[doi 10.1007%2f978!0!585-23095-5_6] taylor, david winship; hickey, leo j. -- flowering plant origin,...

8/10/2019 [Doi 10.1007%2F978!0!585-23095-5_6] Taylor, David Winship; Hickey, Leo J. -- Flowering Plant Origin, Evolution &

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C H A P T E R

The Orig in and

Evolut ion of the

n g i o s p e r m

Carpe l

avid Winship Taylor and Gretchen

Kirchner

The angiosp erm carpel i s one of the def in ing character is tics of f lower ing plants .

Carpels are unique to angiosperms and are found in a l l of i t s members . Yet ,

due to the d is t inct ive s t ructure and funct ion of carpels , deducing homologies

among carpels and other seed-plant organs has been dif f icul t . Progress in

under s tand ing ca rpe l homolog ies and evo lu t ion i s be ing made in a number o f

direct ions . Homologies , as wel l as t ransformat ions between them, have been

proposed am ong ang iosperms and o ther s eed p lan t s. These inc lude hom olog ies

among the reproduct ive s t ructures of Glossopter ids , Caytonia and other foss i l

taxa e .g . , Tho mas , 1925, 1957; An drew s , 1963; S tebbins , 1974; Do yle , 1978;

Retal lack and Dilcher , 1981a; Crane, 1985; Doyle and Donoghue, 1986b) .

Recen t s tud ies have examined the homolog ies and t r ans fo rmat ions among

fema le reproduct ive organs through outgroup compa r ison e .g . , Crane, 1985;

Doyle and Donoghue, 1986b; Taylor , 1991a) and in terpreta t ions of carpel

s truc tu re wi th in ang iosperms Tay lo r , 1991a) . Deve lopm enta l , morphogen ic ,

and genet ic s tudies have a lso provided addi t ional ins ight on carpel s t ructure and

deve lopm ent e .g ., Szym kow iak and Sussex , 1992 ; Gasser and Rob inson-Beers ,

6


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Chap 6 The Origin and Evolution of the Angiosperm Carpel 117

1993; Modrusan e t a l . , 1994) . Together , da ta f rom these d iverse sources are

lead ing to a rev ised v iew of carpel homology and s t ruc ture .

Al though t ransformat ions be tween the carpel and o ther seed p lan t reproduc-

t ive organs (par t icu lar ly foss i l ) have been proposed , d i f f icu l t ies in showing

compel l ing ev idence of these homologies has led to hypotheses based on

st ruc tura l in terpre ta tions o f carpels f rom l iv ing angiosperm s. T hese ef forts have

genera ted numerous hypotheses of carpel o r ig in over the las t cen tury ( see

references in Esau, 1965; Cronquist , 1968, 1988; Takhtajan, 1969, 1991). Yet ,

even though the presence of carpels i s a synapomorphy for l iv ing angiosperms,

carpel morphology is surpr is ing var iab le wi th in basa l ly p laced l iv ing angios-

perms. Taylor (1991a) developed a new terminology to descr ibe th is var ia t ion .

He a lso rev iewed the carpel charac ters found in the fami l ies o f the Magnol i idae

as wel l as the basa l fami l ies o f the Hamamel idae , Caryophyl l idae , Di l len i idae ,

Rosidae , and monocots .

Us ing T ay lo r s t e rmino logy , the ca rpe l morpho logy o f the M agno l iidae

ranges f rom asc id ia te (Fig , 6 .1D ,E-H ,L,M ) to ascopl ica te (Fig . 6 .1 I ,J ) to p l ica te

(Fig . 6 .1K, N,O ) . A scid ia te carpels hav e the ovu les a t tached proxim al ly to the

c losure (e .g . , Fig . 6 .1D,F) , p l ica te ones have them a t tached a long the marg ins

of the c losure (e .g . , Fig . 6 .1K, N ) wh i le ascopl ica te carpels a re in termedia te

between the two (e .g . , Fig . 6 .1 I , J ) . The number of vascu lar t races lead ing in to

the ovu le ( s ) r anges f rom one to many . Al though mos t member s have ca rpe l s

that are free, some are syncarpous.

The p lacement o f the ovules and the p lacen tae i s a lso var iab le (Taylor ,

1991a) and ranges f rom basa l (Fig . 6 .1D,E) , to la tera l [e i ther admedia l and

fac ing toward the f lo ra l ax is (Fig . 6 .1F,H) , m arg ina l and a lon g the c losure (Fig .

6 .1K, N) , exm edia l and fac ing aw ay f rom the f lo ra l ax is , rad ia l and on the la tera l

w al ls perpendicu lar to the f lo ra l ax is (Fig . 6 .1M), o r chaot ic and a long a l l wa l ls

of the carpel (Fig . 6 .1L, O)] to ap ica l (Fig . 6 .1G ) in the i r p lacemen t . T he

placen ta may be s i tua ted in the p lane ex tending f rom the f lo ra l ax is and

bisec t ing the carpel th rough the c losure (e .g . , Fig . 6 .1G) or be nonplanar and

located on e i ther s ide of the c losure (e .g . , Fig . 6 .1F,N) . Fina l ly , the num ber and

ar rangem ent o f ovules and p lacen tae are variab le , ranging f rom s ing le (e .g ., Fig .

6 .D) , double (e .g . , Fig . 6 .F) to few (e .g . , Fig . 6 . I ) o r many in number (e .g . ,

Fig . 6 .K) , and these may be p laced in an a l te rna te (e .g . , Fig . 6 .N) , opposi te

(e.g . , Fig. 6 .K), or clustered arrangement.

The las t type of var ia t ion i s found in carpel development (Taylor , 1991a) .

Some carpels develop f rom two separa te g rowth areas (Fig . 6 .1AI ,AII ) whose

presence may be separa ted spa t ia l ly or tempora l ly . The f i r s t p r imord ium pro-

duced i s U-shaped or cup-shaped and develops in to the gynoecia l appendage .

The second pr imord ium or g rowth area i s sur rounded by the f i r s t and i s the

source of the p lacen tae and ovules . Most carpels in i t ia l ly develop as a cup and

have the p lacen ta p laced a long the admedia l por t ion of the wal l (Fig .


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P r i m o r d i a

D

a t u r e o r p h o l o g i e s

~ E

~

~

K L

~ N

M

~ , . .

m

o

O

~ o

~

O

0 O

~ ~

8


4/25

Chap 6 The Origin and Evolution of the Angiosperm Carpel

9

6.1BI,B II) . Final ly some have placentae along the margins of the closure Fig.

6.1BIII ,C). These carpels develop from ei ther a cup-shaped or U-shaped pri-

mordium.

This variat ion in carpel morphology has led to two major interpretat ions of

carpel evolution, al though both agree with interpretat ions that a port ion is leaf

derived Arb er , 1937; Troll , 1939b). Although these hypotheses describe the

ancestral states, they usually do not address the transformations to the other

states that exist in the basal angiosperms. Most hypotheses suggest that seeds

are phyllosporous Lam , 196 1) in angiosperm s and that the carpel or iginated

from a seed-bearing leaf e.g. , LeinfeUner, 19 50 ; Bailey and Swam y, 1951 ;

Cronquist , 1988; Takhtajan, 1 99 1 and references therein) . Thus, the gyno ecial

appendag e port ion of the carpel is a modif ied leaf on wh ich the ovules are borne

Satt ler , 1974; S att ler and Perl in, 1982). This hypo thesis sugge sts that the carpel

is homologous with a megasporophyll .

The phyllosporous-origin or megasporophyll-homology hypothesis has two

variants. Most authors suggest that the gynoecial appendage is fundamental ly a

folded leaf with a proximal at tachment o f the pet iole e.g. , Bailey and Sw am y,

1951; Cronquist, 1988 ; Takhtajan, 1991). C arpels of this type have been termed

condupl icate Bai ley and Swamy, 1951) and have many ovules a long the

ma rgins or subm argins) of the closure Fig. 6.1N). Others have sugge sted that

the leaf is fundam ental ly pel tate e.g. , Baum , 1949, 19 52 ; Leinfel lner , 19 50;

Baum-LeinfeUner, 1953). This is due, in part , to the cup-shaped primordia

found in many carpels. Although such ovules are st i l l considered to be marginal

Fig. 6.1I ,J) , these authors note that ovules can be few in number and placed

med ial ly at the base of the closure at the cross-zone; Fig. 6.1F). In nei ther

variant of the phyllosporous-origin hypothesis have the transformations to al l

the other carpel types been explained from a developmental , morphological , or

evolutionary perspective.

The second major group of hypotheses suggests that the carpel has a funda-

men tal ly stachyosporous origin Lain , 1961). Thus the gynoec ial append age is

thought to be homologous to a subtending bract and the placenta is homologous

with a shoot bearing distal ly-placed ovules e.g. , Panko w, 1962; M oeliono,

1970; Sattler and Lacroix, 1988). Again, there has been relatively little dis-

cussion of the transformations to other carpel types. Ha gerup 1934 , 1936,

1938) has addressed the transformations most extensively and suggested that

conduplicate carpels also develop from two growth areas see also Melvil le,

1962).

Recently, Taylor 199 1a) has further elaborated the stachyosporous origin

hypothesis of Hag erup 1934 , 1936, 1938) and others e.g. , M elville, 1962;

Moeliono, 1970; Satt ler and Lacroix, 1988) based on outgroup comparison. He

has suggested that the carpel is a bract- terminal ovule system and direct ly

homologous to that found in the outgroups including the Gnetales, the closest


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120

Ch ap 6 The Origin and Evolution of the Angiosperm Carpel

l iv ing s i s te r group. The s te r i le gynoec ia l -appendage of the ca rpe l i s cons idered

homologous w i th a sub t e nd ing b ra c t i n t he a ng iospe rm s i s t e r g roups , w he re a s

the p lacenta l growth a rea i s homologous wi th the ovula r axis . Based on these

homolog ie s , Ta y lo r c onc lude s t ha t a sc id i a t e morpho logy a nd low ovu le -numbe r

1 o r 2 ) a re a nc e s tra l F ig . 6 . 1D , F ,G ) . H e a lso sugge s t s hom olog ie s a mon g

carpe l types wi th the basa l ly to admedia l ly p laced p lacenta in a ca rpe l wi th a

s te ri le gyn oec ia l -app enda ge Fig . 6 .1AI) as hom olog ous wi th the la te ra l p la -

c e n t a o f a n a sc op l ic a t e c arpe l F ig . 6 . 1BI ) o r ma rg ina l p l a c e n t a e o f a c ondup-

l ica te ca rpe l F ig . 6 .1C) . Th e or ig in of the cond upl ica te p l ica te ) and ascopl i -

ca te ca rpe l types would be due to the in tegra t ion of the gynoec ia l pr imordia and

ovu la r p l a c e n t a l ) g row th a rea . The e vo lu t ion o f the se o the r c a rpe l type s ma y

be re la ted to the evolut ion of ca rpe ls wi th h igh ovule numbers .

From these d i f fe rent s tudies of ca rpe l evolut ion , a group of ques t ions can be

posed. F i rs t , which type of ca rpe l found in l iv ing taxa i s most s imi la r to the

ances t ra l form? Second, wha t i s the ances t ra l number of ovules? Thi rd , why i s

there var iabi l i ty among carpe ls in the basa l angiosperms? Fina l ly , wha t a re the

t ra ns fo rma t ions a mong c a rpe l t ype s?

P O L A R I Z A T I O N O F T H E A N C E S T R A L C A R P E L

C H A R A C T E R S

D ue to t he l a c k o f c le a r hom olog ie s be tw e e n re p roduc t ive s t ruc tu res o f a ng ios -

perms and the i r s i s te r groups , the pola r iza t ion of the ances t ra l ca rpe l s ta tes has

be e n d i f fi c ul t. Ta y lo r 199 1a ) e xa m ine s th i s p rob l e m a nd p re se n t s s e ve ra l l ine s

o f e v ide nc e. O ne l i ne is t he f re que nc y o f c a rpe l t ype s a nd nu m be r o f ovu le s in

the ba sa l a ng iospe rm fa mi li e s Ta b le 6 . 1 ) . O f t he m e m be rs o f the Ma g no l i ida e

se nsu Cronqu i s t ) , tw o- th i rds o f t he fa mi l i e s ha ve me mbe rs w i th t he a sc id i a t e

c a rpe l t ype a nd ove r a ha l f ha ve c a rpe ls w i th one o r tw o ovu le s . S t e bb ins 19 74)

a l so no t e s t ha t low ovu le nu m be r i s c om m on a nd sugge s t s i t m a y be a nc e st ra l .

Unl ike for ca rpe ls , i t i s poss ib le to pola r ize many of the ances t ra l s ta tes of

the ovu le us ing ou tg roup c ompa r i son Ta y lo r , 1991a ) . W he n c om pa re d to the

outgroups , the ances t ra l angiosperm ovule appears to have the chaza la oppos i te

the micropyle , an or thoangle , to ta l symmetry , symmetry of the oute r in tegu-

ment , a nuce l la r a t tachment oppos i te the micropyle , f ree in teguments , and the

mic ropy le fo rme d f rom the i nne r i n t e gume nt [ t e rmino logy ba se d on Ta y lo r

1991a)] . In convent iona l t e rms, the ances t ra l ovule i s b i tegmic and or tho-

t ropous . This hypothes i s i s in cont ras t to most ana lyses tha t sugges t tha t the

ances t ra l ovule was b i tegm ic and ana t ropous e .g . , Cron quis t , 1968, 1988;

Takhta jan , 1969, 1991; Bouman, 1974) . In te res t ing , recent mutagenes is ana lys i s

o f

A r a b i d o p s i s

ovules shows tha t s imple muta t ions can resul t in a d i s rupt ion in

the de ve lopme nt o f t he norma l ly a na t ropous ovu le so t ha t i s doe s no t ha ve t he


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2

ab l e 1. General Carpel Type s and Ovule Types for the Orders of the Magnoliidae

(sensu Cronquist).

Carpel Morphology Ovule num ber

Order

Ascidiate Ascoplicate Plicate 1 or 2 Few M any

Magnoliales 6 1 5 7 6 6

Laurales 7 1 0 8 0 0

Piperales 3 0 1 3 1 1

Aristolochiaceae 1 1 1 0 1 1

Illiciales 2 0 0 2 1 0

Nymphaeales 4 1 0 3 1 2

Ranunculaceae 7 2 3 9 5 5

Total 30 6 10 32 15 15

No te : T h e n u m b e r i n e a c h c o lu m n i s t h e n u m b e r o f f a m i l i e s i n t h e o r d e r wh ic h h a v e th e c h a r ac t e r s .

I f t h e f a m i ly is v a ri a b l e, i t is r e c o r d e d u n d e r m o r e t h a n o n e s t at e . So u rc e : Da ta f r o m T a y lo r 1 9 9 1 a ) .

cu rv ed an a t ro p o u s s h ap e (Gas s e r e t a l . , 1 9 9 5 ) . Th i s f i t s w i t h Tay l o r ' s (1 9 9 1 a )

hypothes i s tha t o r tho t ropous i s ances t ra l and tha t the anat ropous fo rm resu l t s

f rom an addi t ional s t ep in the development o f the ovule .

Once the ances t ra l ovu le s t a tes a re po lar ized , i t i s poss ib le to examine the

as s o c i a ti o n b e t ween ca rp e l s t a te s an d p o l a r i zed o v u l es . Tay l o r ( 1 9 9 1 a ) co n s i st -

en t l y fo u n d t h a t a s c i d i a t e m o rp h o l o g y an d o v u l e n u m b er s o f o n e o r t wo a re

associa ted wi th the ances t ra l ovu le s t a tes , bu t the cor re la t ions are no t s ign i f i -

can t . Tay lor d id f ind s ign i f i can t cor re la t ion be tween asc id ia te carpe l s and ovule

n u m b ers o f o n e o r t wo wi t h 7 7 o f t h e a s c i d ia t e ca rp e l s r ep o r t ed f ro m fam i l i e s

hav in g one or two ovules . In con t ras t , 79 of the p l i ca te and 73 of the

ascopl ica te carpe l s a re f rom fami l i es wi th few to many ovules . In add i t ion , 74

of the fami l i es tha t had asc id ia te carpe l s came f rom fami l i es in which i t i s the

only carpe l type . In con t ras t , on ly 8 o f the fam i l i es wi th ascopl ica te carpe l s

h av e t h a t t y p e a l o n e an d 5 4 w i t h p li ca te h av e p l i ca t e a l o n e. A l t h o u g h s o m e

of these associa t ion da ta a re equ ivocal , they do sugges t tha t asc id ia te carpe l s

wi t h o v u l e n u m b er s o f o n e o r two an d p l i ca te ca rp e l s w i t h h i g h n u m b er s a r e

rea l en t i t i es in ang iosperms , and tha t the fo rmer are l ike ly to be ances t ra l .

N e w E v i d e n c e

Th ere i s n o w ad d i t i o n a l ev i d en ce t h a t can b e u s ed t o fu r t h e r u n d e r s t an d

ca rp e l ev o l u t i o n an d o r i g i n . F i r s t , t h e g ro wi n g n u m b er o f an g i o s p e rm

phylogenies a l low for the assessment o f the ances t ra l carpe l s t a tes . Second , as

the unders tand ing of the iden t i ty o f ang iosperm s i s te r g roups and the i r re la t ion-


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1 2 2

Chap. 6 The Origin and Evolut ion of the Angiosp erm Ca rpel

.~ . O V --

. . v . . : p ~ , I . . O * ~ : V l . e , I t _ O

~ ~ V v 11 ~ ~ 11 ~ ~

o v ,- ~ , , ~ s~ = .-

Charater

I

II C r ~ l t i i

[IChar steos: 7

I I

I lunorde red I I

1 I asidiate

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II p.cat, I

-4

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Charater

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umber

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Figur e . 6 .2 . One of three shor tes t t rees f rom Taylo r and Hickey (19 92) w i th the

dis t r ibut ion of carpe l morphologica l s ta tes (A) and ovule number s ta tes (B) . Based on

this phylogeny, the asc id ia te s ta te and ovule number s ta te of one or two are ances t ra l .


8/25


ships has increased, so has the possibi l i ty of using outgroup comparison to

determine a ncestral s tates. Final ly , the understanding of carpel developm ent and

of t ransformations among types al lows tests based on the morphogenesis of

carpels. Each of these areas wil l be discussed in detai l below.

Ingroup Phylogeny There are a grow ing numb er of phylogenet ic ana lyses

of angiosperms based on structural (Donoghue and Doyle, 1989a; Loconte and

Stevenson, 1991; Taylor and Hickey, 1992; Tucker et al . , 1993; Tucker and

Douglas , Chapter 7 ; Loconte , Chapter 10) and DNA sequence [18S rRNA

(Zimmer e t a l . , 1989; Hamby and Zimmer, 1992); rbcL cpDNA (Chase e t a l . ,

1993; Qiu et al . , 1993; Sytsma and Baum, Chapter 12)] datasets . These recent

analyses support different hypotheses of angiosperm origin suggest ing that the

basal ly placed clades are ei ther herbaceous magnoli ids (Zimmer et al . , 1989;

Taylor and Hickey, 1992; Hamby and Zimmer, 1992; Chase et al . , 1993; Qiu

et al . , 1993; Sytsma and Baum, Chapter 12), magnolialeans (Donoghue and

Doyle, 1989a) or lauraleans (Loconte and Stevenson, 1991; Loconte, Chapter

10). A method to assess the ancestral carpel states is to place the carpel states

on these cladograms and see which states are ancestral based on parsimony.

In the t rees from the st ructural dataset of Donoghue and Doyle (1989a), the

woody Magnoliales are basal ly placed. Although the magnolialeans are variable

in carpel morphology, the most parsimonious dist ribut ion of states would have

the ascidiate mo rphology as ancestral . The ancestral ovule num ber in these t rees

is less clear, as the character is variable within a number of famil ies. If ,

however, the taxa that are variable are ignored, the ancestral s tate would then

be one or two ovules. The same polarizat ions (ascidiate and ovule equivocal)

are found in the shortest t rees based on the 18S RNA dataset (Zimmer et al . ,

1989; Hamby and Zimmer, 1992) . In these t rees , the Nymphaeales (sensu

stricto) are the clade closest to the base, and the next closest clade is the

Piper~es (sensu s tdc to) . Both of these groups are herbaceous .

In five other analyses, the most parsimonious dist ribut ion of the characters

have ascidiate and one or two ovules as ancestral . These include two structural

da ta set s, one by Locon te and S t evenson ( 1 ~ 1 ; a lso see ~ n t e , Chap ter 10 )

that has the woody Calycanthaceae and Idiospermaceae as sister groups at the

base, fol lowed ini t i~y by the Magnoliales, Laurales, and l l l ic iales. The other

by Taylor and Hickey (1992; Fig . 6 .2) has the herbaceous fami l ies Chloran-

thaceae and Piperaceae a t the base of the t ree , wi th the former most bas~y

placed. The same polarizat ions are found on the t rees of Chase et al . (1993),

Qiu e t a l . (1993) , and Sytsma and Baum (Chapter 12) based on rbcL c p D N A

sequence da ta . In most o f these t rees , ~e ba s~ c lades a re e i ther the herbaceous

magno l i i d s o r t ha t c l ade m combina t ion ~ th t he he~aceous eu~co~ .

A growing num ber of phylogenet ic ana lyses support Tay lor s (199 1a) hy-

pothes is tha t the asc id ia te c ~ e l wi th one or two ovules i s ances trY. I t i s


9/25


10/25


reproduct ive st ructure of most of these groups below, and propose homologies

and t ransformations among the morphologies. Final ly , we discuss the implica-

t ions for the homology and ancestral s tate of the angiosperm carpel .

The structure of the gnetopsid female reproduct ive system appears to be a

compound organ (Pearson, 1929; Chamberlain, 1935; Eames, 1952; Martens,

1971; Hickey and Taylor, Chapter 8). In Ephedra a single ovule or pair of

ovules each terminate an axis that is distal ly placed on a short shoot . Proximal

to the ovule axes are a series of opposi te and decussately arranged bracts (Fig.

6.3D), of which the distal-most subtend the ovule axes and part ial ly encloses

them. The ovule axes are composed of terminal ov ules and scales with the distal

scales enclosing the ovules, except for the micropylar t ip. These distal scales

form addit ional integuments. For convenience, we wil l cal l the axis with the

distal ly placed ovule(s) and scales a female short-shoot . The ent i re short-shoot

is subtended by a bract or leaf.

In com parison, the st ructure and hom ologies o f the bennet t italean reproduc-

tive structure (Wieland, 1906, 1916; Harris, 1969; Crane, 1985, 1986; Watson

and Sincock, 1992) are much more difficul t to intepret . In gross morphology,

the st ructure is made up of an enlarged, frequent ly elongate receptacle. Attached

to the receptacle are ovules and sterile organs called interseminal scales, and

together these form a dense head (e.g. , Wieland, 1906). Most interpretat ions

suggest that the ovules and interseminal scales are attached directly to the

receptacle and are scat tered across the surface (e .g . , Crane, 1985). The inter-

seminal scales have been suggested to be ei ther bract derived or to be steri le

ovule homologs.

Taylor (1991b) reexamined spec imens of Cycadeoidea a t Yale Peabody

Museum and arrived at a new interpretat ion based on this material , and Wie-

land 's (190 6, 1916) pu bl ished figures and descriptions, First, a single funiculus

may be shared by two ovules. Serial sect ions show that al though this condit ion

is rare, i t does occur. In addi t ion, Wieland (1906) notes and shows that the

interseminal scales are always at tached deeper than the funiculus of the ovules

and, thus, are som ew hat shoot-l ike (W ieland, 1906, p . 118). The funiculus

of the ovule with i ts single vascular st rand joins with several surrounding

interseminal scales just above the point where the ent i re complex is at tached to

the receptacle (see Wieland, 1906, plates XXVII, 4; XXVIII, 7). Thus, the

terminal ovule is attached to a sl ight ly enlarged, apparent ly parench ym ous base,

whereas the interseminal scales are at tached along the margins of the base (Fig.

6.3C). This is seen dearly in many specimens with female reproduct ive st ruc-

tures. In these, the ovules and scales have separated from the receptacle, and in

this condit ion, they do not make an even break (see Wieland, 1906, plate

XXVIII, 7). Rather they separate in blocks, with each block composed of a

central funiculus and several surrounding interseminal scales (see Wieland,

1906, plates XXII, 2; XXIV, XXVII, 4; XXIX, 1, 2). Wieland (1906, p . 118)


11/25

126 C ha p 6 The Origin and Evolution of the Angiosperm Carpel

also notes that the interseminal scales are s imilar to bracts subtending the entire

reproductive axis . Finally, in

Cycadeoidea,

each ovule is usual ly surrounded by

5 or 7 scales .

In terpreta t ions of th is anatomy and morphology must be made with caut ion.

Cycadeoidea i s a la te-occurr ing taxon and is cons idered to be der ived Crane,

1985, 1986). In other taxa e.g. , Vardekloeftia , ovules are rare in com par ison to

the num ber of in terseminal scales Pederso n e t a l ., 1989b) . So me authors have

also descr ibed in terseminal scales that appear to be s t ructural ly in termediate

between fer t i le ovules and s ter i le , in terseminal scales that are sugges ted to be

s teri le ovules . Never theless , another in terpreta t ion is that the o vule- in tersem inal

scale sys tem is d i rectly hom ologo us with the female shor t -shoot of the G netales .

Thus , there is a s ingle som et im es two) terminal ov ule s ) subtended by a ser ies

of scales F ig . 6 .3C) . The fact that there is an odd num ber of scales migh t

sugges t a subtending bract and several pai rs of oppos i te ly ar ranged scales .

Fur ther ser ia l sect ioning is needed to suppor t th is speculat ion . The c lub-shape

of the in terseminal scale could be an adaptat ion to protect the ovules wi th a

t ight ly f i t t ing armor and would make them s imilar in gross s t ructure to ovules

by being dis ta l ly swol len . S imilar c lub-shaped s t ructures have evolved separ-

a te ly in the reproduct ive organs of ma ny t racheophyte groups End ress , 1975) .

As in Gnetales , the in terseminal scales in Bennet t i ta les enclose the ovule , except

for the micropyle .

Unders tanding of conifer s t ructure is poss ib le because of the many foss i l

conifer remains that provide t rans i t ional forms to those l iv ing today e .g . , F lorin ,

1939, 1951, 1954; Harr is , 1969; Clem ent-W esterhof , 1988; M apes and Ro thwel l ,

1991) . Conifers are cons idered to have dis ta l ly p laced ovules on a somet imes

mo dif ied female shor t -shoot F ig . 6 .3 B) . The ov ules may be s ingle , few, or

several , whereas the proximal s ter i le scales may be miss ing, few, many, or

mo dif ied in to an ovul i ferous scale , and the shor t -shoot is usual ly subtended by a

bract . W e cons ider the fem ale shor t -shoot of the gnetop s ids and the poss ib le shor t

shoot of the bennet t i ta leans to be hom olog ous with that of the conifers.

The las t group that we w il l descr ibe is the ext inct Cordai ta les F lor in , 1939,

1951; Rothwel l , 1988; Tr ivet t and Rothwel l , 1991) . This Carboniferous to

Permian group had large, s t rap- l ike , ent i re-margined leaves , and var iable habi t .

The female organs are composed of four to s ix d is ta l funicul i that have a s ingle

ovu le o r tha t may b ranch and have two o r more ovu les F ig . 6 .3 A) . P rox imal ly

to these are a t tached many spira l ly ar ranged scales . This female shor t -shoot is

p laced in the axi le of a bract and the bracts has an a l ternate and dis t ichous

ar rangement . C ompar i sons have been made be tween Corda i ta les and gne tops ids

e .g . , Eames , 1952 ; Bo ld , 1973) and we agree wi th these homolog ies be tween

the female shor t -shoots .

These data for Gnetales , Conifers , and Cordai ta les are c lear , they a l l have a

female shor t -shoot comp osed o f d is ta l ovu le s ) and pro xim al s ter ile scales .


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Chap. 6 The Origin and Evolution of the Angiosperm Carpel 127

These are subtended by bracts that when grouped together form a larger

reproduct ive organ. Ta ylor s (19 91b ) interpretat ion o f these data from

C y c a d e o i d e a

suggest a similar structure for the bennettitaleans. Variable aspects

are the number of ovules and the number of steri le scales. If we look at these

data from a phylogenet ic perspect ive (Fig. 6 .3), we see that the Cordai tales

have many scales and ovules. As we look at groups progressively more closely

related to angiosperms, the number of scales decreases to only a few and the

ovules to one or two. In addition, the distal scales fully enclose the ovules,

except for the micropyle to form addit ional integument(s) (Hickey and Taylor,

Chapter 8).

I t appears that by outgroup comparison the homology is between the

gynoe cial appendage of a carpel and the bract subtending the female short-shoot

in the outgroups (Fig. 6 .3; Hickey and Taylor, Chapter 8). The placenta is then

homologous with a female short-shoot with distal ly placed ovules, each with

scales forming the outer integument . Thus, the placenta is an axis and the ovules

have a stachyosporous origin. I t fol lows then that the angiosperm carpel is the

resul t of a t rend towards the cont inual reduct ion in the number of scales and

ovules and increased protect ion of the ovules by the surrounding organs (see

also Hickey and Taylor, Chapter 8). Under this interpretat ion, the ancestral

states in the carpel would be ascidiate with basal to sl ight ly lateral placentat ion

and an ovule number of one or two.

M o r p h o g e n i c A n a l y s i s .

The different hypotheses of carpel origin have

significant implicat ions for their morphogenesis. One suggests that the carpel is

fundamental ly a fol iar organ, whereas the other suggests that the carpel has a

two-parted, fol iar-shoot origin. Morphogenic data may be used to further test

these hypotheses, including data from studies of mutagenesis, analyses of

chimeras, and the m anipulat ion o f floral apices or primordia. Eac h of these areas

wil l be discussed in context of the carpel hypotheses. We real ize that develop-

mental data do not always direct ly reflect the evolut ion of st ructure, because

select ion for the developmental pathway may have occurred independently and

for separate funct ional efficiency (see discussion in Steeves et al . , 1991).

The understanding of f loral development in

A n t i r r h i n u m

and

A r a b i d o p s i s

has

been grea t ly enhanced by the use of mutagenesis ana lys i s (e .g . , Coen and

Meyerowitz, 1991). Many of these mutat ions affect the placement or the

structure of the carpel . These include mutat ions l ike ov u la ta , p l e n i f lo ra , and

d e f i c i e n s i n A n t i r r h i n u m

(e .g . , Carpenter and Coen, 1990), and

ape ta la ,

a g a m o u s , p i s ti l l a m , and pin in A r a b i d o p s i s (Bowman et al . , 1991; Goto et al . ,

1991). I t has been suggested that development of carpels in a whorl is under

the cont ro l o fpeni f lora

A n t i r r h i n u m ;

Carpenter and Coen , 1990) and

a g a m o u s

A r a b i d o p s i s ;

Bowman et al . , 1991). Other genes are also important for carpel

number such as

p i s t i l l a ta

(Hil l and Lord, 1989). Thus, the control of carpel


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28 Chap 6 The Origin and Evolution of the Angiosperm Carpel

development is beginning to be understood. Yet the relat ionship between the

gynoecial appendage and the placenta and ovules is less clear.

In several mutants, the resul t ing organs superficial ly look l ike open condup-

l icate carpels with marginal ly at tached ovules. However, further studies have

show n that these carpels are m osaic organs e .g . , Hil l and Lord, 1989; Bo wm an

et al., 1989; Irish and Sussex, 1990; Goto et al ., 1991; Bowman et al ., 1991;

Shannon and Meeks-Wagner , 1993) . Thus , a l though por t ions of these mosaic

carpels are frequent ly due to development of carpel t issues, other parts are due

to development of leaf, bract, or sepal t issues. The identification of the different

parts of the mosaic carpel is possible due to the existence of cel l types specific

to a single organ e.g. , Irish and Sussex, 1990). In addi t ion, al though the ovules

are marginal , the st igma is usual ly terminal , unl ike the marginal st igma pro-

posed to be ancestral in conduplicate carpels. These data suggest that open

carpels are a teratology and are not homologous with ancestral conduplicate

carpels.

In all , there do not yet appear to be any data that indicate what the ancestral

state is . However, some data suggest that carpels may be homologous with short

shoots consist ing of distal ly placed ovules on a determinate axis found in the

outgroups see also Hick ey and Taylor, Chapter 8). These m utagenesis studies

show that most f lowers are determinate and that the carpels are placed distal ly .

Flow ers wou ld then have a pseudanthial origin see discussion in Hick ey and

Taylor, Chapter 8) and be composed of reproduct ive axes with distal ly placed

female short-shoots, proximally placed male shoots, and steri le bracts basal ly

placed. In addi t ion, carpel and sepal development is ini t iated by a single gene,

unl ike the init iat ion of stamens and petals Co en and M eyerow itz, 1991). This

wo uld suggest that the basic type of f lower had bracts = sepals) and ovules

enclosed by bracts = carpels). The evolution of the bisexual f lower and petals

was secondary. This occurred with the addi t ion of a whorl of male shoots

stamens) proximal to the carpels, and petals proximal to the stamens and could

be due to the evolut ion of the class B mo difying genes Co en and Mey erow itz,

1991; Doyle, 1994). Final ly , some mutagenesis work examining inflorescence

genes shows that carpel wal ls can tight ly enclose the floral me ristem Sha nno n

and Meeks-Wagner, 1993), as is found in the scales and bracts of gnetopsids

and interseminal scales of bennet t i taleans. All these data suggest that at least

part of the flower may be homologous with the female short-shoots of the sister

groups.

A second area o f study uses chimeras to elucidate floral and carpel st ructure.

Dellaporta et al. 19 91 ) used clonal analysis to study the frui t developm ent in

Zea mays

They used the

Ac

transposon at the

Pericarp

locus as a method for

m arking the cel ls in the pericarps kerne ls). The gynoec ium of Z mays i s made

up of three carpels in which the single basal ly placed ovule is developmental ly

related to the carpel on the germinal face. The carpels are composed of two cel l


14/25


29

l a ye rs , L1 a nd L2 , a nd the e mbryo de ve lops f rom L2 . A l though the se da t a a re

in te res t ing f rom the point of v iew of the seques te r ing of ce l l l ineages for

reproduc t ion and of the ident i ty of the ce l l l ayers f rom which the embryo

deve lops , they provide l i t t l e informat ion on the ca rpe l -ovule re la t ionship . Al -

though the re c a n be t r a nspos i t i on e ve n t s t ha t ma rk t he ovu le on ly (A nde rson

and Brink, 1952; Del lapor ta e t a l . , 1991) , the examina t ion of kerne ls does not

a l low for the ident i f ica t ion of long ce l l - l ineages tha t s ta r t be fore the deve lop-

ment of the ca rpe l wal l s . There fore , f rom these s tudies i t i s not poss ib le to

de t e rmine w he the r t he ovu le de ve lops f rom the c a rpe l on t he ge rmina l f a c e o f

the gynoec ia l appendage or i f i t deve lops f rom a separa te growth a rea .

In t e rp re t a t i on o f c h ime ra s a nd ma n ipu la t i on o f f l o ra l a nd ovu le me r i s t e ms

ha ve be e n use d t o e luc ida t e t he f l o ra l de ve lopme nt o f me mbe rs o f t he

Solanaceae . Sa t ina and Blakes lee (1941, 1943; Sa t ina , 1944, 1945) s tudied the

de ve lopme nt o f c a rpe l s a s w e l l a s o the r o rga ns o f D a t u r a by e xa min ing c h ro -

m osom a l c h ime ra s . The y found tha t the f lo ra l m e r i s te m w a s c om pose d o f th re e

ce l l l ayers , L1, L2 and L3. They a l so found tha t these three ce l l l ayers

cont r ibuted to a l l the f lora l pa r t s of

D a t u r a

in a l l four whorl s (Sa t ina and

Blakes lee , 1941, 1943; Sa t ina 1944, 1945) .

D a t u r a

f lowers have b ica rpe l la te ovar ies wi th axi le p lacenta t ion , as do most

me mbe rs o f t he So la na c e a e . Th i s morpho logy i s mod i f i e d by t he e x i s t e nc e o f

a par t ia l fa l se -septum tha t d iv ides each p lacenta in to two par t s . The ca rpe ls a re

in i t ia l ly composed of two a rcs of ce l l s tha t l a te r deve lop in to the ca rpe l wal l s .

Be tw e e n the se tw o p r imord i a i s a s e pa ra t e r i dge f rom w hic h de ve lop t he

placenta , septum, and fa l se septum. This r idge i s th icker in the cente r and

carr ies on for a cons iderable t ime the func t ions of the f lora l ape x (Sa t ina an d

Blakes lee , 1943, p . 455) . As the ca rpe l wal l s and the r idge deve lop, the septum

and, la te r , fa l se septum become progress ive ly more connec ted to the wal l .

Chimera l da ta show tha t the ca rpe l wal l i s s imi la r in deve lopment to pe ta l s

and leaves (Sa t ina and Blakes lee , 1943) . The d i f fe rence i s tha t the ca rpe l wal l ,

except for the s ty le , i s pr imari ly composed of ce l l s der ived f rom the L3 as

opposed to most ly L2 in the pe ta l s . Ye t , ce l l s de r ived f rom the L2 predomina te

in the m a rg ina l r e g ions w he re t he c a rpe l w a l l me e t s t he se p tum. T he se c h im e ra l

da ta indica te tha t the ridge region is a l so m ost ly L3 der ived and tha t the

placenta l t i ssue i s deve loping independent ly of the septum and of the ca rpe l

w al l (Sa t ina and Blakes lee , 1943 p . 461 ) . From these observa t ions , the authors

concluded that the ent i re carpel is axi le in nature , yet the s tyle has s imilari t ies

to the pe ta l s (Sa t ina , 1944) .

The se D a t u r a da ta suppo r t the hyp othes i s adv anced in th i s chapte r . F irs t , two

type s o f p r imord i a fo rm, t he f i r s t p roduc ing t he tw o gynoe c i a l a ppe nda ge s

(carpe l wal l s ) and the o ther the p lacentae ( r idge) . Second, we infe r tha t the

produc t ion o f t i ssue s de r ive d f rom the L2 a long the ma rg ins o f t he c a rpe l w a l ls

and dis ta lly to prod uce the s ty le show s tha t the gyno ec ia l appen dages a re s imi la r


15/25


to leaf-derived organs. Thus, the gynoecial appendage is a sterile leaf. Finally,

the nature of the ridge is similar to a floral meristem and primari ly consists of

cel ls derived from the L3, the innermost layer. This would suggest an axi le

origin of these placentae.

Another member of the Solanaceae in which ch imera l p lan ts have been

examined is tobacco

Nicotiana;

Dermen, 1960; Burk et al . , 1964; Stewart and

Burk, 1970). Tobacco carpels are similar to those found in

Datura

except they

do not have a fa lse sep tum Hicks and Sussex , 1970; Fig 4A -C ). The ovary of

tobacco is bicarpel late Fig. 6 .4A ) and the septum com pletely separates the two

carpels Fig. 6 .4C ). Sandw ich chim eras in wh ich the L1 is green, the L2 is

white and the L3 is green show that the leaves and sepals are composed of al l

three layers, whereas the carpel wal l appears to be formed only from the L1

and L2, with the m egaspore s developing only from the L2 B urk et al. , 1964).

Similar resul ts have been found in

Pelargonium

Stewart et a l . , 1974).

Addit ional chimeral evidence for carpel development in Solanaceae has been

col lected from

Nicotiana

by our labora tory Fig . 6 .4D -F) . We implemented

clonal analysis on the flowers of tobacco, using the

A c -GUS

reporter system

see Kirchner et al . , 1993). To use the GUS bacterial gene as a marker system

to t race cel l l ineages in plants, i t is necessary to mark an occasional cel l . An

ideal method is to use t ransformed plants containing the GUS construct that has

a t ransposon inserted between the GU S gene and its prom oter Finn egan et al. ,

1989). This prevents enzyme expression unt i l the t ransposon randomly excises

from the DNA and a l lows the ce l l to make the GUS enzyme, which marks the

cell and all of i ts descendants.

In our prel iminary work, we have found pericl inal and mericl inal clones in

the L3. Thes e clones extend from the center of the receptacle Fig. 6 .4D ), into

the central part of the sepal lobes Fig. 6 .4D, top), a nd to the base of the petals .

In the last whorl , the clones extend into the nectaries, to the base of the carpel

walls Fig. 6 .4F), and into port ions of the placenta Fig. 6 .4E ) and central

port ion of the septum Fig. 6 .4F). They are not found where the septum

connects to the carpel wal l nor do they extend into the st igma and style. Our

data confirm previous work showing that the sepals have al l three layers,

whereas the carpel wal ls only have L1 and L2.

The phyl losporous-or ig in or megasporophyl l -homology hypothes is suggests

that the placenta develops from the carpel wal l . Because the clonal data shows

that the carpel wal l is composed of only the L1 and L2, the outermost layers,

the p lacenta would be expected to be composed o f the same layers Fig .

6.4G-I). On the other hand, i f the carpel is composed of two growth areas, the

carpe l wal l codd be composed of L1 and L2 layers , bu t the p lacentae could

have L3 in addit ion Fig . 6 .4J-L ) . O ur da ta de m o~ tra te tha t a ll th ree layers

are present in the placentae Fig. 6 .4E ) and the m iddle of the septum Fig. 6 .4F )

but that the L3 is missing from the carpel wal l . Again, these data support the


16/25

Chap. 6 The Origin and Evolution of the Angiosperm Carpel 131

B

=

, ~iiiiiiiiiii ilii~...... ~:iiiiiiiiiiiiiii iii ii~i~i ili~i iiiiiiiiiiiiii

Figure 6 .4 . Camera- lucida drawings (A -F ) and in terpre t ive drawings (G -L ) of to-

bacco ovaries Nicotiana tabacum). (A -C ) Camera- luc ida drawings of sec t ions through

tobacco carpels, including a cross section, a longitudinal section perpendicular to septum,

and a longitudinal sect ion through septum, respectively. (D-F) Sections of carpels with


17/25

32

C ha p 6 The Origin and Evolution of the Angiosperm Carpel

marked chim eral tissue in cross-hatching. D ) Cross section of a floral receptacle with

all organs removed except for a portion of calyx at to p. The chimeral tissue is found in

the innerm ost layer, the L3. Note that the clone extends into a sepa l lobe at top . E )

Slightly tangen tial, longitudinal sectio n perpendicular to the septu m . The marked cells

form a m ericlinal chimera and in the other half of the section the two m arked area s are

attached. F ) Slightly tangential, longitudinal section throug h the septu m . In places, the

locules are exposed, and to the righ t, the ovules are expo sed. The chimera extends into

the floral nectaries at the base of the carpe l walls. G-- L) Interpretations of the L1, L2

and L3 m akeup of the carp els based on competing hypotheses o f carpel origin. G--I)

Interpretation of the carpe l wall and placenta layer based on the phyllosporous origin o r

megasporophyll hom ology hypothesis. If the placentae are derived from the carp el walls,

they would be expected to consist of the sam e layers L1 and L2). J - L ) Interpretation

of the carp el and placenta based on the stachyosporous hypothesis. The placentae would

be s imilar to a shoot w ith up to thre e layers and would no t be restricted to the two layers

found in the carp el wa ll. The ch imer as found E , F ) are mo st similar to this interpreta-

tion. Note : The outermost lay er, the L1, is black, the m iddle layer, the L 2, is a dark

shade, and the innermost layer, the L3, is a light shade.

composi te na ture of the ca rpe l . The pe ta l s and the ca rpe l appear to be most ly

composed of L2--der ived ce l l s . In cont ras t , the p lacentae a re most ly composed

of L3 . A s i n Da tu ra the megaspore s t i l l deve lops f rom the L2, s ince the ovules

a re usua l ly c om pose d o f on ly L1 a nd L2 Bo um a n , 1984) . Thus , t he c a rpel

a ppe a rs t o be c ompose d o f a s t e r i l e gynoe c i a l -a ppe nda ge t ha t i s homologous

wi th a lea f- de r ived organ and a fe r t i l e p lacenta tha t i s s tem der ived.

Toba c c o f l ow e rs ha ve a l so be e n use d i n a numb e r o f e xc is ion s tud i es . H ic ks

a nd Sussex 1970 , 1971) c u l tu re d f lo ra l p r imord i a a nd spe c i fi c o rga n-p r imo rd i a

in vitro. The y use d t h i s sys t e m to s tudy o rga n re ge ne ra t i on a f t e r b i se c t i on o f

the f lowers a t d i f fe rent s tages . In some of these exper iments , s te r i le ca rpe ls

deve loped a f te r the b i sec t ion of the septum. A s ingle ha l f would deve lop a

com ple te ca rpe l wi th a ca rpe l wa l l inc lud ing s ty le and s t igm a) and p lacenta

whereas the o ther would deve lop only a s ty le and s t igma. Hicks and Sussex

sugges t tha t th i s was due to d i f f icul t ie s in cut t ing the ca rpe ls exac t ly a long the

septa . We sugges t , tha t th i s v iew i s compat ib le wi th the two-growth-a rea

hypothes i s . When the cut i s t angent ia l and para l le l to the septum, one of the

ha lves ge ts both the ca rpe l -wal l pr imordium and placenta l pr imordia . The o ther

ha l f get s on ly t he c a rpe l-w a l l p r imo rd ium a nd , t hus, de ve lops w i thou t p roduc ing

ovules.

F ina l ly , the importance of the L3 in regula t ing ca rpe l number has been

show n in So la na c e a e Sz y m kow ia k a nd Susse x , 1992) a nd o the r t a xa T i lne y-

Basse t t , 1986) . Th is sugges ts tha t the f lora l m er i s tem i s impo rtant in cont ro l l ing

c a rpe l de ve lopme nt be c a use t he L3 i s mi s s ing f rom the c a rpe l w a l l . H ow e ve r ,

t he se da t a do no t show w he the r o r no t t he c a rpe l i s c ompose d o f tw o g row th

areas.


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133

These morphogenic da ta provide tenta t ive support for the hypothes i s tha t the

carpe l or ig ina ted f rom the in tegra t ion of two growth a reas : the gynoec ia l

appendage and an axis wi th d i s ta l ly-placed ovules . Ye t because there have been

few s tudies , i t i s not ce r ta in tha t th i s type of deve lopment i s found in a l l

a ng iospe rms . N e ve r the l e s s , c a rpe l s o f t he So la na c e a e a ppe a r t o ha ve tw o

growth-areas . One deve lops in to the ca rpe l wal l , s ty le , and s t igma (gynoec ia l

appendage) , and the o ther deve lops in to the p lacentae and cent ra l por t ion of the

septum. These da ta do not suppor t the in te rpre ta t ion tha t axi l p lacenta t ion i s

due t o a c ondup l i c a t e c a rpe l i n w hic h t he ma rg ina l p l a c e n t a e ha ve be c ome

fused. In addi t ion , they do not suppor t the pe l ta te phyl losporous hypothes i s

e i ther , a s the p lacenta deve lops f rom the f lora l apex, not f rom the ce l l s of the

carpe l wal l . F ina l ly , some of the evidence does sugges t tha t the gynoec ia l

appendage has pe ta lo id charac te rs and, thus , could be brac t der ived.

E V O L U T I O N O F T H E C A R P E L

The e v ide nc e p re se n t e d a bove s t rong ly suppor t s t he tw o-grow th-a re a mode l o f

carpe l s t ruc ture . Ye t angiosperm carpe ls a re very d iverse in the i r form. In th i s

sec t ion , we w i l l begin wi th the hypo thes i s tha t the an ces t ra l ca rpe l was asc id ia te

wi th a basa l to s l ight ly late ra l p lacenta f ro m w hich deve lo ped o ne or two ovu les .

F rom th i s ba se t ype w e p ropose a n e xp la na t ion fo r w hy the re i s va r i a b i l i t y

a mong the c a rpe l s f rom d i f fe re n t t a xa a nd w ha t t he t r a ns fo rma t ions a re a mong

these types.

E v o l u t i o n o f C a r p e l a n d O v u l e V a r i ab i l i ty

To provide background for the ques t ion of why there i s ca rpe l var iabi l i ty ,

le t us review the probable s tages of ca rpe l evolut ion . The f i rs t s tage i s the

e nc los ing o f t he ovu le a x i s by a sub t e nd ing b ra c t A l though the ovu le ( s ) a re

a l ready enc losed by the sca les and par t ia l ly enc losed by brac ts in Gneta les and

Benne t t i t a les , the micropyle t ip s t i l l pro jec ts pas t the enc los ing organs , and

pol len lands d i rec t ly on the micropyle . The comple t ion of th i s s tage i s the

enc los ing of the ent i re ovule and the concurrent change to s t igmat ic depos i t ion

a nd ge rmina t ion o f t he po l l e n g ra ins . Thus , e nc losu re o f t he ovu le s w ou ld no t

ha ve be e n a s s i gn f i c a n t a s t he a ppe a ra nc e o f t he s t i gma . The a dva n ta ge s o f

s t i gma t i c ge rmina t ion ha ve be e n d i sc usse d by ma ny a u thors (e . g . , H e s lop-

Harr i son and Shivanna , 1977; Lloyd and Wel l s , 1992) . One advantage i s the

evolut ion of compat ib i l i ty sys tems to make for more e ff ic ient pol l ina t ion sys-

t e ms (e . g . , Be a c h a nd K re ss , 1980 ; Be rnha rd t a nd Th ie n , 1987) . A no the r

advantage to s t igmat ic germina t ion i s the poss ib i l i ty tha t sperm compet i t ion

may have increased se lec t ion aga ins t l e tha l recess ive mutants (Mulcahy, 1979;

Mulcahy e t a l . , 1992) .


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We suggest that the second stage of carpel evolut ion involved the direct ing

of the micropyle away from the st igmatic region. This would have increased

the length of the path that the pol len tube would have had to t ravel . Thus, the

diversi ty of ovule types may have to do with carpel evolut ion and st igmatic

germinat ion. Others have suggested that curved ovules have evolved to increase

contact to the transmission t issue, especial ly in mult iovulate st ructures End ress,

1990, 1994a; Lloyd and Wells , 1992). Yet , anatropous ovules curve away from

the closure where the st igma or t ransmission t issue is found, not toward i t , A

final possibi l i ty is that the ovules were directed away from the closure unt i l the

ful ly sealed state or st igma evolved, and later in evolut ion the ovule became

redirected at the transmission tissue.

The third stage wou ld have been the evolut ion o f novel carpel and pist il types

and the evolut ion of high ovule numbers. Numerous funct ional adapt ive possi-

bi l i t ies may have opened up to angiosperms once the ovulary axis was enclosed

by the gynoecial appendage and there was st igmatic germinat ion. This could

have al lowed the evolut ion of morphologies that would have increased the

number of ovules in each carpel , the number of carpels in each flower, and the

number of ovules in each inflorescence.

Ovule Evolution It is s tr iking that outgroups h ave orthotropous ovules; yet ,

in angiosperms, orthotropous ovules are relat ively rare and only weakly corre-

lated with ascidiate carpels and ovule numb ers of one or two Tay lor, 1991a).

In addi t ion, orthotropous ovules are variably placed in relat ion to the gynoecial

appendage. I f we start with the proposed ancestral carpel Fig. 6 .5A, C) an d

the ancestral orthotropous ovule Tay lor, 199 1a) we can propose three direc-

t ions in which these organs could have adapted to place the micropyle further

from the st igma and t ransmission t issue. One strategy would be a curved ovule

with the micropyle directed basaUy Fig. 6 .5I). A seco nd would be to mo ve the

orthotropous ovule to a mo re lateral or apical posi t ion Fig. 6 .5E ). A last

st rategy wo uld be a terminal st igm a Fig. 6 .5B ). Thus, selection for increased

micropyle-s t igma d is tance would resu l t in new carpe l forms as wel l as o ther

ovule types. These adaptat ions wil l be exam ined in the M agnoli idae sensu

Cronquist) below.

The carpel and ovule mo rphologies Tay lor, 1991a) provide considerable

evidence for adapta tions to increased m icropyle-s t igm a d is tances . W e exam ined

these data and looked at the associat ion among carpel types, placentat ion, and

ovule curvature. We note that the proposed ancestral carpel and orthotropous

ovule morphologies Fig. 6 .5A ) do not exist together in any l iving angiosperm.

There are no l iving taxa that have ascidiate carpels with a m arginal st igma, ba sal

placentat ion, and orthotropous ovules. The two fam il ies with carpels mo st similar

are Am borel laceae and Circaeasteraceae, and they have lateral , admedial ly placed

ovules, a l though the ovules in the lat ter fam ily are uni tegm ic.


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4~t 4,,,,,,,~

C

R z :

Figure 6.5. Diagramm atic representations of carpel types containing the two ma jor

types of ovules showin g their evolutionary relationships. The proposed ancestral types

ascidiate with basal to slightly lateral placentation are at top. Note that the carpels with

anatropous ovules or with ascoplicate or plicate morphology are inferred to be derived.

Dark arrows show initial evolution of morphologies having orthotropous ovules. Open

arrows show evolution of derived carpels with anatropous ovules.


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The re a re s e ve n fa mi l i e s t ha t ha ve me mbe rs w i th a sc id i a t e c a rpe l s w i th

margina l c losures and basa l to s l ight ly la te ra l p lacenta t ion [Annonaceae , Myr-

i s t icaceae , M onim iaceae som et im es apica l ) , I l l ic iaceae , Schizan draceae ,

Ra nu nc u la c e a e som e t ime s l a t era l ), a nd Be rbe r ida c e a e ]. Thre e o f t he se ha ve

m e m be rs w i th o the r c a rpe l t ype s a s w e l l A n nona c e a e , Monim ia c e a e , a nd

Ranunculaceae) . In a l l cases , the ovules a re curved to p lace the micropyle away

f rom the s t i gma a nd c losu re . Thus , A nnona c e a e ha ve a na t ropous t o c a mpylo t -

ropous ovu le s , Be rbe r ida c e a e ha ve he mia na t ropous t o a na t ropous ovu le s ,

Ra nu nc u la c e a e ha ve he m ia na t ropous e xc e p t w he n un i t e gmic ) , and t he re ma in -

der a re ana t ropous .

O the r fa mi l ie s ha ve m e m be rs w i th o r tho t ropous ov u le s bu t ha ve a va r ie ty o f

carpe l types and placements of the p lacenta . Al l have e i ther la te ra l or apica l

p l a c e me nt o f t he ovu le s Ch lo ra n tha c e a e , C e ra tophy l la c e a e , Sa uru ra c a e , La r -

dizaba laceae , and Barc laya ceae) . M ost of these ca rpe ls a re asc id ia te e .g . , F ig .

6 . 5 C , E) e xc e p t fo r some me mbe rs o f Sa uru ra c e a e a nd La rd i z a ba l a c e a e w hic h

are p l ica te e .g . , F ig . 6 .5G,H ). Taxa of Sau ruraceae hav e la te ra l , adm edia l ly

F ig . 6 . 5C) o r ma rg ina l l y p l a c e d ovu le s F ig . 6 . 5G ) , w he re a s t hose o f La r -

dizaba laceae can be p laced la te ra lly and m argina l ly F ig . 6 .5G ) or la te ra lly in

a chaot ic man ner F ig . 6 .5H). Ba rc layacea e have ovules in a la te ra l, radia l

a r ra nge m e nt F ig . 6 . 1M) . F ina l ly , Ch lo ra n tha c e a e a nd Ce ra tophy l l a c e a e se e

End ress , 199 4b) hav e the ovules a t tached a t the apex of the ca rpe l e .g . , F ig .

6 .5E) . Aga in , in every case , the micropyle i s d i rec ted away f rom the s t igma.

The l a s t sugge s t e d a da p ta t i on w ou ld be t he e vo lu t i on o f a t e rmina l s t i gma

in t he c ase s w he re t he re w a s a ba sa l o r tho t ropous ovu le F ig . 6 . 5B) . Th i s

condi t ion i s found in some Piperaceae . In fac t , the cyl indr ica l shape of the

carpe l , the te rmina l s t igmat ic region, and mul t ip le s t igmas in some spec ies have

led some to be l ieve tha t these f lowers have a syncarpous ovary . I t should be

obvious tha t syncarpy wi th d i s ta l s t igmat ic -surfaces would a l so increase the

d i s t a nc e be tw e e n the s t i gma a nd the mic ropy le a s i s found in Ca ne l l a c e a e ,

G omor t e ga c e a e , Sa uru ra c e a e , N ympha e a c e a e , Ba rc l a ya c e a e , Sa b i a c e a e ,

Pa pa ve ra c e a e , a nd Fuma r i a c e a e .

The re ma in ing me mbe rs f rom the fa mi l i e s o f t he Ma gno l i i da e ha ve c u rve d

ovules and nonbasa l p lacenta t ion . These ovules a re found in a var ie ty of la te ra l

a nd t e rmina l p l a c e me nt s F ig . 6 .5J --Q ) . M os t ha ve a na t ropous ovu le s w i th t he

e xc e p t ion o f Ca ne l l a c e a e , Ra nunc u la c e a e , Sa rge n todoxa c e a e , Me n i spe rma c e a e ,

and Sabiaceae . We sugges t tha t in these fami l ies both the ca rpe ls and the ovules

have been under se lec t ion , and the der ived s ta tes have evolved mul t ip le t imes .

I t appears tha t the loss of curva ture i s ra re , a l though i t may have occurred wi th

the c ha nge f rom b i t e gmic to un i te gm ic ovu le s e . g ., Ra nun c u la c e a e ) .

In summary, i t appears tha t adapta t ions for a grea te r d i s tance be tween the

mic ropy le a nd s t i gma m a y ha ve be e n fa c to r s i n the e vo lu t i on o f ne w ovu le a n d

c a rpe l c ha ra c t e r s i n a ng iospe rms . Th i s f a c to r ma y ha ve be e n su f f i c i e n t ly a da p-


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37

Sister Groups

ngiosperms

ancestral derived

m a n y f l o w e r s ,

1 o r 2 o v u l e s /

f lower

f e w f l o w e r s ,

m a n y ( > 7 )

c a r p e l s / f l o w e r ,

m a n y f lo w e rs , ' ~

1 o r 2

c a r p e l s ~ f l o w e r

1 o r 2 o v u l e s / c a r p e l

5

f e w f l o w e r s ,

1 o r 2 c a r p e l s / fl o w e r ,

m a n y ( > 7 ) o v u l e s / c a r p e l

Figu re 6.6. Diagram showing the strategies to increase the numb er of seeds, based on

the evolution of carp el and floral types. The ancestral condition for angiosperms is based

on the suggested homologies between the female structures of the sister groups, and

angiosperm flowers and inflorescences. Once the angiosperm carpel evolved, other stra-

tegies to righ t) were available to angiosperms that were not available to the sister group s.

t ive tha t ca rpe ls having our hypothes ized ances t ra l ca rpe l and ovule morpholo-

gies a re no longer found in l iv ing angiosperms.

I n c r e a s e d O v u l e N u m b e r s

The number of ovules and, thus , seeds i s re la -

t ive ly cons t ra ined in the gne tops ids and benne t t i t a leans F ig . 6 .3) . The nu m ber

of seeds i s l imi ted due to the number of ovules a t the t ips of the female shor t -

shoots and the num ber of female shor t -sho ots on a pr im ary axis F ig . 6 .6) . In

the s i s te r group, the re a re many shor t shoots , each usua l ly wi th a s ingle ovule ,

a l though the potent ia l for mul t ip le ovules i s found in the more d is tant outgroups

Fig . 6 .3) . One or two ovules i s sugges ted to be the ances t ra l condi t ion in

angio sperm s Fig . 6 .6) . The s ta tes in the outgrou ps sugges t tha t the ances tra l

a ng iospe rms ha d in f lo re sc e nc e s c on ta in ing ma ny f l ow e rs w i th one o r tw o

carpe ls pe r f lower and only one or two ovules per ca rpe l . Ye t the evolut ion of

the ca rpe l wi th s t igm at ic ge rm ina t ion a l low s for o ther adapta t ions for h igh ovu le

and seed numbers . One der ived s t ra tegy would be to have re la t ive ly few f lowers

wi th many ca rpe ls , each wi th one or two ovules per f lower . A re la ted s t ra tegy

w ould be fe w f low e rs w i th fe w c a rpe l s , bu t e a c h c a rpe l ha v ing ma ny ovu le s .

Obvious ly , combina t ions of these above s t ra tegies might be expec ted as wel l .

To t e s t t he se hypo the se s o f w he the r a ng iospe rms ha ve e vo lve d d i f fe re n t

s t ra tegies to inc rease ovule number , we col lec ted da ta on the number of ca rpe ls

per f lower Ta ylor , 199 1a) , the inf lorescence type , and numb er of f lowers per

in f lo re sc e nc e fo r e a c h fa mi ly o f t he M a gno l i i da e Cronq u i s t , 1981) . W e c on-


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138 Chap 6 The Origin and Evolution of the Angiosperm Carpel

s ide r e d the in f lo r e sc e nc e to ha ve f e w f lowe r s i f t he r e we r e one to f ou r pe r

in f lo r e sc e nc e a nd m a ny i f f ive o r g r e a te r . Fo r the c a r pe l num be r s pe r f lowe r

a nd ovu le num b e r s pe r c a r pe l, we c a te gor i z e d the m a s one o r two , f e w th r e e

to s ix ) a nd m a ny se ve n o r g r e a te r ). B e c a use the se da ta we r e ba se d on f a m i ly -

l e ve l c om pa r i sons , f a m i l i e s wi th g r e a t va r i a b i l i ty W in te r a c e a e , Ann ona c e a e ,

C a nne l l a c e a e , M onim ia c e a e , Ar i s to loc h ia c e a e , R a nunc u la c e a e , a nd

P a p a v e r a c e a e ) w e r e n o t in c l u d e d b e c a u s e w e c o u l d n o t m a t c h t h e c o m b i n a t i o n s

f rom the three charac te r is t ics .

M a n y f a m i l i e s f r o m t h e M a g n o l i i d a e h a v e m a n y f l o w e r s i n r a c e m o s e , s p i -

c a t e, o r c ym ose in f lo r e sc enc e s F ig . 6 .6 ) . I n the se fa m i l i e s , ne a r ly ha l f ha ve

f l o w e r s w i th o n e o r tw o c a r p e ls a n d w i t h o n e o r t w o o v u l e s p e r c a rp e l M y r -

i s t i c a c e a e , T r im e n ia c e a e , La ur a c e a e , He r na nd ia c e a e , C h lo r a n tha c e a e ,

P ipe r a c e a e , B e r be r ida c e a e , Sa b ia c e a e , a nd Fu m a r ia c e a e ) . A l l o f t he se fa m i l i e s

ha ve a sc id ia t e c a r pe ls , e xc ep t f o r B e r be r ida c e a e r a r e ly a sc op l i c a t e ) a nd

Fum a r ia c e a e p l i c a t e ) . Abo u t a qua r t e r ha ve m e m be r s wi th th r e e to s ix c a r pe l s

c o n t a i n i n g o n e o r t w o o v u l e s p e r c a r p el A m b o r e l l a c e ae , G o m o r t e g a c e a e,

P ipe r a c e a e , M e n i spe r m a c e a e , a nd C or ia r i a c e a e ) a nd c a r pe l s wi th a sc id ia t e m or -

pho logy . I n som e c a se s , t he ova r i e s a r e sync a r pous . The r e m a in ing t a xa ha ve a

va r i e ty o f c a r pe l t ype s m os t ly p l i c a t e ) a nd va r ia b le c a rpe l a nd ovu le num be r .

T h u s , t h e m o s t c o m m o n t y p e o f f e m a l e r e p r o d u c t i v e s t r u c t u r e i s a m a n y

f lowe r e d in f lo r e sc e nc e w i th one o r two c a r pe l s pe r f lowe r a nd one o r two ovu le s

pe r c a r pe l . Th i s i s t he c ond i t ion tha t we hypo the s i z e d a s a nc e s t r a l by our

o u t g r o u p c o m p a r i s o n F i g . 6 . 6 ).

A sm a l l e r num be r o f f a m i l i e s ha ve f e w f lowe r s upon a n in f lo r e sc e nc e . I n the

f lowe r s o f the se f a m i l i e s , a bou t ha l f ha ve se ve n o r a g r e a te r num be r o f c a r pe l s

w i t h o n l y o n e o r t w o o v u l e s H i m a n t a n d r a c e a e , E u p o m a t i a c e a e , M a g n o l i a c e a e ,

C a lyc a n tha c e a e , l l l i c i a c e a e , Sc h iz a ndr a c e a e , Ne lum bona c e a e , C a bom ba c e a e ,

a nd C i r c a e a s t e r a c e a e ) . A l l o f t he se f a m i l i e s e xc e p t f o r C a lyc a n tha c e a e ha ve

a sc id ia t e c a r pe l s . One - se ve n th o f the f a m i l i e s ha d m e m be r s wi th one o r two

c a r pe l s c on ta in ing one o r one ovu le s I d iospe r m a c e a e , C e r a toph y l l a c e a e , a nd

B e r be r ida c e a e ) . Exc e p t f o r B e r be r ida c e a e , wh ic h a r e oc c a s iona l ly a sc op l i c a t e ,

th i s g r oup a l so ha s a sc id ia t e c a r pe l s . Thus , t he s t r a t e gy o f low f lo r a l - num be r

a nd h igh c a r pe l -num be r wi th one o r two c a r pe l s is a l so f ound F ig . 6 .6 ) a nd ,

we wou ld sugge s t , i s de r ive d .

Ano the r a da p t ive s t r a t e gy f o r m a gno l i id s wi th f e w f lowe r s i s f e we r c a r pe l s

pe r f low e r wi th m o r e ovu le s F ig . 6 .6 ) . Th i s i s r a r er in ba sa l a ng iospe r m s a nd

i s f o u n d i n D e g e n e r i a c e a e a n d s o m e m e m b e r s o f W i n t e r a c e a e , A n n o n a c e a e ,

C a ne l l a c e a e , a nd A r i s to loc h ia c e a e . A l l o f t he t a xa wi th th i s s t ra t e gy ha ve p l i c a t e

c a r p e l s . T h e r e m a i n i n g f a m i l i e s h a v e m e m b e r s w i t h v a r i o u s c o m b i n a t i o n s o f

c a r pe l t ype s wi th the m a jo r i ty be ing p l i c a t e ) a nd num be r s o f c a r pe l s a nd

ovu le s . A r e l a t e d s t r a t e gy i s t he de ve lopm e nt o f sync a r pous ova r i e s , a s the se

c a n ha ve f e w c a r pe l s tha t c a n ha ve m a ny ovu le s . Th i s s t r a t e gy o f f e w f lowe r s


24/25


139

with few carpels but with high ovule numbers is rare and we suggest i t is also

derived.

In summary, i t appears that angiosperms have used three adapt ive st rategies

to control seed number. The most common strategy is similar to that found in

the sister groups with a high number of f lowers on an inflorescence, each of

which contains a few carpels and ovules. Another st rategy is to decrease the

number of flowers bu t increase the num ber of carpe ls wi th one or two ovules)

in each flower. This st rategy is most frequent ly found in famil ies with low

num bers o f f lowers. In both o f these st rategies, the carpels are usu al ly ascidiate .

In other combinat ions where ovule numbers increase, other carpel morphologies

are found, including ascoplicate and plicate. Thus, we suggest that adaptation

for ovule number has resul ted in mult iple originat ions of these derived carpel

types and related lateral placentation types.

T r a n s f o r m a t i o n s A m o n g C a r p e l S t a t e s

The evolution of carpel diversity appears to be due, in part, to selection for

posi t ioning the micropyle away from the st igma and for increasing or maintain-

ing high ovule numbers. Both of these adaptat ions are possible with the advent

of st igmatic germinat ion. The t ransformations among the various carpel types

are possible through the integrat ion of the two growth areas that produce the

gynoecial appendage and the placenta.

Based on our analyses, the ancestral carpel was ascidiate and had one or two

ovules. Furthermore, the outgroup homologies suggest that i t had basal to

sl ight ly lateral placentat ion and that the ovule was orthotropous Fig. 6 .5A, C ).

From this ancestral morphology, select ion for increased pol len-tube growth

posi t ioned the micropyle away from the st igma. This was accomplished by

evolving an anatropous ovule Fig. 6 .5I), with a lateral to apical placemen t

Fig . 6 .5E) or by m eans of a te rminal s tigma Fig . 6 .5B). M ost o f the remain ing

stages in the evolut ion of carpel types were probably related to increasing the

num ber of ovules per carpel e .g . , Fig. 6 .5, C to F to G, and J to M to N ) and

formation of terminal st igmas e.g. , Fig. 6 .5, J to L). O ur mode l suggests that

curved ovules, part icularly anatropous ones, have evolved m ult iple t imes e.g. ,

Fig. 6.5, A to I, D to O, E to L, and C to J). As cop licate e.g., Fig. 6.5, C to

F, J to M, and O to Q) an d plicate carpels Fig. 6 .5, F to G, M to N, and Q to

R) also appear to have mult iple origins.

C O N C L U S I O N S

Growing evidence from character analysis , phylogenet ic analyses, outgroup

comparison, and morphogenic analysis supports the stachyosporous-origin hy-


25/25

140 C ha p 6 The Origin and Evolution of the Angiospe rm Carpel

pothesis . Our analysis indicates that the gynoecial appendage of the carpel is

hom ologous with the bracts subtending the female short-shoot ovular axis) in

the outgroups. The placenta within the carpel is homologous to the female

short-shoot i tself. Our data consistently support the hypothesis that the ancestral

carpel morphology is ascidiate with a marginal st igma and basal to sl ight ly

lateral placentat ion of one or two orthotropous ovules. Transformations to other

carpel types are l ikely to be a resul t of the integrat ion of the primordia

producing the gynoecial appendage and the carpel wal l , with the placental

growth area. We suggest that the evolut ion of curved ovules and the placement

of the ovules in other posi t ions was to direct the micropyle away from the

st igma or pol len-tube t ransmission-t issue. Based on outgroup comparison, we

suggest that reproduct ive axes with many flowers, few carpels per f lower, and

few ovules per carpel were ancestral . From these evolved two types of inflor-

escences: one wi th few f lowers each of which had m any carpe ls and few ovules

and the other with few flowers each containing few carpels and many ovules.

A C K N O W L E D G M E N T S

The authors thank the reviewers for their insightful comments. We also thank

our research assistants, Carla Kinslow, Greg Bloom, and Gaff Emmert for their

di l igent work on the tobacco research. Final ly , we thank J. H. Zhou for the

transgenic tobacco seeds. This research was supported by grants from the

M cCul lough Fund and the Off ice of Academ ic Affa i rs , Ind iana Univers i ty

Southeast.

[doi 10.1007%2f978!0!585-23095-5_6] taylor, david winship; hickey, leo j. -- flowering plant origin,...

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