Disease Management in Sunflowers

Abstract

The expansion of sunflower can be affected, among other factors, by the presence of diseases, since it hosts over 30 phytopathogenic microorganisms, mostly fungi, which may, depending on climatic conditions that favor the occurrence of pathogens and the infective process, lead to a significant reduction on yield and quality of product. Alternaria leaf spot and Sclerotinia wilt and head rot are the most severe diseases in Brazil. Other important diseases occurring worldwide, like downy mildew, powdery mildew, Phomopsis stem canker and sunflower rust, are likely to affect sunflower, under very diverse climatic conditions. Once installed on the crop, sunflower diseases are hard to control. Therefore, measures of disease management are mostly preventive and should not be used alone. Effective control is based on an integrated program, which includes zoning for climate risk and diverse cultural practices. The present chapter aims to discuss about the most important sunflower diseases and strategies for disease management, in order to give support for the sustainability and competitiveness of the sunflower crop.

Full text

In: Sunflowers ISBN: 978-1-63117-347-9
Editor: Juan Ignacio Arribas © 2014 Nova Science Publishers, Inc.
Chapter
DISEASE MANAGEMENT IN SUNFLOWER
Regina M. V. B. C. Leite*
Embrapa Soybean, Brazil
ABSTRACT
The expansion of sunflower can be affected, among other factors, by the presence of
diseases, since it hosts over 30 phytopathogenic microorganisms, mostly fungi, which
may, depending on climatic conditions that favor the occurrence of pathogens and the
infective process, lead to a significant reduction on yield and quality of product.
Alternaria leaf spot and Sclerotinia wilt and head rot are the most severe diseases in
Brazil. Other important diseases occurring worldwide, like downy mildew, powdery
mildew, Phomopsis stem canker and sunflower rust, are likely to affect sunflower, under
very diverse climatic conditions. Once installed on the crop, sunflower diseases are hard
to control. Therefore, measures of disease management are mostly preventive and should
not be used alone. Effective control is based on an integrated program, which includes
zoning for climate risk and diverse cultural practices. The present chapter aims to discuss
about the most important sunflower diseases and strategies for disease management, in
order to give support for the sustainability and competitiveness of the sunflower crop.
Keywords: Alternariaster helianthi, Sclerotinia sclerotiorum, Plasmopara halstedii,
Erysiphe cichoracearum, Phomopsis helianthi, Puccinia helianthi
INTRODUCTION
Sunflower (Helianthus annuus L.) cropped area is increasing in Brazil, with 74 thousand
hectares in the last growing season (Conab, 2013). In the world, sunflower production in
2012/2013 was 36 million tons of oilseeds, 14 million tons of meal and 13 million tons of oil.
The largest producers were: Ukraine (24.7%), Russia (21.8%), European Union (19.1%),
Argentina (8.8%) and Turkey (2.8%) (United States, 2013).
* Embrapa Soybean, C.P. 231, CEP 86001-970, Londrina, PR, Brazil. Email: regina.leite@embrapa.br.

Regina M. V. B. C. Leite
166
However, there is an enormous potential for expansion if sunflower is planted as a second
summer crop, in succession to soybean, which occupies an area of around 28 million ha in
Brazil (Conab, 2013). The potential for area expansion is also driven by a crescent demand
for special oils for human consumption, for example high oleic oil, and the Brazilian
government demand for biofuel.
The expansion of sunflower can be affected, among other factors, by the presence of
diseases caused by viruses, bacteria, fungi and nematodes. Sunflower hosts over 30
phytopathogenic microorganisms, mostly fungi, which may, depending on climatic conditions
that favor the occurrence of pathogens and the infective process, lead to a significant
reduction on yield and quality of product (Zimmer & Hoes, 1978; Gulya et al., 1997).
It is estimated that diseases are responsible for an average annual loss of 12% of the
world production of sunflower (Zimmer & Hoes, 1978), this being the most limiting factor
for crop production in most regions. In Brazil, there is no accurate data on yield losses caused
by disease, but it is known that can reach 100%, depending on climate conditions. In the state
of Paraná, for example, diseases were considered one of the main factors responsible for the
decline in the production of sunflower in the early 1980s, with the reduction of cultivated area
of approximately 80,000 ha in 1981 to about 5,000 ha in 1984. The yield, which reached 1800
kg per hectare in the previous year, was reduced to 480 kg per hectare, caused by excessive
moisture and low temperatures in the end of the cycle, which favored the occurrence of
Sclerotinia sclerotiorum (Yorinori et al., 1985).
At least 19 diseases have already been reported affecting sunflower in Brazil (Table 1).
Table 1. Diseases affecting sunflower previously reported in Brazil
Disease Pathogen References
Alternaria leaf spot Alternariaster helianthi, Alternaria
zinniae and Alternaria alternata
Embrapa (1983), Yorinori et al. (1985)
Bacterial blight Pseudomonas cichorii Embrapa (1983), Yorinori et al. (1985)
Bacterial leaf spot Pseudomonas syringae pv. helianthi
Kimura et al. (1974)
Bacterial stalk rot and head rot
Pectobacterium carotovorum subsp.
carotovorum
Embrapa (1983), Yorinori et al. (1985)
Charcoal rot Macrophomina phaseolina Embrapa (1983), Yorinori et al. (1985)
Downy mildew Plasmopara halstedii Embrapa (1983), Yorinori et al. (1985)
Gray mold Botrytis cinerea Embrapa (1983), Yorinori et al. (1985)
Phoma black stem Phoma oleracea var. helianthi-
tuberosi
Embrapa (1983), Yorinori et al. (1985)
Phomopsis stem canker Phomopsis helianthi Embrapa (1983), Yorinori et al. (1985)
Powdery mildew Erysiphe cichoracearum Embrapa (1983), Yorinori et al. (1985)
Rhizoctonia root rot Rhizoctonia solani Embrapa (1983), Yorinori et al. (1985)
Rosellinia root rot Rosellinia sp. Embrapa (1983), Yorinori et al. (1985)
Rust Puccinia helianthi Embrapa (1983), Yorinori et al. (1985)
Sclerotinia wilt and head rot Sclerotinia sclerotiorum Embrapa (1983), Yorinori et al. (1985)
Sclerotium wilt and damping
off
Sclerotium rolfsii Embrapa (1983), Yorinori et al. (1985)
Septoria leaf spot Septoria helianthi Maldaner et al. (2009)
Sunflower mosaic virus Bidens mosaic virus (BiMV) Embrapa (1983), Yorinori et al. (1985)
Verticillium wilt Verticillium dahliae Almeida et al. (1981)
White rust Albugo tragopogonis Almeida et al. (1981)

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167
Some diseases have significant importance, like Alternaria leaf spot and Sclerotinia wilt
and head rot, which are the most severe (Embrapa, 1983). Alternaria disease seems to be
prevalent in all sowing dates, in different growing regions (Leite et al., 2006). Sclerotinia
head rot is one of the main diseases occurring worldwide and occurs mainly under conditions
of low temperature and high humidity, making it almost impossible to cultivate sunflower as
a commercial crop during the autumn in southern Brazil (Leite et al., 2000). Furthermore, this
pathogen can leave resistance structures (sclerotia) in the soil, which may remain viable for
many years and constitutes a source of inoculum for other host crops, like soybean, canola,
and beans, which may be affected in the next growing seasons. Otherwise, other important
diseases in the world, like downy mildew, powdery mildew, Phomopsis stem canker and
sunflower rust, are likely to affect sunflower in our country, since it is grown from latitude
31ºS to latitude 2ºN, under very different climatic conditions that can favor diseases.
The present chapter aims to discuss about the most important sunflower diseases and
strategies for disease management, in order to give support for the sustainability and
competitiveness of the sunflower crop.
SUNFLOWER DISEASES
Alternaria Leaf Spot (Alternariaster helianthi)
In areas of tropical and subtropical climates, that are prevalent in Brazil, Alternaria leaf
spot is a major disease, occurring in virtually all regions and in all sowing dates. The damage
caused by the disease can be attributed to a great reduction in photosynthetic area of the plant
(Leite et al., 2006). Severely attacked plants show early maturation, with reduced production
and seed weight. Besides Brazil (Aquino et al., 1971, Ribeiro et al., 1974), the disease occurs
in countries of North America and Africa, Argentina, India, Japan, Australia, Serbia and
Montenegro (former Yugoslavia), Romania and France (Anahosur, 1978; Zimmer & Hoes,
1978; Davet et al., 1991; Pereyra & Escande, 1994).
Typical initial symptoms on leaves are small necrotic lesions with 3 to 5 mm diameter,
variable color from brown to black, and round to angular chlorotic halo (Figure 1).
Characteristic lesions exhibit concentric circles, similar to a target. These lesions may
coalesce, forming large areas of necrotic tissue, causing premature defoliation of plants. The
symptoms occur primarily in the lower leaves, appearing later in the whole plant. However,
there may be generalized infection of the leaves, regardless of their position on the plant. On
stem and petiole, lesions start as small dots or stripes, and when numerous can form large
necrotic areas. Severe attack can result in blight and finally plant death. The fungus also
colonizes floral bracts and receptacle and may even cause head rot (Anahosur, 1978; Almeida
et al., 1981; Davet et al., 1991).
Various fungi species cause similar symptoms in sunflower plants. Three species of the
fungus are reported as pathogenic to sunflower in Brazil: Alternariaster helianthi (Hansf.)
E.G. Simmons (syn. Alternaria helianthi (Hansf.) Tubaki & Nishihara and Helminthosporium
helianthi Hansf.), Alternaria zinniae H. Pape ex M.B. Ellis and Alternaria alternata (Fr.)
Keissler (syn. Alternaria tenuis Nees). The first one is the most commonly found.

Regina M. V. B. C. Leite
168
Figure 1. Alternaria leaf spot in sunflower.
The conidia of A. helianthi are cylindrical to ellipsoidal, colorful and dimension of 74 x
19 µ m. They have five transverse septa, no tail, and are formed singly in cylindrical
conidiophores. The mycelium is olive-brown, septate, branched and colonizes the
intercellular spaces of the mesophyll cells. The fungus grows slowly and sporulates well on
medium potato-dextrose-agar, forming grayish colonies. A. helianthi is also pathogenic to
chrysanthemum and all annual and perennial species of Helianthus. No physiological
specialization is reported (Anahosur, 1978; Gulya et al., 1997; Simmons, 2008).
The fungus can be spread by contaminated seeds, due to its presence internally or in plant
fragments mixed in the lot, which can remain viable for many years (Godoy & Fernandes,
1985a). However, the major source of primary inoculum consists in plant debris infected with
the fungus (Davet et al., 1991). Under favorable conditions, the fungus produces a large
amount of conidia that are spread by wind and rain, and reach other parts of the plant or other
plants. The optimum conditions for conidia germination are high relative humidity and
temperature between 25°C to 30°C. The germ tube penetrates directly through the epidermis
and the cuticle (Davet et al., 1991). The fungus is highly pathogenic under favorable
conditions. The optimum conditions for infection by A. helianthi are leaf wetness for 24 h at
25°C (Leite & Amorim, 2002). The sunflower plants are susceptible at all stages of
development, with a phase of increased susceptibility from the flowering to the beginning of
grain filling (Anahosur, 1978; Davet et al., 1991). The relationship between Alternaria
severity and yield in the R3 (second phase of inflorescence elongation) growth stage proved
that plants with disease severity higher than 10% had yield lower than 500 kg per hectare,
regardless of the sowing date (Leite et al., 2006). The disease progresses rapidly from the
lower leaves to upper leaves. More severe infections occur in later stages of development,
after flowering (Allen et al., 1983; Godoy and Fernandes, 1985b; Pereyra & Escande, 1994).
Genetic resistance is quantitative, based on the intensity of infection. Studies under
condition of natural infection showed that all tested genotypes were susceptible to A.

Disease Management in Sunflower
169
helianthi, with different levels of resistance (Leite et al., 1999; Leite & Oliveira, 2012).
Sunflower breeding program should be directed to higher disease resistance. Studies
developed in India indicate that it is possible to synthesize hybrids with reasonable degree of
tolerance even involving susceptible parents (Keertht et al., 2012). Certain species of
Helianthus as wild H. annuus, H. hirsutus, H. rigidus and H. tuberosus, show resistance to A.
helianthi (Lipps & Herr, 1986; Davet et al., 1991). The interspecific hybridization may allow
the incorporation of resistance genes in cultivated genotypes (Davet et al., 1991).
Survival of the fungi species affecting sunflower crop debris indicates prophylactic
control measures. Sunflower should be included within a system of crop rotation, returning in
the same area only after at least four years. The destruction or incorporation of infected crop
debris is recommended to limit sporulation and the amount of primary inoculum (Davet et al.,
1991).
A key measure to minimize the severity of Alternaria leaf spot is the choice of sowing
date. Adjustment of sowing dates is an obviously good strategy to minimize the disease and
obtain better yields (Gadhave et al., 2011). Late sowing is favorable to high Alternaria disease
severity in sunflower crop in Rio Grande do Sul, Brazil (Loose et al., 2012). Sowing should
be done at a time which satisfies the requirements of the plant at different stages of
development, and not favorable to this disease. To minimize the occurrence of disease, it
should avoid when the flowering coincides with periods of heavy rain.
Chemical control with fungicides can be difficult due to the inability of the conventional
input machines enter the crop, because of high plant height. However, fungicides such as
benomyl, imazalil, iprodione, mancozeb + iprodione, procymidone, propiconazole and
vinclozolin were effective in controlling the disease in other countries, with substantial
increases in yield, achene weight and oil content (Pereyra & Escande, 1994; Gulya et al.,
1997; Karuna et al., 2012). In Brazil, fungicides azoxistrobin + ciproconazole and
difenoconazole are registered for control Alternaria leaf spot in sunflower (Ministério, 2012),
but there are no available data that indicates efficiency on disease control until now.
Sclerotinia Wilt and Head Rot (Sclerotinia sclerotiorum)
This fungus is considered the most important pathogen for sunflower in the world and is
distributed in all regions, under temperate, tropical or subtropical climates (Gulya et al.,
1997).
The losses caused by Sclerotinia sclerotiorum depend on the part of the plant affected by
the fungus, which can infect roots, stem or sunflower head. The losses attributed to basal rot
depend on plant age at the infection. S. sclerotiorum quickly kills the infected plants at
seedling stage, resulting in stand failures. Losses associated with head rot directly affect yield,
reducing the number of seeds per chapter, seed weight and oil content. The oil quality is
lower due to the increased concentration of free fatty acids on seeds infected by the fungus.
Seeds of infected head can fall, resulting in total loss of production (Zimmer & Hoes, 1978;
Davet et al., 1991; Masirevic & Gulya, 1992; Pereyra & Escande, 1994). In the state of
Paraná, Brazil, incidence of stem and head disease was high (17.6% to 100.0%), when
sunflower was cultivated after the harvest of summer crops in 1996-1998 growing seasons
(Leite et al., 2000). Indirect losses occur due to contamination of seeds with sclerotia, often of
the same size, shape and specific weight of these, being impossible their removal during

Regina M. V. B. C. Leite
170
cleaning operation. In addition to these losses, the fungus persists in the soil for many years,
representing a potential danger for sunflower and other hosts (Zimmer & Hoes, 1978; Davet
et al., 1991; Masirevic & Gulya, 1992; Pereyra & Escande, 1994).
S. sclerotiorum can cause different symptoms in sunflower (Zimmer & Hoes, 1978;
Almeida et al., 1981; Davet et al., 1991; Masirevic & Gulya, 1992; Pereyra & Escande, 1994;
Gulya et al., 1997).
The basal rot may occur from the seedling stage to maturity. In seedlings, infection is less
frequent, as plants die quickly and the process does not result in spread to other plants.
Infection is mostly observed near flowering. Diseased plants appear as a group of two or more
plants on the line. Rot starts when the mycelium of the fungus, originating from sclerotia in
the soil, comes in contact with the lateral roots. The first symptom observed is a sudden
wilting of the plant. The infected plant can recover turgidity at night or after a rainfall, but
within a few days, this symptom becomes irreversible, and the disease is named Sclerotinia
wilt. A light brown and soft injury appears at ground level and typically surrounds the rod. If
there is high humidity, the lesion may be covered by white mycelium. The fungus develops
internally and destroys the internal tissues of the stem. Many sclerotia are found within the
colonized portion of the stem, but few are found in the root and in the outdoor area. Diseased
plants can lodge easily.
The rot in the middle portion of the stem occurs in plants from the end of the vegetative
stage to maturity. Infection occurs on leaves wounds and proceeds toward the petiole, ending
the stem. The appearance of the lesion is similar to those of the basal rot. It is most noticeable
in mature stems, because the affected tissue appears lighter than the normal brown coloring
physiological maturity. A white mycelium can cover the lesion, and sclerotia are observed
within the stem. Plants can break at the lesion site.
Figure 2. Sclerotinia head rot in sunflower.

Disease Management in Sunflower
171
Symptoms in sunflower heads occur at the end of flowering or later. The infection may
start in any part of the receptacle. The initial symptoms are characterized by light brown and
soft lesions on the dorsal side of the head covered by portions of white mycelium (Figure 2).
Eventually, the fungus destroys the interior of the head, leaving intact only the vascular
elements. Sclerotia in large numbers and irregular shape are found within the head. Finally,
there is the complete disintegration of the head, which remains with the exposed fibrous
vascular elements, like a broom. A mass of achenes and sclerotia falls into the base of the
plant.
Sclerotinia sclerotiorum (syn. Sclerotinia libertiana Fuckel and Whetzelinia sclerotiorum
(Lib.) Korf & Dumont) form mycelium and sclerotia in the asexual phase and asci with
ascospores in the sexual phase. Microconidia are produced in senescent cultures in the
laboratory, can be functional for asexual reproduction, but their role in the biology of the
pathogen is not known. The mycelium is composed of hyaline multicellular hyphae with 6.5
to 7 µm in diameter (Mordue & Holliday, 1976).
Sclerotia is formed from the anastomosis of a large number of hyphae in a hard body with
variable format, and may reach several centimeters long. Sclerotium germination occurs in
two ways: a myceliogenic way forming only hyphae and another carpogenic way producing
apothecia (Masirevic & Gulya, 1992; Gulya et al., 1997).
The apothecium is a flat or cup-shaped structure that produces sexual spores of S.
sclerotiorum. Many apothecia may be formed from a single sclerotium. The apothecia are
pale brown in color and have 4 to 10 mm in diameter. Moist soil for a long period and light
are essential for the formation of apothecia. The upper layer contains many paraphyses and
asci. The asci are cylindrical and extended to the apex and range 130-163 µm long and 8 to 10
µm wide (Mordue & Holliday, 1976; Zimmer & Hoes, 1978; Davet et al., 1991; Masirevic &
Gulya, 1992; Gulya et al., 1997).
S. sclerotiorum is a polyphagous fungus, having as host plants of 75 families, 278 genera,
408 species and 42 subspecies or varieties. Except one species of the phylum Pteridophyta, all
hosts of S. sclerotiorum belong to phyla Gymnospermae and Angiospermae (Boland & Hall,
1994). No reports of physiological specialization of the fungus are available (Mordue &
Holliday, 1976; Gulya et al., 1997).
The sclerotium begins and ends the life cycle of S. sclerotiorum (Zimmer & Hoes, 1978).
Miceliogenic germination of sclerotia causes infection on tissues of the base of the plant to
produce root rot, stem rot and wilting (Davet et al., 1991). The hyphae penetrate through
tissue injuries or stomata by the cuticle, invading the intercellular spaces, and finally reach the
interior of cells. The fungus causes lesions visible at the base of the stem and wilting of
shoots due to obstruction of the conducting vessels (Pereyra & Escande, 1994). Secondary
contamination is possible through direct contact of the diseased tissue with healthy tissue
from neighboring plants (Davet et al., 1991). Carpogenic germination of sclerotia generates
the apothecia, which emerge on the soil surface and release the ascospores. In conditions of
high relative humidity above 70% a mature apothecium can produce up to 2 x 108 ascospores
over a period of several weeks. The ascospores are released at temperatures of 3ºC to 22ºC,
with greater intensity between 19ºC and 20ºC. Temperatures above 25ºC and relative
humidity below 35% are limiting for ascospore survival. The ascospores germinate in
favorable conditions and infect the host, causing mainly head and stem rot. The susceptibility
to infection of the sunflower head is higher in the period between the initial flowering and up
to two weeks after flowering. After a latent period of 15 to 40 days, the fungus invades the

Regina M. V. B. C. Leite
172
parenchyma and causes tissue rotting. The optimum temperature for development of the
mycelium is between 18ºC and 25ºC. The sclerotia produced within and on the surface of the
colonized tissuse return to the soil and crop debris are responsible for the conservation of the
fungus (Zimmer & Hoes, 1978; Davet et al., 1991; Gulya et al., 1997). The sclerotia can
remain in the soil for many years, keeping intact their pathogenic power (Pereyra & Escande,
1994). Seeds are important vehicles for the dissemination of S. sclerotiorum, as sclerotia
mixed with the seeds or fungus mycelium colonizing the internal tissues (Mordue & Holliday,
1976; Zimmer & Hoes, 1978).
Sclerotinia wilt and head rot control is difficult due to the persistence of sclerotia viable
for a long time in the soil, to the fact that the fungus produces ascospores responsible for
aerial infection until long distances, the lack of effective chemical control and high
susceptibility of sunflower genotypes (Pereyra & Escande, 1994; Gulya et al., 1997). Thus,
the most effective control is based on an integrated program of measures, which include
several cultural practices.
Exclusion measures were adopted, starting in 1984, to prevent the introduction of the
fungus through contaminated seed from other countries. An ordinance of the Brazilian
Ministry of Agriculture, Livestock and Supply established the importation of seeds only from
sunflower production areas free of S. sclerotiorum.
Genetic resistance to Sclerotinia wilt and head rot has been studied in several countries.
Efforts have been made in breeding programs around the world aimed at finding resistance to
the pathogen, but little progress has been made (Zimmer & Hoes, 1978; Gulya et al., 1997).
All studies indicate a lack of immunity in the sunflower cultivated and other wild species,
similar to what is observed in all species of plants are affected by S. sclerotiorum (Gulya et
al., 1997). The resistance of the sunflower to S. sclerotiorum is partial and controlled by
multiple genes. The reaction of the same genotype may vary depending on the mode of
fungus attack, or one genotype can display a high level of resistance to basal rot and show to
be very sensitive to head rot. Furthermore, genes that are expressed in a stage of plant
development may be ineffective in another stage (Davet et al., 1991). Wild species of
Helianthus, such as H. resinosus, H. debilis, H. lenticularis and H. petiolaris, have high
resistance genes (Zimmer & Hoes, 1978; Davet et al., 1991). There are reports of variation
among cultivars for incidence of head rot, but apparently these differences are related to
greater plant height, which would provide less favorable conditions for fungus infection
(Zimmer & Hoes, 1978). Restorers and maintainers oilseed sunflower germplasms with
improved resistance to head rot have already been developed and released (Miller & Gulya,
2006; Miller et al., 2006), but until now there are no hybrids or commercial varieties that have
resistance level suitable for cultivation of sunflower in areas where this disease is endemic.
Methods including mapping of Quantitative Trait Locus (QTL), as they detect relationships
between phenotypic variation and gene polymorphisms in existing germplasm, can be useful
in dissecting complex traits in sunflower, like resistance to Sclerotinia diseases, thus
providing a valuable tool to assist in crop breeding (Fusari et al., 2012).
Crop rotation is a suitable practice to help management of S. sclerotiorum. The use of
crops resistant to this fungus, like grasses, serves to allow time for natural degradation of
sclerotia by their natural enemies. Due to susceptibility to S. sclerotiorum, sunflower
cultivation after soybean, canola, peas, beans, alfalfa, tobacco, tomatoes and potatoes, among
other crops, should be avoided. Rotation with non-host crops during three to five years
reduces the number of sclerotia in the soil and minimizes the impact of the sunflower root

Disease Management in Sunflower
173
infection (Gulya et al., 1997). Weeds should be well controlled, because they may be
alternative hosts for S. sclerotiorum. An obvious recommendation, but very important, is to
avoid the use of seed mixed with sclerotia (Pereyra & Escande, 1994).
A key measure to prevent the occurrence of Sclerotinia wilt and head rot is the choice of
sowing date, in order to reduce periods of high humidity and low temperature during the
cycle, especially at flowering. In southern Brazil, for cultivation of sunflower after the harvest
of summer crops, sowing should be performed until mid-March and early-maturity genotypes
(100 days between emergence and harvest) should be used, considering studies of zoning for
climate risk, to prevent low temperature at the end of the cycle (Leite et al., 2000).
Other cultural practices are important to minimize the problems caused by S.
sclerotiorum. Spatial isolation is a measure effective in reducing the incidence of infection by
ascospores. Generally, it is recommended to choose areas at least 1 km away from crops
infected with S. sclerotiorum in the previous year (Masirevic & Gulya, 1992). It is convenient
to choose lower seeding densities and larger spacing so as to enable adequate plant aeration
and decrease the chances of contact with diseased adjacent plants (Zimmer & Hoes, 1978).
Chemical control has not proven to be effective for several reasons. For sunflower, there
are no products with systemic efficiency (Davet et al., 1991). The duration of flowering and
consequently the susceptibility to head infection requires at least two or three preventive
sprays with fungicides. Furthermore, the penetration of products in floral organs is very
difficult (Davet et al., 1991) and the fungicide needs to be applied to the head face to be
effective (Masirevic & Gulya, 1992). In Brazil, fluazinan is registered for control Sclerotinia
head rot in sunflower (Ministério, 2012), but there are no available data that indicates
efficiency on disease control until now.
Downy Mildew (Plasmopara halstedii)
Downy mildew is a major disease of sunflower in the world, to be potentially very
destructive. Although originating in North America, with the movement of sunflower around
the world, the pathogen is currently endemic in all places where sunflower is grown (Gulya et
al., 1997). Most countries have specific regulations to prevent the introduction or spread of
the pathogen (Pereyra & Escande, 1994), including Brazil, where it is considered quarantine
pest category "A". In Brazil, it was found for the first time in 1982, in the municipalities of
Santo Augusto and Veranopolis, Rio Grande do Sul, and later in 1983 in Londrina, Paraná.
The disease was found in experimental plots and diseased plants were eradicated and
immediately burned (Ferreira et al., 1983; Henning & França Neto, 1985). Plants with downy
mildew were observed again under experimental conditions in Londrina, in the late-1990s,
and were again eradicated (Leite et al., 2007). The damage caused by downy mildew may
result from premature death of plants, decrease of head size, decrease in oil content of
contaminated seeds or finally, complete yield loss (Pereyra & Escande, 1994; Gulya et al.,
1997).
This disease can show different types of symptoms, depending on the amount of
inoculum, plant age, reaction of the genotype and conditions of humidity and temperature
(Zimmer & Hoes, 1978; Almeida et al., 1981; Davet et al., 1991; Pereyra & Escande, 1994;
Gulya et al., 1997; Tourvieille-de-Labrouhe et al., 2000).

Regina M. V. B. C. Leite
174
Damping-off results from infection of the root system of the plants in the early stages of
development, under conditions of low temperature and high humidity. This symptom is
manifested by the presence of primary inoculum in the soil, which may affect the seedlings
before or after emergence, resulting in reduction of stand.
Plants with systemic infection have slow growth or stunting, chlorotic leaves with
abnormally thick, brittle stems with head erect and usually sterile (Figure 3). The initial
symptoms are yellowing of the first pair of true leaves, usually at the base of the leaves or
along the midrib. During flowering, plants infected systemically present height from 0.1 to
1.0m and do not follow the movement of the sun, while healthy plants have 1.5 to 1.8 m and
show heliotropism. In conditions of high humidity and low temperature, grayish-white
structures, composed of conidiophores and conidia, can be seen on the underside of chlorotic
leaves.
The causal agent of downy mildew is Plasmopara halstedii (Farl.) Berl. & de Toni. It is
an systemic obligate parasite, which produces intercellular mycelium with globular haustoria
and sporangia that arise through the stomata. The sporangia are thin and branched
monopodially to form zoosporangia at the ends of the branches. The zoosporangia break up,
release biflagellate zoospores (Zimmer & Hoes, 1978). The structures of the pathogen are
found in all tissues of the seedling and adult plant, but never in contact with the
undifferentiated cells of meristematic tissues, nor in conducting vessels (Davet et al., 1991).
Figure 3. Downy mildew in sunflower.

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P. halstedii causes disease in at least 80 species of 35 genera belonging to the subfamily
Asteroidae and Cichorioidea (Gulya et al., 1997). Besides H. annuus, other species of
Helianthus, such as H. argophyllus, H. debilis, H. divaricatus, H. grosseserratus and, as well
as other genera of the family Asteraceae (including Ambrosia, Artemisia, Bidens, Centaurea,
Gerbera, Solidago, Vernonia and Xanthium) are susceptible to downy mildew pathogen
(Davet et al., 1991; Gulya et al., 1997).
The life cycle of P. halstedii starts with oospores, which are resistance structures with
thin wall that are produced sexually (Gulya et al., 1997). The oospores occur in contaminated
debris from the previous sunflower crop, as well as within the seeds from systemically
infected plants. After the winter, the oospores germinate, especially in moist conditions of
spring. Some oospores, however, remain dormant for up to 14 years (Zimmer & Hoes, 1978).
The percentage of diseased plants drops considerably from the sixth year (Davet et al., 1991).
The oospores germinate producing thin-wall zoosporangia which produce the biflagellate
zoospores. In contact with the host tissue, especially primary roots and hypocotyls of newly
emerged seedlings, the zoospore encysts and emits haustoria into the host cell (Zimmer &
Hoes, 1978). It sporulates on the surface of the invaded tissues by producing zoosporangia
that are responsible for secondary infections. With the advancement of the crop cycle, the
male (antheridia) and female (oogonium) organs of the pathogen are formed in the
intercellular spaces of the roots, stem, and often seeds. Fertilization occurs, giving rise to a
thin wall oospore. Finally, the oospore returns to the soil, completing the life cycle of P.
halstedii (Zimmer & Hoes, 1978).
Disease incidence, type and severity of downy mildew symptoms are determined by the
nature and quantity of the inoculum, by plant age at the time of infection and by
environmental conditions (Zimmer & Hoes, 1978; Pereyra & Escande, 1994). The disease is
favored by high rainfall conditions (relative humidity higher than 95%) and temperature
between 15ºC to 18ºC (Davet et al., 1991).
The nomenclature used to describe the races of downy mildew was very ambiguous,
since races were called by the name of the region of origin (Race Red River, European race),
numbers (races 1-9 of American nomenclature) or letters (races A to D of French
nomenclature). To standardize the nomenclature, a set of nine publicly available lines was
established to be used as differential lines named D1 to D9 regrouped into three sets of three
lines (triplets). To encode the race, a score is assigned to each triplet, based on the reaction of
susceptibility or resistance of each differential line. If the first line of a set of three is
susceptible, it imparts a value of 1; if the second line is susceptible, it imparts a value of 2;
and if the third line is susceptible, it imparts a value of 3. In the case of resistance genotype it
imparts a value of zero. The score is the sum of the coefficients assigned to triplet. The final
race name will be a 3-digit code, one digit from each of the three sets of lines (Gulya et al.,
1998).
In the world, at least eleven physiological races of P. halstedii have been reported
affecting sunflower (Tourvieille-de-Labrouhe et al., 2000). In Brazil, there was, in 1982, the
occurrence of race 2 American (race 300 in the current nomenclature) (Henning & França
Neto, 1985). In recent reports, in Londrina, race 330 or former American race 7 was
identified (Leite et al., 2007). Former American race 7 is also prevalent in Argentina (Castaño
et al., 1998).
Exclusion measures have been adopted, since 1984, to prevent the entrance of downy
mildew in Brazil. An ordinance of the Brazilian Ministry of Agriculture, Livestock and

Regina M. V. B. C. Leite
176
Supply banned the importation of sunflower seeds and other common species of the genus
Helianthus and tubers of H. tuberosus, when coming from the following countries: Argentina,
Canada, Chile, Spain, United States, France, Hungary, Iran, Israel, Serbia and Montenegro
(former Yugoslavia), Japan, Jordan, Pakistan, Dominican Republic, Romania, Russia, Czech
Republic (former Czechoslovakia) and Uruguay, and other countries where the pathogen is
found. Imports from other countries are restricted to seeds produced in areas free of downy
mildew. Since 1995, following the harmonization of quarantine procedures for Mercosur
countries, seeds can be imported from Argentina, Paraguay and Uruguay (Leite & Oliveira,
1998). However, there is a continuous threat of reintroduction of P. halstedii by infected
seeds, especially from Argentina, where the disease is important (Pereyra & Escande, 1994).
The use of resistant cultivars is the most secure method to prevent the disease (Pereyra &
Escande, 1994). The resistant genotypes produce defense reactions against the pathogen,
forming a barrier to disease progression, and the disease does not become systemic (Davet et
al., 1991; Gulya et al., 1997). The resistance to downy mildew is oligogenic dominant and
controlled by several Pl genes. At least nine genes for resistance to downy mildew (Pl1 the
PL9) are the most widely used in breeding programs (Davet et al., 1991). The lines of
germplasm from the USDA (United States) HA-335 to HA-339 and RHA 340 have resistance
to all known races of P. halstedii (Gulya et al., 1997; Gulya et al,. 1998). In France, cultivars
resistant to races 710 and 703, that are prevalent in the country, were used in at least 80% of
the crops, in 2000 growing season (Tourvieille-de-Labrouhe et al., 2000). Also, genotypes from
Argentina have incorporated downy mildew resistant genes (Pereyra & Escande, 1994).
Research on more durable resistance has been undertaken, including examples of host-
parasite interactions to integrate the pathosystem P. halstedii x H. annuus (Sakr, 2012).
Sunflower show a large variability for resistance to downy mildew that is independent of
major Pl genes giving race specific resistance in breeding programs. This quantitative
resistance could be used in breeding programs using a simple method to phenotype progenies.
Infection of the first pair of true leaves and observation of the proportion of plants showing
systemic downy mildew symptoms appear as a promising technique (Tourvieille-de-Labrouhe
et al., 2008).
Cultural measures are also important in the prevention of downy mildew. These include
crop rotation for four years and the destruction of volunteer plants that emerge after
harvesting sunflower (Davet et al., 1991; Gulya et al., 1997).
Chemical control through foliar sprays with fungicides is not recommended in France,
since this treatment can lead to selection pressure on the population of P. hasltedii, which can
answer manifesting resistance to fungicides (Davet et al., 1991; Tourvieille-de-Labrouhe et al.,
2000). Resistant races have been detected in this country since 1994 (Tourvieille-de-Labrouhe
et al., 2000).
Seed treatment with specific fungicides for P. halstedii, such as metalaxyl, is mandatory
in some countries, such as France and Argentina, in susceptible open pollinated varieties or
hybrids. Thanks to its systemic property, metalaxyl allows controlling primary contamination
and ensures good protection in the early stages of crop development (Davet et al., 1991;
Pereyra & Escande, 1994).

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177
Powdery Mildew - Erysiphe cichoracearum
Powdery mildew is a disease distributed worldwide, but occurs in greater intensity in
tropical areas where occasionally cause plant senescence in the flowering stage or later. In
temperate areas, powdery mildew is usually not observed until flowering and rarely has
economic importance (Zimmer & Hoes, 1978; Gulya et al., 1997).
The disease is characterized by the appearance of velvety white or gray structures on the
aerial parts of the plant, especially lower leaves, but occasionally on the stem and bracts
(Figure 4). The lesions may grow and coalesce, covering most of the plant surface. With the
evolution of the cycle, black dots can be observed randomly distributed in velvety areas
(Zimmer & Hoes, 1978; Almeida et al., 1981).
Powdery mildew is caused by the fungus Erysiphe cichoracearum (DC) ex Meret (syn.
Golovinomyces cichoracearum (DC) Heluta), which is an obligate parasite. The velvety
structures are mycelia, conidiophores and conidia of the fungus. The mycelium is usually well
developed. Spores are formed in long chains, have ellipsoid shape and size ranging from 25-
45 µm x 14-26 µ m. At the end of the cycle, the fungus produces cleistotecia, which are black
structures responsible for survival of the pathogen, containing asci with two ascospores
(Kapoor, 1967).
E. cichoracearum is restricted to the Asteraceae family, causing powdery mildew in 230
species belonging to 50 genera. There are reports of at least 13 formae speciales of the fungus
(Kapoor, 1967).
Transmission is primarily through cleistotecia that survive from one growing season to
another. In some cases the conidia can also survive (Kapoor, 1967). Conidia are disseminated
primarily by wind, which can reach long distances. The optimum conditions for infection are
temperatures around 25ºC and relative humidity of 95%. The conidia do not germinate when
there is a water film on the leaf surface. The disease is favored by hot and dry periods
(Kapoor, 1967; Zimmer & Hoes, 1978).
Figure 4. Powdery mildew in sunflower.

Regina M. V. B. C. Leite
178
Although there are specific fungicides for powdery mildew, such as sulfur, chemical
control is not performed due to the low prevalence of the disease (Kapoor, 1967; Zimmer &
Hoes, 1978). In Brazil, fungicides azoxistrobin + ciproconazole and difenoconazole are
registered for control powdery mildew in sunflower (Ministério, 2012), but there are no
available data that indicates efficiency on disease control until now.
Few efforts have been made in the development of cultivars resistant to powdery mildew.
However, there seems to be wide differences in the response of different cultivars to the
pathogen (Zimmer & Hoes, 1978).
Phomopsis Stem Canker - Phomopsis helianthi
Phomopsis stem canker was first reported in Serbia and Montenegro (former Yugoslavia)
in 1980, and has been highly destructive in the countries of Eastern Europe and in France
(Davet et al., 1991; Masirevic & Gulya, 1992; Pereyra & Escande, 1994). The damage is
caused due to breakage and lodging of attacked plants, seriously damaging the crop.
Depending on climatic conditions, the degree of incidence can reach 50% to 80% of the
plants (Masirevic & Gulya, 1992; Pereyra & Escande, 1994; Gulya et al., 1997).
The first symptoms of the disease often occur in foci, usually after flowering. About 10 to
15 days after infection, small necrotic spots surrounded by a yellow halo appear at the margin
of lower or median leaves and evolve towards the midrib of the leaf. Infected leaves wither
and die quickly (Davet et al., 1991; Masirevic & Gulya, 1992; Pereyra & Escande, 1994;
Gulya et al., 1997).
The fungus grows toward the stem, where the most characteristic symptoms appear
(Figure 5). The lesions on the stem, always initiated in the axils of leaves, begin as small
brown spots and grow rapidly, becoming round or ellipsoidal, usually girdling the stem. The
fungus destroys the internal tissues of the lesions and the stem breaks easily, rendering the
plants subject to lodging (Figure 5). Small and dark pycnidia can be observed in diseased
tissues. The final symptom is the complete blight (Davet et al., 1991; Masirevic & Gulya,
1992; Pereyra & Escande, 1994; Gulya et al., 1997).
Figure 5. Phomopsis stem canker in sunflower.

Disease Management in Sunflower
179
This disease is caused by Phomopsis helianthi Munt.-Cvet. et al., which teleomorph is
Diaporthe helianthi Munt.-Cvet. et al. (Davet et al., 1991; Masirevic & Gulya, 1992; Pereyra
& Escande, 1994). Another unidentified species of Phomopsis can also cause disease in
sunflower, but P. helianthi seems to be prevalent (Carriere & Petrov, 1990). Three new
species (P. gulyae, P. kochmanii and P. kongii) are associated with stem canker on sunflower
in Australia (Thompson et al., 2011).
Under natural infection, pycnidia begin to be formed soon after the lesions appear on the
stem. They can be found in leaves, but always fewer in number than the stem. The pycnidia
are globular, dark brown,with 120-190 µ m in diameter, and often immersed in host tissue.
Hyaline beta-conidia, with 17 to 42 µm in length by 0.5 to 2 µ m in width, are formed. The
developing perithecia can be found in sunflower residues in cortical tissues, individually or in
groups. Numerous globular, cylindrical asci, with 60 to 76.5 µm in length by 8.7 to 12.5 µ m
in width, develop in the perithecia. After maturation, eight ascospores per ascus are released
(Masirevic & Gulya, 1992).
Excepted species of the genus Helianthus, no reports of other host plants of P. helianthi
are confirmed. However, a species of Phomopsis isolated from Xanthium italicum is reported
as pathogenic to sunflower (Carriere & Petrov, 1990).
The optimum temperature for fungal growth is around 25ºC. The spores infect plants in
conditions of high humidity for 12 to 15 consecutive hours. Frequent and abundant rains
result in increased infection. The fungus persists in crop debris as mycelium. Under
conditions of temperature between 18ºC and 20ºC and high humidity, perithecia are produced
and they release ascospores, which are then disseminated by wind and rainwater (Pereyra &
Escande, 1994). The fungus can also be found in sunflower seeds (Masirevic & Gulya, 1992).
The ascospores germinate in the insertion of the leaf and initiate infection through the
invasion of the petiole, eventually reaching the stem. The characteristic lesion of the disease
appears 25 to 30 days after initial infection of the leaf.
Increasing plant density favor increased disease incidence and severity, resulting in a
greater proportion of girdling stem lesions, detrimental to yield, because of earlier infection
under dense canopies. The number of girdling lesions per plant also increases with high N
fertilization (Debaeke & Moinard, 2010).
A large number of accessions of wild species of Helianthus have a satisfactory level of
resistance to Phomopsis stem canker: H. tuberosus, H. resinosus, H. decapetalus, H.
divaricatus, H. eggertii, H. giganteus, H. grosserratus, H. hirsutus, H. mollis, H. salicifolius,
H. nuttallii and H. radula. Interspecific crosses between cultivated sunflower and H.
argophyllus or H. tuberosus resulted in lines used for the development of commercial hybrids
with high disease resistance (Masirevic & Gulya, 1992; Gulya et al., 1997). The resistance is
controlled by many genes, with additive effects. Resistance to P. helianthi is connected
positively to resistance to Macrophomina phaseolina, Phoma oleracea var. helianthi-tuberosi
and drought, possibly attributed to linked genes (Masirevic & Gulya, 1992; Pereyra &
Escande, 1994; Deglène et al., 1999).
Cultural control practices such as the use of plant populations below 50,000 plants per
hectare, adequate nitrogen fertilization and crop rotation are necessary to reduce the disease
incidence. Moreover, incorporation or removal of contaminated crop debris helps to reduce
fungus inoculum (Davet et al., 1991; Masirevic & Gulya, 1992; Gulya et al., 1997; Debaeke
& Moinard, 2010).

Regina M. V. B. C. Leite
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Benzimidazole-based fungicides have been used to control the disease in France and
Argentina (Davet et al., 1991; Pereyra & Escande, 1994). Chemical control with two aerial
applications of fungicides, the first in the vegetative stage V8 to V10 and the second during
flowering is recommended by Masirevic & Gulya (1992). Seed treatment has also been
proven effective (Davet et al., 1991). Despite minimizing yield losses, the use of fungicides is
not as efficient as the use of genotypes with resistance genes (Masirevic & Gulya, 1992).
Rust - Puccinia helianthi
Sunflower rust is an important disease in many regions of the world. Severe losses have
been attributed to this disease, which causes premature defoliation. Disease severity is greater
in areas of humid (Zimmer & Hoes, 1978; Pereyra & Escande, 1994; Gulya et al., 1997).
The high incidence of rust in São Paulo state, Brazil in the mid-1960s, was the main
factor responsible for the discouragement of sunflower cultivation in the northwest region of
the state at that time. This occurred due to the high susceptibility of cultivars used by
producers (Lasca, 1993).
Typical symptoms of sunflower rust are small round powdery pustules, with 1 to 2 mm
diameter, pale orange to black, distributed randomly over the entire surface of the plant
(Figure 6). They are more common in lower leaves, progressing to the top. Normally, the
pustules are surrounded by small yellow halos. At high levels of infection, stem, petiole and
floral parts may exhibit symptoms. The coalescence of pustules may occupy almost the entire
leaf surface, causing premature leaf senescence, which causes reduced yield and low seed
quality (Zimmer & Hoes, 1978; Almeida et al., 1981; Pereyra & Escande, 1994, Gulya et al.,
1997).
Rust is caused by Puccinia helianthi Schwein. The fungus develops the whole cycle in a
single host and produces two types of spores: uredospores and teliospores. The uredospores
are the orange powdery mass, which is characteristic of the disease, and are produced in
uredia, during favorable climate conditions for the pathogen. The uredia are formed on the
lower surface of the leaves and have a diameter of 1 mm. The uredospores are ellipsoidal or
sometimes cylindrical, with size ranging from 25-32 x 19-25 µm. Teliospores with 40-60 x
18-30 µ m are produced for survival (Laundon & Waterson, 1965; Zimmer & Hoes, 1978;
Pereyra & Escande, 1994).
Puccinia helianthi is a specific pathogen of the genus Helianthus, affecting more than 35
annual and perennial species (Zimmer & Hoes, 1978; Pereyra & Escande, 1994). There are
several known races of the pathogen: nine races have already been reported in Canada, seven
in Australia and 10 in Argentina, and 20 virulence patterns have been detected by using a
series of nine differential lines in the United States (Laundon & Waterson 1965; Zimmer &
Hoes, 1978; Pereyra & Escande, 1994; Gulya et al., 1997).
The pathogen can be perpetuated in plants of the genus Helianthus, where uredospores
are produced. This is possibly the usual way of perpetuating the fungus in regions where
winter is not severe (Pereyra & Escande, 1994). The uredospores are transmitted to other
plants from contaminated crops, crop debris or volunteer plants. Air currents at high altitudes
may contribute to the spread of uredospores over long distances. The infection occurs shortly
after flowering, when uredospores are deposited on leaves and germinate under conditions of
high relative humidity (Pereyra & Escande, 1994).

Disease Management in Sunflower
181
Figure 6. Sunflower rust.
The disease severity varies with age of the plant, environmental conditions and genotype
resistance. The pathogen is favored by temperatures of 18ºC to 22ºC and high relative
humidity and, under these conditions, can cause epidemics (Pereyra & Escande, 1994).
Measures to reduce the initial inoculum and reduce the risk of severe losses caused by
rust are recommended, as the elimination of sunflower volunteer plants, crop rotation for at
least three years and destruction of crop debris (Laundon & Waterson, 1965; Zimmer & Hoes,
1978; Pereyra & Escande, 1994).
Sulfur or copper-based fungicides, in spite of controlling this fungi, have not been used in
commercial crops (Laundon & Waterson, 1965).
The method of rust control that is universally used is based on resistant cultivars.
Selections and cultivars resistant to this fungus have been developed in countries like Russia,
Peru, Chile, Serbia and Montenegro (former Yugoslavia), United States and Argentina
(Laundon & Waterson 1965; Zimmer & Hoes, 1978; Pereyra & Escande, 1994; Gulya et al.,
1997). Recently, 107 genotypes were screened against sunflower rust under field conditions
in India but none of them were found to be immune to rust (Nargund et al., 2011). The rust
resistance is dominant and inherited by a single gene. Many sources of rust resistance are
known. Collections of wild sunflower, including H. annuus and H. petiolaris, represent a
reservoir of resistance genes that can be used in breeding. R1 and R2 genes have been widely
used for development of resistant cultivars (Zimmer & Hoes, 1978). Many cultivars have
developed resistance to race 1, more frequent and distributed worldwide. However, the use of
resistant cultivars may be limited due to the existence of races of the fungus or the selection
of races that can overcome this resistance (Pereyra & Escande, 1994).
CONCLUSION
Once installed on the crop, sunflower diseases are hard to control, due to the difficulties
of chemical application, because of the dynamics of plant growth, hindering or even

Regina M. V. B. C. Leite
182
preventing the entry of machinery in the field and lack of efficient application of fungicides,
requiring in some situations aerial application of fungicides.
Therefore, measures of disease management are mostly preventive and should not be
used alone. Thus, effective control is based on an integrated program, which includes zoning
for climate risk and diverse cultural practices.
Genetic resistance to diseases is highly desirable because it does not increase directly the
cost of production and many times can dispense other control measures. Studies on the
reaction of genotypes and breeding aiming resistance have been carried out for different
diseases and should be done continuously.
A key measure to minimize the occurrence and severity of diseases is the choice of
sowing date. Considering the different diseases and plant requirements, the date suitable for
sowing sunflower varies with different soil and climatic regions. It should be noted that the
indication of sowing date should be guided by studies of zoning for climate risk in order to
establish the date that will satisfy the requirements of the plant at different stages of
development, and that disfavor diseases.
Another important aspect is to use crop population around of 40,000 to 45,000 plants per
hectare. Sunflower requires deep soils with good nutrient levels and proper pH. Liming and
fertilization should always be made based on soil analysis and technical and economic
criteria.
As many sunflower pathogens are transmitted by seed, it is imperative to use healthy
seeds from known origin. With respect to chemical control, several fungicides are available
and can be used as tool for the farmers.
In addition to these measures, it is noted that sunflower should be included within a
system of crop rotation, returning in the same area only after at least four years.
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