Part 4:

Thesis conclusions and appendices

‘If you want to know the end, look at the beginning’

African Proverb

‘The rule which forbids ending a sentence with a preposition is the kind of

nonsense up with which I will not put’

Sir Winston Churchill

‘If your knees aren’t green by the end of the day, you ought to seriously re-

examine your life’

Bill Watterson

‘The will to overcome a passion is in the end merely the will of another or

several other passions’

Friedrich Nietzsche

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Chapter 15 –

Conclusion

Thesis Page 236

15.1.0 Summary

15.1.1 Part 1 – Eremophila longifolia: ethnopharmacology, essential oil

chemotypes and cytogeography

With regard to the identification and delineation of essential oil chemotypes of

Eremophila longifolia, it is now clear that the first such chemotype identified in 1971

by Della and Jefferies, with an essential oil made up predominantly of the potentially

hepatotoxic carcinogenic phenyopropanoids safrole and methyl eugenol, is confined

to a small geographic region in Australia’s far west, in central-west Western

Australia. This is important since although E. longifolia has a widespread distribution

throughout the Australian landmass perceptions still prevail that this single chemotype

reflects the constituents of all individuals of the species. This is simply not true.

Further clarification reveals that this chemotype is an unusual biotype with diploid

cytology.

In all, a total of three diploid populations were identified in Australia, the other two

being geographically clustered in western New South Wales and producing terpenoid

based essential oils via the mevalonate pathway. These ketone rich chemotypes, as is

the case for the phenylpropanoid type, produce significantly high yields of essential

oils, making them potentially suitable for commercial development. The first of these

types is the isomenthone/menthone type (CT.A), which produces an essential oil yield

at an impressive range of 3-8% g/g wet weight of leaves. The second is the

karahanaenone type (CT.B), yielding at a range of 1-5% for diploid specimens, or 0.3-

0.7% for tetraploid specimens. Both these high yielding diploid types are good

candidates as cultivars for commercial plantations. Should such plantations be

established and developed this would make a significant contribution to Australia’s

essential oil industry. Essential oils and or/extracts from the high yielding CT.A

isomenthone/menthone type could be used to make ointments and lotions suitable for

topical, antifungal, aromatherapeutic and cosmeceutical/aesthetic applications (Table

1). At present it is unclear how CT.B could be utilised, but karahanaenone is already

in demand as a feedstock in the flavour and fragrance industry and may also be useful

as a chemical scaffold for further drug development.

In addition to the five essential oil chemotypes of E. longifolia identified prior to the

current study, four new types have now been characterised. One of these new

essential oils, with dominant components of bornyl- and fenchyl-acetate, is similar in

composition to the antimicrobial essential oil produced from Eremophila

bignoniiflora. Traditional ethnomedicinal use of E. bignoniiflora by Australian

Aboriginal people involved applications consistent with antispasmodic activity and

headache therapy. Because essential oils rich in esters are often associated with

antispasmodic and nervous calming activity, the essential oils from E. bignoniiflora

may have contributed to this effect. The same essential oil produced from the new

chemotype of E. longifolia, in significantly higher yields, could be marketed for

treatment of headaches, nervous tension or gastrointestinal disorders (Table 1).

Interestingly, another of the newly characterised chemotypes of E. longifolia produces

an essential oil comprised predominantly of fenchone and camphor (2-bornanone),

which are analogues of the previous mentioned fenchyl- and bornyl acetate

respectively, after removal of the acetate groups. In the case of fenchone and

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camphor, a ketone is in the place of the ester; however, in the case of the other known

chemotype, dominated by fenchol and borneol, an alcohol functional group is in the

place of the ester. Clearly, the oils produced by these three chemotypes are of very

similar biosynthetic provenance.

The essential oils dominated by the alcohols, fenchol and borneol, demonstrated high

antimicrobial activity against the yeast C. albicans, bacterial species, such as

Staphylococcus aureus, S. epidermidis, and the human pathogenic fungal species

Trichophyton rubrum, T. mentagrophytes and T. interdigitalis. Similar activity was

demonstrated by the fenchyl- and bornyl acetate oils against C. albicans and S.

epidermidis. The fenchone rich essential oil is yet to be tested for antimicrobial

activity.

The third new essential oil chemotype of E. longifolia is rich in α-pinene, sabinene,

limonene and α-terpinolene. At first this essential oil appeared to be consistent with

an earlier type reported in individual E. longifolia from Alice Springs, in the Northern

Territory. However, it’s unusually high concentration of α-terpinolene, makes this

new essential oil unique. The fourth new chemotype is dominated by p-cymen-8-ol,

along with a host of other unidentified compounds.

Currently then, at least nine chemotypes of E. longifolia have been characterised but

preliminary results suggest that others wait to be confirmed. All essential oil

chemotypes occurring outside the small regions of the safrole/methyl eugenol diploid

type, the isomenthone/menthone diploid type and the karahanaenone diploid type

show tetraploid cytology. The karahanaenone and isomenthone/menthone types also

exist as tetraploid forms but produce relatively low essential oil yields by comparison

with the diploid varieties. Such tetraploid types appear as randomly emerging

individuals in isolated patches throughout the range of E. longifolia, probably

emerging as a result of sexual reproduction and assortment of recessive allelic traits

related to biosynthesis.

Consideration within the context of proposals to cultivate commercial scale crops of

E. longifolia species, quality control of plantations of tetraploid chemotypes may

involve the elimination of karahanaenone and isomenthone/menthone chemotypes

emerging in plantations from sexual reproduction. However, in any case, this is not

expected to occur with any great frequency since this species has a preference for

reproduction by root suckers.

With regard to the emergence of unintended chemotypes in populations of known

chemotypes, one may consider the emergence of the safrole/methyl eugenol type a

potential risk in a commercial scale plantation, particularly since safrole and methyl

eugenol have been red flagged as potential hepatotoxic carcinogens. Our research

indicates that the risk of this occurring is vanishingly small. Thus far the

safrole/methyl eugenol type has not been demonstrated to occur in tetraploid form.

However, even if this did occur, the parent chemotype would produce essential oils

via the shikimic acid pathway, because emergent chemotypes may not contradict the

biosynthetic origins of the parent chemotype.

With regard to the role of volatiles in the medicinal efficacy of smoke or steam

fumigation rituals, using E. longifolia, both partially pyrolysed essential oils and the

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more hydrophilic component ‘genifuranal’ are involved. Most of the essential oil

components are present in the leaf tissue before heating, but are accompanied with

other derived artefacts in the steamy smoke that is produced when the leaves are

placed on hot embers for use in medicinal applications consistent with antibacterial or

antifungal applications, as well as lactagogue activity. The smoking procedure was

also used to prepare surgical tools, no doubt for sterilization but conceptualised as a

type of exorcism ritual. The essential oils and artefacts were also accompanied by

pyrolysed derivatives including radical essential oil fragments and other phenolic or

benzoid constituents; together producing significantly enhanced antimicrobial

activity, as demonstrated in our microtitre plate broth dilution assays.

‘Genifuranal’ itself exhibited significant antimicrobial activities, with mean inhibitory

concentrations as low as 100 μg/ml against some species. As we were not able to

detect this compound in the leaves of E. longifolia without heating it into a gaseous

state, we hypothesise that ‘genifuranal’ is the product of heat induced cleavage of a

glycosidic bond. The proposed glycoside is geniposidic acid, already demonstrated to

occur in the leaves of E. longifolia in previous studies, and demonstrated to exhibit

cardioactivity.

In traditional fumigation rituals, ‘genifuranal’ and partially pyrolysed essential oils

are delivered in warm air to the patient. Although the transdermal absorption of

components such as ‘genifuranal’ are expected to produce significant biological

activity, the first application with warm air is itself expected to have enhanced

activity, relative to cooler applications. In this regard, antimicrobial assays produced

in vitro have limited capability of capturing this enhanced activity from warm air

delivery. Thus, antimicrobial activities produced in smoke fumigation rituals are

expected to be higher than those demonstrated in the laboratory.

15.1.2 Part 2 – Ethnopharmacology of medicinal plants used traditionally by

Aboriginal Australians

The medicinal potential of the essential oil of E. bignoniiflora has already been

summarised above. In other studies a dichloromethane extract of the leaves of this

plant demonstrated calcium channel blockage that may be consistent with a number of

traditional medicinal uses. Because the calcium channel subtype was not clarified in

this earlier study, the results have implications for both therapeutic activity related to

headaches and spasmolysis of the intestine. Because activity was expected to vary

from leaves to the fruits, identification of the principal active component may be

achieved by seeking to characterise components present in both the leaves and the

fruits, but more concentrated in the fruits. Although the essential oils could have been

involved in this activity, other important components may also be identified.

Although essential oils from the fruit of Pittosporum undulatum have already been

partly characterised in an earlier study completed in 1905, our recent characterisations

enhanced and extended this earlier study. In our study we were able to tentatively

identify the optically inactive compound referred to in the earlier study, conducted

over a hundred years ago. We believe this was bicyclogermacrene.

Unlike P. undulatum, Pittosporum angustifolium was involved in a significant

number of traditional medicinal applications. The most common of these to be

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recorded in the literature are related to the treatment of coughs and colds, for

lactagogue activity and in the treatment of eczema. More recently, a number of

anecdotal reports have surfaced related to ia cancer inhibition, autoimmune conditions

in the intestines, antimicrobial activity. Previous studies have supported potentially

anticancer activity, as well as possible antiviral activity, particularly the Ross River

Fever virus.

Our study examined the chemical character of volatiles from P. angustifolium,

demonstrating a degree of variation. Compounds with structural similarities to

previously described chemosemiotic compounds identified in mother-infant

communications, were also noted, including acetic acid decyl ester or 1-dodecanol.

Accordingly, we hypothesise that these compounds are involved in the traditional

application as a lactagogue, particularly because the modality of usage involved

heating a compress of leaves to produce such volatiles, which were then used to

fumigate the breasts of the nursing woman.

In our studies most of the essential oils from Geijera parviflora and G. salicifolia

were chemically consistent with previous identified chemotypes; however some

variation was noted and new potential chemotypes were identified. One of these, from

a specimen of G. parviflora (NS374), exhibited an oil comprised of a larger

abundance of bicyclogermacrene and trans-caryophyllene (and unknown B), which

may be the first known sesquiterpene dominated essential oil from Geijera species.

Following hydrodistillation performed on this specimen a dichloromethane partition

of the hydrosol produced a residue that was rich in pyranocoumarin xanthyletine,

furanocoumarin isopsoralen and methoxy coumarin osthole. This hydrosol partition

has not been attempted using other chemotypes.

Here we also present for the first time studies on antimicrobial and free radical

scavenging activity of essential oils from Geijera species. The most active of these

oils is the green oil from G. parviflora, made up predominantly of

pregeijerene/geijerene and linalool. Previous studies on these components indicate

that this green essential oil may have applications as an insect repellent (particularly

mosquitoes) as well as a topical analgaesic agent.

Smoke condensates from G. parviflora (chemotype 3) indicated the possible

occurrence of an alkaloid in the qualitative pharmacological test. This requires further

analysis for confirmation. However, the occurrence of alkaloids in the smoke

condensate may have significance with regard to reported psychoactivity achieved in

smoking the plant. Another possibly fruitful line of investigation would be to examine

the pharmacological and chemical character of coumarins in these smoke condensates

in the context of possible psychoactivity.

In further experiments aimed at simulating traditional use, smoke condensates were

also produced from Callitris endlicheri and C. glaucophylla and these were shown to

contain γ-lactones ferruginol and pisiferal/pisiferol, along with a host of other

phenolic compounds, with high levels of antimicrobial activity.

15.1.3 Part 3 – Phytochemical and chemotaxonomic investigations

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Phytochemical investigations of Zieria species presented in this thesis corroborated

previously published data on representatives of this genus. We have expanded the

available information on this genus by, for the first time, detailing the chemical

character of essential oils from the two species, Z. odorifera subsp. williamsii and Z.

floydii. Considered within the context of the chemotaxonomic approach undertaken in

earlier studies, the remarks of the discoverer of the species, A. G. Floyd, now seem

somewhat prescient. ‘This is a quite oddity! This specimen does not match any known

Zieria taxon. It appears to be allied to 3 closely related species; Z. furfuracea, Z.

granulata and Z. smithii’. The former two species mentioned there, being Z.

furfuracea and Z. granulata, produce an essential oil rich in car-3-en-2-one. The

essential oil from Z. floydii was also dominated by this component.

Although essential oils from Zieria spp. have been previously examined for

antimicrobial activity, here we tested the essential oils against a broader range of

organisms and also compared the activity of essential oils with solvent extracts from

the same species. We found high antimicrobial activity in both solvent extracts and

essential oils. We conclude that a putative essential oil industry based on species of

Zieria would provide a novel range of essential oils, attractive to the aromatherapy

community, as well as providing purified compounds useful as scaffolds in

pharmaceutical development.

In a further chemotaxanomic approach we have for the first time addressed existing

taxanomic concerns regarding the Phebalium squamulosum heterogenous species

aggregate. The first species examined was P. squamulosum subsp. verrucosum, which

was regarded by our esteemed collaborator, Ian Telford, of the Beadle Herbarium at

the University of New England, as having greater morphological alliance with the

Phebalium glandulosum complex. Essential oils of this species were dominated by

dihydrotagetone at concentrations ranging from 95-98%. An identical essential oil,

with the same yield g/g wet weight of leaves, was produced in an earlier study from P.

glandulosum subsp. macrocalyx. In another study this was also demonstrated to be the

case with P. glandulosum subsp. glandulosum. Here we have characterised an almost

identical essential oil from P. glandulosum subsp. nitudum and P. squamulsoum

subsp. eglandulosum. We have therefore concluded that dihydrotagetone dominated

essential oils are a general characteristic of the P. glandulosum subspecies complex.

In a subsequent study other members of the P. squamulosum heterogenous species

aggregate were phytochemically investigated. We demonstrated that all apparent

subspecies currently assigned to this assemblage have separate individual essential oil

chemotypes. Interestingly, several separate chemotypes were demonstrated from

specimens currently assigned to P. squamulosum subsp. squamulosum. In this regard,

a notable chemical characteristic of oils from southern specimens (collected near

Sydney and in the Hunter Valley) was the almost total predominance of a tricyclic

sesquiterpene ketone; squamulosone. By contrast, northern specimens were

characterised by essential oils rich in elemol/hedycaryol.

Our final study aimed at identifying a range of essential oil types from select

Prostanthera species, has made a significant contribution to resolution of taxonomic

problems in this genus. This study particularly emphasised issues surrounding

taxonomy of P. rotundifolia, P. lasinathos and P. ovalifolia, and clearly demonstrated

Thesis Page 241

the need for subsequent comprehensive chemotaxonomic studies, complementing a

morphological and phylogenetic analysis, to delineate new species.

Significant numbers of morphological subtypes are known to occur in the three

species mentioned above, paralleling the existence of discrete essential oil

chemotypes. Despite such variation essential oils from these Prostanthera species

(series racemosae) were almost always characterised by a major representation of 1,8-

cineole. However the differentiating factor is the existence and relative abundances of

tricyclic sesquiterpene alcohols, such as globulol, ledol, prostantherol and maaliol,

which are characterised by a cyclopropane moiety, attached to either a decahydro-

napthalene or –azulene structure. Again, further significant differentiating

components of some essential oils were the tricyclic sesquiterpenes, but with

heterocycle substituents in place of the cyclopropane moiety. Examples include cis-

dihydroagarofuran or kessane, also on a decahydro-napthalene or –azulene structure

respectively.

As with other genera, Prostanthera essential oils were considered within the context

of possible pharmacological activities. Here we demonstrate that oils dominated by

the sesquiterpene alcohols provided the greatest antimicrobial activity against a range

of organisms, most pronounced against some Gram-positive species. Individual

components found in significant amounts in the essential oils were related to this

enhanced antimicrobial activity, particularly prostantherol. Maaliol was also found in

significant amounts in one specimen currently assigned to P. ovalifolia. This is of

considerable potential pharmacological interest, given the importance of maaliol in

the antinociceptive activity of a widely used Indian medicinal plant species

(Valeriana wallichii). This antinociceptive activity is therefore expected to be also

produced by oils from maaliol rich species of Prostanthera. Again, Prostanthera

essential oils have a great potential as novel additions to Australia’s aromatherapy

and/or natural product industry.

Table 1 - Possible commercial scale applications from essential oil yielding flora in Australia

Species Chemotype Use

Geijera parviflora geijerene/pregeijerene (and germacrene D)

Commercial plantation: Insect repellent, topical analgaesia (linalool content)

Geijera parviflora Osthole, isopsoralen, xanthyletine

Commercial plantations:

Zieria floydii car-3-en-2-one Commercial plantations: Chemical scaffold for further drug development and antimicrobial activities

Prostanthera ovalifolia maaliol Commercial plantations: Medicinal applications consistent with the Indian Valeriana willichii

Prostanthera rotundifolia

prostantherol Commercial plantations: Antimicrobial activities

Eremophila longifolia isomenthone/menthone Commercial plantation: topical, gastrointestinal for antimicrobial activities, topical for muscle aches and pains, active in applications for treatment of thrush (Candida)

Eremophila longifolia fenchyl-/bornyl acetate; Commerical plantations: possible activity in gastrointestinal disease, possible activity in aromatherapy for headache sufferers

Callitris glaucophylla NA

1) Bioactive γ-lactones; ferruginol, pisiferal, pisiferol. 2) Occurrence of hydrophilic antibiotic highly active against S. aureus and B. subtilis - requires purification and structure elucidation. Medicinal applications consistent with the Japanese species Chamaecyparis pisifera

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15.2.0 Suggested areas for further research

The demonstration of multiple chemotypes in E. longifolia emphasises the chemical

variability expressed by this species, which may be an intrinsic general character of

this genus. Thus, it is quite probable that other species from Eremophila may

demonstrate this geographical chemical variability. The observed correlation of

diploidy with higher abundances of secondary metabolites may have more general

implications. Therefore it would be worthwhile examining other species for both

chemogeography and karyotype. Perhaps this search should start in E. deserti, as this

has already been shown to possess an abundance of essential oil chemotypes with

high yields of essential oil. Another species, E. glabra, produces no essential oil at all;

however NSW specimens are either hexaploid or tetraploid, but a diploid biotype can

be found in far western WA. It may be worthwhile seeing if this diploid specimen

yields any amount of essential oil. This may be a fruitful area of investigation for all

Eremophila and its allied genus, Myoporum.

With regard to further investigation of species of Eremophila for derivatives produced

in smoke fumigation rituals, no other species was as frequently used for this purpose

as was E. longifolia, meaning that it may be less likely that volatile therapeutic

compounds could be found in other species of Eremophila. Although in Chapter 4 a

handful of other species were examined for the derivative genifuranal, thus far it has

only been produced from E. longifolia.

Other species of Eremophila were in fact used, albeit less frequently in smoke

fumigation rituals, meaning that it may be worthwhile to examine for unknown smoke

artefacts in addition to genifuranal. Other species involved in smoke fumigation

treatments were E. bignoniiflora, E. sturtii, E. mitchellii, E. dalyana, E. freelingi, and

E. duttonii.

Derivatives or larger molecular mass compounds produced/evaporated during smoke

fumigation methodology may alternatively be produced from hydrodistillation.

However, due to the less destructive nature of conventional hydrodistillation such

derivatives or larger molecules could possibly be distilled in higher abundance at

shorter time-intervals if higher temperatures and pressures are employed. In this

regard a modified pressure cooker, with a 15psi pressure release valve positioned for

horizontal airflow into an adjacent condenser, could be used to achieve this end.

At various stages throughout this thesis examination of solvent extracts demonstrated

some degree of antimicrobial activity. This was not observed using E. longifolia or E.

bignoniiflora, but Callitris glaucophylla and C. endlicheri did appear to contain a

polar component with significant discriminating bactericidal activity against two

Gram-positive organisms (Staphylococcus aureus and Bacillus subtilis). It would be

interesting to know what this component is and if it could be used to treat antibiotic

resistant infections, such as VRE or MRSA. In addition, other species of Eremophila

should be examined, particularly the highly aromatic and highly regarded E. dalyana.

Because of the intrinsic chemovariability of other species, another species worthy of

further examination is E. alternifolia, regarded as ‘highly potent’ in some places but

not others.

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An interesting and unexpected outcome of this thesis is the ‘resurrection’ of

chemotaxonomy, which was utilised by botanists in the 70’s and 80’s before

molecular fingerprinting became possible and quickly grew in popularity. Of course it

is not expected that chemotaxonomy could outperform molecular fingerprinting and

phylogenetics in species delimitation, however it certainly has proven to effectively

complement this method. Subsequently to this thesis the phylogenetic approach has

been employed for results with a quick turnaround, to resolve simple questions such

as ‘is this species the same as the one we collected previously’? Already, our

collaborative botanists have been forced to examine voucher specimens in closer

detail because the chemotaxonomic approach has compelled them to do so.

In this regard, the question still begs an answer ‘how do you define a species’?

Chemotaxonomy is challenged by the divide between ‘new species’ and ‘new

chemotype of the one species’. To complicate the matter further, in Part 1 of this

thesis we demonstrated that a correlation could be made between genetics (karyotype)

and chemotype, whilst the classical view is that chemotypes result from differences in

soil climate. In the former, seedlings from one chemotype could be transplanted into

different soil types and different climates without any serious variation to the

chemical character of its essential oil. In the latter more classical view, most certainly

there would be a difference.

The view that chemotype derives from soil type is borrowed from Europe and Great

Britain, where cultivar selection over thousands of years has caused a kind of genetic

uniformity across many species used in cultivation. However, because this cultivar

selection was not a practice employed by Australian Aboriginal people it is more

likely that unique soil types and various climates favour certain biotypes – meaning

the plant itself is different and better suited to that environment.

Over long stretches of time, geographically isolated chemotypes may diverge into

new species, but again, the challenge lies in deciding exactly what amount of

divergence warrants delimitation of a new species. Because of the inherent ambiguity

in answering such a question, the best resolution for now is that consistent

morphological differences should stand alone in defining a new species, but

chemotaxonomy and phylogenetics may be utilised to demonstrate that such

morphological variability is not merely a consequence of naturally occurring

variability within the one species.

Thesis Page 244

Appendix A –

Consolidated list of references

Thesis Page 245

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