S.L.S.B.LVI]
CHEMICAL EVOLUTION I N PLANTS
49
CHEMICAL EVOLUTION IN PLANTS
By R. DARNLEYGIBBS
(McGill University.)
(With 3 Text-figures.)
Some thirteen years before the 1858 meeting of The Linnean Society of London a t
which Charles Darwin and Alfred Russel Wallace presented their memorable papers,
John Lindley’s Vegetable Kingdom appeared. I n the preface he tells us that he was
urged :
‘C
. . . t o introduce among the properties of plants an account of their
proximate principles and ultimate constituents. But after a full consideration
of the subject, he has come to the conclusion that it is not expedient to do so.
I n the first place, such. matters belong to Chemistry, and not to Botany ;
secondly, it does not appear possible to connect them with any known principle
of botanical classification ; and, moreover, the extremely unsteady condition
of the opinions of chemists themselves upon the results of their own researches,
would render the introduction of the supposed results of chemists embarrassing
rather than advantageous.”
Lindley then used the apparently sporadic occurrence of one or two constituents
in plants as a further argument against the use of chemistry as an aid to classification.
Nevertheless he was constrained at times to mention the chemical properties of groups
of plants. Thus we find on p. 614 of the third edition of his book (1853) this paragraph
about the Gentianaceae :
“ The Order [family] of Gentianworts is not more remarkable for the diversity
of its colours than it is for the uniformity of the secretions which its various
species exhibit. Bitterness in every part, root, leaves, flowers, fruit, in annuals,
perennials, and shrubs, is so much their characteristic that the following
account of the purposes t o which they are applied is little more than a list of
repetitions ; with this exception, that they in some cases prove narcotic
and emetic.”
Some twenty-eight years after the Darwin-Wallace papers appeared we find a
remarkable woman-Helen C. de S. Abbott-publishing a paper entitled “ Certain
chemical constituents of plants considered in relation to their morphology and
evolution.” I n it she says :
“ The facts obtained from these studies tend to show a chemical progression
in plants, and a mutual dependence between chemical constituents and change
of vegetable form. . . . The evolution of chemical constituents in which
they follow parallel lines with the evolutionary course of plant forms, the one
being intimately connected with the other, and consequently that chemical
constituents are indicative of the height of the scale of progression, and are
essentially appropriate for a basis of botanical classification. I n other words,
that the theory of evolution in plant life is best illustrated by the chemical
constituents of vegetable form.”
I n the following year she writes :
“ The vegetable kingdom does not usually claim our attention for its intellectual
attainments, although its members would certainly seem t o possess greater
chemical skill than a higher race of beings exhibit in laboratories.”
and (in another paper in the same year) :
“ There has been comparatively little study of the chemical principles of plants
from a purely botanical view. It promises to become a new field of research.”
In 1888 Greshoff was assigned to the great botanical garden at Buitenzorg (Bogor)
in Java to institute a chemico-pharmacological investigation of the plants of what
was then the Dutch East Indies. He returned to Holland in 1892 aqd continued his
50
[J.L.s.z. XLIV,
R. DARNLEY GIBBS:
researches there. Later he worked a t Kew and recorded the results of his studies in
a paper which appeared in 1909. Here we read :
“ Since plants are no longer classified according to a single character (i.e.
according to an artificial system), but attempts are made to unite into natural
groups such plants as are considered to be related, the systematic botanist
desires to know that relationship in all its manifestations.”
He defines “‘ Comparative phytochemistry ” as “ the knowledge of the connection
between the natural relationship of plants and their chemical composition.” He notes
that there are whole families of plants of which we know nothing chemically, and goes
on to say that :
“ Strictly speaking one might demand that every accurate description of a
new genus or of a new species should be accompanied by a short ‘chemical
description ’ of the plant.”
It is evident that there was growing up a belief that if plants are related to one
another as the views of Darwin and Wallace would suggest, then their chemistry
should reflect these relationships ; nearly-related plants being more alike in their
chemical make-up than distantly-related ones. It is but a step further to argue
that a “ primitive” plant will be chemically primitive and an “ advanced ” one
chemically advanced. This was assumed to be the case by such men as Baker &
Smith in Australia.
Smith was associated for a while with Maiden and started with him his work on
the Eucalypts. I n 1899 he and Baker came together and worked as a remarkable
team until their retirement in 1921. They published in 1902 “ A research on the
Eucalypts, especially in regard to their essential oils.” I n this they summarized work
on the botany and chemistry of more than 100 species of Eucalyptus L’HBrit. They
concluded that the genus has evolved from Angophora Cav. and that new species
have arisen as it has spread through Australia and Tasmania from the north-west to
the south-east. They were able to arrange the species studied in groups which differ
both morphologically and chemically. The more primitive species have feather-veined
leaves and much pinene in their essential oils ; more advanced ones have intermediate
venation and oils with pinene and cineole ; still more recent species have butterflywing venation and oils with phellandrene, and piperitone or geranyl acetate. We
have reproduced their chart of relationships in modified form (fig. 1).
I
i
I
2
I
I
l
l
,
1
~-7
i
FIG. 1.-Relationships within the genus Eucalyptus. The numbers indicate the groups to which
Baker & Smith assigned the species in 1902. Compare with Table I.
,,
J.L.S.B. LVI]
51
CHEMICAL EVOLUTION I N PLANTS
I n 1920 the second edition of their ‘’ Research ” appeared. This contains information on no less than 176 species of Eucalyptus which are arranged in groups differing
slightly from those of the first edition. We give, in Table I, a summary of the
groupings from the two editions.
TABLE1.-Classification of Eucalypts (Baker & Smith, 1902 and 1920).
1920
1902
Group.
Species
I
1-14
I
Largely pinene.
Little or no cineole.*
No phellandrene.
1-21
15-29
Pinene. < 40y0 cineole.
No phellandrene.
22-46
30-56
Pinene. > 40% cineole.
No phellandrene.
47-70
I1
I
Group.
Species
Composition of oils
IIIa
IIIb
57-62
IIIC
63-64
IV
65-71
I1
IIIa
Pinene less. > 40% cineole.
No phellandrene.
Aromadendral appearing.
IIIb
71-91
Composition of oils
Largely pinene.
Little or no cineole.
No phellandrene.
Pinene. < 40% cineole.
No phellandrene.
No arornadendralt.
Pinene. 40-55y0 cineole.
No phellandene.
Aromadendral rare.
Pinene. > 55% cineole.
No phellandrene.
No aromadendral.
> 40% cineole.
Phellandrene appearing.
Pinene. < 30% cineole.
No phellandrene.
Aromadendral present.
IVn
92-101
IVb
102-106
Pinene less. > 40% cineole
No phellandrene.
Aromadendral appearing.
> 40% cineole.
Phellandrene appearing.
Pinene. < 30% cineole.
Phellandrene present.
V
107-124
Pinene. < 40% cineole.
Usually no phellandrene.
Aromadendral present.
< 30% cineole.
Phellandrene present.
Piperitone$ present.
VI
92-95
125-148
Pinene. < 40% cineole.
Phellandrene present.
96-102
Little or no cineole.
Phellandrene present.
Piperitone present.
l v
72-91
VIIa
Oils not readily placed.
149-155
VIIb
156-166
~
40% cineole.
Phellandrene present.
Piperitone present.
Little or no cineole.
Phellandrene present.
Piperitone present.
~
VIII
167-176
Oils not readily placed.
Little or no cineole.
* Called Eucalyptol in 1902.
t A name used for the mixture of aldehydes (cuminaldehyde, cryptal, etc.).
1 Called ‘‘ Peppermint ketone in 1902.
“
”
”
52
[J.L.s.z.
R. DARNLEY QIBBS:
mrv,
Read (1944) gives an interesting survey of this work. Penfold & Morrison, in the
fourth volume (1950)of Guenther’s treatise on the essential oils, are somewhat critical
of the claims of Baker & Smith, their own researches having revealed more variation in
chemistry than those authors found. We must remember, however, that we have, in
the work of Baker & Smith, a remarkable pioneer effort to study chemical as well as
morphological evolution and to relate the two. There are all too few researches of
this nature even to-day.
What Baker & Smith tried to do for a genus, McNair tried to do for the plant
kingdom, and with less success, as might be expected. Between 1929 and 1945 he
produced a series of papers dealing with plant chemistry and systematics. I n 1935,
for example, he writes on “ Angiosperm phylogeny on a chemical basis ”. Here he
assembles data on molecular weights of alkaloids, on iodine numbers (as measures of
unsaturation of fats), and so on. His criteria are that the most highly evolved alkaloids have the highest molecular weights (i.e. are most complicated ? ) ; that the most
highly evolved fats have the highest iodine numbers (i.e. are most unsaturated) ;
and that the most highly evolved volatile oils have the highest specific gravities and
the lowest refractive indices. A sample table, from which it is concluded that the
family Magnoliaceae is the most primitive of the families being considered, is reproduced here (Table 11).
TABLE11.
Dominant
Alkaloids
(mol. wts.)
Fats
(iodine Nos.)
Tree - shrub
Shrub
Shrub-herb
Herb
-
95.5
78.4
139.1
145.0
Family
I
Magnoliaceae
Lardizabalaceae
Berberidaceae
Ranunculaceae
330
543
Embryos
pi&
Sympet.
~
:a
~
General
contents
Albumen
91
Personal communication, 28 October, 1957.
1
:i
~
1
%a
~
:1
1
J.L.S.B. LVI]
CHEMICAL
53
EVOLUTION IN PLANTS
In the same paper he deals with the occurrence of cyanogenetic glycosides in plants.
He writes that they :
occur more generally in the more advanced of the older groups and
"
In the Archialso in the more advanced families of the different orders
chlamydeae of the dicotyledons cyanogenetic glycosides have not been found
in the first eleven orders (which consist mostly of woody plants). 2 They have
As to the occurbeen found in nearly all of the remaining 19 orders.
rence of cyanogenetic glycosides in the more advanced families of the various
orders the following examples may be considered as indicative. In the Rosales
the substances mentioned are found in the 4. Crassulaceae, 6. Saxifragaceae,
14. Platanaceae, 16. Rosaceae, and 18. Leguminosae. In the Parietales the
containing families are 17. Winteranaceae (Canellaceae), 19. Flacourtiaceae,
and 23. Passifloraceae. In the Myrtiflorae the producing families are: 9.
Lecythidaceae, 14. Myrtaceae, 15. Melastomaceae, 16. Onagraceae, and 17,
Haloragidaceae.''
Now McNair apparently used the arrangement and numbering of Engler's
" Syllabus ", edition 7 (see key at the end of Willis, 1955). The " first eleven orders "
referred to are now regarded as advanced and reduced rather than as primitive.
In Benson (1957), for example, they are numbered 56, 19, 47, 53, 51, 50, 48, 55, 49,
54, and 52; and the HCN-producing orders have a "below average" numerical
placing. As to the occurrence of cyanogenetic glycosides in the Rosales, the position
of the families having these glycosides is only a little "above average" (treating the
order as a linear series of families, as McNair seems to have done). If McNair had
used the ll th edition of Engler's " Syllabus ", which appeared nine years before his
paper, the occurrence would have seemed even nearer to average.
His reference to HCN in the Parietales is of great interest to the writer. Cyanogenetic glycosides occur not only in the families mentioned by McNair-Winteranaceae (Canellaceae), Flacourtiaceae, and Passifloraceae-but also in the Turneraceae.3 Now these families to not constitute families 17, 19, 21, and 23 (using the
numbering of " Syllabus " edition 7) of a linear series, but they are all members of a
suborder Flacourtiineae, as Engler makes clear in edition 2 of Die natiirlichen Pflanzenfamilien (vol. 21, p 5, 1925). They are also exactly the order Violales of Benson
(1957). That is, they are closely related. We have summarized the occurrence in
them of cyanogenetic glycosides in Table IV. It will be seen that we have no informaTABLE IV.-Occurrence of cyanogenetic glycosides in the sub-order Flacourtiineae
of the Parietales.
HCN
Family
Genera /Species
Present
Canellaceae
Violaceae
Flacourtiaceae
Stachyuraceae
Tumeraceae
Malesherbiaceae
Passifloraceae
Achariaceae
5/11
16/850
84/850
1/5--6
7/110
l-2/35
11 /600
3/3-4
1/1
Absent
Doubtful
-
9/17
-
3/11
-
3/31
-
-
5 /20*
9/10t
1/2
2/2
-
-
2/3t
-
1 /It
-
I
* From herbarium material in 1 /5.
"4/4.
t
t
Henry (1906) says they have been reported from Sa1icaceae (order 3).
record of this.
a Gibbs (unpublished data).
2
I have no other
54
R. DARNLEY QIBBS:
[J.L.s.z. XLIV,
tion on 3 of the 8 families involved, and that only a small proportion of the genera
and species of the other families have been investigated : a state of affairs typical of
our knowledge of comparative plant chemistry.
The Violaceae may well be out-of-place here. Copeland (1957) places them in the
Rhoeadeae (Rhoeadales), while Hallier (1912) puts them in the Polygalinae (Polygalales). If the Violaceae do belong in the Flacourtiineae we might argue that they
have lost or are losing the power to synthesize cyanogenetic glycosides. Camp (in
Gundersen, 1950) argues that the family is primitively a woody one, which arose in
South America and gave rise to our herbaceous northern violets. It would be interesting to know if HCN can be found in the most primitive surviving woody members in
South America.
While we may not be able to decide whether the occurrence of HCN in the Parietales is advanced or no, we may well conclude that the occurrence in this order of
ruphides (one of the few directly-visible chemicals) is a primitive character. They are
found in Dilleniaceae (where they are sometimes small and unarranged), in Actinidiaceae (except Sladenia Kurz.), in Marcgraviaceae, and in Theaceae, all members
of Engler’s first suborder-Theineae. The Dilleniaceae are certainly primitive (see
discussion in Gibbs, 1954, pp. 26-28), as are the Actinidiaceae. Sladenia, which
does not contain raphides, should, perhaps, be placed in the Theaceae. The Marcgraviaceae are closely related to the Theaceae, says Engler.
The Theaceae do not for the most part contain raphides. They have been observed
there only in Tetrumerista Miq., Pelliciera Planch. & Triana, and Trematanthera
F. Muell., a11 of which may be removed from the family. The first two have sometimes
been placed in the Marcgraviaceae (where raphides do occur, see above), while Tremutanthera has sometimes been included in the genus Sauruuia Willd. of the Actinidiaceae,
which contains raphides.
These “ primitive ” raphide-forming families of the Parietales have evolved, we
suppose, from woody members of the Ranales (in the Englerian sense). The latter
order (in the 11th syllabus of Engler & Diels) has nineteen families in four suborders.
The first seven families do not, so far as we know, contain raphides. The eighthMenispermaceae-is said by Santos (1031) to have two genera which produce them,
Anamirta Colebr. and Archangelisia Becc. A study of Santos’ drawings, however,
show needle-crystals but not true raphides in the tissues of these plants. The following
six families also seem to lack raphide-forming members. The fifteenth-Myristicaceae
-forms acicular crystals but not true raphides. The sixteenth-Gomortegaceaeforms needle-like crystals. The next family-Monimiaceae-is
said by Metcalfe &
Chalk (1950)to form raphides “ . . . often in special cells in the dignified tissues”.
These would seem to be true rap hide^.^ I n the family Lauraceae, which is placed next,
acicular crystals are found, and Santos (1930) has reported “ raphides ” in two
species of Ginnumomum L. His drawing (PI. 6, fig. 24) of a cell from C. cassiu B1.
certainly shows needle-crystals in more or less parallel bundles, but the cell is hardly a
typical raphide-sac. I n the last family-Hernandiaceaeacicular
crystals, and
perhaps also raphides, are said to occur.
If we consider Hutchinson’s (1926) arrangement of the families mentioned above
we find that, with the exception of the Menispermaceae a t the “ top ” of the RanalesBerberidales “ tree ”, the families which have anything approaching raphides all
lie in his Laurales (fig. 2). Is it from this group that the Dilleniaceae, etc. arose 1
The chemistry of the monocotyledons is not very different from that of the
dicotyledons. This would seem to support the view that one group has arisen from
the other, or that they have a common ancestry. One view is that the monocotyledon.
arose from primitive dicotyledons such as the herbaceous members of the Ranaless
Metcalfe (letter of 17 December, 1957) says “ Raphides were actually observed at Kew in
Doryphora sassajras Endl., Peumus boldus Molina and Laurelia novae-zeylandiae A. Cunn. Judging
from Solereder’s remarks, however, raphides appear to occur generally in the MonimiaGeae”.
J.L.S.B.
LVI]
r 23.
Menisperniaceae?
22. Sargentodoxaceae-
BERBERIDALES
f
55
CHEMIOAL EVOLUTION IN PLANTS
14. Myristicaceae?
13. Hernandiaceae?
Gomortegaceae?
11. Lauraceae?
10. Monimiaceaef
4I
21. Lardizabalaceae20. Circaesteraceae119. Berberidaceae-
(Winter)
9. Eupomatiaceae8. Annonaceae4
. 7. Cercidiphyllaceae-
RANALES
6. Trochodendraceae5. Lactoridaceae4. Himantandracea+3. Schismdraceae2. Winteraceae1. Magnoliaceae-
18. Nymphaeaceae17. Ceratophyllaceae-
Common
ancestor?
I
FIG.2.-Essentially the families of the Ranales of Engler & Diels as arranged by Hutchinson.
Families which seem to be without acicular crystals and ‘‘ raphides ” are marked (-) ;
those with acicular crystals and/or “ raphides ” are marked ( ? ) ; those known to have
true raphides are marked (+).
Now we have seen above that these do not have raphides : and neither do the primitive
monocotyledons. Kimura (1956)has published one of the most recent “ arrangements ”
of the whole group of monocotyledons. He would have the Alismatales (1) arising
from proto-Polycarpicae (proto-Ranales) and giving rise to Hydrocharitales ( 2 ) and
Scheuchzeriales (3). From the proto-Scheuchzeriales he would derive Triuridales
(6) and Potamogetonales (4), and from the proto-Potamogetonales he would derive
the Najadales (5). Now raphides seem t o be absent from all these groups, though our
knowledge of them is far from complete. They do occur, however, in the Liliales
(7) and in many other orders of the monocotyledons. If Kimura’s arrangement
(fig. 3) is correct then raphides arose independently in the monocotyledons after they
FIQ. 3.-Kimura’s arrangement of the orders of Monocotyledons. Orders knpwn to contain
raphide-producing species are marked (+) ; those believed to lack them (-).
56
R. DARNLEY QIBBS:
[J.L.s.z. XLIV,
had diverged from the dicotyledons-an example of parallel evolution. They arose
only once in this group, it would seem, and dropped out in a t least one branch (Kimura’s
Sicciflorae fig. 3, E 13-17). I n the dicotyledons they must have arisen several times,
for they occur not only in the families mentioned above, but in several other groups.
They are found, for example, in Creyia Hook. & Harv. of the Melianthaceae (or
Greyiaceae), the only occurrence in the family, and in the Balsaminaceae (Impatiens
Riv. ex L. and Bydrocera Bl.). Both of these families are placed in the Sapindales,
where raphides seem otherwise to be absent. They do not occur in Trapa L., but are
present in the Oenotheraceae (see Gibbs, 1954, pp. 4-5 and 17) ; in several families of
the Centrospermae ; and in the subfamily Rubioideae of the Rubiaceae (Bremecamp,
1952).
It would not be just to leave this discussion of the occurrence of raphides in the
flowering plants without a tribute to the pioneer work of Gulliver, who published, in
1866, a paper “ On raphides as natural elements in the British flora ”. In this paper
he records their distribution in considerable detail, and says that it may be of use in
taxonomy. Further, and importantly, he stresses the constancy as a character of
these crystals :
“ I n short, I know of no means by which a raphidean plant can be grown in
health, if a t all, so as to extinguish this character, nor by which a plant regularly
devoid of raphides can be made to produce them.”
I n this article I have tried to show some of the biochemical lines along which our
taxonomic thinking has developed in the hundred years that have passed since
Darwin and Wallace electrified the scientists (and others) of the nineteenth century.
Organic evolution, and with it biochemical evolution, are now generally accepted as
facts, but we know all too little of the biochemical facts. At least one book (Florkin,
1949) has appeared with the title Biochemical Evolution. Its translator (Morgulis)
points out that “ It is, of course, unfortunate that the factual material is drawn
entirely from the animal kingdom ”. We may consider it unfortunate that this was
not indicated in its title !
The development of modern methods-such as those of chromatography-make
it ever easier to investigate the chemistry of living organisms. We may be confident
that the coming century will see the publication of books on the biochemical evolution of
plants that will be based upon incomparably better evidence than is available to us
in 1958.
DE S.
1886. Certain chemical constituents of plants considered in relation
to their morphology and evolution. Bot. ffaz., 11, 270.
- 1887a. Comparative chemistry of higher and lower plants. Amer. Nut., 21, 719, 800.
- 1887b. The chemical basis of plant forms. J. Franklin Inst., 124, 161.
BAKER,R. T. & SMITH, H. G. 1902 and 1920. A research on the Eucalypts, especially in regard
to their essential oils. Ed. 1 and 2. Sydney.
BENSON,
L. 1957. Plant classi$cation. Boston.
BREMECAMP,
C. E. B. 1952. The African species of Oldenlandia L. sensu Hiern e t K. Schumann.
Verh. Akad. Wet. Amst. (Nut.), 48, 1.
COPELAND,
H. F. 1957. Forecast of a system of the dicotyledons. MadroAo, 14, 1.
ENQLER,A. 1925. I n Engler & Prantl’s Die Natiirlichen Pjlanzenfamilien, Ed. 2, v. 21, 1.
-& DIELS,L. 1936. Syllabus der PjZanzenfantilien. Ed. 11. Berlin.
FLORKIN,
M. 1949. Biochemical Evolution. Ed., trans1 and augmented by S. Morgulis. New
York.
GIBBS, R. DARNLEY. 1954. Comparative chemistry and phylogeny of flowering plants. Trans.
Roy. Soc. Canada (3), Sect. V, 48, 1.
GRESHOFF,
M. 1909. Phytochemical investigations at Kew. Kew Bull., p. 397.
GUZNTHER,
E. 1950. The essential oils, 4, 437. New York.
GULLIVER,
G. 1866. On raphides as natural characters in the British flora. Quart. J . MZ’cr.Sci..
(N.S.), 6, 1.
GUNDERSEN,
A. 1950. Families of dicotyledons. Waltham, Mass.
ABBOTT,HELENC.
.
.
J.L.S.B. LVI]
CHEMICAL EVOLUTION
IN PLANTS
57
1912. L’Origine e t le systeme phylhtique des angiospermes exposes zt l’aide de
leur arbre g8nhalogique. Arch. nkerl. Sci., Nat. (3B), 1, 146.
HENRY,T. A. 1906. On the occurrence of prussic acid and its derivatives in plants. Sci.
Progr., 1, 39.
HUTCHINSON,
J. 1926. The families of flowering plants, 1. London.
KIMURA,
Y. 1956. SystPme et phyIog8nie des Monocotyledones. Mus. Nut. Hist. Nut. Notul.
Syst., 15, 137.
LINDLEY,J. 1846, 1853. The Vegetable Kingdom. Ed. 1, Ed. 3. London.
MCNAIR,
J. B. 1935. Angiosperm phylogeny on a chemical basis. Bull. Torrey bot. Cl., 62, 515.
- 1945. Some comparisons of chemical ontogeny with chemical phylogeny in vascular
plants. Lloydia, 8, 145.
METCALFE,C. R. & CHALK,L. 1950. Anatomy of the Dicotyledons. 2 vols. Oxford.
READ,J. 1944. Chemistry of the Australian bush. Endeavour, 3, 47.
SANTOS,J. K. 1930. Leaf and bark structure of some cinnamon trees, with special reference to
the Philippine species. Philipp. J. Sci., 43, 305.
- 1931. Anomalous stem structure in Archangelisia jZava and Anamirta cocculus from the
Philippines. Ibid., 44, 385.
WILLIS,J. C. 1955. A dictionary of the flowering plants and ferns. Ed. 6. Cambridge.
HALLIER,H.
.
.