GENETIC CONTROL OF DWARF MISTLETOE-17
Lewis F. ~ o t &
ABSTRACT
T r e e s i n n a t u r a l ecosystems i n t h e c o u r s e of t h e i r e v o l u t i o n have a c q u i r e d
l e s s r e s i s t a n c e t o dwarf m i s t l e t o e s t h a n t o many o t h e r n a t i v e d i s e a s e s .
N e v e r t h e l e s s t r e e s d o r e s i s t m i s t l e t o e by: 1 ) taxonomic r e s i s t a n c e , a s a
consequence o f e v o l u t i o n , 2 ) s i n g l e gene, v e r t i c a l r e s i s t a n c e , 3 ) p o l y g e n i c
h o r i z o n t a l r e s i s t a n c e and 4 ) e s c a p e by means of h e r i t a b l e s t r u c t u r a l
characteristics.
S i l v i c u l t u r a l c o n t r o l b y change of s p e c i e s i s based on
taxonomic r e s i s t a n c e . P r a c t i c e s i n c l u d e : s e l e c t i v e t r e a t m e n t i n mixed s t a n d s ,
s p e c i a l r e g e n e r a t i o n p r o c e d u r e s , u n d e r p l a n t i n g of s h e l t e r w o o d s , o r
e s t a b l i s h m e n t of non-host b a r r i e r s t o s p r e a d . I n t h e a b s e n c e of v e r t i c a l
r e s i s t a n c e s i l v i c u l t u r a l c o n t r o l o f t e n i s a c h i e v e d a t t h e p r i c e of reduced
p r o d u c t i v i t y . The s i l v i c u l t u r a l o b j e c t i v e s c a n b e met t o a d e g r e e by h o r i z o n t a l
resistance.
E x i s t i n g h o r i z o n t a l r e s i s t a n c e c a n be f u r t h e r s t r e n g t h e n e d by
s i l v i c u l t u r a l improvement of i n f e c t e d s t a n d s .
Consequently g e n e t i c c o n t r o l of
dwarf m i s t l e t o e i s immediately a v a i l a b l e .
G e n e t i c a l l y based r e s i s t a n c e t o i n f e c t i o n
r e s u l t i n g from cc-evolution of f o r e s t t r e e s
and t h e i r pathogens h a s been t h e c h i e f means
o f d i s e a s e c o n t r o l i n n a t u r a l ecosystems (Van
d e r P l a n k 1975). S e r i o u s d i s e a s e o u t b r e a k s
a r e a b s e n t from t h e f o r e s t e x c e p t when t h e
environment f l u c t u a t e s w i d e l y o r i s
a r t i f i c a l l y modified; o r when i n t r o d u c t i o n of
e i t h e r f o r e i g n h o s t s o r pathogens o c c u r s .
C o n t r a r i l y , t h e n a t i v e dwarf m i s t l e t o e s a r e
regularly destructive i n natural forests.
Consequently t h e y a r e p r o p e r l y r e g a r d e d a s
e x c e p t i o n s . However, t h e i r dominance o v e r
t h e i r h o s t s i s o n l y p a r t i a l and g e n e t i c
resistance is a potential tool for their
c o n t r o l . It i s a p p r o p r i a t e t h e r e f o r e t o a s k
why s o l i t t l e a t t e n t i o n h a s been g i v e n t o
g e n e t i c c o n t r o l and t o c o n s i d e r f u t u r e
prospects.
G e n e t i c a l l y b a s e d f e a t u r e s have been
used by f o r e s t managers, f o r c o n t r o l o f dwarf
m i s t l e t o e f a r more e x t e n s i v e l y t h a n i s
generally realized.
At t h e same t i m e g e n e t i c
r e s i s t a n c e h a s been i n a d v e r t e n t l y , i f n o t
i n t e n t i o n a l l y , i g n o r e d i n t r e e improvement
programs.
The a s s u m p t i o n used t o j u s t i f y t h i s
Ñ'presente
a t t h e Symposium on Dwarf M i s t l e t o e C o n t r o l Through F o r e s t Management, Berkel e y , C a l i f . A p r i l 11-13, 1978.
-"professor
of Botany and P l a n t P a t h o l o g y ,
Oregon S t a t e U n i v e r s i t y , C o r v a l l i s , Oregon
97331.
omission h a s been t h a t t h e whole m i s t l e t o e
c o n t r o l r e q u i r e m e n t c a n b e e x p e d i t i o u s l y met
by s i l v i c u l t u r a l t r e a t m e n t .
Although s i l v i c u l t u r a l methods a r e l i k e l y
t o dominate t h e c o n t r o l e f f o r t i t w i l l b e w e l l
t o examine our s i l v i c u l t u r a l p r a c t i c e s more
a n a l y t i c a l l y and t o broaden o u r c o n c e p t of
genetic control a s these p r a c t i c e s concern
management of t h e dwarf m i s t l e t o e problem.
T r e e s r e s i s t damage by dwarf m i s t l e t o e i n
f o u r g e n e t i c a l l y r e l a t e d ways:
1 ) by immunity
accompanying c o - e v o l u t i o n of t h e P i n a c e a e and
Arceuthobium d u r i n g , p e r h a p s , t h e l a s t 20
m i l l i o n y e a r s , 2 ) by v e r t i c a l r e s i s t a n c e
(possession of s p e c i f i c r e s i s t a n t genes t h a t
match m i s t l e t o e g e n e s f o r p a t h o g e n e s i s ) (Van
d e r P l a n k 1975), 3 ) by h o r i z o n t a l r e s i s t a n c e
( p o s s e s s i o n of p o l y g e n i c a l l y r e g u l a t e d f a c t o r s
which i n t h e a g g r e g a t e s u p p r e s s i n f e c t i o n and
l i m i t d i s e a s e (Robinson 1976) and 4 ) by
d i s e a s e e s c a p e based on h e r i t a b l e c h a r a c t e r s .
I n s p i t e of i t s g r e a t p o t e n t i a l , v e r t i c a l
r e s i s t a n c e i s o u r l e a s t used g e n e t i c t o o l .
T h i s i s p a r t l y b e c a u s e of c h a l l e n g i n g
technical d i f f i c u l t i e s , including the
n e c e s s a r y p a i n f u l l y slow c o n v e n t i o n a l b r e e d i n g
methods t h a t have d i s c o u r a g e d i t s development.
It i s u n f o r t u n a t e t h a t t h e h i s t o r i c a l
dominance of s i n g l e gene ( v e r t i c a l ) r e s i s t a n c e
i n t h e t h i n k i n g of f o r e s t s c i e n t i s t s s h o u l d ,
f o r s o l o n g , have obscured o t h e r o p p o r t u n i t i e s
f o r m i s t l e t o e c o n t r o l by g e n e t i c means.
Immunity t o p l a n t d i s e a s e i s r e g a r d e d by
some (Robinson 1976) t o b e t h e r u l e r a t h e r
t h a n t h e e x c e p t i o n . The form of immunity most
o f t e n encountered by t h e dwarf m i s t l e t o e s h a s
developed d u r i n g t h e c o u r s e of e v o l u t i o n
accompanying h o s t s p e c i a t i o n (Hawksworth and
Weins 1972). It i s expressed i n t h e i n a b i l i t y
of one m i s t l e t o e ,
d o u g l a s i i Engelm. on
Douglas-fir f o r example, t o a t t a c k a n o t h e r
c o n i f e r s u c h a s ponderosa p i n e , when t h e two
t r e e s grow t o g e t h e r i n a mixed s t a n d . Host
immunity t o t h e dwarf m i s t l e t o e s i s n o t
absolute.
One t r e e s p e c i e s o c c a s i o n a l l y may be
p a r a s i t i z e d by a m i s t l e t o e having a n o t h e r t r e e
s p e c i e s a s i t s p r i n c i p a l h o s t . Thus secondary
h o s t s occur which, though i n f e c t e d , u s u a l l y
cannot alone s u s t a i n t h e mistletoe population.
Larch m i s t l e t o e (A. l a r i c i s [ P i p e r ] S t . John)
f o r example, may o c c u r on white f i r s , mountain
hemlock, l o d g e p o l e and ponderosa p i n e s ,
Engelman s p r u c e and w h i t e p i n e s , b u t never i n
damaging amounts i n t h e absence of t h e
p r i n c i p l e host, western larch.
S i n g l e gene r e s i s t a n c e t o dwarf m i s t l e t o e
probably i s r a r e .
Such r e s i s t a n c e i s known
a g a i n s t a n endemic l e a f pathogen, Didymascella
t h u j i n a i n w e s t e r n r e d c e d a r (Soegaard 1964).
H y p e r s e n s i t i v e r e a c t i o n (sudden d e a t h of c e l l s
a t t h e p o i n t of h o s t p e n e t r a t i o n ) which i s
commonly r e g a r d e d a s a n i n d i c a t o r of s i n g l e
gene r e s i s t a n c e , h a s been observed w i t h dwarf
m i s t l e t o e on ponderosa p i n e by Roth and Adams
( u n p u b l i s h e d data). Roth (1966) pointed o u t
t h a t s u r v i v a l of young ponderosa p i n e s e l e c t e d
o u t o f t h e e x i s t i n g gene pool a s r e s i s t a n t t o
A . campylopodum i s a l m o s t i m p o s s i b l e under
f o r e s t circumstances favorable f o r selection.
The h i g h f l a m m a b i l i t y o f t h e h e a v i l y i n f e c t e d
s t a n d s where s e l e c t i o n i s p r o g r e s s i n g h a s made
them p a r t i c u l a r l y v u l n e r a b l e t o d e s t r u c t i o n by
f i r e . Host s p e c i e s of o t h e r m i s t l e t o e s may
f a r e better.
I f s i n g l e gene r e s i s t a n c e o c c u r s , n o t h i n g
i s known of i t s h e r i t a b i l i t y and hence l i t t l e
of i t s u s a b i l i t y .
H o r i z o n t a l r e s i s t a n c e seems
more l i k e l y t o occur because i t can develop i n
It can
t h e absence of s e l e c t i o n p r e s s u r e .
a l s o a r i s e from a wide range of g e n e
combinations so i s l i k e l y t o be more
immediately u s a b l e .
Discovery of t r e e s t h a t a r e good
c a n d i d a t e s f o r r e s i s t a n c e i s d i f f i c u l t because
s o many f o r e s t i n f l u e n c e s determine whether a
t r e e w i l l be i n f e c t e d . Among non-genetic
f a c t o r s a r e t r e e s i z e , c h a r a c t e r i s t i c s of t h e
inoculum s o u r c e and, p o s i t i o n of t h e s u s c e p t
t r e e i n t h e stand. Nevertheless, considerable
r e s i s t a n c e o c c u r s among some i n d i v i d u a l s i n
n a t u r a l s t a n d s even though a l l s t a n d s a r e s o
susceptible, a s canmunities, a s to require
p r o t e c t i o n o r c o n t r o l i n t h e presence of t h e
p a r a s i t e . T h i s r e s i s t a n c e of i n d i v i d u a l s i s
horizontal resistance.
It i s s e e n , f o r example,
i n g r a f t s of 40 t o 50 ponderosa p i n e s s e l e c t e d
and t e s t e d under f i e l d c o n d i t i o n s . These
t r e e s have remained mostly m i s t l e t o e f r e e
d u r i n g 10 o r more y e a r s (23 f o r 7 t r e e s ) o f
t e s t i n g (Roth, unpublished d a t a , Roth 1974a).
Occasional m i s t l e t o e p l a n t s have appeared over
t h e y e a r s on most of t h e " p a r e n t " t r e e s .
However, one n o t a b l e p a r e n t h a s s t o o d i n t h e
annual m i s t l e t o e seed shower from a h e a v i l y
i n f e c t e d , l a r g e p i n e f o r more t h a n 100 y e a r s
w i t h o u t becoming i n f e c t e d . T h i s p i n e a p p e a r s
t o be immune t o p i n e dwarf m i s t l e t o e (&
campylopodum)
Older t r e e s a r e more r e s i s t a n t t o dwarf
m i s t l e t o e t h a n young t r e e s (Roth 1974a). While
s m a l l t r e e s may remain p r a c t i c a l l y u n i n f e c t e d
under a n i n f e c t e d o v e r s t o r y f o r a s long a s 10
y e a r s t h e s e t r e e s should n o t be r e g a r d e d a s
resistant.
Their s a f e t y l i e s i n the small
t a r g e t they present t o t h e mistletoe seeds
(Wicker and Shaw 1967). Large t r e e s c o l l e c t
many more m i s t l e t o e s e e d s t h a n s m a l l t r e e s .
I f l a r g e t r e e s remain s u b s t a n t i a l l y m i s t l e t o e
f r e e under c o n d i t i o n s of h i g h exposure t h e y
probably a r e e x h i b i t i n g h o r i z o n t a l r e s i s t a n c e
a t a useful level.
A f u r t h e r e x p r e s s i o n of h o r i z o n t a l
r e s i s t a n c e h a s been n o t e d (Roth 1974b)in t h e
d i f f e r e n t i a l a b i l i t y o f ponderosa p i n e s t o
t o l e r a t e i n f e c t i o n by & campylopodum. T r e e s
i n which d i s e a s e d t i s s u e i s l o c a l i z e d because
of r e s i s t a n c e of t h e phloem t o i n v a s i o n of t h e
endophytic ( a b s o r p t i v e ) system of t h e
Such t r e e s
m i s t l e t o e a r e l i g h t l y damaged.
produce s h o r t , o n l y s l i g h t l y damaging,
spindleshaped s w e l l i n g s i n t h e presence of t h e
endophyte. These t r e e s c o n t r a s t s h a r p l y w i t h
t h o s e l a c k i n g r e s i s t a n c e of t h e phloem.
Branches on t h e l a t t e r a r e abnormally
t h i c k e n e d w i t h l o n g and t a p e r e d s w e l l i n g s .
T h e i r t i s s u e s a r e e x t e n s i v e l y occupied by t h e
endophyte. We assume them t o be e x t e n s i v e l y
damaged p h y s i o l o g i c a l l y .
Disease escape i s a f u r t h e r means of
l i m i t i n g dwarf m i s t l e t o e . Escape mechanisms
expressed through h o s t morphology may be
d i r e c t l y u s e f u l t o t h e manager during s t a n d
improvement work o r i n d i r e c t l y i n a b r e e d i n g
program. Drooping f o l i a g e i n ponderosa p i n e
i s a n example. Dwarf m i s t l e t o e s e e d s a r e
i n t e r c e p t e d by n e e d l e s of t h e p o t e n t i a l h o s t
and depend on r a i n i n o r d e r t o s l i d e i n t o stem
p o s i t i o n s on thin-barked b r a n c h l e t t i p s
f a v o r a b l e f o r i n f e c t i o n (Roth 1959, Scharpf
and P a n n e t e r 1967). Most seeds on drooping
n e e d l e s a r e washed from t h e n e e d l e t i p s o n t o
.
t h e ground. On good s i t e s i n s o u t h w e s t e r n
Oregon where drooping n e e d l e s a r e a
predominent f o l i a r h a b i t , m i s t l e t o e i s r a r e .
Geographic escape should p e r h a p s b e
mentioned a l s o . Though t h e r e s p e c t i v e h o s t s
a r e s u s c e p t i b l e , e s c a p e i s seen, f o r example,
i n D o u g l a s - f i r dwarf m i s t l e t o e t h a t does n o t
s i g n i f i c a n t l y e n t e r t h e h e a r t of t h e Douglasf i r region.
S i m i l a r l y , s o u t h w e s t e r n dwarf
m i s t l e t o e (& vaginatum Engelm.) d o e s n o t
o c c u r on ponderosa p i n e , i t s p r i n c i p a l h o s t ,
i n t h e P a c i f i c Northwest.
Now b r i e f l y c o n s i d e r a p p l i c a t i o n s of
t h e s e r e l a t i o n s h i p s i n f o r e s t management.
Immunity accompanying s p e c i a t i o n (taxonomic
immunity) i s a m a i n s t a y o f s i l v i c u l t u r a l
c o n t r o l o f dwarf m i s t l e t o e .
It a l l o w s
reforestation with an alternate tree species
when s i t e s a n i t a t i o n i s n o t p o s s i b l e . It
e n a b l e s s a f e u n d e r p l a n t i n g of s h e l t e r w o o d s and
i s p a r t i c u l a r l y v a l u a b l e where t h e o v e r s t o r y
must b e k e p t f o r l o n g e r t h a n 10 y e a r s (Wicker
1975). It a l l o w s p l a n t i n g s of a l t e r n a t i v e
s p e c i e s around c u t t i n g u n i t s i n o r d e r t o
e s t a b l i s h immune b o r d e r s t r i p s a g a i n s t
i n f e c t e d s t a n d s . I n mixed s t a n d s i t a l l o w s t h e
manager t o s a c r i f i c e t h e s e v e r e l y d i s e a s e d and
damaged s p e c i e s and t o c a r r y t h e r e s i d u a l
s t a n d of a l t e r n a t i v e s p e c i e s t o r o t a t i o n age.
It must b e c o n s i d e r e d , however, t h a t a mixed
f o r e s t i s more t h a n t h e sum of i t s s p e c i e s .
I t i s u n l i k e l y t h a t any o f t h e components,
a l o n e o r i n c o m b i n a t i o n , can occupy t h e s i t e
t o t h e p r o d u c t i v i t y l e v e l achieved by t h e
n a t u r a l m i x t u r e , even though f u l l y s t o c k e d .
I n many c a s e s , i f n o t i n most, a t r a d e - o f f i n
p r o d u c t i v i t y w i l l be r e q u i r e d t o accomplish
the mistletoe control.
I n t h i s t r a d e - o f f l i e s t h e m i s f o r t u n e of
o u r f a i l u r e long ago t o pursue a breeding
program f o r dwarf m i s t l e t o e c o n t r o l , i n c l u d i n g
v e r t i c a l resistance.
With s t o c k p o s s e s s i n g
h i g h r e s i s t a n c e , o r immunity s u c h a s t h a t of
t h e p i n e mentioned e a r l i e r , a l l of t h e
p r e c e d i n g s i l v i c u l t u r a l p r a c t i c e s c o u l d be
accomplished w i t h no s a c r i f i c e of s t a n d
q u a l i t y . F o r t u n a t e l y , t h e r e i s a chance t h a t
o b j e c t i v e s of some of t h e s e p r a c t i c e s c a n be
a c h i e v e d through h o r i z o n t a l r e s i s t a n c e even
though of a lower l e v e l t h a n immunity.
A v a i l a b i l i t y of s u c h r e s i s t a n t s t o c k might n o t
b e t o o d i s t a n t i f i t wave a g g r e s s i v e l y
pursued.
Though i t h a s n o t been e x p e r i m e n t a l l y
demonstrated, there a r e indications t h a t
s t r o n g g a i n s i n h o r i z o n t a l r e s i s t a n c e a r e made
when h e a v i l y d i s e a s e d young s t a n d s a r e t r e a t e d
f o r m i s t l e t o e c o n t r o l during timber stand
improvement. Thinning a f t e r s t a n d s a r e 50
y e a r s o l d w i l l have allowed most of t h e h i g h l y
susceptible trees, during t h e i r juvenile
p e r i o d , t o d i s c l o s e t h e i r s u s c e p t i b i l i t y and
need f o r removal. By t h i s time, also, t h e
l a r g e r b u t l e s s r e s i s t a n t t r e e s w i l l have
become c o n s p i c u o u s l y i n f e c t e d - , o r '-ill a l r e a d y
have weakened i n c o m p e t i t i o n w i t h t h e i r more
r e s i s t a n t , l e s s heavily infected associates
and w i l l be removed.
The r a t e o f d i s e a s e
development i n t h e s e s t a n d s a f t e r t r e a t m e n t
c e r t a i n l y w i l l be slower t h a n would have been
t h e c a s e i n s t a n d s of e q u a l s t o c k i n g of t h e
o r i g i n a l genotypic composition a t equivalent
spacings.
Many s t a n d s of ponderosa p i n e i n t h e
P a c i f i c Northwest t r e a t e d f o r m i s t l e t o e i n
t h e e a r l y y e a r s of t h e young-growth c o n t r o l
program s h o u l d be n e a r i n g r e p r o d u c t i v e age and
might q u i t e r e a s o n a b l y be examined f o r g a i n i n
r e s i s t a n c e i f n o t f o r p o t e n t i a l of development
a s s e e d o r c h a r d s . I f s t a n d s c a n n o t be found
t h a t a r e s u i t a b l e f o r o r c h a r d development, t h e n
t i m e l y s t e p s should be t a k e n t o d e v e l o p s u c h
stands.
I n c l o s i n g , o p p o r t u n i t i e s f o r improved
" r e s i s t a n c e " t h r o u g h e s c a p e from i n f e c t i o n
should be b r i e f l y mentioned. T r e e s l i k e l y t o
e s c a p e , e s p e c i a l l y t h o s e w i t h growth
c h a r a c t e r i s t i c s conducive t o n o n - r e t e n t i o n of
dwarf m i s t l e t o e s e e d , d r o o p i n g n e e d l e s b e i n g
perhaps t h e b e s t known, c a n i n some c a s e s be
r e c o g n i z e d and l e f t i n t h e s t a n d d u r i n g
t h i n n i n g . Morphological f e a t u r e s c o n t r i b u t i n g
t o escape a r e a p p r o p r i a t e m a t e r i a l f o r t h e
t r e e breeder.
Clearly genetic considerations
have a p a r t t o p l a y now and i n t h e f u t u r e i n a
complete m i s t l e t o e c o n t r o l p o l i c y .
LITERATURE CITED
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Robinson. Raoul A.
1976. P l a n t pathosystems.
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Forest
Roth, Lewis F.
1966. F o l i a r h a b i t of ponderosa p i n e a s a
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