F990 HELIA 29 PG 63

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HELIA. 21. Nr. 29. p.o. 63-72. t1998)

UDC 632.4:633.854.78

Altcrnaria. DISEASE DEVELOPMDNT Llt\[DER
TROPICAL COI\IDITIONS

C. Dudienasl, M. R. G. Ungaro2 and S. A. Moraesl*
1 Centro
2 Centro

de Fitossanidad,e, lnstttuto Agronômico, Secretaria d.a Agricultura
Instttito Agronômico, Caixa Postat 28, 13OO 1-g7O,

d,e Plantas Granlferas,
Carnpinas, SP, Brazil

Receiued: June 16, 1998
Accepted: December 3. 1998
SUMMARY

A field experiment with 12 sowing dates, ranging from February 2, l9B9
to January 19, 1990, in monthly intervals, was carried out in a randomized
block design, with four replications, with the objective to evaluate the development of Alternorid. disease in three sunflower genotlpes. The disease level was
evaluated at lo-day interva.ls, up to physioiogical maturity. The interaction
between sowing dates and genot,?es was statistically significant; furthermore,
the genotype Conti 621 showed less disease severity than VNIIMK 8931 and
IAC-Anhandy. August sowing date showed, on the average, the lower area
under disease progress curve (AUDPC) and disease index (DI), which should
be a consequence ofthe low rainfall during this period.
Key

words: d.lternaria"

disease development, disease severity,

Helianthus

artrtutrs j sunllower

INTRODUCTION
Alternaria leaf spot, câused mainly by Alternaria helianthi (Hansford) Tubaki
& Nishihara, is the main sunflower disease in Sâo Paulo State, Brazil. Lack of vertical resistance, low efficiency of fungicidal control, and possibility of occurrence in
different plant development stages make the disease a potential problem for sunflower crops. The pathogen can cause leaf, stem, petiole, head and flower spots.
The leaf spots are round, necrotic, dark brown with chlorotic halo. These spots
enlarge up to 1.5 cm in diameter, and coalesce, causing leaf drying and defoliation
in severely infected plants. The stem and petiole lesions are brown linear streaks,
that coalesce to form large blackened lesions.
In Brazil, the disease was first observed in 1969 in the States of Pernambuco
(Aquino et aI., l97l), and Sâo Paulo (Ribeiro et al., 1974). According to Carson
(1985), it can cause up to 600/o loss, which depend on the cultivar and the weather
* With

research grants from the National Research Council - CNPq

HELIA,21, Nr. 29, p.p. 63-72, (i998)

conditions. In India, Balasubrahmanian & Kolte (1980) related grain losses up to
80% caused by Alternarta disease in 1995. In China, the yield reduction was 50%
(Li & chi, 1996).
Many factors influence the disease severity. According to Jeffrey et al. (1984)
the cultural debris are a significant source of inoculum. The weather conditions
have great influence in the disease development, specially total rainfall (Sentelhas et
al., 1996). Islam and Marié, mentioned by Abbas et al. (1995), verified that the disease development was greatly favored by temperatures between 24 and 27oC. Aôlmovié (1979) determined the temperature between 25 and 3OoC as the best forA.
heli"anthi infection.
Allen et al. (1983) pointed out that the occurrence of epidemics of Alternaria in
sunflower are much more frequent and severe in areas with long wet summer
together with daily mean temperatures between 25 and 3OoC. Godoy & Gimenes
Fernandes (1985) discussed the possibility of this disease to become a limiting factor to the sunflower culture expansion in Brazil, specially in the sowings from September to December since at this time the conditions for the fungus development
can be ideal.

High humidity is essential for the infection to take place. The conidia need free
water for germination and infection (Frezzl et aL, 1979; Aéimovié, 1979). The infection degree is directly proportional to the water retention period on sunflower
plants, increasing faster when the retention period increases from 12 to 48h (Aéimovié. 1979).
The objective of this research was to evaluate the development of Alternaria
disease in three sunflower genotypes over 12 sowing times'

MATERIALS AND METHODS
The study was carried out in a field experiment with 12 sowing dates ranging
from February 2, 1989 to January 19, f990, in the Experimental Station of Monte
Alegre do Sul (Latitude: 22o4O'S: Longitude:46o40'W).

The genotypes used in the experiments were the varieties tAC-Anhandy and
VNIIMK 8931, and the hybrid Contisol 621. tAc-Anhandy is an open pollinated
variety developed in the Instituto Agronomico (IAC) from cv. Peredovick; VNIIMK
8931 is a Russian variety developed in Krasnodar. They were sown monthly in a
randomized block design with four replications.
Disease severity was recorded during the plant cycle, at lO-day intervals, up to
physiological maturity. In the evaluations done with 10 plants per plot, the percentage of dried leaves and the foliar area affected by the fungus were studied using a
diagrammatic scale proposed byAllen & Brown (1969). With these data a disease
index was calculated for each evaluation and the disease amount in each cycle was
obtained. The disease index was calculated using the following expression:

HELIA,21, Nr.29, p.p. 63-72, (1998)

oI = [(Ar +Aù/2 + DLI /2
where,
Ar : o/" of disease level on the first live bottom leaf
A2 = "/" of disease level on the second live bottom leaf
DL

number of dried leaves multiplied by lOOo/"
With those indices, determined for each evaluation, an Alternaria leaf spot
progress curve was constructed, and the disease amount calculated using the area
under disease progress curve (AUDPC), according to Moraes et at. (1988):
AUCDP= X[(Yi+r +Yi)/2] {(4+r -Xi)1}
where,
Yi+ r : 7o of disease - infected area in the ith+ I observation

Yi = o/o of disease - infected

area in the i6 observation
X i+r = number of days from sowing in the in * I observation
Xi : number of days from sowing in the i6 observation
All data acquired were transformed to DI and AUDPC and submitted to analysis
of variance. The Duncan test at 5% was used for mean comparisons.
Table

Accumulated diseâse indexl for the three genotlpes, in twelve sowing dates, under
natural field infection. Means of four renlications
Genotype

Sowing date
15112189
3o/1 o/892

05104189
07103189
03/1 0/89
01

/09/89

05/05/89
19/01/90
o2106189
02102189
05107189
1

1/08/89

Mean

IAC-Anhandy

a
228.81 a
204.36 b
228.29 a
'193.20 bc
191 .21 bc
166.81 de
178.25 cd
157.84 e
131.53 f
161.44 de
133.83 f
183.s4
226.91

VNIIMK 8931
A

219.69 a

Conti 621
A

222.77 a

Mean
223.12 a

214.74 ab

210-87 a

218.14 a

198.37 bc

't81 .95 b

194.89 b

188.79 cd

159.07 c

190.39 cd

185.23 b

186.95 cd

177.28 b

189.61 b
'185.14 b

172.30 d

149.87 c

162.99 c

186.91 cd

121 .95 d

162.37 c

188.59 cd

130.86 d

159.10 c

175.72 d

151.27 c

152.84 cd

151 .29 e

127.63 d

146.79 d

121.41 t
'182.93

119.44 d

124.90 e

tot.cz

192.05 b

Cv(%) = 6.72
Means followed by the same letter in the column and the same capital letter in the line are not
statistically different by Duncan at 5%.
1
Sum of individual evaluations of disease index.
2
Designated as November sowing because the emergency period occurred in November.

RESULTS AND DISCUSSION
The statistical analysis indicated significant differences between the diseases
index (DI) and the values of the area under disease progress curve (AUDPC) for
sowing dates and genotypes. Table I presents the sum of individual evaluations of

HELIA,21, Nr. 29, p.p. 63-72, (1998)

DI for the three genotypes. The lowest DI was obtained in August sowing for all cultivars and also in February in the case of cv. IAC-Anhandy. The interaction between
sowing dates and genotypes was statistically significant; furthermore, On the average, the genotype Conti 621 showed less disease severity in comparison with the
other two. Comparing the DIs, November and December had similar disease levels.
According to Figure l, the DI values of August sowing showed, until 54 days after
emergence, the maximum of 13.15% for IAC-Anhandy and, at the end of this cycle,
this index did not reach 31"/o. The low level of disease development presented in
August sow'ing should be a consequence of the low rainfall in the period. In the first
22 days after emergency the total rainfall was 76 mm, which decreased after that,
having no rain at all during the flowering period and 95.6 mm befween 73rd and
B2ttd day after emergency.
80
70

x60
Èi ro

Zqo
a

.< 30
(n

À20
l0
0
22

DAYS AFTER EMERGENCY

Fi.gure

Seasonal patterns oJ Dl in three su4flower genotApes sor,n in August

According to Godoy & Gimenes Fernandes (1985), the disease can have a fast
development under favorable conditions, leading to conspicuous differences each
seven days. The same happened in the present research in which, that when the
total rainfall between two evaluations showed a significative volume, there was a
disease index increasing in the subsequent interval.
The DI data were statistically equal in May, June and January (Table 1). For
May (Figure 2) the DI almost did not change, staying between 7 and l5o/" until the
middle of the flowering period; after that, it increased fast till physiological maturity. Between 88h and 99ù day after emergence (11 days) the DI doubled, reaching
3O% for'r'NIIMK 8931. Until 68 days after emergence the total rainfall was only 40.5
mm, and the disease was kept at very low levels; between the 69m and the BBU day
after emergence the total rainfall was 98.7 mm which favored the disease development and showed that the DI of the following period was almost two times greater,
for all cultivars. In the sowing of June, according to Figure 3, the DI stayed near

HELIA, 21, Nr. 29, p.p. 63-72, (1998)

untll94h day after emergence; it jumped up to 30% in the next evaluation and
stayed at this level until I15ft day after emergence for lAC-Anhandy and Conti-621.
2Oo/o

80
70

l**w*vNilMK

660

l--e--coNï

tso
o

I
I

Z+o
o
fi30
o
e,20
uJ

10
0
'r

109

tzu

DAYS AFTER EMERGENCY

Figure

Seasonal patterns oJ Dl in three su4flotter genotApes sotun tn May

80
70

660
ôso
o
zao
UI

tt,

fi30
U'
-a

20
10
0

104 15
1

122

DAYS ÀFTER EMERGENCY

Ftgure

Seasonal patterns oJ DI in three sunJTouer genotgpes sotun in June

As the genotypes evaluated in the present research showed cycle interaction
with sowing time, they sometimes presented different total cycles, and the number
of observations were not the same in all growing seasons. According to Allen ef al.
(1983), the susceptibility to A. heltanthi changes at different development stages of
the sunflower plant. Sowings in May and June resulted in the larger life cycles of
sunflower cropp. As VNIIMK 8931 enlarged its life cycle, compared with the other
genoqæes, in June sowing (Figure 3), its DI almost reached 4oo/o al the end of the

HELIA, 21, Nr. 29, p.p. 63-72, ( i998)

cycle, although the initial DIs were not high. The same happened for May sowing
(Figure 2) but for all cultivars.
80
70

660
Ëuo
o
2

;40

(t,

ff30
L
o20
10

DAYS AFTER EMERGENCY

Figure

Seasonal patterns oJ Dl in three su4flotuer genotApes sotun in October

80
70

660

tso
o
lqo
ul

o
fi39
o
c-20
10

DAYS AFTER EMERGENCY

Figure

Seasonal patterns oJ DI in three su4flotuer genotApes sorun in Nouember

During the first 30 days after emergence, the disease was maintained at low levll-13o/o) and in the subsequent 40 days it increased about four times in
the sow'ing in October (Figure 4). November showed the DI near lO% only 24 days
after the emergence and just before harvest it reached more than 7O"/" for Conti 621
(Figure 5). At the same periods, the sow'ing of December showed 25o/o in the 4th
week after emergence and near 4Oo/o at physiological maturity (Figure 6). In relation
els (DI:

HELIA,21, Nr. 29, p.p. 63-72, (1998)

to disease index the sowing in February was classified between the lowest ones onlv

for cv. IAC-Anhandy (Figure

7).

80
70

îuo
ôso
o

4rc
ul

(t,

fi30
â20
U'

DAYS AFTER EMERGENCY

Figure

6: seasonal patterns

DI in three su4flotoer genotapes sourn in December

80
70

ôou

*uo
e
:40
u
u,

fi30
I
.9 zo
10

3101735455473
DAYS AFTER EMERGENCY

Figure 7: seasonal patterns

DI in three sunflou:er genotapes

so:uln

in Februarg

Table 2 shows the AUDPC for all cultivars and sowing times. Mean AUDpc for
July and January sowings was l5olo and 3s% higher, respectively, than August sowing; however, the AUDPC for Conti 621 was not statistically different in tiose three
sowing dates. May and June presented intermediate data for AUDpc. The AUDpc
for May was statistically equal to January sowing date, except for cont 621.
November showed the highest AUDpc, followed by December (Table 2). Data of
AUDPC for the sowing in March, April and october were intermediate.

HELIA,2l, Nr. 29, p.p. 63-72, (1998)

Table 2: Area under the curve of disease progress (AUCDP) in three sunflower genotlpes
evaluated in twelve sowing dates under natural field disease infection. Means of four

replications
Genotype
date
30/1 0/89
15112189
03/1 0/89

021o2189

05/04/89
07103189
01

/09/89

02106189

05/0s/89
19/01/90
051o7189
1 1

/08/89

Mean

IAC-Anhandy

a
abc
1856.06 bc
1522.42 eI
1758.27 cd
1978.36 ab
1647.65 de
1489.62 ef
1560.83 ef
1573.26 e
1410.30 f
1154.34 g
2024.47

1875.15

A
A
A
B

A
A
A
A

1654.23

a
1836.95 abc
1842.93 abc
1943.17 a
1762.43 bcd
1693.60 cde
1608.90 de
1896.77 ab
1589.25 e
1642.22 de
1304.38 f
1050.61 g
1939.22

1678.37

Mean

Conti 621

VNIIMK 8931
AB

1854.48 a

1939.39 a

1819.47 a

1843.86 b

1765.00 a

1579.42 b

1691 .67 c

1542.54 b

1333.77 cd

1465.29 bc

'1213.30 d

821 .33 b

1687.75 c
1668.58 c

1573.95 d

1355.26 cd

1501 .78 de

1068.18 e

1427.88 e

1008.20 e

1240.96t

1027.11 e

1077.35 g

1s33.23 d

1419.34

CV(%) = 6.45
Means followed by the same letter in the column and the same capital
statistically difierent by Duncan at 5%.

in the line are not

conti 621 showed, in all sowing times, lower or equa-l accumulation of DI and
AUDPC than the other genotypes (Tables I and 2). This fact is probably related to
the hybrid precocity since Sentelhas et al. (1996) related that Conti 621 susceptibilIty to Alternaria leaf spot was greater than in VNIIMK 8931'
The level of disease incidence seems not to be strongly related to the primary
inoculum; the disease evaluations were realized during the second year of trial, in
area with great amount of initial inoculum since the disease appeared in the previous sowings and the debris stayed in the field. The variation in the disease level was
(1996)'
clearly related to climatic factors, already discussed by Sentelhas et al'
Figures 5 and 6 exhibit the disease progress curves for November and December sowing dates, which presented the higher mean values for the AUDPC and corresponded to ttre periods of the greatest rainfall amount' reaching more than 600
mm for the whole culture cYcle.
The difference between the genotypes susceptibility level in sunflower lines was
discussed by carson (i985) and by Lipps & Herr (1986) fot 497 Helianthus
annuus introductions.
The climatological data of the studied cycles with great level of Alternaria incidence presentèd high humidity and temperature (Sentelhas et al.. 1996), which
(1979) observed
agree with Allen et al. (1983). Frezzi et aL (1979) and Aéimovié
to germinate
in
order
free
water
of
hours
two
that the conidia need between one and

HELIA, 21, Nr. 29, p.p. 63-72, (r998)

and to develop the infection. The infection rate increases fast when the water retention goes up to 48 hours (Aéimovié, 1979).
In a greenhouse inoculation done by Moraes ef al. (1988), it was observed that
young leaves had isolated necrotic spots while in the old leaves the spots tend to be
coalescent, the leaves present increasing dried areas, and often fall down seven
days after inoculation, leading to an early senescence.

CONCLUSIONS
The geno[rpes showed different levels of disease susceptibility. Conti 621 was
less susceptible than the others genotlpes.

Conti 621 showed the lowest DI in the sowings in January, June, July and
August; \,T{IIMK 8931 was less affected by the disease in the sowing in August, and
IAC-Anhandy, in the sowing in August and February.
The level of disease incidence was not strongly related to primary inoculum.
There was a clear relationship between disease level and climatic factors.

REFERENCES
Abbas, H.K., Egley, G.H. and PauI, R.N., 1995. Effect of conidia production temperarure on
germination and infectivity of Alternaria hetianthi. phytopathol., 85 (6) : 6Z Z -6g2.
Aéimovié, M., 1979. Effect of some ecologica-l factors on sporulation of Alternaria helionthi
(Hansf.)Tub. & Nish. and on infection of sunflower. Zaïtita Bilja,30: b9-68.

Allen,S.J.,Brown,J.F.andKochman,J.K., lg83.Productionofinoculumandfieldassessment
of Alternaria helianthi on sunflower. Piant Dis., 67: 665-668.
Aquino, M.L.N., Bezerra, J.L. and Lira, M.A., 1979. ocorrência do crestamento do Éirassol
(Helianthus annLr-us L.) em Pernambuco. Revista de Agricultura, 46: lbl-156. Balasubrahmanian, N. and Kolte, S.J., 1980. Effect of different intensities of Alternartablipl-tt
on yield and oil content ofsunflower. J. Agr. Sci., 44:249-ZSl.
Carson, M.L., 1985. Reaction of sunflower inbred lines to two foliar diseases. Plant Dis., 6g:
986-988.
Frezzi,M.J., Giorda, L.M. andLjubich,A,. IgT9.HelminthosportumhelianthiHansford, agente
causal de la Helmisthosporiosis de1 girasol (Heliqnthus annllus L.) en Argenltina.
Informacion Tecnica, 83. Estaci6n Experimental Agropecuaria Manfredi. INTA. Càrdoba.
I

lp.

Godoy, J.R. and Gimenes Fernandes, N., 1985. Alternaria heltanthi (Hansf.) Tubaki &
Nishihara em girassol (Helianthus annuus L.): Influência da idade da planta na suscetibilidade e na infecçâo das sementes. Summa phytopathologica, l l(3-4): la6-rc2.
Jeffrey, K.K., Lipps, P.E. and Herr, L.J., 1984. Effects of isolate virulence, plant age, and crop
residues on seedling blight of sunflower caused by Alternarin heliànthi. Phytopathol.,
74(9): lr07-lllO.
Li, Y. and Chi, L., 1996. Study on black spot of sunflower. In: International Sunflower
Conference, f 4, Beijing/Sheniang, I 996. Proceedings. p. 8 I O-8 I 5.
Lipps, P.E. and Herr, L.J., f 986. Reaction of Heli.anthus (annuus and H. tuberosus plant
introductions To Alternaria helianthi. Plant Dis., 7Ot9): 831-835.
Moraes, S.4., Godoy, I.J., Gerin, M.A.N., Pedro Jr., M.J. and pereira, J.C.V.N.A.. 1988.
Epidemiologr of Cercosporidium personatum em genôtipos de amendoim. Fitopatologia

Brasileira, l3(3): 255-260.
Moraes, s.4., ungaro, M.R.G. and Mendes, B.M.J., rg93. Alternarta helianthi, âgente causal
de doença em girassol. Fundaçâo Cargill, Campinas. 2Op.

HELIA, 21, Nr. 29, p.p. 63-72, ( 1998)

Ribeiro, I. J. A., Paradela F'., O.; Soave, J. and Cerveliini, G. S., 1974 OcorrênciadeAlternaria
helianthi(Hartsf. ) Tubaki & Nishihara sobre girassol (Helianthus annuus L. ). Bragantia,
33: 8l-85, (nota n'17).
sentelhas, P.c.,Pezzoparte, J.R.M., Ungaro, M.R.G., Moraes, S.A. and Dudienas, c., 1996.
Aspectos climâtiôos relacionados à ocorrência da mancha de Alternaria em cultivares de
girassol. Fitopatologia Brasileira, 2l(4) :464-469.

DESARROLLO DE LA ENFERMEDAD ALTERNARIA EN
CONDICIONES TROPICALES
RESUMEN
Un campo experimental fue sembrado mensualmente del febrero de 1989

al enero de 199O, con el objetivo de evaluar eI desarrollo de la enfermedad

Alternaria en tres genotipos de girasol, siguiendo un diseflo de bloques aleatorios con cuatro repeticiones. El nivel de la enfermedad fue evaluado en un
intervalo de lo dias hasta la madurez fisiolôgica. La interaccciôn entre las
fechas de siembra y los genotipos eran estadistcamente significativas; ademâs,
la severidad de Ia enfermedad era menor en el genotipo Conti 621 que en VNIIMK 893f e lAC-Anhandy. La fecha de siembra de agosto mostraba, en general,
el nivel mâs bajo ârea bajo la curva del progreso de la enfermedad (AUCDP) y
de indice de la enfermedad (DI), lo cual podria ser una consecuencia de la baja
pluviosidad durante este periodo.

DEVELOPPEMENT DE LA IT{ALI\DIE ALTERNARIA EN
CONDITIONS TROPICALES
RESUME

Un champ expérimental a été planté mensuellement, de féwier 1989 à
janvier 199O, avec pour objectif, l'évaluation du développement de la maladie
Alternaria pour trois génotypes de tournesol, selon un dispositif de blocs aléa-

toires avec quatre répétitions. Le niveau de Ia maladie a été évalué tous les lo
jours jusqu'â la maturité physiologique. L'interaction entre dates de plantation
et génot,?es est significativement différente; deplus, la sévérité de la maladie a
été moins importante sur le génot]?e Conti 621 que sur VNIIMK 8931 et IACAnhandy. La date de plantation d'août a montré, en moyenne, la plus baisse
aire en dessous de la courbe du progrès de la maladie (AUCDP) et le plus bas
index de la maladie {DI), ceci pourrait être Ia conséquence de la faible pluviosité pendant cette Période.

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