Origins of Resistances to Rust and Late Leaf Spot in
Peanut
(Arachis hypogaea,
Fabaceae)l
P.
SUBRAHMANYAM.
V.
RAMANATHA
RAO,
D.
MCDONALD.
J.
P.
Moss,
AND
R.
W.
GIBBONS'
7'hcc~ulti~utedpc~a,r1~/
(Arachis hypogaea.
Fubaccac) is belic~ved to have orlginutcjd
ulorrg I/?(,
C~USIC~II
slo/)c,s
(?f
ihr ..lnrl(s in Bo111.ia und northerr1 Argentina. The crop
1s t~orc groLt,tr thronghout iro~~ic~ul utid
warm
tonpiJralr regron.c. .4rnong diseases
uttac.krn,q pc,ut~lrrs, rlitr cwlr.,c~/
hjl
Puccinia arachidis
arid larr, Ieuf'spot cuuscd
hj,
Phaeoisariopsis personata
urea
flic r?io.sl rt?iportan/ and dcstrurttvc~ on a ~,orld~,idr
.\c,olc. noti? pa//iogc,tr~, rr,stric./cd rn host run@, to
Arachis,
prohahly
originated
and
c,oc,vol\,ed irl .Siiut/r .,ltnrriiu alclt~y ~i'ith thrir /~ost.s. In rcwnr years there has heen
1?11i(./r
~rtlphusr.\
OIL
.SC~(~CIIIII~
c!f
pcwn~rt gcrtnpla.\t?i fi?r rerlstuncp to thmr di,seases,
:I/
tile It~tcrtiut~o~ld C~OIJX Rc,~eurc.h It~.sti/tttc~,J~r tho St7tni-.-lrrd Troprc,s IICRIS.4
T).
Iticlra. .\ottrc7
10.000
i~cntt~tt ,yc,rr)ipIa.s~~~ uc,c.c.~.sions u,crc .sc,rccnc,d fhr reslstuncc to
rlrst and Iutcz I(,u/ .spot d~rrtn,y 1977-1
4X.F
u~id sourc,es (?fresi.vt~tii,(, inderiti/rcd,[i)r
c,itltrr or both put1iogrtr.c.
(If
/lie t.r~.vistut~r g~~trotjpc:~, uboul 87% helon~erl to
A.
hypogaca
rur.
fastigiata
utitl 1.?"0
lo
vtrr.
hypogaea:
84%
origrtiarc~d
in
Sorirh .-lt?ier-
11
u or liud So~irlt
.
Ittli~ric~ati c.o?ltlc,c,troti.r.
.4
high pc2rccntagc (75"/r,i had therr origln
111
I'c2rrr ihc,lrc~~~c,cl to /I(,
ci
tc7c~rjtrilug' ,qrvicr c.ctitcr,fi~r r,ur.
hirsuta
and var.
Sastigiatai.
sit,ygc.strtii: tlrul t~csr.cturic~~ to rlrrt ant/ /arc Icaf\pot drscasc,s miiyhr hur'c cvolv~d rn
it1ut c~outltl.J*.
Origine des Sources de RCststance
h
la Rouille ct
a
la Cercosporiose Tardive
dc
I'Arachidc
(:lru~~lrrc Ii\po,yucu,
Fabaceae).
1-'aruchide cultlvk
{Arachis hypo-
gaca.
I.irl~ac.c,clc~l .\rt.ui/ orrjitticirrc~ tlu ~~e~r.satit oricnrul df~ :ltidr.s, cw Bolrvic~
ct
1.n
.-lrgiJutrr~c 1/11 .l?~rc/. C't,ttcz
c~rrif~rt'c~
cat t?iurri~r~r~utit pratrqltPc duns toutfi Ics r6,qions
ft.oprc~a1c.i
PI
tct~i~)(:r(:e\
~C/U/I~'L~~?~C~II
C/IIIIIC/~'J
dir ttiondcp
.,I
I'bchc~llc tnondralr, la
ro~rilic~.
Puccinia arachidis.
r.i lir c~c,rc~i~~~~orcos~~ turdr,,c,.
Phaeoisariopsis personata,
son/ 1r.s deii.\- prinripcllcs txuladic,s
ck,
I
hrac,hidc,. Le.r d~u.u ugenls puthog$t~~s. don/
Arachis
rsr
I'licitcl rrtrtylic,. .cot11 prot~ul~Ic~r?r(~t~t uli.~ei orr,~inu~r~~
IjC
I:.l~??(;riqii(, dti
Sltd. oir 11s
\(,
cr.rii~c~tr/ ilC~,c~loppk u~,cc 1c.urs ltcitcs. ,411 c,oirrs d6.s dc)rnihrcs annkc,.~,
lo? cgi~ri put~ttc~~rlrc~r u 616 ,fuit [~olir crthlcr ic7s rcssoitrccs gPtiPtiqur~s pour lcrrr rP-
sr.stur~c~c~
ci
c.(,.\ r?ruluriic~.v
.I
l'lt~.srrt~it Itltcrt~utrot~ul
d~,
Rcc-hcrchc~s sur
1c.y
C'ulturc,~
(A,.\
/~III(:\ 7'ri)/11c,u/t,\ .SCI?II-.
1
rtdc,.s IIC'RIS
4
TI.
cjn Indc, y~tc,lquc~ 10,Ooo g6norjper
d'urac,l~rdc i)trt 61; c~rtl~lC's, cJtrrrr
1977
1.1
lYS5. pour icitr r6.srsratic.e
d
la ro~rrllr cr
lu c~c~ri~ospo~.ii~.~(' turdr~'(p. L/(,.Y .c011rcc~.s ilr 1.6~1.stati~~~~
a
I'un ou I'uutr~, c7u uu.~ dru.~
ugc7t1rs patiio,yi.rrc.s otrl 61; cdcnt~fiPcc. PrPs dr 87% dc7.\ g6notlpc.s rbsrslu?lls uppar-
rc3tiuic,~7i
d
A. hypogaea
~wr
fastigiata
ct 13'S1
u
var.
hypogaea;
840.0 d'c7ntrc eu.v
prol~c~~lurrtit d:.1tr1Prtyite drr Sud, o~i poiivilre7trf htre appurc.nt6.v
d
do., sourc,cs sud-
ut~rc'ric~arnc,.r. 1'11 fi1r.t po~irc~c~tifu,.i~c~ 1'75(~oi ~)ro\,rnair dl1 I'6roli icmfr~, gkniqrcc. sewn-
darrc' ,qPn4ro/i~tt1c~t11 r~cotit~~r
~f('
vur.
hirsuta
PI
I'UY,
Sastigiatai,
sug~runl ait1.c.r qrre
1c.s .SOLII.~~C,S d~, ~(:~.ISIU~ILI' ci ia rouilli~ c,r ia i,cbrc,osporro.stJ /urcli\,r'sc scruicnt d6veIopp6t~s
durls
ce
pa~s.
'
Reccived 12 Deccrnhcr
1986:
accepted 10 Ma>
1988.
Approved as .lournal Article
No,
629 by
the International Crops Kcscarch Institutc for thc Semi-Arid Tropics (ICRISAT).
:
Plant Pathologtst. Botanist. Princ~pal Plant Pathologist. Pnncipal Cytogenet~c~st. and Principal
Plant Breeder. ICRISAT, Patanchcru
P.O.,
Andhra Pradesh
502
324. India: present address of last
author: lCKlSAT Sahelian Center.
B.P.
12404. Niamey, Niger (via Paris).
Econom~c
Botan,,.
40(4). 1989, pp. 444-455
Q
1989,
by
the New York Rotanlcal Garden. Bronx.
NY
10458
19891
SUBRAHMANYAM
ET
AL.:
PEANUT
PATHOGENS
44
5
It is generally accepted that the primary and secondary gene centers of cultivated
plants are the best locations to find genuine sources of resistance to common pests
and pathogens (Dinoor and Eshed 1984; Leppik 1970). During the coevolution
of host and parasite, both participants develop complementary genetic systems
if they have long been associated in their centers of origin (Anikster and Wahl
1979; Browning 1974; Dinoor 1970: Harlan 1976; Leppik 1970; Segal et al. 1980).
The evolution of new and more virulent races of the pathogen may be counter-
balanced by the development of higher levels of resistance in its host system due
to selection pressure in the coevolution
(nor 1956). Gene centers of many cul-
tivated plants have been well established, but the origin and evolution of the
parasites
of these plants are still unexplored even after Leppik (1 970) emphasized
this point. Some investigations have shown that certain specialized parasites and
their distribution on particular plant groups can serve as reliable indicators that
help to trace back
thc origin and evolutioi? of their hosts (Leppik 1966).
Systematic exploration in the gene
centcrs for sources of resistance to some
pests and diseases has been carried out for a few crop species (Qualset 1975).
Very little is known regarding the relationship between the gene centers of the
cultivated peanut (Aruchis
hypogacu
L.,
Fabaceae) and sources of the resistance
to diseases. Hennen
et al. (1 976) and Leppik
(1
97 1) suggested that the exploration
of gene centers of peanut in South America may provide new germplasm for
varietal improvement and breeding for resistance to pests and diseases. Our report
discusses evolution of resistances to two major foliar diseases on the basis of
screening of
Arat<hrs germplasm collected from gene centers and maintained at
the International Crops Research Institute for the Semi-Arid Tropics (ICRISAT).
IC'RISAT,
25
km northwest of Hyderabad, Andhra Pradesh, India, has the
world's largest collection of peanut germplasm: over 10,000 accessions
(Ramana-
tha Rao 1987). During 1977-1985 these were screened against rust caused by
Yuccrnra arachidis Speg. and late leaf spot caused by Phaeozsuriopsls personata
(Berk.
&
Curt.) von Arx; several sources of resistance were identified for either
or both pathogens
(Subrahmanyam and McDonald 1983, 1987; Subrahmanyam
et al. 1980, 1982, 1983,
1985b).
ORIGIN AND DISTRIBUTION OF
PEANUT
.,lrachis is confined to a region in South America, east of the Andes, south of
the Amazon, and north of La Plata. The assumed center of origin of the genus is
in the
Mato Grosso of Brazil, close to the Gran Pantanal (Gregory et al. 1980).
.4ruchis hypogaea is the only member of Arachis cultivated on a large scale. It is
believed to have originated somewhere along the eastern slopes of the Andes in
Bolivia (Gregory et al. 1980) and in northern Argentina (Krapovickas, pers. comm.
1984). Aruchis
hypogaea is broadly classified into two subspecies, each with two
varieties (Krapovickas 1969). Krapovickas (1 969, 1973) indentified five gene
centers in relation to the distribution of subspecies and botanical varieties of
A.
hypogaea (Fig. 1):
(1)
The Guarani region, which includes a large part of the basins of the rivers
Paraguay and upper
Paran6 bordering northeastern Argentina (Corrientes and
Misiones, eastern Paraguay, and southern
Mato Grosso and western
S5o
Paulo
in Brazil): subsp.
.fastigiata (var. fastigiata and var. vulgaris).
ECONOMIC
BOTANY
as
Gerais
1
Brazil
Fig.
1.
Centers of origin and diversity of
the
cultivated peanut. Arrows indicate
the
spread (adapted
from Gregory and Gregory
1
976).
(2)
The regions of Goias and Minas Gerais in Brazil: subsp.
.fastigiata
(var.
fastigiata
and var.
vulgaris).
(3)
The region of Rondonia and northeastern Mato Grosso of Brazil, which is
part of the Amazon basin: subsp.
hypogaea
(var.
hypogaea).
(4)
The Bolivian region including the eastern foothills of the Andes: subsp.
hypogaea
(var.
hwvpogaea)
and a few subsp.
.fastigiata
(var.
fastigiata).
(5)
The Peruvian region: subsp.
hypogaea
(var.
hirsuta)
and subsp.
.fastigiata
(var.
-fastigiata).
Gregory and Gregory
(1
976)
identified the sixth gene center to include north-
eastern Brazil: subsp.
fastigiata
(var.
fastigiata
and var.
vulgaris).
The Bolivian
region is believed to be the primary gene center of
A.
hypogaea,
and the other
five regions are assumed to be secondary gene centers (Gregory et al.
1980)
(Fig.
1).
19891
SUBRAHMANYAM
ET
AL.:
PEANUT
PATHOGENS
447
Fig.
2.
Geographical distribution
of
peanut rust (based on Commonwealth Mycological Institute
map
160
issued in
1980).
The peanut is grown throughout tropical and warm temperate regions, approx-
imately between latitudes 40
N
and 40
S.
Peanuts are known to have been cul-
tivated in Peru ca. 2000
B.C.
(Hammons 1973; Krapovickas 1969); this country
is
a
center of diversity for var.
hirsutu
and var.
fastigiara.
From its centers of
origin, peanut spread to the rest of
the world in post-Columbian times (Krapovic-
kas 1969).
ORIGIN
AND
DISTRIBUTION
OF
THE
RUST
AND
LATE
LEAF
SPOT
PATHOGENS
Peanut yields are adversely affected by rust and late leaf spot diseases (Subrah-
manyam et al. 1984). The first record of peanut rust dates back to 1827 or 1828
in a collection made in Surinam by
C.
Weigelt (Hennen et al. 1987). Prior to
1969, the disease was confined largely to South America, although occasional
outbreaks in the peanut-producing areas of the southern U.S.A. were reported
from 19 18 onwards (Hammons 1977). However, peanut rust is not a serious
problem in the U.S.A.
(Mixon et al.
1
983). By the early 1970s rust had spread to
all major peanut-producing areas of Asia, Africa, Australasia, and Oceania
(Brom-
field 1974; Subrahmanyam and McDonald 1983) (Fig. 2). The source(s) of in-
oculum and means of spread responsible for this movement of rust from South
America into these areas are undetermined. The pathogen is known almost ex-
clusively by its uredinial stage. There are a few records of the telial stage on
A.
hypogaeu
and on wild
Arachis
spp. (Hennen et al. 1976, 1987). but the role of
teliospores in the life history of the pathogen is not known. There is no record of
occurrence of any collateral hosts of this pathogen outside of
Arachis.
It is not
known whether the fungus produces pycnia and aecia or whether any alternate
host is involved in its life cycle (Hennen et al. 1987). Hennen et al. (1 976, 1987)
speculated that the fungus produces its sexual life cycle in South America, and
genetic diversity of the pathogen is predicted to have accumulated there. Under-
standing the races of the pathogen and their distribution would help to identify
448 ECONOMIC
BOTANY
[VOL.
43
Fig.
3.
Geographical distribution of peanut late lcaf spot (based on Commonwealth Mycologcal
Institute
map
152
issued
in
1967).
the center of origin. Peanut rust is thought to have originated in South America
along with the domestication of the peanut in prehistoric times (Leppik 197
1).
The restricted distribution of the pathogen in South America until 1969, and its
host restriction to members
3f
,4rachrs,
strongly support this hypothesis.
The late leaf spot pathogen occurs wherever peanuts are grown (McDonald et
al. 1985) (Fig.
3).
Members of
Arachrs
are ~ts only reported hosts (Subrahmanyam
et al.
1985a). The restricted host range within
Aruchls
suggests that the pathogen
might have originated and evolved independently along with its hosts in South
America. The present worldwide distribution of the pathogen is very likely not
an
indigcnous condition, but the result of extensive cultivation of peanut by
humans.
Rust and late leaf spot pathogens may have originated and cocvolved along
with their hosts in South America. However, there are several unanswered ques-
tions regarding the evolution and spread of these two pathogens. Why did the late
leaf spot pathogen spread to the rest of the world from South America much
earlier than rust? When did the late leaf spot pathogen spread to the rest of the
world? How did rust and late spot pathogens spread to peanut-producing countries
outside South America? What and how are the evolutionary changes, if any, in
the centers of origin themselves-in the pathogen by itself, and under the influence
of its host; in the host itself under the influence of
pathogen(s)?
SOURCES
OF
RESISTANCE
TO
RUST
AND
LATE
LEAF
SPOT
The most important peanut foliar diseases causing severe yield losses on a
worldwide scale are the leaf spots (Cercospora arachidicola Hori and
P.
personata)
and rust. Losses in yield due to leaf spots have been estimated at around
10%
in
the U.S.A., where fungicide application is normally practised (Jackson and Bell
1969). In the semi-arid tropics, where chemical control is generally prohibitive,
losses in excess of
50%
are common (Gibbons 1979). In India, combined attacks
