Plant metabolites being renewable in nature have tremendous significance for the development of a sustainable society. In this manuscript we show that, terpenoids having nanometric lengths, commonly having several functional groups and several centers of chirality, can be utilized as renewable Molecular Functional Nanos (MFNs). The terpenoids spontaneously self-assembled in liquids yielding different morphologies such as vesicles, tubes, flowers, petals and fibers of nano- to micro-meter dimensions and supramolecular gels. The self-assemblies were utilized for the entrapment and release of fluorophores including anticancer drug, pollutant capture, generation of hybrid materials and catalysis.
Terpenoids are the largest class of natural products containing multiple of isoprene (C5) units , . Otto Wallach’s isoprene rule (1914) which states that, the terpenoids can be hypothetically constructed from the C5 isoprene building blocks, provided a unified concept of easy structural correlation among this class of natural products (Fig. 1). Later, this concept was refined by L. Ruzicka (1954) who proposed the famous biogenetic isoprene rule for the biosynthesis of terpenoids which involved a cation olefin chain elongation, cyclization and rearrangements to produce thousands of terpenoids. Over 55 000 terpenoids have been isolated both from plant and animals till recently and the number has been increasing steadily . The terpenoids play significant roles in plants as hormones, photosynthetic pigments, electron carriers, attracting pollinators, communication and defense, etc. . There has been a paradigm shift in the last decade in the use of plant metabolites as renewable chemicals instead of petroleum based raw materials because of the fast depletion of petroleum resources , , . As the plants can be grown in every season, the renewable supply of plant metabolites holds a great promise for the development of a sustainable society. Since the famous lecture of Richard Feynman on “There’s Plenty of Room at the Bottom” there has also been a paradigm shift in materials chemistry research towards ‘miniaturization’ by creating and controlling objects of nanometer dimensions (1–100 nm) , . The atomic building blocks of organic compounds such as C, H, O, N are much smaller in diameters than the diameters of Au, Ag, Pd which have been commonly explored for metal nanoparticles (Figs. 1 and 2). Detailed computations with naturally occurring terpenoids have revealed that, starting from monoterpenoids (C10) to sesqui- (C15), di- (C20), sester- (C25), tri- (C30) and tetra- (C40) terpenoids, all have nanometric lengths. Thus the terpenoids commonly having different functional groups at different positions can be termed as molecular functional nanos (MFNs, Figs. 1 and 3) , , . The plant based terpenoids can also be termed as renewable molecular functional nanos because of their intrinsic renewable nature. Functional nano-entities have drawn considerable research interest in recent years because of their prospective and realized applications in diversified areas , , , .
The molecular functional nanos (MFNs) have several unique features compared to the functional metal nanoparticles (FMNPs) some of which are: (i) FMNPs are mainly clusters of atoms consisting of either elementary metal or metal oxides/sulfides but the MFNs consists of mainly covalently linked C, H, N, O’s; (ii) the FMNPs need stabilizers or capping agents for their stabilities but MFNs require no such stabilizer or capping agents; (iii) functional groups such as COOH, NH2, SH are attached either via ligand exchange or via bilayer formation in FMNPs but MFNs usually have properly positioned functional groups; (iv) the MFNs can self-assemble due to the amphiphilic character of MFNs having large lipophilic backbone and properly positioned functional groups yielding different morphologies but FMNPs usually do not show such properties.
Molecular self-assembly is a process by which an ordered structure is obtained from discrete molecular components by means of specific local interactions without external directions , , , , , , . Studies in this area have been in the forefront of research during the last two decades for improving the understanding of self-assembly process in liquids , , ,  and also to investigate the applications of the resulting self-assemblies , , , , , . In this manuscript, we report the recent advances made in the utilization of terpenoids as renewable molecular functional nanos (MFNs). The MFNs spontaneously self-assemble in liquids yielding flowers, vesicles, tubes and fibrillar networks of nano- to micrometer dimensions. The utilization of the self-assemblies has also been demonstrated in drug entrapment, pollutant capture, thermochromic material, liquid crystal, heterogeneous catalysis  etc.
Schematic representation of the self-assembly of molecular functional nanos
Functional terpnoids can be schematically represented as I in Fig. 3 having a lipophilic backbone and polar functional groups M, N, O, P, Q and R. The lipophilic backbone helps the terpenoids to assemble via dispersion interactions (II) and polar functional groups can interact via H-bonding and/or electrostatic interaction forming a dimer (III). Such interactions can be extended to form a 1D chain (V and VI) and bilayer (IV and VII), which can yield fibrillar network, monolayer or bilayer vesicles, sheets, petals and flowers some of which are discussed in Section “Vesicular and tubular self-assembly from functional di- and tri-terpenoids and their applications”.
Vesicular and tubular self-assembly from functional di- and tri-terpenoids and their applications
Self-assembly of di- and tri-terpenoids yielding vesicles and tubules and their morphological characteristics
The terpenoids having lipophilic backbone and polar head groups such as –COOH are, in general, poorly soluble in water but are soluble in polar liquids such as DMSO, DMF and THF. The diterpenoids are C20 subset of terpenoids derived from geranylgeranyl diphosphate . Crotocembraneic acid 1, a macrocyclic diterpenoid was extracted from the leaves of Croton oblongifolius Roxb , . On treatment of a solution of the diterpenoid in the polar organic liquids under hot condition with water, cloudy suspensions were obtained. Evidences for the formation of vesicular self-assemblies from the macrocyclic diterpenoid crotocembraneic acid  were obtained by optical, electron and atomic force microscopy (Fig. 4). The mono-, di- and tri-hydroxy triterpenoids oleanolic 2 , ursolic 3 , maslinic 4 , corosolic 5  and arjunolic 6  acids isolated from the plants Lantana camara, Plumeria rubra, Olea Europaea, Psidium guajava, Terminalia arjuna, respectively, all formed vesicular self-assemblies in aqueous binary liquid mixtures. The vesicular self-assemblies having sufficiently bigger space inside could entrap cationic fluorophore rhodamine-B, anionic fluorophore carboxyfluorescein and the anticancer drug doxorubicin. Such a property of the functional terpenoids, many of which possess anticancer and antitumor properties, opens up their use in targeted drug delivery , , , , , , .
A 2D circular bilayer membrane can be extended to form a 3D tubular structure (Fig. 4). Evidence for the formation of such tubular morphology was obtained from the self-assemblies of ursolic acid 3 in ethanol-water (3:1 v/v, Fig. 5h). This was the first observation of tubular self-assemblies of naturally occurring triterpenoids. The solubility of the triterpenic acids in water and aqueous binary liquid mixtures could be increased by transforming them to their corresponding sodium and potassium salts 7–14. Interestingly, vesicular self-assemblies were obtained from all the sodium and potassium salts of triterpenic acids in aqueous binary liquid mixtures as characterized by optical, electron and atomic force microscopic techniques , .
Application in entrapment and release of fluorophores and generation of hybrid materials
Investigations on the delivery of drugs via biocompatible nano carriers to a targeted site inside physiology has been one of the most significant areas of research to reduce the side effects in chemotherapy , , . Evidence for the formation of microsized vesicular self-assemblies of the di- and tri-terpenoids 1–6 in suitable aqueous-organic binary liquids prompted us to investigate the entrapment of guest molecules inside the vesicular self-assemblies. The vesicular self-assemblies of crotocembraneic acid 1, were capable of entrapping both cationic fluorophores rhodamine B (Rho-B) and crystal violet (CV) as well as the anionic fluorophore 5,6-carboxyfluorescein (CF) including the anticancer drug doxorubicin inside the vesicles (Fig. 6). Similarly the 6-6-6-6-6 pentacyclic triterpenoids 2–6 are also capable of entrapping fluorophores including the anticancer drug doxorubicin inside the vesicular self-assemblies. Release of the entrapped drug was also demonstrated by fluorescence emission spectroscopy by adding a well-known membrane-disrupting agent Triton X-100 or by changing the pH of the medium by using dilute hydrochloric acid (0.5 N) . In another application, a trihybrid material was generated from arjunolic acid 6, leaf-extract of Chrysophyllum cainito and Pd nanoparticle that acted as a recyclable catalyst for Heck reaction and Suzuki reaction and reduction reaction in aqueous medium .
Flowers, petals and fibrillar networks by spontaneous self-assembly of terpenoids
Hierarchical self-assembly of triterpenoids yielding flowers
Functional terpenoids offer a lipophilic terpenoid backbone for dispersion interactions. The polar functional groups attached with the lipophilic backbone can take part in H-bonding and electrostatic interactions. The dihydroxy triterpenoid betulin 15 isolated from the bark of Betula papyrifera (white Birch) spontaneously self-assembled in organic liquids yielding flowers of nano- to micrometer diameters as characterized by optical microscopy, FESEM, HRTEM and X-ray diffraction studies (Figs. 7 and 8). Detailed investigation revealed that 1D fibers formed by intermolecular H-bonding and dispersion interactions among the betulin molecules formed the 3D flowers via the 2D petals .
Such flowers were also obtained from a C2 symmetric di-hydroxy triterpenoid α-onocerin 16 isolated from Lycopodium clavatum  and the mono-hydroxycarboxy triterpenoid 18β-glycyrrhetinic acid 20 isolated from Glycyrrhiza glabra . Though nano-flowers have been reported from the inorganic oxides such as ZnO, TiO2, Fe2O3, SnO2, flowers of nano- to micrometers diameters are rare from organic compounds , .
Betulinic acid 17 isolated from the bark of Ziziphus jujuba  self-assembled in 22 neat organic liquids studied forming strong gels in 19 liquids. In all the cases, hierarchical self-assembly of molecular components were revealed by systematic investigations using optical, electron and atomic force microscopy. On transformation of betulinic acid 17 to sodium and potassium salts 18 and 19, the solubilities increased in aqueous binary liquid mixtures. Strong gels were obtained from both the salts in aqueous binary liquid mixtures including a hydrogel via the formation of densely packed fibrillar networks . Gel-gold nanoparticle (AuNP) hybrid material was obtained by in-situ generation of AuNPs utilizing the leaves extract of Ziziphus jujuba as the reducing and stabilizing agents.
Adsorption and release of fluorophores including the anticancer drug doxorubicin
The porous microstructure of the self-assemblies of terpenoids provides a large surface for the adsorption of fluorophores. Removal of toxic dyes and other pollutants from contaminated water is highly significant for environmental reasons , , , . Flower-like architectures obtained from hierarchical self-assembly of betulin 15 provide a large surface area which could adsorb fluorophores like rhodamine B (Rho-B) and the anticancer drug doxorubicin. Removal of organic dye molecules such as rhodamine 6G (Rho-6G), crystal violet (CV), methylene blue (MB) and cresol red (CR) was demonstrated by using the dried self-assemblies of 15 from their aqueous solutions. The adsorption of dyes from their respective aqueous solution was monitored by UV-visible spectroscopy and it was observed that the dried self-assemblies obtained from o-xylene (1% w/v) could remove the cationic dyes Rho-6G (78.0%), CV (99.0%) and MB (62.0%) from their respective aqueous solutions  (Fig. 9). Photographs of the dried self-assemblies before adsorption and colored self-assemblies after adsorption of dyes are given in Fig. 9c–f. A gel of α-onocerin 16 in aqueous DMSO loaded with fluorophores like Rho-B, 5,6-carboxyfluorescein (CF) and the anticancer drug doxorubicin when kept in contact with PBS buffers at pH 7.2, the loaded fluorophores including doxorubicin was released slowly (Fig. 9g) as monitored by UV-visible spectrometry .
Conclusions and outlook
Plant metabolites being renewable in nature, it has a highly significant role to play for the development of sustainable society. Terpenoids, the major component of the plant secondary metabolites, being intrinsically renewable, nano-sized and functional, offers innumerable opportunities for their use as renewable molecular functional nanos (MFNs) in science and technology. Research investigations carried out during the last decade have shown that the renewable MFNs having nanometric lengths, lipophilic backbone and several functional groups and chiral centers, spontaneously self-assembled in liquids yielding nano- to micro-sized architectures such as vesicles, tubes, fibers, flowers, fibrillar network of nano- to micrometer dimensions. Formation of vesicular self-assemblies has been observed with one diterpenoid crotocembraneic acid and five triterpenoids oleanolic, ursolic, maslinic, corosolic and arjunolic acids. All the five triterpenoids 2–6 have 6-6-6-6-6 rigid pentacyclic backbones with one to three hydroxyl groups attached at the ‘A’ ring and one carboxy group attached at the ring junction of ‘D’ and ‘E’ rings. The di-hydroxy triterpenoids betulin 15 and α-onocerin 16, both having two OH groups at the extreme ends of the molecules yielded nano- to micro-sized flowers and fibrillar networks in organic and aqueous-organic binary liquid mixtures. Though some structural analogy is present in all the five triterpenoids 2–6 yielding vesicles and the two triterpenoids betulin 15 and α-onocerin 16 yielding flowers and fibrillar networks, the predictability of the morphology by self-assemblies of MFNs is still in its infancy. For example, oleanolic acid 2 and betulinic acid 17 both are pentacyclic mono-hydroxy and mono-carboxy acids with minute change in the triterpenoid skeleton: 2 having 6-6-6-6-6 fused ring system and 17 having 6-6-6-6-5 fused ring system. Oleanolic acid 2 yields vesicular self-assembly whereas betulinic acid 17 yields fibrillar network in liquids. Thus, studies with newer triterpenoids with different functional groups at different positions will provide a better understanding of the structure-property relations. The properly positioned functional groups provide a useful tool for the synthesis of derivatives for the study of their self-assembly properties and application. Utilization of the renewable MFNs derived self-assemblies has been demonstrated for the entrapment and release of fluorophores including the anticancer drug doxorubicin, removal of toxic dyes, generation of hybrid materials, etc. providing opportunities for further applications in targeted drug delivery, in reducing health hazards and in designing recyclable catalysts.
A collection of invited papers based on presentations at the 8th IUPAC International Conference on Green Chemistry (ICGC-8), Bangkok, Thailand, 9–14 September 2018.
We thank SERB (EMR/2017/000069), Indo-Srilanka (DST/INT/SL/P25/2016), DST-FIST, UGC-SAP and Vidyasagar University for financial and infrastructural support. We thank Professor Supawan Tantayanon, Chulalongkorn University, Bangkok for helpful discussion. ACB, SKP, SNH thank UGC and SG thanks CSIR for research fellowships.
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