The
Journal
of
Heredity
78:126-128.
1987.
Inheritance of resistance to
clover yellow vein virus In
Plsum sathnim
R. Prowtdentl
ABSTRACT:
Most
of the
cuttlvars
of
Plsum sativum
resistant
to
bean
yellow
mosaic
virus
(BYMV)
were
found
to be
resistant
to
clover yellow
vein
virus
(CYW).
However,
some
accessions from
Ethiopia
(PI
193586
and PI
193835)
and
India
(PI
347464, PI
347465,
PI 347466, PI 347467, and
PI
347492)
were
resistant
to CYW, but
suscep-
tible
to
BYMV.
Conversely,
others from
China
(PI
391630)
and the
USSR
(PI
262818)
were
resis-
tant
to
BYMV,
but
susceptible
to
CYVV,
Indicat-
ing
that
resistance
to
these
two
viruses
is
conferred
by
distinct
genetic
entitles.
In the
BYMV+CYW-reslstant
cuWvar
Bonnevllle,
re-
sistance
to
CYVV
was
found
to be
Inherited
monogenlcally
recessive
(cyv).
This
gene
ap-
pears
to be
closely
linked
to
that
conferring
resistance
to
BYMV
(mo),
which
is
located
on the
second
chromosome.
In the
accessions from
Ethiopia
and India,
resistance
to CYW Is condi-
tioned
by a
second recessive
gene
(cyv-2),
that
Is
situated
In a
different
linkage
group. In the
lines
from
China
and the
USSR,
resistance
to
BYMV
is
conferred
by mo. The
possible origin
of
two
distinct genes
for
resistance
to the
same
Isolate
of CYW Is discussed.
CLOVER
yellow vein virus (CYVV) is the caus-
al agent of devastating diseases occurring in the
bean and pea in the northeast United States
10
.
Susceptible pea cultivars respond to the preva-
lent strain of the virus (formerly known as the
severe strain of bean yellow mosaic virus
510
'
13
,
with prominent veinal chlorosis, apical and
stem necrosis, followed by premature
death
5810
-
1113
).
Resistance to CYVV has been
associated with that to BYMV
2
^
8
'
13
suggesting
that the mo gene
15
would confer resistance to
both viruses. However, recently we have deter-
mined that some pea lines of foreign introduc-
tions are resistant to CYVV, but susceptible to
BYMV and vice versa. These findings indicated
distinct genetic factors for resistance to these
two viruses. This study concerns the inheritance
of resistance to CYVV in Pisum sativum
L.
and
its relationship to BYMV.
Materials and Methods
Seed of pea cultivars were obtained from sev-
eral commercial sources. Accessions of foreign
The
author
is
professor
in the
Department
of
Plant
Pathology,
New
York State
Agricultural Experiment
Station,
Cornell
University,
Geneva,
New
York
14456.
© 1987,
American
Genetic
Association.
lines were secured from the USDA Northeast
Plant Introduction Station, Geneva, New York.
Genetic populations were derived from the fol-
lowing crosses: a) BYMV+CYVV-resistant
Bonneville with the BYMV+CYVV-suscepti-
ble Ranger; b) Bonneville with BYMV-resis-
t'ant/CYVV-susceptible PI 391630 and PI
269818;
and c) Bonneville or Ranger with
BYMV-susceptible/CYVV-resistant PI
347492. Cultures of BYMV and CYVV were
the same as those used in previous studies
10
"
12
.
Inocula were prepared from Ranger plants in-
fected with either one of these viruses, by ho-
mogenizing infected leaves with 0.05 M phos-
phate buffer (K+) (pH 8.5). Extracts were
rubbed onto the first two leaves of each plant
previously dusted with Carborundum. To avoid
escapes among susceptible genotypes, test
plants were reinoculated on the third
leaf.
In
screening for resistance, 16 to 20 plants of each
pea line were inoculated with BYMV or
CYVV. All plants, regardless of their reaction,
were assayed for viral infection using Ranger
pea, or by enzyme-linked immunosorbent as-
says (ELISA). Tests were conducted in an in-
sect-free greenhouse that was maintained at
25-30 C.
Results
Pea lines resistant to BYMV and CYW.
Ace,
Aurora, Bonneville, Bridger, Canjoy, Can-
ner
1281,
Canner King, Canner Prince, Champ,
Cascade, Climax, Dark Skin Perfection, Davis
Perfection, Early Frost, Early Harvester, Early
Perfection, Early Perfection 3040, Early Sweet
20,
Early Sweet A45, Ericson Perfection, Eure-
ka, Famous, Frazer, Freezer, Freezer 626,
Freezer 640, Freezer 5147, Freezer 68178,
Freezer 73152, Galaxie, Greater Progress,
Greenfeast, Hundredfold, Hylate, Improved
Surprise, Ivy, Jade, Knight, Laxton Progress,
Laxton Superb, Little Marvel, Maestro, Mars,
Medalist, Melody, Midway, Mini, Morse's 55,
Midfreezer, Neptune, Pacific Perfection, Per-
fected Freezer, Perfected Freezer 60, Perfected
Freezer 70A, Perfection 25, Perfection 42, Per-
fection
400,
Premium Gem,
Pride,
Progress No.
9, Rally, Resistant Early Perfection 326, Ron-
do,
Shoshone, Signet, Small Sieve Perfection,
Sirod, Sparkle, Surprise, Sybo, Target, Trojan,
Trumpet, Venus, Viking, Wando, Wisconsin
Perfection, and numerous breeding lines. The
following plant introductions also were resis-
tant to these two
viruses:
PI 140295,PI 174319,
PI 174924, PI 180669, PI 236493, PI 347420,
PI 347422, and PI
356851.
Pea lines resistant to CYW, but susceptible
to
BYMV.
PI 193586 and PI 193835 (Ethio-
pia),
PI 347464, PI 347465, PI 347466, PI
347467, and PI 347492 (India).
Pea lines resistant to
BYMV,
but susceptible
to CYW. PI 391630 (China) and PI 269818
(USSR).
Inheritance studies. Plants of the resistant
parents Bonneville and PI 347492 remained
free of local and systemic infection following
inoculations with CYVV, thus they were con-
sidered highly resistant or immune to this virus.
Conversely, those of the susceptible parents
Ranger and PI 391630 developed a prominent
foliar chlorosis that involved all veins and vein-
lets followed by stem streak, apical necrosis,
and eventual death. Plants of F] (Bonneville X
Ranger), (Bonneville X PI 391630), and
(Ranger X PI 347492) reacted with systemic
symptoms closely resembling those of the sus-
ceptible parents, indicating that resistance was
inherited recessively. The reaction of F
2
popula-
tions of these crosses revealed a segregation
close to the ratio of 3 susceptible plants to 1
resistant. Plants of the backcrosses (Bonneville
X Ranger) X Ranger, (Bonneville X PI
391630) X PI 391630, and (Ranger X PI
347492) X Ranger were all susceptible, where-
as those of (Bonneville X Ranger) X Bonne-
H
ville,
(Bonneville X PI 391630) X Bonneville,
and (Ranger X PI 347492) X PI 347492 segre-
gated approximately to the ratio
1
resistant to 1
susceptible. From the data presented in Table I,
it is concluded that resistance to CYVV in Bon-
neville and PI 347492 is inherited monogenical-
ly recessive.
Linkage
between
resistance factors. Plants of "
each of
50 F3
families deriving from (Bonneville
X Ranger)
F2
were divided into groups of equal
numbers and inoculated with BYMV or
CYVV. The data in Table II show that 12 fam-
ilies were resistant to both viruses, 14 were sus-
ceptible, and 24 cosegregated for these two vi-
ruses.
The absence of recombinations indicate
^
that in Bonneville, the genes for resistance to
BYMV and CYVV are closely linked.
Evidence
for two
loci
for CYW resistance.
When F| plants resulting from the crosses be-
tween the CYVV-resistant Bonneville with
CYVV-resistant PI 193586, PI 193835, PI
347464, PI 347465, PI 347466, PI 347467, or
PI 347492 were inoculated with this virus, all«
plants were susceptible. In addition, plants of
(Bonneville X PI 347492) F
2
segregated ap-
proximately in the ratio: 7 resistant to 9 suscep-
tible.
The data presented in Table III indicate
the presence of
two
distinct loci for resistance to
CYVV, one in Bonneville and another in PI
347492. The symbols cyv and cyv-2 (clover yel-
low virus) are assigned to these genes, respec-
tively.
Evidence for one locus for resistance to
BYMV.
Plants of F,, F
2
, and reciprocal back-
cross populations of the crosses between
BYMV + CYVV-resistant Bonneville and,
BYMV-resistant/CYVV-susceptible PI
269818 and PI 391630 were all resistant to
BYMV. The data shown in Table IV demon-
strate the existence in these lines of one locus for*
resistance to BYMV.
Discussion
The identical reactions to BYMV and CYVV
of a large number of domestic cultivars and
several foreign introductions of
P.
sativum ini-
tially suggested a common gene for resistance-*
to both viruses. This hypothesis was considered
plausible, because these two viruses were, for
years,
believed to be strains of the same vi-
rus
51013
.
However, the finding of some lines
1
resistant to CYVV, but susceptible to BYMV
and vice versa, indicated the existence of two
distinct genetic entities.
This study has shown that: a) resistance to
CYVV in P. sativum is monogenically reces-
sive;
b) in Bonneville the gene cyv is closely
126 The Journal of Heredity
Notes
linked to mo, known to be located on chromo-
some 2
6
and is linked to Pgm-p
14
; c) some lines
from India (PI 347464, PI 347465, PI 347466,
PI 347467, and PI 347492) and Ethiopia (PI
193586 and PI 193835) possess a second gene,
cyo-2,
that appears to be located in a different
Table L Segregation ratio* of croa and backcross populations of Pitum ativum lines resistant and
susceptible to clover yellow vein virus
Cultivars
and lines
Bonneville
Ranger
(Bonneville X Ranger)Fi
(Bonneville X Ranger)
F2
(Bonneville X Ranger)Fi
X Bonneville
(Bonneville X Ranger)F|
X Ranger
PI 391630
(Bonneville X PI 391630) F,
(Bonneville X PI 391630)F
2
(Bonneville X PI 391630)F
2
X Bonneville
(Bonneville X PI 391630)F,
X PI 391630
PI 347492
(Ranger X PI 347492)F,
(Ranger X PI 347492)F
2
(Ranger X PI 347492)F,
X PI 347492
(Ranger X PI 347492)F,
X Ranger
No.
resistant
33
0
0
86
32
0
0
0
20
15
0
16
0
44
36
0
plants
susceptible
0
35
15
268
38
77
16
11
64
20
41
0
10
120
41
61
Exp. ratio
1:3
1:1
1:3
1:1
1:3
1:1
Goodnes3-of-fit
P
0.76
0.48
0.80
0.42
0.61
0.59
Table IL Reaction to bean yellow mosaic virus (BYMV) and clover yellow vein virus (CYW) of
JO
Fj families of the cross Bonneville X Ranger
No.
families Viruses
_—BYMV
CYMV
,-— BYMV
CYW
,^-BYMV
' CYW
No.
resistant
174
171
68
70
0
0
plants
susceptible
0
0
240
244
194
198
Exp. ratio
1:3
1:3
Goodness-of-fit
P
0.24
0.27
linkage group; and d) in BYMV-rcsistant/
CYVV-Susceptible PI 269818 and PI 391630,
and in Bonneville, resistance to BYMV
is
condi-
tioned by the same gene (mo).
Published reports also have associated resis-
tance to BYMV with resistance to other poty-
viruses such as pea mosaic virus (PMV)
1
, wa-
termelon mosaic virus 2 (WMV-2)
12
, the lentil
strain of pea seed-borne mosaic virus (PSbMV-
L)
4
,
and to the NL-8 strain of bean common
mosaic virus (BCMV-NL8)
9
. Bonneville and
many of the BYMV+CYVV-resistant cultivars
also are resistant to these viruses
1
'
9
-
12
. Thus, it
appears that in most of BYMV-resistant culti-
vars,
there is a cluster of closely linked loci that
during breeding are transferred as a unit. Re-
cently, the name linkat has been proposed for a
such unit
3
.
Preliminary studies have suggested that ad-
ditional loci for resistance to the same strains of
BCMV-NL8, PMV, and PSbMV-L, are
present in other linkage groups (unpublished
data).
Demarly
3
has speculated that linkats
may be ancestral genes that, in the course of
evolution, gave rise to duplicates that in some
cases,
moved to other loci. This hypothesis ac-
counts for the observed linkage on chromosome
2 and may explain the presence of additional
resistance genes for the same strains of CYW,
BCMV-NL8, PMV, and PSbMV. Conversely,
it could be hypothesized that mutant loci for
recessive resistance to BYMV, BCMV-NL-8,
CYW, PMV, and PSbMV-L may have origi-
nated as independent mutations in different
linkage groups and through translocations may
have converged in chromosome 2. However,
both hypotheses assume repetition of genes for
resistance. No duplicate genes have been re-
ported for resistance to viruses, but there are
several cases of specific genes conferring resis-
tance to specific strains or pathotypes of the
same virus. Hence, cyv and cyv-2 may have
been the result of two independent mutations
conferring resistance to two distinct pathotypes
of CYW, but they cannot be differentiated by
the strain used in this study. For example, in the
tomato, Tm-2 and Tm-2
2
for resistance to to-
bacco mosaic virus cannot be differentiated if
strain 0 and 1 are used. However, plants with
Tm-2 are infected by strains 1.2 and 2, and
those with 7m-2
2
only by strain 2
27
.
Recent data, however, seem to indicate that
Table III. Reaction of Fi and Ft populations of the cross between clover yellow mosaic
virus-resistant Bonneville with CYW-resistant plant introductions from Ethiopia and India
Table IV. Reaction of F
t
and Fj populations
from crosses between bean yellow mosaic virus-
resistant lines
.. Cultivars and Pis
(Bonneville X PI 193586)F,
(Bonneville X PI 193835)F,
(Bonneville X PI 347464)F,
(Bonneville X PI 347465)F,
(Bonneville X PI 347466)F,
(Bonneville X PI 347467)F,
(Bonneville X PI 347492)F,
(Bonneville X PI 347492)F
2
No.
resistant
0
0
0
0
0
0
0
63
plants
susceptible
6
6
6
6
6
6
12
81
Exp. ratio
7:9
Goodness-of-fit
P
0.14
Cultivars and Pis
Bonneville
PI 269818
(Bonneville X PI269818)F,
(Bonneville X PI 269818)F
2
PI 391630
(Bonneville X PI 391630)F,
(Bonneville X PI 391630)F
2
Ranger
No.
res.
15
16
12
104
12
14
98
0
plants
susc.
0
0
0
0
0
0
0
16
Notes
March/April 1987 127
resistance
to
BYMV, CYVV,
and
PMV
is
not
strain-
or
pathotype-specific. Barnett (pers.
comm.) demonstrated that
the pea
cultivar
Greenfeast
is
resistant to a number of isolates of
BYMV, CYVV, and PMV from Canada, Aus-
tralia, and the USA although these isolates ex-
hibited divergence
by
molecular hybridization
(cDNA) and serology.
Work
is in
progress
to
elucidate
the
inheri-
tance
of
resistance
to
BCMV-NL8, PMV,
and
PSbMV-L as well as several other points raised
by this investigation.
References
1.
BARTON,
D.
W.,
W. T.
SCHROEDER,
R.
PROV-
VIDENTI,
and W.
MISHANEC.
Clones from seg-
regating progenies
of
garden
pea
demonstrate
that resistance
to
BV2
and
PV2 is conditioned
by
the same genotype. Plant Dis.
Reptr.
48:353-355.
1964.
2.
Bos, L., K.
LINDSTEN,
and D. Z.
MAAT.
Simi-
larity
of
clover yellow vein virus
and pea
necrosis
virus. Neth.
J.
Plant.
Path. 83:104-108
1977.
3.
DEMARLY, Y. The concept of linkat. Proc.
Conf.
Broadening
Genet.
Base Crops. Pudoc. Wagenin-
gen.
p.
257-265.
1979.
4.
GOODELL,
J. J. and R. O.
HAMPTON.
Interac-
tion
of
Pisum genes
sbm and mo
with
pea
seed-
borne mosaic virus (PSbMV). Sympton expres-
sion
and
immunity
to
three variant strains.
Phy-
topathology 73:789 (Abst.).
1983.
5.
GROGAN,
R. G. and J. C.
WALKER.
A pod-
distorting strain
of the
yellow mosaic virus
of
bean
J
Agr.
Res.
77:301-314.
1948.
6.
MARX,
G. A. and R.
PROVVIDENTI.
Linkage
relations
of
mo. Pisum
Newsl.
11:28-29.
1979.
7.
PELHAM,
J.
Strain-genotype interaction
of to-
bacco mosaic virus
in
tomato.
Ann.
Appl.
Biol.
65:293-297.
1970.
8.
PRATT,
M.
J.
Clover yellow vein virus
in
North
America. Plant Dis.
Reptr.
53.201-212.
1969.
9.
PROVVIDENTI,
R., M. J.
SILBERNAGEL,
and W.
Y.
WANG.
Local epidemicof NL-8 strain
of
bean
common mosaic virus
in
bean fields
of
western
New York. Plant Disease 68:1092-1094.
1984.
10.
and
W. T.
SCHROEDER.
Resistance
in
Phaseolus vulgaris
to the
severe strain
of
bean
yellow mosaic virus. Phytopathology 63:196-
:
197.1973.
11. SCHROEDER,
W. T. and R.
PROVVIDENTI.
Evaluating Pisum sativum
for
resistance
to
pea
mosaic.
N.YS.
Agr.
Exp Sta.
Bull.
806,
10 pp.
<
1964.
12.
and .
Resistance
to
watermelon
mo-
saic virus
2 in
Pisum sativum conditioned
by the
gene
for
resistance
to
bean yellow mosaic virus.
(
Phytopathology 60:1312-1313.
1970.
13.
THOMAS,
H.R. and W. J.
ZAUMEYER.
A strain
of yellow bean mosaic virus producing local
le-
sions
on
tobacco. Phytopathology 43:11-15. H
1953.
14.
WEEDEN,
N. F., R.
PROVVIDENTI,
and G. A.
MARX.
An isozyme marker
for
resistance to bean
yellow mosaic virus
in
Pisum saticum.
J.
Hered.
l
75:411-412.
1984.
15.
YEN,
D. E. and P. R.
FRY. The
inheritance
of
immunity to pea mosaic virus
Austr.
J.
Agr.
Res.
7:272-281.1956.
f.
The Journal
of
Heredity 78:128-129.
1987
Brown and rust mutants
of the
Syrian hamster
are
p
and
b
genes
of
mammalian
coat colors
Roy RoMnaon, C.
V.
Beeclwy, and
ABSTRACT.
The
mutant genes
of
the
Syrian ham-
ster,
which were originally designated
as
brown
(6) and rust (r),
are
shown
by
morphological
and
phenotyplc criteria,
as
well
as by
linkage studies
In
the
case
of
brown,
to be
homologous with
pink-eyed dilution
(p)
and brown (b), respective-
ly,
two
well established loci
In the
genetics
of
mammalian pigmentation.
It
Is
proposed that
the
two mutants
be
appropriately redesignated.
THE SYRIAN HAMSTER
{Mesocricctus
aura-
tus)
is a
light-bellied agouti more auburn
in
color than
the
mouse
or rat. The
dorsum
is
The first author's address
is: St.
Stephens Road
Nursery, Ealing, London
W
13
8HB;
the
second
and
third authors' address
is:
Medical Research Council
Radiobiology Unit, Chilton, Didcot, Oxon OX
11
0RD England. They thank
Dr.
Mary
F.
Lyon
for
her
critical comments
and Dr.
Dennis
A.
Stephenson
for
allowing them to quote his unpublished information.
© 1987, American Genetic Association.
overlaid with black tipped guard hairs while the
under parts
of
the body
are
pale cream
or
off-
white.
The
skin
of
the ears
are
black,
and the
eyes have dark brown irises and black pupils.
Nineteen mutant genes
are
known
to
affect
color and pattern
in the
hamster, two
of
which
have similar phenotypes. These
are the
reces-
sive genes designated
as
brown
(b)
3
* and
rust
(r)
12
.
The brown gene produces a bright orange-
brown coat, overlaid with light colored guard
hairs.
The skin
of
the ears
is
light brown while
the eyes have pale brown irises
and red
pupils;
the overall effect
is
that
of
a
red
eye that dark-
ens with age. The rust gene produces a similarly
colored coat but of a duller tone. The skin
of
the
ear
is
medium brown while the eyes have light
brown irises and a dark pupil that glows dull red
under bright illumination. Again, the eye color
darkens with age.
Materials
and
Methods
Hair samples were obtained from wild-type,
rust, and brown golden hamsters, and,
for
com-
parison, from wild-type, brown
(b) and
pink-
eyed dilute
(p)
mice. Hairs were mounted
by
a
method based on that
of
Gruneberg
1
:
1)
placed
on slides thinly smeared with albumin;
2)
cov-
ered with O.P.74 (95 percent ethyl alcohol) that
was then allowed to dry on
a
hot-plate;
3)
dried
in
an
oven overnight
and
then passed through
O.P.74 alcohol,
1:1
O.P.74 alcohol
+
xylene,
xylene for
at
least 2,
1,
and
I
days, respectively,
in
a
vacuum; and 4) mounted
in
Euparal. They
were then examined microscopically under
oil
immersion.
Results
Figure
1
shows that there were marked
dif-
ferences
in
granule size
and
shape between
brown
in the
hamster
and
brown
in the
mouse,
although wild-type granules
in
the
two species
were
a
similar ovoid shape. Instead, brown
granules
in the
hamster resembled those
of '
pink-eyed dilution
in the
mouse (Figure
IF)
which
are
very small
and
irregular
in
shape,
with
a
tendency
to
form flocculent clumps
and
with reduced numbers
in
cortical cells
9
.
The^
largest ones seemed
to
be only about 0.3
^m in
diameter, compared with
1.2 /im for
the
long
axis
of
the hamster wild-type granules.
On the
other hand, granules of the hamster rust mutant
closely resembled those
of the
brown mouse
„
(Figure
1£)
in
their spherical shape
9
but
vari-
able size, with an average diameter
of
about 0.8
,
The first indication that the brown gene may*
be misnamed
was the
discovery that
it was
linked
to
albino
7
. This finding invited compari-
son with
the
known linkages
of
albino
(c) and
pink-eyed dilution
(p)
genes
in
the
deermouse,«
house mouse, and Norway rat
6
. The implication
is that brown could
be
pink-eyed dilution.
The
"
red eye color
is
typical
of
this type
of
coat
mu-
tant although
the
coat color
is
brighter than*
that shown by pink-eyed dilution phenotypes in
the other three species. However, this could
be
accounted
for
by the rich color
of
the wild-type
agouti
in
the
hamster.
On the
other hand,
the
crossover value
for
the hamster genes
is
30.9
± ,
1.8, which differs from
the
remarkably similar
crossover values
of
17.4
± 2.5
(deermouse)^,
15.1 ±0.3 (house mouse), and 18.4
±
0.4 (Nor-
way
rat)
of
the other species
6
,
but
agrees with
,
the recently discovered linkage
of
30
±
5
for the
c
and
p
loci
of
the
Mongolian gerbil
(B.
D,<
Leiper and
R.
Robinson, in press).
Linkage between brown and rust
in
the ham-
ster also has been tested for, by intercrossing F[
progeny of crosses between them. Phenotypes
of
F
2
offspring were 122 ++, 37 +r and 54 b+ or b
r, with
b
epistatic over r, total
203.
This
is
a very
128 The Journal
of
Heredity
Notes