Phytochemical aspects angiosperm origin and evolution Comparative studies the growing ...

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Acta801. Neerl.33(4),November 1984,p.457-468,
Phytochemical aspects of
angiosperm origin and evolution
K.Kubitzki1andO.R.Gottlieb2
1InstitutfurAllgemeineBotanik undBotanischerGarten,UniversitatHamburg,2000Hamburg52,
F.R.Germany
2InstitutedeQuimica, Universidadede SaoPaulo,05508 SaoPaulo,Brasil
SUMMARY
Itishypothesizedthatthesuccessful originalevolution andsubsequentradiation oftheangiosperms
wasfacilitated,amongotherfactors,by theirextraordinary chemical versatilityascomparedwith
previouslyexistingplantgroups.Thisbroadchemical spectrumwasbroughtabout bytwo factors,
(1)theclimaxin theexpansionoftheshikimate pathway,alreadyreached atthelevelofthegymno-
sperms; (2)areduction-oxidation potential much higherthatthat ofpteridophytes and gymno-
sperms.Together,thesetraitsprovidedtheangiospermswithamuchbroadercapacityformicromole-
cularvariation then waspresentinearlierplantgroups.Co-evolution withherbivores andpathogens
(apartfrompollinatorsand seed dispersers),and consequentlythepressure toproducenoveland
lesseasilydetoxifiedsubstances,arecommonlyadduced asthecausativefactorsinthephytochemi-
caldiversification oftheangiospermsatthelevel ofpopulations,species andgenera.Hereweapply
thishypothesistothehigherlevelsofthetaxonomic hierarchy.The sequence ofprimaryprecursors
ofthe shikimate pathway for the synthesis ofsecondarymetabolites which follows aretrograde
biosyntheticsequence, andthegradualreplacementofshikimate derivedmetabolitesbymevalonate-
acetate derived compoundsis interpreted asresultingfromnatural selection;itexemplifiesacase
ofcanalized evolution. Possible relationshipsbetween oxidation level and easeofdetoxification
ofsecondarymetaboliteswith theaid ofthe animals’ mixed functionoxidases arediscussedin an
evolutionarycontext.Itisconcluded thatthechemical potentialoftheangiospermspavedtheway
for intense evolutionaryinteractions between plants and animals, interactions which must have
been conducive in augmentingthe diversityofangiospermand animal species since Cretaceous
times.
1. INTRODUCTION
Ever since the timeofDarwin the questfor the originand early differentiation
ofthe angiosperms hasattracted theinterestofbotanists.Comparative studies
ofcontemporaneousseedplants, aswellas thegrowing knowledge ofearly an-
giosperms inthe fossilstate,have brought uscontinually nearer to the solution
ofthe“abominablemystery”. Atpresentitappearsthatearly angiosperms were
moresuccessful than their putative gymnospermousforebears by virtue of a
numberofstructural andfunctionalinnovations.Vegetative structures such as
the improved conductive tissuesofthexylem and phloem, reproductive struc-
tures andsystems (Stebbins 1974), mainly theelaborationofbisexual, animal
pollinatedfunctionalreproductive units(Meeuse 1978, 1979),theirabbreviated
458 K,KUBITZKIANDO.R.GOTTLIEB
lifecycles (Takhtajan 1976), theiroccupation of specialized habitats(Retal-
lack & Dilcher 1981),and theelaborationofaluxurioussecondary metabo-
lism(Ehrlich & Raven(1965)havebeenadducedtothisend.
Although thereis little doubtthat theinitialupswing ofthe angiosperms was
not due to a single characteristic but rather to the advantageous combination
of differenttraits, it is instructive to analyse the differentcomponentsof the
adaptive syndrome ofearly angiosperms. In aprevious publication (Kubitzki
& Gottlieb 1984) we hypothesized thatthe successful original radiationofan-
giospermswasfacilitated, amongotherfactors, through theclimaxintheexpan-
sionoftheshikimate pathway, that hadbeenattainedby theirgymnospermous
forebears. This, and a wider oxidation/reduction potential, provided angio-
spermswithabroadercapacity formicromolecularvariationthan was present
inthegymnosperms.Thepresentpaperis anattempttoanalyse theevolutionary
mechanismunderlyingthisparticularmodeofmicromolecularvariation.
2. EXTENSION AND ABBREVIATION OF THE SHIKIMATE PATHWAY IN
GREEN LAND PLANTS
Theshikimate pathway for the synthesis ofaromaticaminoacids is ubiquitous
in microorganisms, fungi andplants. Herewe dealwith the shikimatepathway
leading to primary precursors ofsecondary metabolites.Itis only in greenland
plants that a post-tyrosine chemistry, based on cinnamicacid, appears really
important (Luckner 1972). Deaminationofaromaticaminoacids takes place
infungi (Turner&Aldridge1983)andmayoccur sporadically inothergroups
oflower plants. However, in bryophytes the special relevance thatcinnamoyl
unitsacquired is duetotheiractivationbycoenzymeA.Polyketides, compounds
formedbythecondensationofacetyl-CoA for chaininitiationand(via malonyl-
CoA)extension, dominatethe secondary chemistry ofbacteria, fungi and algae
(Luckner 1972).Inthisprocessthesubstitutionofthestarter unitbycinnamoyl-
CoAinbryophytes led to flavonolsand flavones.Flavonoidsabsorb UV-light
andseemto actas photoscreens (MacClure 1975),forming anessentialprereq-
uisitefortheconquestoftheterrestrial partofthebiosphere by plants.
Inadditionto condensations, reductionsare also activatedby the thiolester
functionofcinnamoyl-CoA. Theresultingcinnamyl alcoholspolymerize oxida-
tively into lignins which stabilize the cellulose cell wall of pteridophytes and
seedplants, anotherconditionfortheexistenceoflandplants. Ingymnosperms,
furtherelaborationofcinnamyl alcoholsled to theiroxidative dimerizationto
lignans andreductiontoallyl-andpropenylphenols (Gottliebetal. 1978).Thus
thesequencecinnamicacids -*■cinnamyl alcohols -»allyl-andpropenylphenols
accompanies theevolutionoflandplants untilreaching its climax1 attheinter-
face gymnosperms/angiosperms. Inangiosperms, wherethereappearcompara-
tively many more highly oxidized substances (see following section), a reverse
1 Theoreticallythereductive sequencecould continue ton-propylphenols.That suchcompounds
have rarely,ifever,been foundmay be due totheir possiblelackofreactivityand hence relevance
toplantlife.
PHYTOCHEMICALASPECTSOFANGIOSPERMEVOLUTION 459
trendstartswhichimplies agradualabbreviationofstepsoftheshikimate path-
way inthesynthesis ofprecursors ofbiosynthetic groupsofsecondary metabo-
lites(seefig. 1). Theoxidativedimersofpropenyl- and/or allylphenols (neolig-
nans, seeGottlieb 1978) from present-day Myristicaceae and Lauraceae, and
perhaps thehighlyreducedflavonoidsofthevirolantypefromtheMyristicaceae
(Braz Filhoetal. 1973) maybereminscent ofthe micromolecularconstitution
oftheearliest angiosperms.
Furtherutilizationofshikimate-derivedprecursors for the synthesis of sec-
ondarycompounds ischaracterizedbya gradual reductionofbiosynthetic steps
ofthispathway. WithintheMagnoliidae, phenylalanine and/ortyrosine are still
utilizedfortheproduction ofbenzylisoquinoline alkaloidswhichare onlyrarely
foundoutsidethissubclass. Biogenetically relatedcompounds, suchas phenyl-
ethylisoquinoline and benzylphenylethylamine alkaloids, and betalains(chro-
moalkaloids), are based onthe same aminoacids. They occur inthe Magnolii-
dae, the monocotyledons and the centrosperms, which form the magnolialean
block(Kubitzki& Gottlieb 1984).Thesomewhatadvancedstateofbenzyliso-
quinoline synthesis explains why some familiesof thewoody Magnoliidae, as
the Winteraceae, Myristicaceae and Canellaceaeare devoidofthesealkaloids,
a problem thathas puzzled phytochemists timeandagain. Furthersteps inthe
abbreviationofthe shikimatepathway includetheutilizationofchorismicacid
for thesynthesis ofanthranilate-derivedalkaloids and finally that ofshikimic
acidforthesynthesisofgallo-andellagitannins. Bothanthranilate-derivedalka-
loidsandgallicandellagic acid-derivedtanninsare widelydistributedthrough-
outthebasicgroupsoftheremaining dicotyledons, forming therosiflorean block
intheterminology ofKubitzki&Gottlieb(1984).
Thegradualtransitionfromwoody toherbaceousgrowth, occurring inparal-
lelin severallineages ofangiosperms, corresponds chemically to a decrease in
quantitative importance ofthe shikimate pathway. Cinnamatesurplus, from
reducedconsumption fortheproduction oflignins, may account fora certain
abundanceoflignans, coumarinsand even flavonoids, although the latterare
subjected to selectiveforces differentfromthosegoverning thepresenceofother
secondary metabolites(Gottlieb 1982; Kubitski 1984) in herbaceous forms.
Oneinstructivecase inpointisprovidedbytheAralialeswhichcontaintheclose-
ly alliedfamiliesAraliaceae and Apiaceae. Whilethe latterare mainly herba-
ceousandmakeample useof cinnamatein thesynthesis ofcoumarins, nosuch
substances have beendetected sofarin thepredominantly woody counterpart,
the Araliaceae.Nevertheless, insuch advancedangiosperm lineages shikimate
derived secondary metabolitesplay a relatively minor role. In these lineages,
thefull potential ofmevalonateutilizationhasledto steroidalkaloids, iridoids,
iridoidalkaloidsandsesquiterpene lactones, that ofacetate to polyacetylenes.
3. THE PARTICULAR OXIDATION-REDUCTION POTENTIAL OF
ANGIOSPERMS
Secondary metabolites, such as flavonoids, lignoids, polyketides, terpenoids and
460 K.KUBITZKIANDO.R.GOTTLIEB
Fig. I. Distribution ofmajorgroupsofallelochemicals in angiosperms,showingagradualreplace-
mentofmainlyshikimate derived constituents(dotted)bypredominantlymevalonate and acetate-
derived constituents(hatched)inadvanced angiosperms.Condensed tannins,isoflavonoids and in-
dole alkaloids are ofmixed origin. Examplesare given for different constellations ofsecondary
compounds.Nolinear ancestor-descendant relationshipisimpliedbythe sequence oftaxa.
PHYTOCHEMICALASPECTSOFANOIOSPERMEVOLUTION 461
steroids, as well as alkaloids, which are foundin gymnospermsmayalso occur
in angiosperms, where they are frequently accompanied by more highly oxi-
dized,andoccasionally by lesshighlyoxidized, derivativesofthesamebiogenetic
group.This observation was quantified for flavonoids(Gottlieb et al. 1982).
Averaging the data for theoxidationpatterns ofall known flavonoids, both
the triketideandthecinnamatederivedmoietiesappearatconspicuously lower
oxidationstates for gymnospermousthanfor angiospermous compounds. Iso-
flavonoids, whicharisethrough oxidative transformationofchalcones, are re-
stricted to angiosperms. Thewell known high relative proportion of coniferyl
(4-hydroxy-3-methoxycinnamyl) alcoholversus sinapyl (4-hydroxy-3,5-dimeth-
oxycinnamyl) alcoholin gymnospermversus angiosperm lignins (Sarkanen &
Ludwig 1971)is viewed as furtherevidence for the higher oxidationlevel in
angiosperms withrespect to cinnamatederivedmoieties.Thevast majority of
lignans ingymnospermsstem from coniferyl alcohol, whilein theangiosperms
lignans and neolignans are frequentlyderivedfromtrioxycinnamyl alcoholsas
well.In regard to polyketide moieties,accumulationof highly oxidized deriva-
tives (e.g. acetophenones, polyacetylenes) is restrictedto angiosperms. Terpen-
oidsandsteroidsas highlyoxidizedasthemonoterpenoid iridoids,thesesquiter-
penoid lactones, the diterpenoidtanshinones, royleanones andcoleones, thetri-
terpenoid cucurbitacinsand limonoidsand the steroidal whithaferins-areall
known only from the angiosperms. The formationof indole (tryptophane-
monoterpenoid) alkaloids as well asbenzylisoquinoline alkaloidsinvolves oxi-
dative steps and is also restricted to the angiosperms. The transformationof
theubiquitous protein aminoacidsintocyanogenic glycosides alsorequires oxi-
dative steps. Thusit is not surprising thatthe numberofcyanophoric gymno-
spermsis sosmallincomparison to the numberofsuch angiosperms (6 ; 2,000
according to Hegnauer 1977).
Therecan be littledoubtthat the origin ofthe angiosperms coincidedwith
a substantialamplification ofthe oxidation-reductionpotential ofenzymatic
catalysts fortheformationofmicromolecules.Butwhat abouttheangiosperms
themselves? Does theoriginofnewevolutionary lineswithinthisplant division
followthe sametrend?Indeed, this seems tobe thecase fortaxaof higher hier-
archiclevels, i.e.superordersandpossiblyalsoorders. TableIlistssome correla-
tionsofthe meanoxidationlevelsofthecompounds belonging to differentbio-
genetic groupswith Sporne’s(1980) evolutionary advancement indices ofthe
angiosperm families(or themean indices forthe familiesofanorder or super-
order) inwhichthey occur.
Theexistenceofapositive correlationbetweenoxidationlevelsofcompounds
andevolutionary advancementofthetaxawhichproduce themmeansthat,just
as for the origin ofthe angiosperms themselves, the radiationof each major
subgroup coincidedwith anabrupt amplification ofthe oxidationlevel of its
micromolecules.Aclearunderstanding oftheevolutionary polarityofmicromo-
lecularoxidation states for taxaoflowerhierarchic levels is yetless well docu-
menteddueto the lack ofadvancement indicesfor generaand species, making
quantitative correlationsofmorphology withchemistry impossible. Descriptive
462 K,KUBITZKIANDO.R.GOTTLIEB
Table 1.Biogeneticgroupsofcompoundscontained inplanttaxa characterizedby thecorrelation
ofmeanoxidationlevel/evolutionaryadvancementindicessensuSporne(1980).Thevaluesofoxida-
tion levels are internallycomparablefor eachbiogeneticgroup (see ref. for their determination
ineach case).Advancement indices areavailable forfamilies. Advancement indices for ordersand
superordersaremeansfromthoseoffamilies. Classification afterDahlgren(1980).
Flavonoid-ring A(Gottliebet al. 1982).GroupsofSuperordersR(Rosiflorae,Myrtiflorae,
Rutiflorae, Sanlaliflorac,Malviflorae, Violiflorae,Theiflorae,Primuliflorae,Balanophoriflorae,
Araliiforae,Comiflorae,Fabiflorae)104.7/46.8;M(Magnoliiflorae,Nymphaeiflorae,Ranunculif-
lorae,Caryophylliflorae, Polygoniflorae)113.7/50.4;A(Asteriflorae,Solaniflorae,Gentianiflorae,
Lamiiflorae)116.6/64.5.
Benzylisoquinolinealkaloids(Barreirosetal. 1984).Superorders:Magnoliiflorae(sineAris-
tolochiaceae)—0.27/45, Ranunculiflorae —0.20/48.Families ofMagnoliiflorae: Magnoliaceae
—0.31/25,Annonaceae —0.28/40, Monimiaceae —0.28/47.Lauraceae —0.25/52,Hemandiaceae
—0.22/61,Aristolochiaceae +0.15/50;ofRanunculiflorae: Berberidaceae —0.21/45,Menisperma-
ceae—0.22/47,Ranunculaceae —0.19/53,Papaveraceaeincl.Fumariaceae —0.19/48.
Iridoids (Kaplan&Gottlieb1982).Superorders:Comiflorae9.8/51.6,Gentianiflorae 10.5/62,
Loasiflorae 10.0/64,Lamiiflorae 10.0/64.Orders ofComiflorae: Eucommiales 10.8/40,Fouquie-
riales 10.3/47,Sarraceniales 9.3/48,Ericales 11.2/49.4,Cornales 10.3/56,Dipsacales 10.5/67;ofGe-
ntianiflorae:Gentianales 10.4/59.6,Oleales 10.9/62,Goodeniales 10.2/64.5;ofLoasiflorae: Loasales
10,0/64;ofLamiiflorae: Lamiales 10.6/71,Scrophulariales11.1/71,Hippuridales11.5/83.Families
ofEucommiales: Eucommiaceae 10.8/40;ofFouquieriales:Fouquieriaceae10.3/47;ofSarracenia-
les: Sarraceniaceae 9.3/48; ofEricales:Ericaceae 11.3/45,Pyrolaceae11.0/54;ofCornales: Davidia-
ceae 10.4/46.Symplocaceae 10.0/48,Garryaceae 10.7/50,Alangiaceae9.0/52,Icacinaceae 10.3/56,
Sambucaceae 10.3/56,Coraaceae 9.9/57,Stylidiaceae11.3/62,Adoxaceae9.8/78;ofDipsacales: Ca-
prifoliaceae 10.6/60,Calyceraceae 10.5/67,Valerianaceae 9.2/83,Dipsacaceae9.8/87; ofGentiana-
les: Rubiaceae 10.2/48:Apocynaceae10.4/57,Loganiaceae9.4/61,Gentianaceae 9.9/63, Menyan-
thaceae 9.8/69; ofOleales: Oleaceae 10.9/62;ofGoodeniales: Goodeniaceae 10.2/64;ofLoasales:
Loasaceae 10.0/64;ofLamiales: Verbenaceae 11.3/67,Lamiaceae 10.2/72,Callitrichaceae 11.5/74;
ofScrophulariales:Myoporaceae 10.9/63,Scrophulariaceae11.3/67,Plantaginaceae10.8/69,Glo-
bulariaceae 10.8/69,Buddlejaceae11.8/70,Pedaliaceae 12.0/70,Acanthaceae 11.0/72,Martyniaceae
10.6/75,Lentibulariaceae 11.8/75,Bignoniaceae11.6/80;ofHippuridales:Hippuridaceae11.5/83.
Polyacetylenes (Ferreira&Gottlieb 1982). Superorders: Rutiflorae -1.6/52,Santaliflorae
— 1.3/56,Araliiflorae —1.1/57,Asteriflorae —0.7/72.OrdersofRutiflorae: Rutales — 1.6/49;of
Santaliflorae: Santalales —1.3/61;ofAraliiflorae: Araliales —1.1/56,Pittosporales— 1.2/58;ofAs-
teriflorae: Campanulales —0.8/61, Asterales —0.7/72. Families of Rutales: Simaroubaceae
— 1.6/40; ofSantalales: Olacaceae —1.29/46, Santalaceae —1.30/64, Loranthaceae —1.40/65;of
Araliales:Apiaceae — 1.12/51,Araliaceae — 1.10/55;ofPittosporales:Pittosporaceae— 1.20/63;of
Campanulales:Campanulaceae—0.80/63;ofAsterales: Asteraceae —0.67/72.
Table 2.Reportedcasesforwhichadecrease ofmeanoxidationlevelsofcompoundswithinbiogene-
ticgroupscorrespondstoapresumedevolutionaryadvancement inplanttaxa.
FFllaavvoonnooiiddss((GGoommeesseettaall.. 11998811))::DDeerrrriiss,,LLoonncchhooccaarrppuuss..
IIrriiddooiiddss((KKaappllaann&&GGoottttlliieebb 11998822))::sseeeeffaammiilliieesswwiitthhiinnoorrddeerrssiinnttaabbllee II..
PHYTOCHEMICALASPECTSOFANGIOSPERMEVOLUTION 463
correlationsfor some micromoleculargroups withevolutionary considerations
based on morphological evidencefor generaor species {table 2) could indicate
thereversal ofthetrend, i.e. withineachtaxon orevolutionary lineevolutionary
diminutionoftheoxidationleveloccurs.
In conclusion, our working hypothesis states that an increase inthe degree
ofreductionofmicromoleculeswhich constitutes the general trendin angio-
sperms, is opposed by areverse oxidative trend which is most pronounced at
theonsetofeachmajorphyletic line.
4. MICROMOLECULAR PATTERNS AND HERBIVORY
The wide-ranging replacement of gymnospermsby angiosperms in the Creta-
ceous was not a unique phenomenon in the history of plant life. Earlier, the
upswing ofnovelmajorgroupshadbeenaccompanied bythe neardisplacement
ofthepreviously existing groups. Thisis documentedby thestatistical analysis
ofthe sequence Silurian-Devonianearly landplants-» Devonian-Carbonifer-
ous pteridophytes -> late Palaeozoic-Mesozoic gymnosperms->Cretaceous-
Tertiary angiosperms (Niklas etal. 1983).While thefloristic change inthe late
Palaeozoiccoincidedwithprofound environmentalalterations, the appearance
of the pteridophytes and angiosperms was associated with a decline in the
numberofspecies in thepreceding dominantgroup.Thissuggeststhe competi-
tive displacement of older taxa by newer ones. It has even been argued that
competition, eventually leading to extinction, mayhave beenmore important
in plant than in animalevolution (Lewin 1983). This maybe due to the fact
that plants areall rathersimilarin theirphysical and nutritionalneedsand the
general organisation thatresulted therefrom. Becauseofthisitisassumed that
someofthefactorsthathavedeterminedtherise oftheangiosperms were subtle
traitsthat are todaydifficultto recognize. Itis our conviction thatthe extreme
chemicalversatilityoftheangiosperms musthavebeensuch atrait.
Intheforegoing, wehavedealtwithtwo phenomena: thesequentialabbrevia-
tionofthe shikimatepathway inthesynthesisofprimary precursorsforsecond-
ary metabolites, and the extraordinarily high reduction-oxidationlevel that
characterizesthe secondary metabolismofangiosperms. Wewillnow attempt
to determinethe evolutionary significance of these striking phenomena. Itis
widelyagreed thatselectionofsecondary metabolitesby, andcoevolutionwith,
phytophagous and pathogenic organisms are the prime factors operational in
shaping the diversityofnaturalproducts(Ehrlich& Raven1965;Swain 1977).
The acquisition ofoptical and olfactoricluresin coevolutionwith pollinators
andseeddispersersmayalsohaveplayed animportant roleinthiscontext. How-
ever, thisinterplay didnot achieve its full expression untilthe appearanceof
the angiosperms. The defence chemistry ofpteridophytes and gymnosperms,
incontradistinction, isstillunspecialized, eitherpredominantly physical through
464 K.KUBITZKIANDO.R.GOTTLIEB
hard, lignified tissue1 or impregnation with silica, or chemicalthrough con-
densedtannins.Thetanningactionofthelatterprecipitates viralnucleoproteins,
produces leafprotein-tannin complexes which are indigestible for microorgan-
isms andinsects, and inhibitsthedigestive enzymes ofmammalsas well as the
degradative enzymes of fungi. This general defence (for defence theory see
Rhoades 1979) requires that substantial amounts of chemicals be deposited in
all organs that need protection. Specialized defence through toxic micromole-
cules, as itoccurs onabroadscaleinangiosperms, is energetically morefavour-
ablebuthas thedrawbackthatselectioncan leadtodetoxificationmechanisms.
Coevolutionwith herbivores is widely accepted as the driving force behind
phytochemical change at the levelofpopulations andspecies, butthisexplana-
tionhas seldombeenusedinconjunction withphytochemical evolutioninhigher
categories. Only Cronquist (1977) has hypothesized that the shifts from one
majorgroupofsecondary constituentsto theotherreflectasuccessionofgroups
ofsecondary compounds thatwere usedin plant defence, havediversified and,
afterbeing exhausted, were superseded by compounds ofanovel groupofsec-
ondary compounds. A similar view is held by Gardner(1977) whois mainly
concerned with the replacement of defences based on tanninsand crystals, as
occur inprimitiveRosidae, bydefencesbasedonavariety oftoxicandrepellent
substances. Whilethis hypothesis isattractive in principle, thereare some diffi-
culties in its application because Cronquist (1977) implied a sequence from
benzylisoquinolines to condensedand hydrolysable tannins, andfarther to iri-
doids, polyacetylenes, sesquiterpene lactonesandlatex. Toaccept a systematic
continuity oreven anancestor-descendantrelationship inthesequenceMagno-
liidae -*■Rosidae and from there to the other major clusters of dicotyledons
wouldimplythatfromthespecial defenceoftheMagnoliidae bybenzylisoquin-
olines areversal hadoccurredinthe Rosidae to theuse ofthe oldbulk defence
by condensedtannins, already employed by gymnosperms and pteridophytes.
Fortheseandotherreasons, severalauthors(Kubitzki 1969;Bate-Smith1972;
Meeuse1970;Swain 1974)havearguedthatthemagnolialean families, although
harbouring the most archaic characters of the angiosperms, could hardly be
consideredtoresemblethedirectancestor(s)ofallotherdicotyledons. Itis more
likely that themagnolialean and rosifloreanblocks, which must have an old
origin, diverged at an early, as yet unknown stage of angiosperm evolution.
Otherwise, the presenceofwinteraceous(Walkeret al. 1983), possibly protea-
ceous (Serlin 1982), and other angiosperms as early as the LowerCretaceous
wouldbe difficultto explain.
Oncetheexistenceofparallelisms, convergencesandreticulationsintheevolu-
tionofthe angiosperms is accepted, the logic ofnaturalselection as the major
forceresponsible for the observed succession of“chemicalweapons” becomes
more obvious. However,this does not explain why thesequenceofprecursors
ofthe shikimate pathway follows a reversed biosynthetic sequencerather than
1 Ligninsnotonly contribute to the compressivestrength ofthe cell wall but may also act asa
feedingdeterrent (Rhoades 1979)andasa meansofpreventingfungalinfection ofepidermalcells
(Grisebach 1981).
PHYTOCHEMICALASPECTSOFANGIOSPERMEVOLUTION 465
occurring at random. Chemicalchanges follow a fine-tunedhierarchy which
atthepopulation levelbegins withsubstitutionalchanges andis followed, after
exhaustionofthe possibilities ofa given level, byconfigurational andconstitu-
tionalchanges. Inthishierarchy, switch-overs to anovelprimary precursorrep-
resent the most drastic innovationof secondary chemistry. Inthe case ofthe
shikimatepathway,aftertheelaborationofthemosthighly reducedprecursors,
propenyl- and allylphenols, there is virtually no choice other than to retrace
the biosynthetic sequence.Thusthe use ofprimaryprecursors ofthe shikimate
pathway inasequenceopposed to their biosynthetic origin follows the lineof
leastresistance and exemplifies whatStebbins(1974) has called“evolutionary
canalisation”.Thisretrograde biosynthetic sequencedoesnotstopwith theuse
of shikimic acid as the primary precursor forthe synthesis ofmicromolecules.
After theexhaustionof the shikimate theme, the enhancementofimportance
of mevalonate-acetatederived metabolites takes place. This decrease in the
quantitative importance oftheshikimate pathway is accompanied by atransi-
tionfromwoodyto herbaceousgrowth. Inlightofourfindings, thereplacement
ofligneous by herbaceousformsis acorollary ofthecoevolutionary relationship
betweenplants and herbivoresratherthanreflecting increasing economyasof-
ten hasbeenclaimed.
Anotherinstructiveexampleofcanalisedevolutionis provided bythesequen-
tial employment of hydroxycoumarins, linearfuranocoumarins, and angular
furanocoumarinsintheUmbelliferae(Berenbaum 1983).Thesegroupsofsub-
stancesare progressively lesssuitabletopolyphagous insects,yetsomeoligopha-
gousspecies havecounteradapted bothphysiologically as wellas behaviourally.
Berenbaum(1983)findsthespecies diversityincoumarin-containing subgroups
oftheUmbelliferaegreater thaninsubgroups thatlack coumarins, andinsect
groupsassociated with coumarin-containing Umbellifersare more diversified
thanrelatedgroupsonplantswithoutcoumarins.Thiscorroboratesthehypoth-
esis thatreciprocalevolutionary interactions,focusing onsecondary plantchem-
istry,havebeenconduciveinaugmenting the diversityofplantandanimalspe-
ciessinceCretaceaoustimes.
A similar explanation may be be envisioned for the extraordinarily broad
rangeofoxidation-reductionlevelsthatcharacterizeangiosperm secondary me-
tabolites.Ithasbeenshownthattherateofformationandthemolecularproper-
tiesoflaccase infungi depend upon the presenceofinducerssuch as coumaric
acidandgallicacid(Marbach etal. 1983).Although thefunctionoftheseoxida-
tiveenzymes is not yetclear, they maywell operate inthe detoxificationofthe
hostplant’sallelochemicals.Thisfunction, together withtheconversionoflipo-
philiccompounds to water soluble, excretablecompounds, is usually attributed
to themixedfunctionoxidases(MFO) whichare ubiquitous inanimals(Bratt-
sten 1979).The potencyofthe MFOsystems increases frommonophagous to
polyphagous species(KRiEGERetal. 1971; Brattsten1979) aswellaswithlarval
developmentandtheconcomitantincreaseoffoodconsumption (Ahmad 1982).
ThissuggeststhatthepotencyoftheMFOsmayalsohaveincreasedevolutionar-
ily, withthediversificationofplantspecies andtheirsecondary metabolites.
466 K.KUBITZKIANDO.R.GOTTLIEB
Thusitistobeexpected thatallelochemicalsshould bemoreandmorereduced
inorderto beless andless easilyoxidized, i.e., detoxified.Indeed, the sequence
cinnamicacids -* cinnamyl alcohols -*■allyl- and propenylphenols (fig. I) ac-
companies the evolutionofearlylandplants and thereis no reason to suppose
thatthis generalreductive trendshouldcease with,theappearanceofthe angio-
sperms. In this plant group,the origin ofeach new lineage coincideswith the
production ofrelatively higly oxidizedcompounds. Nevertheless, the general
reductive trendpersists, andin parallel ineach lineage the oxidativepowergra-
dually decreases.
5. CONCLUSION
Ifthesudden appearanceofmore highly oxidizedmicromoleculeshascontrib-
utedto thesuccess ofangiosperm evolutionanddiversification, therelativeease
ofdetoxificationatthebeginningofeach majorevolutionarylinemayconstitute
the attractive counterpoint oftheplant-herbivore coadaptation. Thus the high
oxidationstateofsecondary metabolitesfoundin early angiosperms andatthe
onsetofmajorlineages withintheangiosperms mayhaveintensifiedtherelation-
ship between plants and animalswhich, according to an attractive hypothesis
(that canbetracedto Dobzhansky 1950)wasconduciveinproducing the diver-
sityofplantandanimalspecies sinceCretaceoustimes.Thiswouldbe atvariance
withthe widely accepted ideasexpressed by Ehrlich& Raven(1965) that the
early radiation of angiosperms took place behind the biochemical “shield”
formedby benzylisoquinolines. Subsequently, the diminishing oxidationlevel
withindifferentlineages couldbeexpected to makedetoxificationmoredifficult
andhencemoreselective.
Whatevertheinterpretation, thefactremainsthatabroadrangeofoxidation-
reductionlevelsand a considerablenumberofprecursors characterize the sec-
ondary metabolismoftheangiosperms. Consequently, theexistenceofanample
oxidation-reductionpotential and ofa flexibleactivation-deactivationmecha-
nismofenzymesintheircellsmustbeimportantcauses oftheenormousdiversity
ofangiosperm natural products and angiosperm species as well. This adds a
fascinating new facet to the framework of hypotheses that have been erected
aroundthe questionofwhy early angiosperms were sosuccessful.
ACKNOWLEDGEMENTS
Professor E.Sprecher,Dr. H.-H. Poppendieckand Dr. M. Fallen made valuable suggestionson
themanuscript,and Dr.Fallen verykindlycorrectedthe English,forwhichweareverygrateful.
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