) genes were active in this process to facilitate mycelial growth. During the second transition, pathways related to stress reactions, such as the MAPK signaling (Mkk1_2 and PBS2) and cAMP signaling (PKA) pathways, were active, as were NADPH oxidase enzyme (Noxs) and the genes encoding glucosidase (gld) and laccase (lcc). These pathways and genes might be associated with primordium initiation. During the last transition, pathways related to nitrogen starvation, such as nitrogen metabolism (ats, nrd), mTOR signaling (mTOR) and Ca2+ signaling (Ca2+-ATPase), might be more important in fruit body maturation than in other stages. Genes encoding ribosomal protein (rbp), rho guanine nucleotide exchange factor scd1 (rho) and STE3-like pheromone receptor (ste3) had higher expression levels in fruit body maturation than in the other stages. The solid line indicates that the results were confirmed by transcriptomic analysis and RT-PCR; the dotted line indicates that the results were only confirmed by transcriptomic analysis.

Mentions: While H. marmoreus is an important edible mushroom species in Asia, the molecular/genetic basis of mushroom morphogenesis remains largely uncharacterized. In this work, the transcriptomes of four developmental stages of H. marmoreus were profiled and summarized in a schematic model (Fig 11). It was found that light affects initiation of the fruit body and that the expression of the genes encoding Tyr, MAPK, PKC, and BLR were altered during the mushroom initiation. In the transition from H-V to H-P, environmental stresses might be associated with primordium initiation, which leads to alterations in the expression of genes such as PKA, Pbs2 and Noxs. In addition, the carbon metabolism genes encoding glucose-6-P dehydrogenase, alcohol dehydrogenase, laccase and glucosidase were expressed at higher levels in the H-V and H-P stages than in the other stages. In addition, genes involved in nitrogen metabolism and mTOR signaling pathway were the most active during the transition from H-P to H-F. To the best of our knowledge, this is the first report that studied the transcriptome of H. marmoreus. These data may provide a valuable resource for further studies of this mushroom. Further functional characterization of the unigenes that were found to be associated with the regulation of the four development stages may lead to an in-depth understanding of the network that that regulates fruit body development.


Transcriptome analysis and its application in identifying genes associated with fruiting body development in basidiomycete Hypsizygus marmoreus.

Zhang J, Ren A, Chen H, Zhao M, Shi L, Chen M, Wang H, Feng Z - PLoS ONE (2015)

Pathways and genes associated with the three transitions between the four developmental stages in H. marmoreus.Light may play a crucial role during the first transition as determined by the potential involvement of tyrosinase (Tyr), the blue light transduction signal pathway (WC), the MAPK signaling pathway (MAPK), the cAMP signaling pathway (PKC) and the two-component system pathway (HDK). In addition, the cytochrome P450 (P450s) and alcohol dehydrogenase (adh) genes were active in this process to facilitate mycelial growth. During the second transition, pathways related to stress reactions, such as the MAPK signaling (Mkk1_2 and PBS2) and cAMP signaling (PKA) pathways, were active, as were NADPH oxidase enzyme (Noxs) and the genes encoding glucosidase (gld) and laccase (lcc). These pathways and genes might be associated with primordium initiation. During the last transition, pathways related to nitrogen starvation, such as nitrogen metabolism (ats, nrd), mTOR signaling (mTOR) and Ca2+ signaling (Ca2+-ATPase), might be more important in fruit body maturation than in other stages. Genes encoding ribosomal protein (rbp), rho guanine nucleotide exchange factor scd1 (rho) and STE3-like pheromone receptor (ste3) had higher expression levels in fruit body maturation than in the other stages. The solid line indicates that the results were confirmed by transcriptomic analysis and RT-PCR; the dotted line indicates that the results were only confirmed by transcriptomic analysis.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4383556&req=5

pone.0123025.g011: Pathways and genes associated with the three transitions between the four developmental stages in H. marmoreus.Light may play a crucial role during the first transition as determined by the potential involvement of tyrosinase (Tyr), the blue light transduction signal pathway (WC), the MAPK signaling pathway (MAPK), the cAMP signaling pathway (PKC) and the two-component system pathway (HDK). In addition, the cytochrome P450 (P450s) and alcohol dehydrogenase (adh) genes were active in this process to facilitate mycelial growth. During the second transition, pathways related to stress reactions, such as the MAPK signaling (Mkk1_2 and PBS2) and cAMP signaling (PKA) pathways, were active, as were NADPH oxidase enzyme (Noxs) and the genes encoding glucosidase (gld) and laccase (lcc). These pathways and genes might be associated with primordium initiation. During the last transition, pathways related to nitrogen starvation, such as nitrogen metabolism (ats, nrd), mTOR signaling (mTOR) and Ca2+ signaling (Ca2+-ATPase), might be more important in fruit body maturation than in other stages. Genes encoding ribosomal protein (rbp), rho guanine nucleotide exchange factor scd1 (rho) and STE3-like pheromone receptor (ste3) had higher expression levels in fruit body maturation than in the other stages. The solid line indicates that the results were confirmed by transcriptomic analysis and RT-PCR; the dotted line indicates that the results were only confirmed by transcriptomic analysis.
Mentions: While H. marmoreus is an important edible mushroom species in Asia, the molecular/genetic basis of mushroom morphogenesis remains largely uncharacterized. In this work, the transcriptomes of four developmental stages of H. marmoreus were profiled and summarized in a schematic model (Fig 11). It was found that light affects initiation of the fruit body and that the expression of the genes encoding Tyr, MAPK, PKC, and BLR were altered during the mushroom initiation. In the transition from H-V to H-P, environmental stresses might be associated with primordium initiation, which leads to alterations in the expression of genes such as PKA, Pbs2 and Noxs. In addition, the carbon metabolism genes encoding glucose-6-P dehydrogenase, alcohol dehydrogenase, laccase and glucosidase were expressed at higher levels in the H-V and H-P stages than in the other stages. In addition, genes involved in nitrogen metabolism and mTOR signaling pathway were the most active during the transition from H-P to H-F. To the best of our knowledge, this is the first report that studied the transcriptome of H. marmoreus. These data may provide a valuable resource for further studies of this mushroom. Further functional characterization of the unigenes that were found to be associated with the regulation of the four development stages may lead to an in-depth understanding of the network that that regulates fruit body development.

Bottom Line: During the transition from H-V to H-P, stress signals associated with MAPK, cAMP and ROS signals might be the most important inducers.Our data suggested that nitrogen starvation might be one of the most important factors in promoting fruit body maturation, and nitrogen metabolism and mTOR signaling pathway were associated with this process.This study advances our understanding of the molecular mechanism of fruiting body development in H. marmoreus by identifying a wealth of new genes that may play important roles in mushroom morphogenesis.

View Article: PubMed Central - PubMed

Affiliation: College of Life Science, Nanjing Agricultural University, Key Laboratory of Microbiological Engineering of Agricultural Environment, Ministry of Agriculture, Nanjing, Jiangsu, China; National Research Center for Edible Fungi Biotechnology and Engineering, Key Laboratory of Applied Mycological Resources and Utilization, Ministry of Agriculture, the People's Republic of China, Shanghai Key Laboratory of Agricultural Genetics and Breeding, Institute of Edible Fungi, Shanghai Academy of Agricultural Sciences, Shanghai, China.

ABSTRACT
To elucidate the mechanisms of fruit body development in H. marmoreus, a total of 43609521 high-quality RNA-seq reads were obtained from four developmental stages, including the mycelial knot (H-M), mycelial pigmentation (H-V), primordium (H-P) and fruiting body (H-F) stages. These reads were assembled to obtain 40568 unigenes with an average length of 1074 bp. A total of 26800 (66.06%) unigenes were annotated and analyzed with the Kyoto Encyclopedia of Genes and Genomes (KEGG), Gene Ontology (GO), and Eukaryotic Orthologous Group (KOG) databases. Differentially expressed genes (DEGs) from the four transcriptomes were analyzed. The KEGG enrichment analysis revealed that the mycelium pigmentation stage was associated with the MAPK, cAMP, and blue light signal transduction pathways. In addition, expression of the two-component system members changed with the transition from H-M to H-V, suggesting that light affected the expression of genes related to fruit body initiation in H. marmoreus. During the transition from H-V to H-P, stress signals associated with MAPK, cAMP and ROS signals might be the most important inducers. Our data suggested that nitrogen starvation might be one of the most important factors in promoting fruit body maturation, and nitrogen metabolism and mTOR signaling pathway were associated with this process. In addition, 30 genes of interest were analyzed by quantitative real-time PCR to verify their expression profiles at the four developmental stages. This study advances our understanding of the molecular mechanism of fruiting body development in H. marmoreus by identifying a wealth of new genes that may play important roles in mushroom morphogenesis.

No MeSH data available.


Related in: MedlinePlus