In the growth condition(s) of plants, numerous secondary metabolites (SMs) are produced by them to serve variety of cellular functions essential for physiological processes, and recent increasing evidences have implicated stress and defense response signaling in their production. The type and concentration(s) of secondary molecule(s) produced by a plant are determined by the species, genotype, physiology, developmental stage and environmental factors during growth. This suggests the physiological adaptive responses employed by various plant taxonomic groups in coping with the stress and defensive stimuli. The past recent decades had witnessed renewed interest to study abiotic factors that influence secondary metabolism during in vitro and in vivo growth of plants. Application of molecular biology tools and techniques are facilitating understanding the signaling processes and pathways involved in the SMs production at subcellular, cellular, organ and whole plant systems during in vivo and in vitro growth, with application in metabolic engineering of biosynthetic pathways intermediates.

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Stress and defense responses in plant secondary metabolites production

Ultraviolet-B (UV-B) radiation has, for many decades now, been widely studied with respect to its consequences on plant and animal health. Though according to NASA, the ozone hole is on its way to recovery, it will still be a considerable time before UV-B levels reach pre-industrial limits. Thus, for the present, excessive UV-B reaching the Earth is a cause for concern, and UV-B related human ailments are on the rise. Plants produce various secondary metabolites as one of the defense strategies under UV-B. They provide photoprotection via their UV-B screening effects and by quenching the reactive oxygen- and nitrogen species produced under UV-B influence. These properties of plant secondary metabolites (PSMs) are being increasingly recognized and made use of in sunscreens and cosmetics, and pharma- and nutraceuticals are gradually becoming a part of the regular diet. Secondary metabolites derived from medicinal plants (alkaloids, terpenoids, and phenolics) are a source of pharmaceuticals, nutraceuticals, as well as more rigorously tested and regulated drugs. These metabolites have been implicated in providing protection not only to plants under the influence of UV-B, but also to animals/animal cell lines, when the innate defenses in the latter are not adequate under UV-B-induced damage. The present review focuses on the defense potential of secondary metabolites derived from medicinal plants in both plants and animals. In plants, the concentrations of the alkaloids, terpenes/terpenoids, and phenolics have been discussed under UV-B irradiation as well as the fate of the genes and enzymes involved in their biosynthetic pathways. Their role in providing protection to animal models subjected to UV-B has been subsequently elucidated. Finally, we discuss the possible futuristic scenarios and implications for plant, animal, and human health pertaining to the defense potential of these secondary metabolites under UV-B radiation-mediated damages.

Defense potential of secondary metabolites in medicinal plants under UV-B stress

As sessile organisms, plants are unable to avoid being subjected to environmental stresses that negatively affect their growth and productivity Instead, they utilize various mechanisms at the morphological, physiological, and biochemical levels to alleviate the deleterious effects of such stresses Amongst these, secondary metabolites produced by plants represent an important component of the defense system Secondary metabolites, namely phenolics, terpenes, and nitrogen-containing compounds, have been extensively demonstrated to protect plants against multiple stresses, both biotic (herbivores and pathogenic microorganisms) and abiotic (eg drought, salinity, and heavy metals) The regulation of secondary metabolism by beneficial elements such as silicon (Si) is an important topic Silicon-mediated alleviation of both biotic and abiotic stresses has been well documented in numerous plant species Recently, many studies have demonstrated the involvement of Si in strengthening stress tolerance through the modulation of secondary metabolism In this review, we discuss Si-mediated regulation of the synthesis, metabolism, and modification of secondary metabolites that lead to enhanced stress tolerance, with a focus on physiological, biochemical, and molecular aspects Whilst mechanisms involved in Si-mediated regulation of pathogen resistance via secondary metabolism have been established in plants, they are largely unknown in the case of abiotic stresses, thus leaving an important gap in our current knowledge

Integration of silicon and secondary metabolites in plants: a significant association in stress tolerance.

Saline–alkali stress is a severely adverse abiotic stress limiting plant growth. Malus halliana Koehne is an apple rootstock that is tolerant to saline–alkali stress. To understand the molecular mechanisms underlying the tolerance of M. halliana to saline–alkali stress, an integrated metabolomic and proteomic approach was used to analyze the plant pathways involved in the stress response of the plant and its regulatory mechanisms. A total of 179 differentially expressed proteins (DEPs) and 140 differentially expressed metabolites (DEMs) were identified. We found that two metabolite-related enzymes (PPD and PAO) were associated with senescence and involved in porphyrin and chlorophyll metabolism; six photosynthesis proteins (PSAH2, PSAK, PSBO2, PSBP1, and PSBQ2) were significantly upregulated, especially PSBO2, and could act as regulators of photosystem II (PSII) repair. Sucrose, acting as a signaling molecule, directly mediated the accumulation of D-phenylalanine, tryptophan, and alkaloid (vindoline and ecgonine) and the expression of proteins related to aspartate and glutamate (ASP3, ASN1, NIT4, and GLN1−1). These responses play a central role in maintaining osmotic balance and removing reactive oxygen species (ROS). In addition, sucrose signaling induced flavonoid biosynthesis by activating the expression of CYP75B1 to regulate the homeostasis of ROS and promoted auxin signaling by activating the expression of T31B5_170 to enhance the resistance of M. halliana to saline–alkali stress. The decrease in peroxidase superfamily protein (PER) and ALDH2C4 during lignin synthesis further triggered a plant saline–alkali response. Overall, this study provides an important starting point for improving saline–alkali tolerance in M. halliana via genetic engineering.

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Integrated physiologic, proteomic, and metabolomic analyses of Malus halliana adaptation to saline–alkali stress

Content determination and microscopic observation proved that dendrobine accumulation in the stem of Dendrobium nobile Lindl. increased after infection with mycorrhizal fungus MF23 (Mycena sp.). Large-scale transcriptome sequencing of symbiotic and asymbiotic D. nobile revealed that 30 unigenes encoding proteins were possibly related to the biosynthesis of dendrobine sesquiterpene backbone. A qRT-PCR experiment of 16 unigenes, selected randomly, proved that there were significant changes in the expression levels of AACT, MVD, PMK and TPS21 at 9 weeks after inoculation. These results implied that MF23 might stimulate dendrobine biosynthesis by regulating the expressions of genes involved in the mevalonate (MVA) pathway. The biogenetic pathway of dendrobine was suggested systematically according to the structural features of dendrobine alkaloids and their sesquiterpene precursors, which implied that post-modification enzymes might play a major role in dendrobine biosynthesis. Thus, genes encoding post-modification enzymes, including cytochrome P450, aminotransferase and methyltransferase, were screened for their possible involvement in dendrobine biosynthesis. This study provides a good example of endophytes promoting the formation of bioactive compounds in their host and paves the way for further investigation of the dendrobine biosynthetic pathway.

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Transcriptome Analysis of Genes Involved in Dendrobine Biosynthesis in Dendrobium nobile Lindl. Infected with Mycorrhizal Fungus MF23 ( Mycena sp.)

Catharanthus roseus is an important medicinal plant, which produces a variety of indole alkaloids of significant pharmaceutical relevance. In the present study, we aimed to investigate the potential stress-induced increase of indole alkaloid biosynthesis in C. roseus using proteomic technique. The contents of the detectable alkaloids ajmalicine, vindoline, catharanthine, and strictosidine in C. roseus were significantly increased under binary stress. Proteomic analysis revealed that the abundance of proteins related to tricarboxylic acid cycle and cell wall was largely increased; while, that of proteins related to tetrapyrrole synthesis and photosynthesis was decreased. Of note, 10-hydroxygeraniol oxidoreductase, which is involved in the biosynthesis of indole alkaloid was two-fold more abundant in treated group compared to the control. In addition, mRNA expression levels of genes involved in the indole alkaloid biosynthetic pathway indicated an up-regulation in their transcription in C. roseus under UV-B irradiation. These results suggest that binary stress might negatively affect the process of photosynthesis in C. roseus. In addition, the induction of alkaloid biosynthesis appears to be responsive to binary stress.

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Jingkui Tian

Papers

Binary stress induces an increase in indole alkaloid biosynthesis in Catharanthus roseus