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© 2012 Plant Management Network.
Accepted for publication 5 November 2012. Published 14 December 2012.


Sunflower Diseases Remain Rare in California Seed Production Fields Compared to North Dakota


Thomas J. Gulya, USDA-ARS Northern Crop Science Laboratory, Fargo, ND 58105; Suzanne Rooney-Latham, California Department of Food and Agriculture Plant Pest Diagnostics Laboratory, Sacramento, CA 95832; Jean S. Miller, Glenn County Department of Agriculture, Willow, CA 95988; Kathleen Kosta, California Department of Food and Agriculture Plant Health and Pest Prevention Services, Sacramento, CA 95814; Colleen Murphy-Vierra, California Department of Food and Agriculture Plant Health Data Analysis, Sacramento, CA 95814; Carrie Larson, North Dakota Department Agriculture, Plant Industries Division, Bismarck, ND 58505; William Vaccaro, Sunfield Seeds, Chico, CA 95928; Hans Kandel, Department of Plant Science, North Dakota State University, Fargo, ND 58108; and John F. Nowatzki, Agricultural and Biosystems Engineering, North Dakota State University, Fargo, ND 58108


Corresponding author: Thomas J. Gulya. thomas.gulya@ars.usda.gov


Gulya, T. J., Rooney-Latham, S., Miller, J. S., Kosta, K., Murphy-Vierra, C., Larson, C., Vaccaro, W., Kandel, H., and Nowatzki, J. F. 2012. Sunflower diseases remain rare in California seed production fields compared to North Dakota. Online. Plant Health Progress doi:10.1094/PHP-2012-1214-01-RS.


Abstract

The majority of United States sunflower production is in seven Midwestern states, but hybrid planting seed is almost exclusively produced in California. Due to the lack of summer rains and furrow irrigation, California-produced seed is relatively disease free and thus it regularly meets phytosanitary restrictions imposed by many countries. For the 15-year period from 1997 to 2011, 7231 seed fields in northern California were inspected and samples processed at the state diagnostic laboratory (California Department of Food and Agriculture). Rust (Puccinia helianthi) was the most prevalent quarantine disease, found in 4.3% of fields. Stalk rot (Sclerotinia sclerotiorum) and downy mildew (Plasmopara halstedii) were the only other quarantine pathogens observed, found in 2.6% and 0.5% of the 7231 fields, respectively. Many sunflower pathogens have never been recorded in California, including Phoma macdonaldii, Phomopsis helianthi, or any virus. North Dakota, the state with the highest US sunflower production, had quarantine pathogens in 88% of 1263 fields surveyed from 1995 to 2011. Phoma macdonaldii, Sclerotinia sclerotiorum, Puccinia helianthi, Phomopsis helianthi, Plasmopara halstedii, and Verticillium dahliae were recorded in 62, 54, 37, 33, 14, and 12%, respectively, of North Dakota fields.


Introduction

Hybrid sunflower planting seed, whether destined for use in the United States or for export to other countries, is now largely produced in California. Approximately 95% of US-produced sunflower planting seed is grown in seven counties in northern California (Fig. 1), on 18,000 to 21,000 ha currently (22). In some years, up to 60% of California seed production is destined for overseas markets, primarily China, the EU, Russia, and the Ukraine. Five companies, based in Woodland and Chico, CA, are responsible for all sunflower seed production in California. Sunflower production practices in California (23) differ from those in Midwestern US states (1), and this influences disease occurrence. All US planting seed is treated with a fungicide mix consisting of either azoxystrobin, fludioxonil, and mefenoxam (Dynasty, Maxim and APRON XL, respectively, Syngenta Crop Protection, Greensboro, NC) or fenamidone, metalaxyl, and iproconazole (Idol, Allegiance, and Vortex, respectively, Bayer Crop Science, Research Triangle Park, NC) to control downy mildew and seedling blights (25). Sunflowers in California are planted between March and June, at the end of the rainy winter period, which provides a frost-free period of 240+ days (Fig. 2A). Seeds are planted in raised beds for furrow irrigation. Hybrid seed production fields generally consist of 6, 10, or 12 rows of the female and two rows of male line. Fields are rogued to remove “off-type” plants and any diseased plants. Male rows are removed after bloom is complete, and harvest begins in early August. In contrast, North Dakota has a short 120-day growing season; fields are planted in May/June and harvested in September/October. Nearly all fields are “dryland,” with 0.5% of North Dakota fields under center-pivot irrigation. The majority of precipitation in North Dakota occurs during the summer months (Fig. 2B). The hot, dry summer climate and long growing season in north-central California (Fig. 2A) facilitates high seed yield and low incidence of most foliar and head diseases. The relative lack of diseases has been documented previously (13,19), but since those studies are 21 to 36 years old, it appears prudent to update the status of California sunflower diseases, and to compare that with the disease situation in North Dakota, the major sunflower production state in the US.


 

Fig. 1. Map of California showing the location of the major sunflower producing counties (left) and the average percent of the state sunflower production area by county (right).

 

 

Fig. 2. Monthly precipitation and low/high temperatures in (A) Yolo Co., Woodland, CA, and (B) Bottineau Co., Bottineau, ND, the counties with the highest sunflower production in California and North Dakota. Data from www.usclimatedata.com.

 

Field Inspection and Pathogen Identification Protocols

Phytosanitary inspection protocols are well defined and documented in California (2,3). Field inspections are the responsibility of each county’s agricultural department, who use plant pathologists or trained biologists. The exact inspection protocol varies with field size, but for a field of 8 to 20 ha (20 to 50 acres), the inspector is required to walk a minimum of 17 passes through the entire length of the field, giving a 95% confidence level of detecting an infection level of 0.1%. Inspections are mandated to be done twice; once before bloom, which is primarily to observe virus, downy mildew, and seedling diseases, and a second inspection after the male plants are removed. Diseases and pathogens specified to be monitored include Alternaria leaf blights (Alternaria helianthi and A. zinniae), Phoma black stem (Phoma oleracea = P. macdonaldii), Phomopsis stem canker (Phomopsis helianthi), downy mildew (Plasmopara halstedii), bacterial leaf blights (Pseudomonas cichorii and P. helianthi (= P. syringae pv. helianthi), rust (Puccinia helianthi), Sclerotinia stalk and head rot (Sclerotinia sclerotiorum), Septoria leaf blight (Septoria helianthi), Verticillium wilt (Verticillium dahliae), sunflower mosaic, and any other virus. Any suspected disease sample is sent to the state diagnostic laboratory operated by the California Department of Food and Agriculture (CDFA) for identification. Scientific staff at the CDFA diagnostic laboratory consists of several phytopathologists, including two mycologists, two bacteriologists, and a virologist (4). The laboratory also maintains a database of their analyses dating back to 1997. Once the sample has been determined to be free of any quarantined plant pathogens, phytosanitary certificates are issued by the respective county where the sample originated.

Sunflower disease incidence in North Dakota is monitored both in seed production fields and in regular commercial fields. Inspections of seed production fields, mainly in eastern North Dakota, are done by the North Dakota Department of Agriculture (NDDA) in a manner similar to that in California, with disease confirmation performed by field inspectors. To augment the data on North Dakota disease incidence, we included data from the annual surveys of commercial fields coordinated by the National Sunflower Association (NSA) (18,21). These surveys, initiated in 2001, encompass a representative sample of fields, proportional to the state production area in seven Midwestern states (North Dakota, South Dakota, Minnesota, Kansas, Colorado, Nebraska, and Texas). Teams of trained personnel collect data on the incidence of weeds, insects, and diseases, as well as information on yield and agronomic practices. The surveys are done when plants are at physiological maturity, in late September to early October. Diseases are identified in the field with no laboratory confirmation. Diseases monitored in North Dakota include many of the same monitored in California seed fields (downy mildew, rust, Phoma black stem, Phomopsis stem canker, Sclerotinia head, mid-stem and basal stalk rot, and Verticillium wilt). Charcoal rot (Macrophomina phaseolina) and Rhizopus head rot (R. oryzae) are also monitored but are not of quarantine significance. Foliar diseases caused by Alternaria, Septoria, and Pseudomonas spp., which are monitored in California, are not in North Dakota, owing to the difficulty of field identification and leaf senescence obscuring symptoms with surveys at physiological maturity.

Countries which have published phytosanitary import restrictions currently list one viral, three bacterial, and 12 fungal pathogens (Table 1). Other countries specify which pathogens they prohibit via import permits, which change periodically (and are not published). Most phytosanitary certificates can be fulfilled by field inspections, but some countries require the statement that the seed be free of a particular pathogen, necessitating seed testing.


Table 1. Sunflower pathogens currently listed by one or more countries as being of quarantine significance and guidelines for issuing a phytosanitary certificate.x

Pathogen
Common
name
Australia X           G                
Argentina X                            
Bangladesh X                           G
Bulgaria X           G                
Brazil             T                
Canada             T                
Chile     G     G                  
China X F     F F F       F        
France             T                
Hungary             T                
India                              
Israel   G G     G G G G       G G  
Italy             T               G
Kenya X             G G            
Mexico X   G       G           G G  
Namibia X           G                
New Zealand             G           G   G
Pakistan             F     F   F F F  
Peru X           G                
Romania             T                
Russia X                            
Slovakia             T                
South Africa                              
Spain             T                
Turkey X           T                
Ukraine X                            
Uruguay X         G                  

Abbreviations: G = Growing season inspection required, and pathogen not found in field; F = Declaration that seed be free of pathogen; T = Seed must be treated with fungicide registered for pathogen control.

 x Data retrieved from USDA Phytosanitary Export Database (PExD) available to registered users at: https://pcit.aphis.usda.gov/pcit.



Quarantine Diseases Identified in California

A total of 7231 seed production fields, predominantly in seven counties of the Sacramento River valley (Fig. 1) were inspected for phytosanitary certification between 1997 and 2011. Rust, caused by Puccinia helianthi, was the most frequently observed quarantine disease on sunflower in California, confirmed in 4.3% of fields (Table 2). Incidence ranged from a low of 0% in three years to a high of 12% in 2011. Of the rust-infected fields, 53% occurred in Sutter Co., with less frequency in Glenn (25%), Solano (16%), Colusa (3%), and Yolo (3%) counties.


Table 2. Incidence over a 15-year period of quarantine pathogens found in California sunflower seed production fields by county inspectors and identity confirmed by the California Department of Food and Agriculture diagnostic laboratory.

Year # fields
inspected
Total
area
(ha)
Avg.
field
size
(ha)
% fields
with any
quarantine
pathogen
% fields
with
Puccinia
helianthi

(rust)
% fields
with
Sclerotinia
sclerotiorum

(stalk rot)
% fields
with
Plasmopara
halstedii
(downy
mildew)
1997 361 7,350 20 4.2 1.9 2.8 0
1998 363 7,196 20 13.2 1.4 8.5 4.7
1999 505 10,420 21 8.3 4.4 4.0 0.2
2000 282 5,077 18 12.8 9.6 5.0 1.4
2001 206 3,637 18 0.5 0 0 0.5
2002 309 5,316 18 0.3 0 0 0.3
2003 396 8,346 21 5.1 3.5 2.0 0.3
2004 466 10,237 22 2.4 0.6 1.5 0.4
2005 588 14,768 25 6.8 2.2 3.9 0.7
2006 686 15,547 23 3.2 1.5 1.5 0.4
2007 473 11,870 25 9.3 7.2 2.5 0.4
2008 541 13,664 25 1.5 0 1.5 0
2009 730 18,651 26 10.4 8.9 1.8 0.1
2010 589 20,919 36 11.5 10.7 1.5 0
2011 736 18,350 25 14.0 12.2 2.7 0
Total 7231 171,348
Avg. 482 11,423 22.7 6.9 4.3 2.6 0.5

Sclerotinia stalk rot (S. sclerotiorum) was confirmed in 2.6% of the 7231 fields, over the 15-year period. Annual incidence ranged from 0% in two years to a high of 8.5% in 1998. Glenn Co. had the majority of Sclerotinia-positive fields (36%), followed by Yolo (29%), Solano (26%), Tehama (5%), and Colusa (2%), with no S. sclerotiorum observed in Butte or Sutter counties. The phytosanitary certificates do not distinguish between Sclerotinia head rot and stalk rot (as importing countries specify only the pathogen, and not the disease), but nearly all Sclerotinia-positive samples were stalk rot.

Downy mildew (Plasmopara halstedii) was recorded in 37 fields (0.5%) during the 15-year period. Glenn Co. had the majority of positive fields (89%), and this was primarily due an abnormal precipitation pattern in 1998. Rainfall in Glenn Co. for the three month planting period of March to May in 1998 totaled 215 mm, well above the 120-mm average. Downy mildew has only been found once in Tehama and Yolo counties, twice in Butte Co., and never in Colusa or Solano counties in the 15-year period. Downy mildew incidence remained below 1% annually since 2001 (Table 2).

None of the bacterial leaf spots common on Midwestern-grown sunflowers, such as apical chlorosis (Pseudomonas syringae pv. tagetis) or bacterial leaf spot (Ps. syringae pv. helianthi), nor non-quarantine bacterial stalk rot/head rot (Erwinia = Pectobacterium carotovora) have been documented in California. Although two viruses have been cited on sunflower in California (10), no viruses were identified during this 15-year period. Suspected viral samples were first examined by electron microscope, using the leaf dip method, followed by a minipurification if particles were observed. All suspect virus samples taken during this 15-year period were diagnosed as herbicide injury or chimeras. The one virus that has been found on sunflower in the US, the potyvirus “sunflower mosaic virus,” has only been found in Texas to date (14). Other sunflower quarantine pathogens which were not seen in California during the period of this survey include Albugo tragopogonis, Alternaria helianthi, A. zinniae, Phoma macdonaldii, Phomopsis helianthi, and Septoria helianthi.


Non-Quarantine Diseases Identified in California

Several non-quarantine diseases, such as powdery mildew (Erysiphe = Golovinomyces cichoracearum) and Rhizopus head rot (R. oryzae) are recognized by field inspectors and thus generally not sent to the CDFA laboratory for confirmation. Soilborne pathogens, not of quarantine significance, identified during the 15-year period (data not shown), included Macrophomina phaseolina (0.7% incidence), Sclerotinia minor (0.4%), and Sclerotium rolfsii (0.2%). In total, approximately two-thirds of the samples received by the laboratory were free of quarantine pathogens and their symptoms were due to abiotic or genetic causes, insect damage, or non-quarantine pathogens.

There have been several unique, infrequent pathogens isolated from sunflower over the 15-year period. For example, in 2010, leaves of ornamental sunflower from two coastal county greenhouses had numerous, small (2 to 4 mm), round necrotic lesions on them, without any chlorotic haloes (Fig. 3). Hyaline, oblong-fusoid conidia measuring 11-20 × 2.5-3.5 µm were seen fruiting hypophyllously on the leaves. The causal agent was identified as Ramularia helianthi, which, while not a first record, has not been noted in California since 1894 (8). Ramularia spp. are foliar pathogens of numerous crops in California, including artichoke, strawberries, sugarbeets, and many ornamental plants, and lesions on sunflower are similar in appearance to those on artichoke (20). Elsewhere in the US, Ramularia helianthi has been noted on sunflower only in Wyoming (9). Another minor, non-quarantine pathogen was found, Phytophthora cryptogea, which causes a girdling black lesion at the soil line (Fig. 4), and causes affected plants to wilt and die. These stalk lesions are similar to that caused by Phoma macdonaldii in Midwestern states (7). Phytophthora lesions are larger, extending up to 15 to 20 cm, and unlike Phoma, Phytophthora causes a black discoloration of the woody tissue of the stalk (Fig. 4). Phytophthora collar rot is seen mainly on plants at the ends of rows where the soil is saturated during irrigation. This pathogen has been noted in California previously (13,19) but has not been identified from any Midwestern state. Another unusual disease, leaf smut caused by Entyloma polysporum, was confirmed several times on ornamental sunflowers in southern California nurseries by the CDFA and others (6) (Fig. 5). This pathogen has not been recorded from field grown sunflowers, either in California or in any other state, although it is seen on ornamental Compositae in other states (17).


 

Fig. 3. Leaf spots caused by Ramularia helianthi on ornamental sunflowers grown in a greenhouse, on lower (A) and upper leaf surfaces (B).


 

Fig. 4. Basal collar rot caused by Phytophthora cryptogea, showing girdling black lesion at soil line (A) and black internal necrosis (B), which differentiates it from Phoma macdonaldii.


 

Fig. 5. Leaf smut, caused by Entyloma polysporum, on greenhouse-grown ornamental sunflowers in California. Lesions on upper (A) and lower leaf surface (B).


Quarantine Diseases Absent in California

Many quarantine pathogens have never been detected in California seed production fields. Among foliar pathogens, neither of the excluded Alternaria species (A. helianthi and A. zinniae), Albugo (Pustula) tragopogonis, Septoria helianthi, nor any Pseudomonas species have been documented in the 15-year period. It should be noted that besides the two quarantine Alternaria species there are five other species that occur on sunflower plants or seeds, including A. cirsinoxia, A. helianthicola, A. helianthinficiens, A. protenta, and A. roseogrisea (5,26). Conidial morphology among these species is quite distinct, which should make laboratory identification routine.

Quarantine pathogens causing stem lesions, Phoma macdonaldii and Phomopsis helianthi, still have not been detected in California. The identification of Phomopsis species on sunflower has recently become more complicated, however. Three new Phomopsis species pathogenic on sunflower (P. gulyae, P. kochmanni, P. kongii) have been reported from Australia (27) and Phomopsis species other than P. helianthi have been isolated from diseased sunflower in North Dakota (24). Accurate identification of the causal Phomopsis species may now necessitate integrating morphological and molecular methods (28).


Sunflower Disease Incidence in North Dakota

Between 1995 and 2011 the NDDA inspected only 49 seed production fields. Eight of the twelve quarantine pathogens were found and many fields had multiple pathogens (Table 3), with only 2% of the fields having no quarantine pathogens. The NSA-sponsored survey, monitoring disease in commercial fields, tabulated data on a large number of fields across North Dakota. These surveys, beginning in 2001, have data on 1214 grower fields over 10 years (survey not done in 2004). Combining both surveys, Phoma macdonaldii and Sclerotinia sclerotiorum were the major pathogens, found in over half of the fields, with Puccinia helianthi, Phomopsis helianthi, P. halstedii, and V. dahliae found in lower incidence (Table 3). Quarantine pathogens were found in 88% of surveyed fields. Pathogens which were not detected in either North Dakota survey include Albugo tragopogonis and Sunflower mosaic virus. White rust (A. tragopogonis) has been observed on US sunflower to date only in Kansas and Nebraska (15). No Pythium species were recorded, but since neither survey is done early in the season, these surveys are unlikely to detect the quarantine pathogen P. splendens.


Status of Quarantine Diseases in California: Conclusions

Sunflower seed produced in California continues to be nearly disease-free, based on field inspections and laboratory tests during the past 15 years, with quarantine diseases found in only 6.9% of fields. Comparison with disease incidence in North Dakota (Table 3) highlights the impact of the dry growing season in California in eliminating or drastically reducing many diseases. Also, the isolation restrictions (~ two km between seed production fields) and the elimination of wild and volunteer sunflowers further decreases inoculum dispersal between fields and thus disease incidence of foliar disease. Sunflowers in California are generally rotated with beans, cucurbits, corn, and tomatoes, with a minimum of three years between sunflowers.


Table 3. Incidence of quarantine diseases of sunflower found in California and North Dakota from field inspection data by California Department of Food and Agriculture (CDFA), North Dakota Department of Agriculture, and the National Sunflower Association.

    California North Dakota
CDFA
Inspection
(1998-2011)
ND Dept. of
Agriculture
(1995-2011)
Natl. Sunflower
Assoc.
(2001-2011)
ND
total
# fields examined 7231 49 1214 1263
Pathogen found Percent of fields with given pathogen
Albugo tragopogonis 0 0 0 0
Alternaria helianthi 0 67 NE −*
Diaporthe/
Phomopsis helianthi
0 2 34 33
Phoma macdonaldii 0 12 64 62
Plasmopara halstedii 0.6 33 13 14
Pseudomonas syringae
pv. helianthi & tagetis
0 0 NE −*
Puccinia helianthi 4.3 10 38 37
Pythium splendens 0 0 NE
Sclerotinia sclerotiorum 2.6 53 54 54
Septoria helianthi 0 51 NE −*
Verticillium dahliae 0 33 11 12
Sunflower Mosaic Virus 0 0 0 0
Any quarantine
disease
6.9 98 88 88

NE = not enumerated.

 * Not tabulated since pathogens not included in both surveys.


Puccinia helianthi was the most frequently observed quarantine pathogen in both this and a previous survey (13). While there were no records from the CDFA on P. helianthi in the earlier study, rust was not a quarantine pathogen until 1988. A 1989 survey found it in 31% of fields, mostly in the Sacramento delta area, which currently has no seed production fields. Race determinations have not been made on California P. helianthi isolates, but in the Midwest sunflower production area, a total of 39 races from ~ 500 samples were identified over a three-year period (11). In light of Midwestern rust diversity, it would be prudent to study the California P. helianthi population.

Of the quarantine pathogens (Table 1), Plasmopara halstedii appears to be the one of utmost concern for exclusion, being listed by 15 countries. The pathogen is found very infrequently in California fields (0.5% over the 15 years), and incidence has remained < 1% since 2001. The one anomaly was 1998, in which it was found in 4.7% of fields. This is likely due to both the atypical, early season rainfall creating soil conditions suitable for infection, and to possible fungicide resistance. Seed treated with either metalaxyl or mefenoxam had been very effective in controlling this pathogen until the late 1990’s. By 1999, > 90% of fungal isolates from North Dakota were resistant to both fungicides (16), but no studies were done on California isolates. An alternative seed treatment fungicide was not available until 2003 when azoxystrobin was registered, followed by fenamidone a few years later. Currently, all seed planted in the US is treated with either of these fungicides. Import restrictions from all EU countries require that seed either be produced in an area free of P. halstedii or that seed be treated with an "appropriate fungicide," but neither azoxystrobin nor fenamidone are registered for use on sunflower in any European country.

While Sclerotinia sclerotiorum is the second most frequent quarantine pathogen (2.6% of fields), the majority of instances were basal stalk rot, and not head rot. While seed transmission is likely with Sclerotinia head rot, there is no research indicating that root infection by S. sclerotiorum can result in seed transmission (12). Thus, it would seem logical to differentiate between the two disease phases, especially if importing countries worded their restrictions appropriately.

This current study, encompassing 15 years, supports the overall view that California-produced hybrid sunflower seed is largely free of quarantine pathogens. The stringent field inspections coupled with professional laboratory confirmation of any suspected disease lends assurance that phytosanitary certificates truly reflect the absence of quarantine pathogens.


Acknowledgments

The authors wish to thank the National Sunflower Association for use of the data from their surveys, to the numerous field inspectors in California and North Dakota, and to a myriad of technical staff who made this study possible.


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