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Role of Steroids and Triterpenoids in Plant Growth, Development and Stress Response

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A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Plant Sciences".

Deadline for manuscript submissions: closed (30 October 2023) | Viewed by 16363

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Prof. Dr. Anna Szakiel

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Department of Plant Biochemistry, Faculty of Biology, University of Warsaw, 1 Miecznikowa Street, 02-096 Warsaw, Poland
Interests: triterpenoids; steroids; plant general and specialized metabolism; plant in vitro cultures; elicitation; bioactive natural products; occurrence of triterpenoids in edible and medicinal plants; plant chemical defense
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Dear Colleagues,

Steroids and triterpenoids are isoprenoids produced by folding and cyclization of their common C30 precursor, the long-chain hydrocarbon squalene. These two groups of squalene derivatives distinctly differ in the functions they perform in plants, and therefore they are commonly regarded as primary and secondary (or more aptly: general and specialized) metabolites, respectively. Sterols, a characteristic subgroup of steroids, are integral components of plant membranes and contribute to maintaining the membrane permeability and fluidity. Some sterols form special structures with sphingolipids, referred to as microdomains (also known as nanodomains or lipid rafts), that are believed to play an important role in processes such as channel regulation, protein trafficking, signal transduction and plant-pathogen interactions. Thus, in addition to their membrane architectural function, sterols also affect the activity of integral membrane proteins, including enzymes, ion channels, receptors and components of signal transduction pathways such as ATPases. Moreover, sterols also serve as precursors of brassinosteroid hormones and some specialized metabolites, such as steroidal sapogenins, steroidal glycoalkaloids or cardenolides, therefore, they are involved in many processes occurring in plants, ranging from regulation of growth and development to stress resistance. In turn, triterpenoids, considered typical specialized metabolites, are believed to play an important role in plant chemical defense and interactions with the environment. The interplay between steroids and triterpenoids, compounds sharing the biosynthetic pathway up to the common precursor, seems to be crucial in the metabolic strategy of the plant facing stress factors.

This Special Issue invites researchers to contribute original research or updated review articles that aim to cover a wide spectrum of aspects concerning the role of steroids and triterpenoids in plant growth and development, as well as in stress response to various abiotic and biotic factors.

Prof. Dr. Anna Szakiel
Guest Editor

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Keywords

biosynthesis
chemical defense
plant growth and development
steroids
sterols
stress response
triterpenoids

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Published Papers (8 papers)

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Research

14 pages, 2817 KiB

Open AccessArticle

Arabidopsis 3β-Hydroxysteroid Dehydrogenases/C4-Decarboxylases Are Essential for the Pollen and Embryonic Development

by Jiawen Pan, Weifeng Li, Binzhao Chen, Linchuan Liu, Jianjun Zhang and Jianming Li

Int. J. Mol. Sci. 2023, 24(21), 15565; https://doi.org/10.3390/ijms242115565 - 25 Oct 2023

Viewed by 1416

Abstract

The biosynthesis of C_27–29 sterols from their C₃₀ precursor squalene involves C24-alkylation and the removal of three methyl groups, including two at the C4 position. The two C4 demethylation reactions require a bifunctional enzyme known as 3β-hydroxysteroid dehydrogenase/C4-decarboxylase (3βHSD/D), which removes an oxidized methyl (carboxylic) group at C4 while simultaneously catalyzing the 3β-hydroxyl→3-keto oxidation. Its loss-of-function mutations cause ergosterol-dependent growth in yeast and congenital hemidysplasia with ichthyosiform erythroderma and limb defect (CHILD) syndrome in humans. Although plant 3βHSD/D enzymes were well studied enzymatically, their developmental functions remain unknown. Here we employed a CRISPR/Cas9-based genome-editing approach to generate knockout mutants for two Arabidopsis 3βHSD/D genes, HSD1 and HSD2, and discovered the male gametophytic lethality for the hsd1 hsd2 double mutation. Pollen-specific expression of HSD2 in the heterozygous hsd1 hsd2/+ mutant not only rescued the pollen lethality but also revealed the critical roles of the two HSD genes in embryogenesis. Our study thus demonstrated the essential functions of the two Arabidopsis 3βHSD/D genes in male gametogenesis and embryogenesis. Full article

(This article belongs to the Special Issue Role of Steroids and Triterpenoids in Plant Growth, Development and Stress Response)

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13 pages, 2249 KiB

Open AccessArticle

The Functional Characterization of DzCYP72A12-4 Related to Diosgenin Biosynthesis and Drought Adaptability in Dioscorea zingiberensis

by Weipeng Wang, Lixiu Hou, Song Li and Jiaru Li

Int. J. Mol. Sci. 2023, 24(9), 8430; https://doi.org/10.3390/ijms24098430 - 8 May 2023

Cited by 3 | Viewed by 1691

Abstract

Dioscorea zingiberensis is a perennial herb famous for the production of diosgenin, which is a valuable initial material for the industrial synthesis of steroid drugs. Sterol C26-hydroxylases, such as TfCYP72A616 and PpCYP72A613, play an important role in the diosgenin biosynthesis pathway. In the present study, a novel gene, DzCYP72A12-4, was identified as C26-hydroxylase and was found to be involved in diosgenin biosynthesis, for the first time in D. zingiberensis, using comprehensive methods. Then, the diosgenin heterogenous biosynthesis pathway starting from cholesterol was created in stable transgenic tobacco (Nicotiana tabacum L.) harboring DzCYP90B71(QPZ88854), DzCYP90G6(QPZ88855) and DzCYP72A12-4. Meanwhile, diosgenin was detected in the transgenic tobacco using an ultra-performance liquid chromatography system (Vanquish UPLC 689, Thermo Fisher Scientific, Bremen, Germany) tandem MS (Q Exactive Hybrid Quadrupole-Orbitrap Mass Spectrometer, Thermo Fisher Scientific, Bremen, Germany). Further RT-qPCR analysis showed that DzCYP72A12-4 was highly expressed in both rhizomes and leaves and was upregulated under 15% polyethylene glycol (PEG) treatment, indicating that DzCYP72A12-4 may be related to drought resistance. In addition, the germination rate of the diosgenin-producing tobacco seeds was higher than that of the negative controls under 15% PEG pressure. In addition, the concentration of malonaldehyde (MDA) was lower in the diosgenin-producing tobacco seedlings than those of the control, indicating higher drought adaptability. The results of this study provide valuable information for further research on diosgenin biosynthesis in D. zingiberensis and its functions related to drought adaptability. Full article

(This article belongs to the Special Issue Role of Steroids and Triterpenoids in Plant Growth, Development and Stress Response)

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12 pages, 1812 KiB

Open AccessArticle

Epi-Brassinolide Regulates ZmC4 NADP-ME Expression through the Transcription Factors ZmbHLH157 and ZmNF-YC2

by Yuanfen Gao, Xuewu He, Huayang Lv, Hanmei Liu, Yangping Li, Yufeng Hu, Yinghong Liu, Yubi Huang and Junjie Zhang

Int. J. Mol. Sci. 2023, 24(5), 4614; https://doi.org/10.3390/ijms24054614 - 27 Feb 2023

Cited by 2 | Viewed by 2013

Abstract

Maize is a main food and feed crop with great production potential and high economic benefits. Improving its photosynthesis efficiency is crucial for increasing yield. Maize photosynthesis occurs mainly through the C4 pathway, and NADP-ME (NADP-malic enzyme) is a key enzyme in the photosynthetic carbon assimilation pathway of C4 plants. ZmC4-NADP-ME catalyzes the release of CO₂ from oxaloacetate into the Calvin cycle in the maize bundle sheath. Brassinosteroid (BL) can improve photosynthesis; however, its molecular mechanism of action remains unclear. In this study, transcriptome sequencing of maize seedlings treated with epi-brassinolide (EBL) showed that differentially expressed genes (DEGs) were significantly enriched in photosynthetic antenna proteins, porphyrin and chlorophyll metabolism, and photosynthesis pathways. The DEGs of C4-NADP-ME and pyruvate phosphate dikinase in the C4 pathway were significantly enriched in EBL treatment. Co-expression analysis showed that the transcription level of ZmNF-YC2 and ZmbHLH157 transcription factors was increased under EBL treatment and moderately positively correlated with ZmC4-NADP-ME. Transient overexpression of protoplasts revealed that ZmNF-YC2 and ZmbHLH157 activate C4-NADP-ME promoters. Further experiments showed ZmNF-YC2 and ZmbHLH157 transcription factor binding sites on the −1616 bp and −1118 bp ZmC4 NADP-ME promoter. ZmNF-YC2 and ZmbHLH157 were screened as candidate transcription factors mediating brassinosteroid hormone regulation of the ZmC4 NADP-ME gene. The results provide a theoretical basis for improving maize yield using BR hormones. Full article

(This article belongs to the Special Issue Role of Steroids and Triterpenoids in Plant Growth, Development and Stress Response)

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15 pages, 3325 KiB

Open AccessArticle

Methyl Jasmonate- and Salicylic Acid-Induced Transcription Factor ZjWRKY18 Regulates Triterpenoid Accumulation and Salt Stress Tolerance in Jujube

by Cuiping Wen, Zhong Zhang, Qianqian Shi, Xiaoshan Duan, Jiangtao Du, Cuiyun Wu and Xingang Li

Int. J. Mol. Sci. 2023, 24(4), 3899; https://doi.org/10.3390/ijms24043899 - 15 Feb 2023

Cited by 12 | Viewed by 2233

Abstract

Triterpenoids are important, pharmacologically active substances in jujube (Ziziphus jujuba Mill.), and play an important role in the plant’s resistance to abiotic stress. However, regulation of their biosynthesis, and the underlying mechanism of their balance with stress resistance, remain poorly understood. In this study, we screened and functionally characterized the ZjWRKY18 transcription factor, which is associated with triterpenoid accumulation. The transcription factor is induced by methyl jasmonate and salicylic acid, and its activity was observed by gene overexpression and silencing experiments, combined with analyses of transcripts and metabolites. ZjWRKY18 gene silencing decreased the transcription of triterpenoid synthesis pathway genes and the corresponding triterpenoid content. Overexpression of the gene promoted the biosynthesis of jujube triterpenoids, as well as triterpenoids in tobacco and Arabidopsis thaliana. In addition, ZjWRKY18 binds to W-box sequences to activate promoters of 3-hydroxy-3-methyl glutaryl coenzyme A reductase and farnesyl pyrophosphate synthase, suggesting that ZjWRKY18 positively regulates the triterpenoid synthesis pathway. Overexpression of ZjWRKY18 also increased tolerance to salt stress in tobacco and Arabidopsis thaliana. These results highlight the potential use of ZjWRKY18 to improve triterpenoid biosynthesis and salt stress tolerance in plants, and provide a strong basis for metabolic engineering to improve the content of triterpenoids and breeding of jujube varieties that are resistant to stress. Full article

(This article belongs to the Special Issue Role of Steroids and Triterpenoids in Plant Growth, Development and Stress Response)

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12 pages, 4547 KiB

Open AccessArticle

Principal Component Analysis to Assess the Changes of Yield and Quality in Pinellia ternata at Different Stages after Brassinolide Treatments

by Chenchen Guo, Yanfen Zhang, Dengyun Wu, Mengyue Wang, Yu Du, Jianzhou Chu and Xiaoqin Yao

Int. J. Mol. Sci. 2022, 23(23), 15375; https://doi.org/10.3390/ijms232315375 - 6 Dec 2022

Cited by 4 | Viewed by 1711

Abstract

Brassinolide (BR) is the “sixth class” plant hormone, which plays an important role in various physiological and biochemical processes of plants. The wide variety of functions of Pinellia ternata means that there is huge demand for it and thus it is in short supply. This paper mainly assessed the changes of yield and quality in P. ternata at different stages after BR treatments by principal component analysis, in order to improve the yield and quality of P. ternata and at the same time determine the best harvest time. The results showed that the tuber yield of P. ternata was significantly increased by BR treatments at different stages (except for the 15th day). After the 15th, 45th, 60th, 75th, 90th, and 105th day of treatments, the tuber yield of P. ternata reached peak values at 0.10 (0.65 g), 0.50 (1.97 g), 0.50 (1.98 g), 1.00 (2.37 g), 1.00 (2.84 g), and 2.00 mg/L (3.76 g) BR treatment, respectively. The optimal harvest time was the 75th day after 0.10, 0.50, and 1.00 mg/L BR treatments, which not only significantly improved the yield of P. ternata, but also retained high level of total alkaloids in the tubers (20.89, 5.37, and 13.44%) and bulbils (9.74, 20.42, and 13.62%), high total flavone content in the tubers (17.66, 16.26, and 12.74%) and bulbils (52.63, 12.79, and 38.69%), and high β-sitosterol content in the tubers (25.26, 16.65, and 0.62%) of P. ternata, compared with the control, respectively. Full article

(This article belongs to the Special Issue Role of Steroids and Triterpenoids in Plant Growth, Development and Stress Response)

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14 pages, 2338 KiB

Open AccessArticle

Tomato Sterol 22-desaturase Gene CYP710A11: Its Roles in Meloidogyne incognita Infection and Plant Stigmasterol Alteration

by Alessandro Cabianca, Andrea Caroline Ruthes, Katharina Pawlowski and Paul Dahlin

Int. J. Mol. Sci. 2022, 23(23), 15111; https://doi.org/10.3390/ijms232315111 - 1 Dec 2022

Cited by 8 | Viewed by 1938

Abstract

Sterols are isoprenoid-derived lipids that play essential structural and functional roles in eukaryotic cells. Plants produce a complex mixture of sterols, and changes in plant sterol profiles have been linked to plant–pathogen interactions. β-Sitosterol and stigmasterol, in particular, have been associated with plant defense. As nematodes have lost the ability to synthesize sterols de novo, they require sterols from the host. Tomato (Solanum lycopersicum) plants infected by the plant parasitic nematode Meloidogyne incognita show a reduced level of stigmasterol and a repression of the gene CYP710A11, encoding the sterol C-22 desaturase that is responsible for the conversion of β-sitosterol to stigmasterol. In this study, we investigated the role of the tomato sterol C-22 desaturase gene CYP710A11 in the response to infection by M. incognita. We explored the plant–nematode interaction over time by analyzing the plant sterol composition and CYP710A11 gene regulation in S. lycopersicum after M. incognita infection. The temporal gene expression analysis showed that 3 days after inoculation with M. incognita, the CYP710A11 expression was significantly suppressed in the tomato roots, while a significant decrease in the stigmasterol content was observed after 14 days. A cyp710a11 knockout mutant tomato line lacking stigmasterol was analyzed to better understand the role of CYP710A11 in nematode development. M. incognita grown in the mutant line showed reduced egg mass counts, presumably due to the impaired growth of the mutant. However, the nematodes developed as well as they did in the wild-type line. Thus, while the suppression of CYP710A11 expression during nematode development may be a defense response of the plant against the nematode, the lack of stigmasterol did not seem to affect the nematode. This study contributes to the understanding of the role of stigmasterol in the interaction between M. incognita and tomato plants and shows that the sterol C-22 desaturase is not essential for the success of M. incognita. Full article

(This article belongs to the Special Issue Role of Steroids and Triterpenoids in Plant Growth, Development and Stress Response)

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16 pages, 4077 KiB

Open AccessArticle

Brassinolide Soaking Reduced Nitrite Content and Extended Color Change and Storage Time of Toona sinensis Bud during Low Temperature and Near Freezing-Point Temperature Storage

by Xihang Xu, Chenchen Guo, Chunying Ma, Minghui Li, Ying Chen, Cunqi Liu, Jianzhou Chu and Xiaoqin Yao

Int. J. Mol. Sci. 2022, 23(21), 13110; https://doi.org/10.3390/ijms232113110 - 28 Oct 2022

Cited by 15 | Viewed by 1684

Abstract

Low temperatures are often used to preserve fruits and vegetables. However, low-temperature storage also causes problems, such as chilling injury, nitrite accumulation, and browning aggravation in plants. This study investigated the effects of brassinolide (BR,1.0 mg L⁻¹) solution soaking, storage temperatures (−2 ± 0.5 °C, 4 ± 0.5 °C, and 20 ± 1 °C), and their combinations on nitrite content, color change, and quality of stored Toona sinensis bud. The results showed that low temperature (LT, 4 ± 0.5 °C) and near freezing-point temperature (NFPT, −2 ± 0.5 °C) storage effectively inhibited the decay of T. sinensis bud compared to room temperature (20 ± 1 °C, the control). The combined treatments of BR with LT or NFPT reduced nitrite content and maintained the color and the contents of vitamin C, carotenoids, saponins, β-sitosterol, polyphenol, anthocyanin, flavonoids, and alkaloids in T. sinensis bud. BR soaking delayed the occurrence of chilling injury during NFPT storage. Meanwhile, BR soaking enhanced the DPPH radical scavenging activity, ABTS activity, and FRAP content by increasing SOD and POD activity and the contents of proline, soluble, and glutathione, thus decreasing MDA and hydrogen peroxide content and the rate of superoxide radical production in T. sinensis bud during NFPT storage. This study provides a valuable strategy for postharvest T. sinensis bud in LT and NFPT storage. BR soaking extended the shelf life during LT storage and maintained a better appearance and nutritional quality during NFPT storage. Full article

(This article belongs to the Special Issue Role of Steroids and Triterpenoids in Plant Growth, Development and Stress Response)

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22 pages, 5365 KiB

Open AccessArticle

The Influence of Exogenous Jasmonic Acid on the Biosynthesis of Steroids and Triterpenoids in Calendula officinalis Plants and Hairy Root Culture

by Agata Rogowska, Małgorzata Stpiczyńska, Cezary Pączkowski and Anna Szakiel

Int. J. Mol. Sci. 2022, 23(20), 12173; https://doi.org/10.3390/ijms232012173 - 12 Oct 2022

Cited by 21 | Viewed by 2714

Abstract

The interplay between steroids and triterpenoids, compounds sharing the same biosynthetic pathway but exerting distinctive functions, is an important part of the defense strategy of plants, and includes metabolic modifications triggered by stress hormones such as jasmonic acid. Two experimental models, Calendula officinalis hairy root cultures and greenhouse cultivated plants (pot plants), were applied for the investigation of the effects of exogenously applied jasmonic acid on the biosynthesis and accumulation of steroids and triterpenoids, characterized by targeted GC-MS (gas chromatography-mass spectroscopy) metabolomic profiling. Jasmonic acid elicitation strongly increased triterpenoid saponin production in hairy root cultures (up to 86-fold) and their release to the medium (up to 533-fold), whereas the effect observed in pot plants was less remarkable (two-fold enhancement of saponin biosynthesis after a single foliar application). In both models, the increase of triterpenoid biosynthesis was coupled with hampering the biomass formation and modifying the sterol content, involving stigmasterol-to-sitosterol ratio, and the proportions between ester and glycoside conjugates. The study revealed that various organs in the same plant can react differently to jasmonic acid elicitation; hairy root cultures are a useful in vitro model to track metabolic changes, and enhanced glycosylation (of both triterpenoids and sterols) seems to be important strategy in plant defense response. Full article

(This article belongs to the Special Issue Role of Steroids and Triterpenoids in Plant Growth, Development and Stress Response)

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