Dataset Information

Evolutionary Conservation and Divergence of Genes Encoding 3-Hydroxy-3-methylglutaryl Coenzyme A Synthase in the Allotetraploid Cotton Species Gossypium hirsutum.

ABSTRACT: Polyploidization is important for the speciation and subsequent evolution of many plant species. Analyses of the duplicated genes produced via polyploidization events may clarify the origin and evolution of gene families. During terpene biosynthesis, 3-hydroxy-3-methylglutaryl coenzyme A synthase (HMGS) functions as a key enzyme in the mevalonate pathway. In this study, we first identified a total of 53 HMGS genes in 23 land plant species, while no HMGS genes were detected in three green algae species. The phylogenetic analysis suggested that plant HMGS genes may have originated from a common ancestral gene before clustering in different branches during the divergence of plant lineages. Then, we detected six HMGS genes in the allotetraploid cotton species (Gossypium hirsutum), which was twice that of the two diploid cotton species (Gossypium raimondii and Gossypium arboreum). The comparison of gene structures and phylogenetic analysis of HMGS genes revealed conserved evolution during polyploidization in Gossypium. Moreover, the expression patterns indicated that six GhHMGS genes were expressed in all tested tissues, with most genes considerably expressed in the roots, and they were responsive to various phytohormone treatments and abiotic stresses. The sequence and expression divergence of duplicated genes in G. hirsutum implied the sub-functionalization of GhHMGS1A and GhHMGS1D as well as GhHMGS3A and GhHMGS3D, whereas it implied the pseudogenization of GhHMGS2A and GhHMGS2D. Collectively, our study unraveled the evolutionary history of HMGS genes in green plants and from diploid to allotetraploid in cotton and illustrated the different evolutionary fates of duplicated HMGS genes resulting from polyploidization.

SUBMITTER: Liu W

PROVIDER: S-EPMC6562921 | biostudies-literature | 2019 May

REPOSITORIES: biostudies-literature

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Evolutionary Conservation and Divergence of Genes Encoding 3-Hydroxy-3-methylglutaryl Coenzyme A Synthase in the Allotetraploid Cotton Species Gossypium hirsutum.

Liu Wei W Zhang Zhiqiang Z Zhu Wei W Ren Zhongying Z Jia Lin L Li Wei W Ma Zongbin Z

Cells 20190503 5

Polyploidization is important for the speciation and subsequent evolution of many plant species. Analyses of the duplicated genes produced via polyploidization events may clarify the origin and evolution of gene families. During terpene biosynthesis, 3-hydroxy-3-methylglutaryl coenzyme A synthase (HMGS) functions as a key enzyme in the mevalonate pathway. In this study, we first identified a total of 53 HMGS genes in 23 land plant species, while no HMGS genes were detected in three ...[more]

PMID: 31058869

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Project description:The wood-rotting mushroom Stereum hirsutum is a known producer of a large number of namesake hirsutenoids, many with important bioactivities. Hirsutenoids form a structurally diverse and distinct class of sesquiterpenoids. No genes involved in hirsutenoid biosynthesis have yet been identified or their enzymes characterized. Here, we describe the cloning and functional characterization of a hirsutene synthase as an unexpected fusion protein of a sesquiterpene synthase (STS) with a C-terminal 3-hydroxy-3-methylglutaryl-coenzyme A (3-hydroxy-3-methylglutaryl-CoA) synthase (HMGS) domain. Both the full-length fusion protein and truncated STS domain are highly product-specific 1,11-cyclizing STS enzymes with kinetic properties typical of STSs. Complementation studies in Saccharomyces cerevisiae confirmed that the HMGS domain is also functional in vivo Phylogenetic analysis shows that the hirsutene synthase domain does not form a clade with other previously characterized sesquiterpene synthases from Basidiomycota. Comparative gene structure analysis of this hirsutene synthase with characterized fungal enzymes reveals a significantly higher intron density, suggesting that this enzyme may be acquired by horizontal gene transfer. In contrast, the HMGS domain is clearly related to other fungal homologs. This STS-HMGS fusion protein is part of a biosynthetic gene cluster that includes P450s and oxidases that are expressed and could be cloned from cDNA. Finally, this unusual fusion of a terpene synthase to an HMGS domain, which is not generally recognized as a key regulatory enzyme of the mevalonate isoprenoid precursor pathway, led to the identification of additional HMGS duplications in many fungal genomes, including the localization of HMGSs in other predicted sesquiterpenoid biosynthetic gene clusters.IMPORTANCE Hirsutenoids represent a structurally diverse class of bioactive sesquiterpenoids isolated from fungi. Identification of their biosynthetic pathways will provide access to this chemodiversity for the discovery and synthesis of molecules with new bioactivities. The identification and successful cloning of the previously elusive hirsutene synthase from the S. hirsutum provide important insights and strategies for biosynthetic gene discovery in Basidiomycota. The finding of a terpene synthase-HMGS fusion, the discovery of other sesquiterpenoid biosynthetic gene clusters with dedicated HMGS genes, and HMGS gene duplications in fungal genomes give new importance to the role of HMGS as a key regulatory enzyme in isoprenoid and sterol biosynthesis that should be exploited for metabolic engineering.

Project description:The cotton genus (Gossypium) provides a superior system for the study of diversification, genome evolution, polyploidization, and human-mediated selection. To gain insight into phenotypic diversification in cotton seeds, we conducted coexpression network analysis of developing seeds from diploid and allopolyploid cotton species and explored network properties. Key network modules and functional associations were identified related to seed oil content and seed weight. We compared species-specific networks to reveal topological changes, including rewired edges and differentially coexpressed genes, associated with speciation, polyploidy, and cotton domestication. Network comparisons among species indicate that topologies are altered in addition to gene expression profiles, indicating that changes in transcriptomic coexpression relationships play a role in the developmental architecture of cotton seed development. The global network topology of allopolyploids, especially for domesticated G. hirsutum, resembles the network of the A-genome diploid more than that of the D-genome parent, despite its D-like phenotype in oil content. Expression modifications associated with allopolyploidy include coexpression level dominance and transgressive expression, suggesting that the transcriptomic architecture in polyploids is to some extent a modular combination of that of its progenitor genomes. Among allopolyploids, intermodular relationships are more preserved between two different wild allopolyploid species than they are between wild and domesticated forms of a cultivated cotton, and regulatory connections of oil synthesis-related pathways are denser and more closely clustered in domesticated vs. wild G. hirsutum. These results demonstrate substantial modification of genic coexpression under domestication. Our work demonstrates how network inference informs our understanding of the transcriptomic architecture of phenotypic variation associated with temporal scales ranging from thousands (domestication) to millions (speciation) of years, and by polyploidy.

Project description:BackgroundBase editors (BEs) display diverse applications in a variety of plant species such as Arabidopsis, rice, wheat, maize, soybean, and cotton, where they have been used to mediate precise base pair conversions without the collateral generation of undesirable double-stranded breaks (DSB). Studies of single-nucleotide polymorphisms (SNPs) underpinning plant traits are still challenging, particularly in polyploidy species where such SNPs are present in multiple copies, and simultaneous modification of all alleles would be required for functional analysis. Allotetraploid cotton has a number of homoeologous gene pairs located in the A and D sub-genomes with considerable SNPs, and it is desirable to develop adenine base editors (ABEs) for efficient and precise A-to-G single-base editing without DSB in such complex genome.ResultsWe established various ABE vectors based on different engineered adenosine deaminase (TadA) proteins fused to Cas9 variants (dCas9, nCas9), enabling efficient A to G editing up to 64% efficiency on-target sites of the allotetraploid cotton genome. Comprehensive analysis showed that GhABE7.10n exhibited the highest editing efficiency, with the main editing sites specifically located at the position A5 (counting the PAM as positions 21-23). Furthermore, DNA and RNA off-target analysis of cotton plants edited with GhABE7.10n and GhABE7.10d by whole genome and whole-transcriptome sequencing revealed no DNA off-target mutations, while very low-level RNA off-target mutations were detected. A new base editor, namely GhABE7.10dCpf1 (7.10TadA + dCpf1), that recognizes a T-rich PAM, was developed for the first time. Targeted A-to-G substitutions generated a single amino acid change in the cotton phosphatidyl ethanolamine-binding protein (GhPEBP), leading to a compact cotton plant architecture, an ideotype for mechanized harvesting of modern cotton production.ConclusionsOur data illustrate the robustness of adenine base editing in plant species with complex genomes, which provides efficient and precise toolkit for cotton functional genomics and precise molecular breeding.

Project description:Histone modification is an important epigenetic modification that controls gene transcriptional regulation in eukaryotes. Histone methylation is accomplished by histone methyltransferase and can occur on two amino acid residues, arginine and lysine. JumonjiC (JmjC) domain-containing histone demethylase regulates gene transcription and chromatin structure by changing the methylation state of the lysine residue site and plays an important role in plant growth and development. In this study, we carried out genome-wide identification and comprehensive analysis of JmjC genes in the allotetraploid cotton species Gossypium hirsutum. In total, 50 JmjC genes were identified and in G. hirsutum, and 25 JmjC genes were identified in its two diploid progenitors, G. arboreum and G. raimondii, respectively. Phylogenetic analysis divided these JmjC genes into five subfamilies. A collinearity analysis of the two subgenomes of G. hirsutum and the genomes of G. arboreum and G. raimondii uncovered a one-to-one relationship between homologous genes of the JmjC gene family. Most homologs in the JmjC gene family between A and D subgenomes of G. hirsutum have similar exon-intron structures, which indicated that JmjC family genes were conserved after the polyploidization. All G. hirsutumJmjC genes were found to have a typical JmjC domain, and some genes also possess other special domains important for their function. Analysis of promoter regions revealed that cis-acting elements, such as those related to hormone and abiotic stress response, were enriched in G. hirsutum JmjC genes. According to a reverse transcription-quantitative polymerase chain reaction (RT-qPCR) analysis, most G. hirsutumJmjC genes had high abundance expression at developmental stages of fibers, suggesting that they might participate in cotton fiber development. In addition, some G. hirsutumJmjC genes were found to have different degrees of response to cold or osmotic stress, thus indicating their potential role in these types of abiotic stress response. Our results provide useful information for understanding the evolutionary history and biological function of JmjC genes in cotton.

Dataset Information

Evolutionary Conservation and Divergence of Genes Encoding 3-Hydroxy-3-methylglutaryl Coenzyme A Synthase in the Allotetraploid Cotton Species Gossypium hirsutum.

Publications

Evolutionary Conservation and Divergence of Genes Encoding 3-Hydroxy-3-methylglutaryl Coenzyme A Synthase in the Allotetraploid Cotton Species <i>Gossypium hirsutum</i>.

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