Potential ecological roles of flavonoids from Stellera chamaejasme

Abstract

Stellera chamaejasme L. (Thymelaeaceae), a perennial weed, distributes widely in the grasslands of Russia, Mongolia and China. The plant synthesizes various secondary metabolites including a group of flavonoids. To our knowledge, flavonoids play important roles in the interactions between plants and the environment. So, what are the benefits to S. chamaejasme from producing these flavonoids? Here, we discuss the potential ecological role of flavonoids from S. chamaejasme in protecting the plant from insects and other herbivores, as well as pathogens and competing plant species, and new data are provided on the phytotoxicity of flavonoids from S. chamaejasme toward Poa annua L.

Keywords:

• allelopathy
• antifeedant
• antimicrobial
• flavonoids
• Stellera chamaejasme

Flavonoids are small molecular secondary metabolites synthesized only by plants.¹ Due to the strong antioxidative properties, flavonoids display various biological activities. Also, the flavonoids are beneficial to plants themselves from participating in plants’ interactions with other organisms and their reactions to environmental stresses.² S. chamaejasme synthesizes a group of flavonoids, which gained much attention due to their biological activities to cancer cells and virus.^3,4 Additionally, their relevance to the plant itself also deserve extensive investigations. Several reports demonstrated that flavonoids from S. chamaejasme had insecticidal effects or showed contact toxicity to pathogenic nematodes. The antifungal and antibacterial effects of S. chamaejasme were well studied. Flavonoids from S. chamaejasme displayed relatively high level of phytotoxicity, indicating that allelopathy could be a beneficial function of the flavonoids to the producing plant.

The populations of S. chamaejasme have been increasing constantly in recent years.⁵ As one of the most toxic weeds in the grassland, S. chamaejasme can poison or even kill the cattle if they eat the leaves or flowers of the weed by mistake.⁶ Total flavonoid obtained from S. chamaejsme showed strong toxicity to mice and rabbit.⁷ Chamaechromone and isochamaejasmin isolated from S. chamaejasme displayed cytotoxicity to canine kidney MDCK cells.⁸ Therefore, the flavonoids may be a benefit to S. chamaejsme for deterring grazing of vertebrate herbivores. Additionally, S. chameajasme showed antifeeding activity to plant pathogenic insects. Ethanol extract of S. chameajasme strongly inhabited the growth of insect pests Pieris rapae, Myzus persicae and Ostrina furnacalis,⁹ and displayed contact and oral toxicities against Sesamia inferens and Chilo suppressalis walker.¹⁰ Furthermore, (+)-epiafzelechin had strong acaricidal activity against Tetranychus cinnabarinus B, while, quercetin displayed relatively weaker activity.¹¹ Chamechromone possessed strong effect of antifeedant and stomach poison on the 5th instar larvae of P. rapae.¹² Ethanol extract of S. chamaejasme showed significantly nematicidal activity against pine parasitic nematodes Bursaphelenchus xylophilus and Bursaphelenchus mucronatus. Ten nematicidal compounds were isolated by a bioassay guided fractionation. Among them, chamaejasmenin C induced the highest mortality against B. xylophilus, and chamaechromone exhibited strongly nematicidal activity against B. mucronatus. Biflavonoids ruixianglangdusu B, 7-methoxyneochaejasmin A, (+)-chamaejasmine, isosikokianin A, isoneochamaejasmin A and neochamaejasmin B also exhibited significantly nematicidal activities.^13,14 These results indicated that S. chamaejasme has strong antifeeding effects to phytophagous animals such as livestock, pests, acarid and nematodes, and the antifeeding effects are at least partially dependent on the flavonoids synthesized by the weed.

Ethanol extract, ethyl acetate and methanol fractions of S. chamaejasme showed antimicrobial activity against 14 phytopathogens.¹⁵ Bioassay guided fraction of S. chamaejasme led to the isolation of neochamaejasmine B and chamaechromone, and both compounds could effectively inhibit the growth of Bakeri rehm, Fusarium graminearum, Alternaria solani, Fusarium bulbigenum, Exserohilum turcicum, Alternaria alternata and Phytophthora capsici.¹⁶ Moreover, chamaechromone had antifungal activities on Botrytis cinerea, Colletotrichum acutatum and Monilinia fructicola.¹⁷ Biflavanones chamaejasmenin A, chamaejasmenin D and isochamaejasmenin B displayed potent antimitotic and antifungal activity against Pyricularia oryzae, which cause rice blast to affect rice production grown in upland and wet-land.¹⁸ Another biflavanone 4′, 4, 5, 5″, 7, 7″-hexahydroxy-3, 3″-biflavone also exhibited antibacterial activity.¹⁹ Further study of the relationship between structure and antibacterial activity of neochamaejasmine B indicated that 7-OH and 7″-OH were the main active groups.²⁰ These results indicated that flavones maybe the main antimicrobial compounds of S. chamaejasme.

Water and ethanol extracts of S. chamaejasme inhibited seed germination and/or seedling growth of 13 plant species,^21-23 and the phytotoxic effects were more stronger on dicotyledonous plants than monocotyledonous plants. As a result of decomposition in the soil, the tissues of S. chamaejasme reduced seedling growth of Melilotus suaveolens Ledeb, Lolium perenne L., Psathyrostachys juncea, Onobrychis viciifolia, Bromus inermis and alfalfa,^24-27 and dicotyledonous plants were more sensitive to the decomposed tissues than monocotyledonous plants. In our previous research, a bioassay guided fractionation of root extracts of S. chamaejasme led to the isolation of 8 flavonoids. Most of these compounds displayed strong phytotoxic effects on seedling growth of Arabidopsis. Among them, neochamaejasmin B, mesoneochamaejasmin A, 7-methoxylneochaejasmin A and dihydrodaphnodorin B were found in soils associated with S. chamaejasme, and these potential allelochemicals also showed phytotoxicity to Clinelymus nutans L., an associated grass of S. chamaejasme.²⁸ Another grass (P. annua) was also used as a receptor plant to evaluate the phytotoxicity of the allelochemicals. Results showed that the allelochemicals could inhibit shoot and root elongation, and seedling growth of P. annua (Fig. 1). In consistent with bioassay on C. nutans, all compounds displayed stronger inhibitory effects on root than shoot because the root shoot ratio of P. annua dropped after treatments (Fig. 1). A similar result was also found in the phytotoxic effects of water extract of S. chamaejasme, which strongly reduced the root length of rapeseed, sesame, wheat and maize, while slightly inhabited the shoot elongation. Moreover, dicotyledonous plant (Arabidopsis) was more sensitive to the flavonoids than monocotyledonous plants (C. nutans and P. annua). These results indicated that S. chamaejasme is more phytoxtoxic to dicotyledonous plants than monocotyledonous plants, and showed tissue-specific phytotoxicity on root growth. Flavonoids are at least partly responsible for the strong phytotoxic effects of S. chamaejasme. The potential allelopathic behavior may facilitate this weed to become a good competitor against other plant species in the environment.

Figure 1. Phytotoxic effects of potential flavonoid allelochemicals from S. chamaejasme on P. annua seedlings. Five-day-old seedlings were treated with neochamaejasmin B, mesoneochamaejasmin A, 7-methoxylneochaejasmin A and dihydrodaphnodorin B at concentrations of 25, 50, 100 and 200 μg/mL for 3 days, respectively. Root length (A), shoot length (B), and fresh weight (C) of the seedlings were collected, and root shoot ratio (D) was calculated. Values in the table are presented as percentage of the mean compared to the control. SE is one standard error of the mean, n = 12.

In conclusion, the multifunctional flavonoids synthesized by S. chamaejasme may play important ecological roles in protecting the plant from vertebrate herbivores, insects, pathogenic microorganisms, as well as competitive plant species. These benefits may contribute to the competitive behavior of S. chamaejasme, one of the most ecologically-threatening weed in the grassland.

Disclosure of Potential Conflicts of Interest

No potential conflicts of interest were disclosed.

Funding

We would like to thank the National Natural Science Foundation of China (31070386 and 31300290), around five top priorities program of “One-Three-Five” Strategic Planning of Lanzhou Institute of Chemical Physics, CAS, the Open Project of Key Laboratory of Tobacco Diseases and Insect Pests Monitoring Controlling and Integrated Management, Institute of Tobacco Research, Chinese Academy of Agricultural Sciences (IPM201404) and the Province-academy Cooperation Program of Henan Province of China (102106000021) for the funding that made this work possible.