Molecular Mechanism of Secondary Metabolic Pathways in Forest Trees

A special issue of Forests (ISSN 1999-4907). This special issue belongs to the section "Genetics and Molecular Biology".

Deadline for manuscript submissions: closed (30 September 2023) | Viewed by 10842

Special Issue Editors


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Guest Editor
College of Horticulture and Gardening, Yangtze University, Jingzhou 434025, China
Interests: Ginkgo biloba; plant secondary metabolism; flavonoid synthesis; terpene metabolism; genetic improvement; mechanisms of secondary metabolite biosynthesis
College of Horticulture, Nanjing Agricultural University, Nanjing 210095, China
Interests: Camellia sinensis; plant genetics; plant molecular biology; plant cell biology; fluoride accumulation mechanism; aluminum accumulation mechanism; plant signal transduction
Chinese Academy of Forestry, Beijing 100091, China
Interests: larch; gene regulation; tree breeding; plant molecular biology; life cycle; regulation of metabolism

Special Issue Information

Dear Colleagues,

Over the years, secondary compounds have been known to be associated with many photochemical processes in forest plants, such as improving the resistance of conifer xylem to insects and fungi, mediating plant responses to biotic or abiotic environmental stresses, and contributing to fruits’ flavor and flower colors. The production and distribution of secondary metabolites are usually specific to plant species, organs, tissues, and growth stages. In many forest trees, the biosynthetic pathways of secondary metabolites are complex and diverse, and the discovery of regulatory genes and enzymes involved in the accumulation of their secondary metabolites is still very limited. Research on improving important biological traits of forest trees through genetic improvement is lagging behind. Therefore, this Special Issue plans to provide an overview of the most recent advances in the discovery and characterization of secondary metabolic pathways in forest trees. This Special Issue is aimed at providing selected contributions on advances in the synthesis, characterization, and applications of secondary metabolites in different forest trees.

Potential topics include, but are not limited to, the following:

  • Secondary metabolite biosynthesis of forest trees;
  • Mining of gene clusters in biosynthetic pathways;
  • Functions of key genes in secondary metabolic pathways;
  • Regulatory networks of secondary metabolites;
  • Prospects of secondary metabolites in forest trees.

Prof. Dr. Feng Xu 
Dr. Yuhua Wang
Dr. Wanfeng Li
Guest Editors

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Keywords

  • forest trees
  • secondary metabolism
  • bioactive compounds
  • biosynthesis
  • flavonoids
  • alkaloids
  • phenylpropanoids
  • terpenoid

Published Papers (7 papers)

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Research

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19 pages, 7747 KiB  
Article
Comparative Physiological, Transcriptomic, and Metabolomic Analyses of Acacia mangium Provide New Insights into Its Molecular Mechanism of Self-Incompatibility
by Ruping Zhang, Liejian Huang and Bingshan Zeng
Forests 2023, 14(10), 2034; https://doi.org/10.3390/f14102034 - 11 Oct 2023
Viewed by 811
Abstract
Acacia mangium is well known as a valuable commercial tree species in the Acacia genus. A. mangium was recently found to be self-incompatible (SI), but its SI mechanism is not clear, which has hindered the progress of genetic improvement of A. mangium with [...] Read more.
Acacia mangium is well known as a valuable commercial tree species in the Acacia genus. A. mangium was recently found to be self-incompatible (SI), but its SI mechanism is not clear, which has hindered the progress of genetic improvement of A. mangium with strong resistance. To confirm the SI type of A. mangium, pollen germination was observed via fluorescence microscopy at 0 h, 3 h, 6 h, 9 h, 12 h, and 24 h after self-pollination. We found over ninety percent of the pollen grains produced no pollen tube growth on the stigma/style. To further explore the SI molecular mechanism of A. mangium, tests of the transcriptome and metabolome were carried out after self-pollination. Observations of pollen germination after self-pollination using fluorescence microscopy suggested that the SI type of A. mangium is gametophytic self-incompatibility (GSI). A combined transcriptomic and metabolomic analysis showed that DEGs (differentially expressed genes) related to SI (6 S-glycoproteins, 93 F-box proteins, 69 26S proteasomes, 38 calcium-dependent protein kinases/calmodulin and 41 thioredoxin genes) were significantly enriched in six KEGG (sulfur metabolism, tyrosine metabolism, phenylalanine metabolism, butanoate metabolism, and valine, leucine, and isoleucine degradation). Further analysis of these six pathways revealed the enrichment of SI-related DEGs corresponding to succinate, methylmalonate, and 3-hydroxypropane. These three metabolites were significantly downregulated. The analysis of transcripts and metabolites suggested that transcripts of SI-related gene families (thioredoxin and F-box protein) were significantly upregulated under the regulation of transcription factors (TFs) after self-pollination, leading to a decrease in metabolites (such as succinate, methylmalonate, and 3-hydroxypropionate). We also further speculated that TFs (MYB, HB-HD-ZIP, AP2/ERF-ERF, and bZIP) and gene families (thioredoxin and F-box protein) were important factors related to the SI of A. mangium. Full article
(This article belongs to the Special Issue Molecular Mechanism of Secondary Metabolic Pathways in Forest Trees)
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17 pages, 6098 KiB  
Article
Integrated Volatile Metabolome and Transcriptome Analyses Provide Insights into the Formation of Benzenoid–Phenylpropanoid Aroma Substance Eugenol in the Rosa hybrida ‘Lanxing’ Flowering
by Pei Sun, Yuan Yang, Hua Wang, Maofu Li, Yanhui Kang, Shuting Zhou and Wanmei Jin
Forests 2023, 14(10), 1973; https://doi.org/10.3390/f14101973 - 28 Sep 2023
Viewed by 780
Abstract
Scent is the key character of the horticultural ornamental plant rose, and benzenoid–phenylpropanoid compounds are the main source of scent. However, the underlying biosynthesis mechanism of these benzenoid–phenylpropanoid scent metabolites during Rosa flowering is poorly understood. In this study, the volatile metabolome and [...] Read more.
Scent is the key character of the horticultural ornamental plant rose, and benzenoid–phenylpropanoid compounds are the main source of scent. However, the underlying biosynthesis mechanism of these benzenoid–phenylpropanoid scent metabolites during Rosa flowering is poorly understood. In this study, the volatile metabolome and transcriptome conjoint analysis was conducted on the six stages petals of the variety ‘Lanxing’ to investigate the synthesis of benzenoid–phenylpropanoid metabolites. A total of 25 benzenoid–phenylpropanoid volatile compounds were identified, of which eugenol possessed the highest content. Meanwhile, transcriptome analysis produced 87.9 million clean reads and 22,004 differentially expressed genes (DEGs). Group pairwise comparison of gene ontology (GO) and Kyoto encyclopedia of genes and genomes (KEGG) enrichment analysis found DEGs were enriched into phenylpropanoid compound synthesis related pathway. Weighted gene co-expression network analysis (WGCNA) found a MEgreenyellow gene module (650 DEGs) correlated with phenylpropanoid compounds. Based on the eugenol content variation and gene spatio-temporal expression, a key candidate gene RcEGS32 related to the synthesis of eugenol was identified. Co-expression network analysis found that five transcription factors, RcMYB1, RcBES1, RcERF2, RcbHLH1, and RcTUB, may act as regulators in the eugenol synthesis process by directly binding to RcEGS32 or forming a complex unit. This study provided key insights into the formation of the scent substance eugenol during flowering, offering a valuable volatile metabolome and transcriptome resource for the future target trait-related gene discovery of roses. Full article
(This article belongs to the Special Issue Molecular Mechanism of Secondary Metabolic Pathways in Forest Trees)
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16 pages, 32347 KiB  
Article
Disentangling the Potential Functions of miRNAs in the Synthesis of Terpenoids during the Development of Cinnamomum burmannii Leaves
by Chen Hou, Boxiang He, Peiwu Xie, Yingli Wang, Dongcheng Liang, Huiming Lian, Qian Zhang and Yanling Cai
Forests 2023, 14(3), 555; https://doi.org/10.3390/f14030555 - 11 Mar 2023
Viewed by 1034
Abstract
The essential oil of Cinnamomum burmannii (Nees and T. Nees) Blume is rich in monoterpenes and sesquiterpenes. The post-transcriptional regulatory mechanisms controlling the expression of terpenoid-related genes have not yet been clarified in C. burmannii. Here, we conducted a metabolomic analysis of [...] Read more.
The essential oil of Cinnamomum burmannii (Nees and T. Nees) Blume is rich in monoterpenes and sesquiterpenes. The post-transcriptional regulatory mechanisms controlling the expression of terpenoid-related genes have not yet been clarified in C. burmannii. Here, we conducted a metabolomic analysis of the leaves of C. burmannii across four developmental stages using gas chromatography–mass spectrometry. We also identified miRNAs and their target genes involved in terpenoid biosynthesis using small RNA sequencing. A total of 135 differentially expressed metabolites were detected, including 65 terpenoids, 15 aldehydes, and 13 benzenes. A total of 876 miRNAs from 148 families were detected, among which 434 miRNAs were differentially expressed, including three known miRNAs and 431 novel miRNAs. Four miRNAs (gma-miR5368, novel_miR_377, novel_miR_111, and novel_miR_251) were predicted to regulate the expression of four differential expressed genes involved in the monoterpenoid and sesquiterpenoid synthesis. miRNAs families miR396, miR5185, and miR9408 were predicted to play diverse regulatory roles in monoterpenoid and sesquiterpenoid synthesis during the leaf development of C. burmannii. The results of our study shed new light on the roles of regulatory genes in terpenoid biosynthesis. Our findings also have implications for the further promotion of essential oil production using the leaves of C. burmannii. Full article
(This article belongs to the Special Issue Molecular Mechanism of Secondary Metabolic Pathways in Forest Trees)
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17 pages, 3593 KiB  
Article
Identification of Key Genes for Oleoresin Biosynthesis in High and Low Oleoresin-Yielding Slash Pine Based on Transcriptome Analysis
by Min Yi, Lu Zhang, Zishan Cheng, Rong Hu, Yuan Gao, Cangfu Jin, Shenggui Yuan, Shiwu Sun and Meng Lai
Forests 2022, 13(8), 1337; https://doi.org/10.3390/f13081337 - 22 Aug 2022
Cited by 4 | Viewed by 1565
Abstract
Slash pine (Pinus elliottii Engelmann) is a pine species widely cultivated for its high oleoresin production capacity. However, little is known about the underlying molecular mechanism of oleoresin biosynthesis between high and low oleoresin-yielding slash pines. In this study, the terpenoid compositions [...] Read more.
Slash pine (Pinus elliottii Engelmann) is a pine species widely cultivated for its high oleoresin production capacity. However, little is known about the underlying molecular mechanism of oleoresin biosynthesis between high and low oleoresin-yielding slash pines. In this study, the terpenoid compositions of oleoresin harvested from high- and low-yielding slash pines were identified using gas chromatography/mass spectrometry (GC-MS) analysis. The monoterpenes and diterpenes are the major constituents, of which the α- and β-pinenes are the overwhelming majority of turpentines, and abietic acid, levopimaric acid, and neoabietic acid are the most abundant in rosin. The transcriptomic analysis was also performed with secondary xylem tissues of high- and low-yielding slash pines. After functional annotation, the DEGs of RNA-seq data between high- and low-yielding pines in April, July, and October were screened, and many key enzyme genes were found to be implicated in terpenoid backbone biosynthesis. Moreover, weighted gene correlation network analysis (WGCNA) was carried out to uncover the gene modules highly related to α- and β-pinene biosynthesis in slash pine. Twenty-three modules were attained in this study. Focusing on the total oleoresin yield, the MEblue module exhibited the highest positive correlation, while the MEgreen module exhibited the highest negative correlation. A total of 20 TFs were identified in gene modules. Among these genes, the c215396.graph_c0 encoding an MYB TF is the key differentially expressed gene (DEG) between high- and low-yielding pines. The subsequent one-hybrid yeast assay verified that c215396.graph_c0 can activate the transcription of Apetala 2 (AP2) and 1-deoxy-d-xylulose 5-phosphate synthase (dxs), which are also two DEGs between high- and low-yielding pines. Thus, our study identified a set of key enzymes and TFs that are involved in regulating oleoresin and composition between high- and low-yielding slash pines and provided us a deep insight into oleoresin biosynthesis. Full article
(This article belongs to the Special Issue Molecular Mechanism of Secondary Metabolic Pathways in Forest Trees)
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17 pages, 16022 KiB  
Article
Identification and Analysis of JAZ Gene Family in Ginkgo biloba Reveals Candidate Genes for Biosynthesis of Terpene Trilactones
by Xiao He, Xiaomeng Liu, Jiarui Zheng, Jiabao Ye, Yongling Liao and Feng Xu
Forests 2022, 13(5), 781; https://doi.org/10.3390/f13050781 - 18 May 2022
Cited by 2 | Viewed by 2147
Abstract
Terpene trilactones (TTLs) are the main secondary metabolites in Ginkgo biloba L. with efficacious pharmacological activity. Jasmonate ZIM-domain (JAZ) protein is a key regulatory factor of the JA signaling pathway, which regulates the biosynthesis of secondary metabolites such as terpenes, alkaloids, and flavonoids. [...] Read more.
Terpene trilactones (TTLs) are the main secondary metabolites in Ginkgo biloba L. with efficacious pharmacological activity. Jasmonate ZIM-domain (JAZ) protein is a key regulatory factor of the JA signaling pathway, which regulates the biosynthesis of secondary metabolites such as terpenes, alkaloids, and flavonoids. In this study, GbJAZ01~GbJAZ11 were identified from the genome data in G. biloba, which contained TIFY-, Jas-, and weakly conserved NT-domains, and the promoters in most of them contained light, hormone, and stress-responsive elements. Phylogenetic analysis divided all JAZ proteins of Arabidopsis thaliana, Oryza sativa, Picea sitchensis, Taxus chinensis, and G. biloba into nine groups, in which GbJAZs belong to Group VI-IX. GbJAZs have similar functional motifs to A. thaliana and O. sativa, but also contain three specific motifs of gymnosperms, indicating that, although gymnosperms and angiosperms have some conservative structures and functions, their evolutionary processes are independent. Expression pattern analysis showed that the expression levels of GbJAZs were significantly up-regulated by MeJA, but the change pattern and amplitude were different, indicating that the function of GbJAZs in response to a JA signal may be different. After ABA and SA treatment, the expression of GbJAZs was up-regulated or inhibited in varying degrees, and different GbJAZs may be involved in the synergistic or antagonistic effects between JA and other hormone signals. The MeJA significantly increased the content of TTLs in G. biloba leaves, which were significantly positively correlated with the expression levels of GbJAZ01, 02, 07, and 11, and negatively correlated with the expression of GbJAZ04. They may play an important role in JA signaling pathways and the interactions between JA and other hormone signals, and participate in the regulation of the biosynthesis of TTLs. Our results provide a reference for the discovery that GbJAZs are involved in JA signaling pathways, and lay a theoretical foundation for analyzing JA signaling pathways to regulate the synthesis of secondary metabolites. Full article
(This article belongs to the Special Issue Molecular Mechanism of Secondary Metabolic Pathways in Forest Trees)
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Review

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9 pages, 1017 KiB  
Review
Research Advances in Oxidosqualene Cyclase in Plants
by Pengqing Wang, Guo Wei and Liguo Feng
Forests 2022, 13(9), 1382; https://doi.org/10.3390/f13091382 - 30 Aug 2022
Cited by 3 | Viewed by 1719
Abstract
Triterpenes are natural products of plants that can defend against microorganisms and various stresses. Oxidosqualene cyclase (OSC), the key rate-limiting enzyme of the triterpene biosynthetic pathway, catalyzes 2,3-oxidosqualene into sterols and triterpenes with different skeletons through the chair–boat–chair (CBC) conformation or chair–chair–chair (CCC) [...] Read more.
Triterpenes are natural products of plants that can defend against microorganisms and various stresses. Oxidosqualene cyclase (OSC), the key rate-limiting enzyme of the triterpene biosynthetic pathway, catalyzes 2,3-oxidosqualene into sterols and triterpenes with different skeletons through the chair–boat–chair (CBC) conformation or chair–chair–chair (CCC) conformation. They were expanded in plants mainly by tandem duplication and are distributed in many plant lineages. They have multiple biological activities, including as functional foods and drugs. Here, we summarize the current characterized forest OSCs and their potential functions, especially for pharmacological applications. The study of triterpene-catalyzed enzyme OSC has an important scientific role and potential economic value. This paper summarizes the research advances of the main members of the OSC family in plants, their structure and function, the biosynthesis of triterpenes, and the molecular evolution of OSC. Full article
(This article belongs to the Special Issue Molecular Mechanism of Secondary Metabolic Pathways in Forest Trees)
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13 pages, 1798 KiB  
Review
Advances in Biosynthesis and Pharmacological Effects of Cinnamomum camphora (L.) Presl Essential Oil
by Yuqing Du, Hua Zhou, Liying Yang, Luyuan Jiang, Duanfen Chen, Deyou Qiu and Yanfang Yang
Forests 2022, 13(7), 1020; https://doi.org/10.3390/f13071020 - 28 Jun 2022
Cited by 6 | Viewed by 2161
Abstract
Cinnamomum camphora (L.) Presl essential oil (CCEO) is a volatile oil with aroma and is extracted from various tissues of Cinnamomumcamphora. It is traditionally used as a spice, preservative, as an anti-inflammatory and for sterilization. Terpenoids are the main active components [...] Read more.
Cinnamomum camphora (L.) Presl essential oil (CCEO) is a volatile oil with aroma and is extracted from various tissues of Cinnamomumcamphora. It is traditionally used as a spice, preservative, as an anti-inflammatory and for sterilization. Terpenoids are the main active components in CCEO. Based on currently available research, considerable effort is still needed to study the biosynthesis and regulation of terpenoids in CCEO. In this review, the research progress related to terpenoid biosynthesis and bioactivity in CCEO in recent years is summarized, with the data compiled and presented mainly from online resources such as PubMed, Scopus and CNKI in China up to May 2022. The research advances related to key enzymes in the terpenoid biosynthesis pathway are mainly discussed. Previous studies have isolated some genes encoding key enzymes involved in terpenoid biosynthesis; however, among these genes, only a few TPS genes have been verified to catalyze the production of terpenoid synthases at the protein level. Most genes encoding key enzymes have been cloned and isolated, but no transgenic experiments have been carried out to verify gene function. In-depth study of the biosynthesis of terpenoids in CCEO may contribute to a better understanding of the differential accumulation of terpenoids in different types of C. camphora and provide reference for improving terpenoid content in CCEO. Full article
(This article belongs to the Special Issue Molecular Mechanism of Secondary Metabolic Pathways in Forest Trees)
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