T h e o r . A p p l . G e n e t . 50, 89-101 (1977)

9 by Springer-Verlag 1977

Evolution of Incompatibility Systems in Plants: Complementarity and the Mating Locus in Flowering Plants and Fungi K. K. P andey Genetics Unit, Grasslands

Division,

D.S.I.R.,

Palmerston

North

(New

Zealand)

Summary. The restriction of sexual pairing by a specificity gene is considered to be an ancient development in the plant kingdom. The diversity and general parallelism of incompatibility systems seen amongst the phyla at the present time can be rationalized in terms of the association of various derived forms of the ancestral specificity unit with differing spectra of accessory factors controlling sexual physiology in the different phyla. Sexual morphogenesis has become divided into distinct phases under the control of complementary genes. These phases are initiated by a regulatory system of "Co-ordinator genes" which control the order in which groups of morphogenetic genes are expressed during development. The entire sexual cycle will be completed only if all the complementary groups are activated in the appropriate sequence. The present article discusses essential features of the evolution of the breeding locus in different phyla. These features are consistent in themselves with the present data and are not dependent on the proposed ancient origin of the specificity gene. The above hypothesis throws light on the (I) evolution of the complex mating loci in flowering plants and fungi ; (2) evolution of complementary incompatibility and heteromorphic incompatibility in flowering plants; (3) anomalous cross-compatibility behaviour of mutants in the fungus Schizophyll~ co~ne; (4) nature of homothallism in higher fungi; (5) mode of origin of new functional self-incompatibility alleles ; and (6) "homogenic" and "heterogenic" incompatibility. Key

words:

Incompatibility

- Evolution

- Flowering

Plants - Fungi

Introduction

- Complementarity

The widely occurring "homogenic" incompatibility (Esser 1959) prevents the fusion of gametes carry-

There

are two basic components

of eukaryotes:

meiosis,

and karyogamy,

to the sexual cycle

giving rise to haploid cells ;

recreating

the diploid state by fusion

of haploid sexual nuclei. To achieve karyogamy haploid participants contact,

must

be brought

the

of "Donor"

and "Recipient"

physio-

fogies, usually leading to sexual morphogenesis. completion

of the sexual process phases

complementarity

of the donor and recipient.

complementarity haploid gametes phase

whose

cess.

For

is based on physiological

logical interaction between

the diploid somatic gametophyte

The requirement

as sexual complementarity fungi where

with the sexual pro-

in higher plants there is a physio-

the style and the haploid male

vegetative fusion occurs

ion of g a m e t e s .

cells of

bearing the

for vegetative as well

is even more

marked

prevent unsuitably matched individuals from complettegrated with the genes controlling other aspects of donor and recipient sexuality. The following discussion

will develop the theme

that the evolution of a specificity gene to restrict

kingdom.

involves not only the two combining

function is connected

factors in higher fungi. This system has evolved to

sexual pairing is an ancient development

This

but also all cells of the vegetative

example,

actual gametes.

The

including pre- and

post-conjugation

such as the S locus in higher plants and the A and B

ing the sexual cycle, and has become thoroughly in-

into effective

and this has been facilitated in evolution by

the development

ing identical alleles at a particular genetic locus,

in the

in addition to un-

The diversity of incompatibility

seen amongst

in the plant systems

the phyla of the present day can be ra-

tionalised in terms

of primary,

secondary

or tertiary

developments

based ultimately on the association

one ancestral

specificity gene with differing spectra

of accessory

factors governing

sexual reproduction major

theme

of

the various aspects of

in the different phyla. The second

of the discussion,

not necessarily

de-

pendent upon the first, will be the concept of complementation

- genetic,

necessitated

physiological

by the harmonizing

and morphological-

requirements

of the

90

T h e o r . A p p l . G e n e t . 50 (1977)

Table 1. Comparative incompatibility s y s t e m s in angiosperms and fungi Genetic systems

Angiosperms

Fungi

(1) One l o cu s with two a l l e l e s

Primula, Linum, Pulmonaria, Fagopyrum, Forsythia.

U s t i l a g i n a l e s and U r e d i n a l e s ( " C o n i o m y c e t e s " - Whitehouse

(2) One locus with multiple alleles

A l a r g e n u m b e r of g a m e t o p h y t i c and s p o r o p h y t i c s p e c i e s .

H y m e n o m y c e t e s ( R a p e r 1960).

(3) One locus with multiple alleles and second locus with two alleles

So lanum pinnatisectum, S. ehrenbergii.

Ustilago seae ( Ustilaginales ) (Rowell and De Vay 1954; Rowell 1955).

(4) Two loci with two alleles each

Lythrum, Oxalis.

1951).

( C o n s i d e r e d u n l i k e l y on t h e o r e t i c a l g r o u n d s - M a t h e r 1942; W h i t e h o u s e 1949, 1951). (5) Two loci e a c h with m u l t i p l e alleles

Physalis ixocarpa.

(6) Two loci e a c h with m u l t i p l e a l l e l e s and i n t e r l o c u s complementation

Gramineae.

B a s i d i o m y c e t e s ( E s s e r 1967).

(7) T h r e e o r m o r e l o c i e a c h with m u l t i p l e a l l e l e s and i n t e r l o cu s c o m p l e m e n t a t i o n

Ranunculus acris, Beta vulgaris.

Psathyrella coprobia

(Basidiomycetes) ( J u r a n d and K e m p 1973).

Donor and Recipient components of the system. Sexual

l e l e to a n o t h e r h a v e not been o b s e r v e d in e i t h e r g r o u p ,

morphogenesis has become divided into distinct phas-

and a r t i f i c i a l m u t a g e n e s i s r e s u l t s only in l o s s of f u n c -

es under the control of complementary genes. The en-

t i o n . In addition c e r t a i n of t h e s e s y s t e m s , s u c h as the

tire sexual cycle can only be completed if all of these

h o m o m o r p h i c s i n g l e l o c u s g a m e t o p h y t i c s y s t e m in

complementary groups are activated in the appropriate

h i g h e r p l a n t s and t h e b i f a c t o r i a l s y s t e m of the h i g h e r

sequence. It will be shown that the specificity elements

b a s i d i o m y c e t e s , show a s i m i l a r i t y in t h e i r p o t e n t i a l

themselves may have a part to play in the regulation of

d i v e r s i t y of i n c o m p a t i b i l i t y p h e n o t y p e s . In both phyla

this complementary activation process.

the s p e c i f i c i t y u n i t s a r e b e l i e v e d to act as " s w i t c h e s " f o r l i n k e d g r o u p s of g e n e s c o n t r o l l i n g a s p e c t s of s e x ual p h y s i o l o g y . A l s o in both g r o u p s s p e c i f i c i t y units

Comparative Incompatibility Systems T h e r e is a g e n e r a l p a r a l l e l i s m a m o n g h o m o g e n i c i n c o m p a t i b i l i t y s y s t e m s w h e r e v e r they a r e found in the

within a c o m p l e x f a c t o r a r e a l w a y s c o m p l e m e n t a r y in f u n ct i o n . In c o n t r a s t to t h e ab o v e p a r a l l e l s the h i g h e r

plant k i n g d o m . F o r e x a m p l e , m a n y s i m i l a r s y s t e m s

p l a n t s and fungi show a n u m b e r of d i v e r g e n t p r o p e r -

o c c u r a m o n g the a n g i o s p e r m s and fungi (Table 1 ).

t i e s which a r e thought to r e s u l t f r o m the c o m b i n a t i o n

This g e n e r a l p a r a l l e l i s m has l e d to th e s u g g e s t i o n

of the a n c e s t r a l s p e c i f i c i t y unit with d i f f e r i n g s p e c t r a

that all s u c h s y s t e m s a r e m a n i f e s t a t i o n s of a s i n g l e

of a u x i l i a r y s e x u a l f a c t o r s , and the s u b j e c t i o n of the

p r i m e v a l s p e c i f i c i t y e l e m e n t which has g r o w n in c o m -

r e s u l t i n g g e n e c o m p l e x e s to d i f f e r e n t e v o l u t i o n a r y r e -

p l e x i t y and has b e c o m e i n t e g r a t e d with a g r e a t v a r i e -

s t r u c t u r i n g and s e l e c t i o n p r e s s u r e s .

ty of g e n e s c o n t r o l l i n g d i f f e r e n t a s p e c t s of s e x u a l p h y s -

e x a m p l e , p r i m i t i v e i n c o m p a t i b i l i t y i s b e l i e v e d to be

In the fungi, f o r

i o l o g y but which r e t a i n s c e r t a i n b a s i c p r o p e r t i e s by

r e p r e s e n t e d by a s i n g l e f a c t o r w i t h t w o a l l e l e s as s e e n

which it can be i d e n t i f i e d in the v a r i o u s p h y l a ( P a n -

in the l o w e r fungi ( W h i t e h o u s e 1951) (Table 1; 1) . In

dey 1 9 6 9 c). In addition to this p a r a l l e l i s m in g r o s s o r -

t h e h i g h e r p l a n t s , h o w e v e r , the h o m o m o r p h i c g a i n -

ganisation, flowering plants and fungi show certain

e t o p h y t i c s y s t e m with a s i n g l e m u l t i a l l e l i c l o c u s i s

other parallel features which may represent the in-

considered p r i m i t i v e . Also, relationships between

trinsic properties of a common ancestral specificity

s e p a r a t e f a c t o r s a r e a l w a y s c o m p l e m e n t a r y in the

gene. For example, mutations from one functional al-

fungi but m ay be c o m p l e m e n t a r y o r i n d ep en de nt in

K . K . P a n d e y : E v o l u t i o n of I n c o m p a t i b i l i t y S y s t e m s in P l a n t s

91

h i g h e r p l a n t s . This p r o p e r t y and the g r e a t e r p l a s t i c i -

Primeval specificity element

Accessory sexual elements

ty of fungal i n c o m p a t i b i l i t y s y s t e m s , i . e . the g r e a t e r ~VVV~

r e l a t i v e e a s e with which o n e - f a c t o r and t w o - f a c t o r

0

S~tia,conv~e~

,

/

s y s t e m s a p p e a r to be i n t e r c o n v e r t i b l e (Koltin, S t a m b e r g and Lemke 1972), a r e thought to r e s u l t f r o m a v e r y e a r l y i n t r o d u c t i o n of i n t e r u n i t functional c o m p l e -

|

~VVV~

Ex Situ duplication

andmutation

~ ......... ~

1

m e n t a r i t y in the h i g h e r fungi. In the evolution of g a m etophytic i n c o m p a t i b i l i t y in f l o w e r i n g p l a n t s , w h e r e

i Spatial convergence

s t y l e , the r e q u i r e d s e l e c t i o n for i n d e p e n d e n t a c t i o n of

I

I

l

t//

(~) / V V V V ~

the r e a c t i o n o c c u r s b e t w e e n haploid pollen and diploid

i

~

(~

J}

'

.~I" .....

'

In situ duplications and mutations

Ex situ duplications and

"'~

mutations

a l l e l e s in the s t y l e m e a n t that c o m p l e m e n t a r i t y b e -

l

~ e e

13

;,

6

"",,

,

tween s e p a r a t e f a c t o r s was only i n t r o d u c e d l a t e a s a s e c o n d a r y d e v e l o p m e n t to r e s t o r e s e l f - i n c o m p a t i b i l i tVVV ~

@

ty u n d e r s p e c i a l c o n d i t i o n s ( P a n d e y 1976b). In the

~

, p

,

~

,~ , o

'

,

~convergence

,

I

,

fungi, h o w e v e r , w h e r e h a p l o i d - h a p l o i d i n t e r a c t i o n d e S p l i t by ~ translocation ~

t e r m i n e s i n c o m p a t i b i l i t y , s e l e c t i o n for independent a c -

~-~ / ~ A A A A _ (~ ~" " " " " "

,

1~

i ~ , o t Partial or full

tion of a l l e l e s has not b e e n a b a s i c r e q u i r e m e n t , and t h e r e f o r e c o m p l e m e n t a r y s y s t e m s could have evolved Two or more complex loci

e a r l y . Differing s p e c t r a of a u x i l i a r y g e n e s a s s o c i a t e d with the b a s i c s p e c i f i c i t y u n i t s may also a c c o u n t for Specificity elements

d i f f e r e n c e s in o b s e r v e d m u t a t i o n r a t e s and t y p e s of m u t a t i o n a s s o c i a t e d with i n c o m p a t i b i l i t y f a c t o r s .

~/VM

Associated processes

As a unifying h y p o t h e s i s for the d e r i v a t i o n of c o m plex i n c o m p a t i b i l i t y s y s t e m s , the b a s i c e v o l u t i o n a r y

,

c h a n g e s in a r c h i t e c t u r e of the p r i m e v a l s y s t e m a r e

genes concerned

Possible stages in evolution, fungal systems

with various particularly

sexual in

Alternative processes which may have occurred more frequently in specificity elements

v i s u a l i s e d as : (1) C o n v e r g e n c e ( i n c r e a s i n g l y tight l i n k a g e ) with o t h e r g e n e s c o n t r o l l i n g p h y s i o l o g i c a l and m o r p h o l o g i cal a s p e c t s of s e x e x p r e s s i o n to give a c o m p l e x locus ( M a t h e r and De Winton 1941; M a t h e r 1950; E s s e r and S t r a u b 1956, 1958; R a p e r and F l e x e r 1970). (2) P a r t i a l o r full d u p l i c a t i o n of the c o m p l e x e l s e w h e r e i n the g e n o m e often l e a d i n g to functional b r e a k down of the s y s t e m .

Fig. I. Diagrammatic representation of the conceptual processes involved in evolution of complex incompatibility systems (1) Breeding system gene complex with two or a few specificity alleles. (2) Duplication breaks down incompatibility and is followed by selection for independent action and finally for co-operation of c~ and _~_ to give a single specificity. Spatial convergence of separate co-operating units will be favoured. (3) Two-factor multiallelic complementary system. (4) One-factor multiallelic system with subunits co-operating to produce a single specificity. (5) Two or more complex loci

(3) R e s t r u c t u r i n g of d u p l i c a t e d c o m p l e x e s to r e s t o r e efficient b r e e d i n g b e h a v i o u r ; e . g . by s e l e c t i o n for i n d e p e n d e n t a c t i o n and s u b s e q u e n t l y for c o - o p e r a -

tionary changes

tive p r o d u c t i o n of a s i n g l e functional s p e c i f i c i t y by

val gene. Splitting of such a locus into two or three

the d u p l i c a t e d l o c i .

groups

(4) F u r t h e r c y c l e s of c o n v e r g e n c e , d u p l i c a t i o n

Basidiomycetes.

F i g u r e 1 i l l u s t r a t e s the c o n c e p t s e m b o d i e d in the broad evolutionary

complementary multi-unit,

of linked complementary

duce a multifactorial

and r e s t r u c t u r i n g . above

hypothesis.

factors would,

Convergence

in effect, produce

potentially multiallelic,

complex

similar to those acting on the prime-

of a

locus

to be operating

system

factors would proof the type seen in higher

Similar basic processes

for both the higher plants and the fungi.

The evolution of sex in eukaryotes the development Three

major

are believed

of a process

evolutionary

also involved

of nuclear

migration.

phase s can be distinguished:

with a single functional specificity. This locus in turn

(1) cell fusion accompanied

by nuclear

would be affected by further combinations

otic algae and lower fungi);

(2) cell fusion accompa-

of evolu-

fusion (eukary-

92

Theor. Appl. G e n e t . 50 (1977)

S~.l..~

mP..-poir.~o.m,o.i-poiii..u~.m

Stylor I ~ t (RecipTent)

9

-~