AGRICULTURAL AND FOOD SCIENCE AGRICULTURAL AND FOOD SCIENCE

Vol. 20 (2011): 62–73. Vol. 20(2011): 62–73.

The emergence of fungal diseases and the incidence of leaf spot diseases in Finland

Marja Jalli, Pauliina Laitinen and Satu Latvala MTT Agrifood Research Finland, Production Research, FI-31600 Jokioinen, Finland, email: [email protected]

Fungal plant pathogens causing cereal diseases in Finland have been studied by a literature survey, and a field survey of cereal leaf spot diseases conducted in 2009. Fifty-seven cereal fungal diseases have been identified in Finland. The first available references on different cereal fungal pathogens were published in 1868 and the most recent reports are on the emergence of Ramularia collo-cygni and langsethiae in 2001. The incidence of cereal leaf spot diseases has increased during the last 40 years. Based on the field survey done in 2009 in Finland, teres was present in 86%, sativus in 90% and Rhynchosporium secalis in 52% of the investigated fields.Mycosphaerella graminicola was identi- fied for the first time in Finnish spring fields, being present in 6% of the studied fields.Stagonospora nodorum was present in 98% and Pyrenophora tritici-repentis in 94% of spring wheat fields. fields had the fewest fungal diseases. Pyrenophora chaetomioides was present in 63% and Cochliobolus sativus in 25% of the oat fields studied. Key-words: Plant disease, leaf spot disease, emergence, cereal, barley, wheat, oat

Introduction nbrock and McDonald 2009). Changes in cropping systems and in climate are likely to maintain the plant-pathogen interactions (Gregory et al. 2009) Plant diseases are an outcome of the long-term in- and are assumed to play a key role in the emergence teraction between and pathogens. Plants have of infectious plant diseases (Anderson et al. 2004). evolved defence mechanisms while pathogens have The term ‘emerging disease’ refers to a recent evolved effectors to overcome plant defences (Stuke- disease on a new host and/or in a new area, or it is

© Agricultural and Food Science Manuscript received October 2010 62 63 AGRICULTURAL AND FOOD SCIENCE AGRICULTURAL AND FOOD SCIENCE

Vol. 20 (2011): 62–73. Vol. 20(2011): 62–73.

a disease that has recently become important due ha), barley being the main one (0.45 million ha) to an increase in virulence (Giraud et al. 2010). A (Matilda 2010a). A total of 4.2 milliard kilos of recent example of a new disease is Ramularia leaf grain were produced in 2008, over half of which spot on barley (Walters et al. 2008). Examples of was used to feed livestock (Matilda 2010b). pathogens with increased virulence are the Ug99 Plant diseases cause significant yield losses in pathotype of wheat stem rust (Singh et al. 2008) cereal crops and reduce grain quality, threatening and a new type of Puccinia striiformis (causal food safety (Gregory et al. 2009). Oerke (2006) agent of stripe rust) adapted to warmer climates estimated that despite current crop protection (Hovmøller et al. 2008). A change in virulence may practices, the average global yield loss in wheat result from plant disease control methods as in the attributable to plant pathogens is about 10%. In case of the rapid emergence and spread of QoI Finland, the average yield increase from fungicide resistance in Mycosphaerella graminicola popu- treatments in field trials over four years was 11% in lations (Torriani et al. 2009) or Puccinia triticina barley, and 13% in spring wheat (Laine et al. 2009). isolates able to overcome the resistance gene Lr9 However, environmental conditions, amount of (McCallum et al. 2010). inoculum, host susceptibility, host physiological Cereal cultivation has a long history in Finn- growth stage and timing of the epidemic, all af- ish agriculture. There are records of barley, oat, fect the degree of damage significantly (Duveiller , and wheat cultivation from the 14th century. 2007). Barley was the main cereal until the end of the 19th Reports on causal agents of cereal fungal dis- century, when it was replaced by oat (Grotenfelt eases in Finland have existed since the end of the 1922). The acreage of barley cultivation began to 19th century (Karsten 1868). Liro (1917) and Gro- increase rapidly again at the end of 1950 (Figure 1) tenfelt (1922) informed farmers of the importance (Tike 2010). The total agricultural area in Finland of destroying smut and other disease-causing fungi in 2010 was 2.3 million hectares, of which from cereal seed. Since then, the methods to con- were cultivated on almost half the area (1.0 million trol plant diseases have developed considerably

1 000 ha 1 600

1 400

1 200

1 000

800

600

400

200

0 0 4 9 4 9 4 9 4 9 4 9 4 9 4 9 4 9 4 9 1 2 2 3 3 4 4 5 5 6 6 7 7 8 8 9 9 0 0 Fig. 1. The area of cereal crops 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 0 0 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 2 2 cultivated in Finland in 1910–

Other grain Mixed crops Spring Spring barley Rye Spring wheat Winter wheat 2009 (Tike 2010). 62 63 AGRICULTURAL AND FOOD SCIENCE AGRICULTURAL AND FOOD SCIENCE

Jalli, M. et al. The emergence and incidence of cereal fungal diseases in Finland Vol. 20(2011): 62–73. and have concentrated on various important plant The disease survey was co-organized with a weed diseases at different times. Currently, 73% of Finn- distribution study (Salonen et al. 2011) and by ish farmers treat cereal fields with fungicides an- ProAgria Rural Advisory Centres in order to cover nually (Mäenpää 2010). The sale of fungicides in the main cereal production area (Fig. 2). The total agriculture (in active ingredients) increased from number of investigated fields was 107 in barley, 18 tonnes to 158 tonnes between 1953 and 2008 84 in spring wheat, and 64 in oats. The selected (Evira 2010). At the same time, there has been sub- fields represented the most common cereal culti- stantial development in disease resistance breeding vars grown in Finland under both ploughed and (Jalli 2010). reduced tillage systems, as well as for conventional Pest surveys recognise the changes of pest sta- and organic farming. tus in time and also identify the indigenous and Leaf samples were collected between flowering non-indigenous pest species. In Finland, the pest and milk ripening growth stages from mid-July till surveys are made on weeds (Salonen et al. 2011) early August. For 10 sites per field, 10 leaves were and on insects (Vappula 1962). Previous survey on collected from 10 randomly selected plants; 100 cereal leaf spot pathogens in Finland was conduct- leaves per field in total. The aim was to collect the ed by Mäkelä (1975a,b). The aim of this study was oldest green leaves, usually the second or third leaf to evaluate the current state of cereal leaf diseases from the apex. in Finland with reference to historical and current The leaves were dried and pressed between research data. The questions addressed were: i) tissues immediately after collection. The visual which cereal pathogen species have been identi- symptoms were recorded for all dried leaves. The fied in Finland; and ii) what is the incidence and pathogen identifications were made using the agar distribution of the main leaf spot diseases in the plate method (barley and oat) or a PCR-test method Finnish spring cereal fields? The objective was to (wheat). The oat and barley leaf tissues with le- get a base for better understanding on the possible sions were surface sterilized in 50% ethanol for risks caused by plant pathogens in the Finnish ce- 15 s and in 2% NaOCI for 30 s, and then rinsed real production. The updated information on the with distilled water and placed on water agar in incidence of pathogens and their distribution is in sterile Petri dishes. Petri dishes were kept under the key role in advisory services, in developing near UV light and a 12:12 h L:D photoperiod at novel durable plant protection methods and in dis- 18° C for 7–14 days. The pathogens were identi- ease resistance breeding strategies for future needs. fied using a light microscope. From wheat sam- ples, Stagonospora nodorum (stagonospora leaf blotch), Pyrenophora tritici-repentis (tan spot) and Mycosphaerella graminicola (septoria tritici leaf blotch) were identified using a specific PCR-test Material and methods method as described by Jalli et al. (2011).

The first part of this study, based on literature survey, is an evaluation of the earliest records on cereal fungal pathogens diagnosed in Finland. The earliest available references on pathogen occurrence Results and collection year were surveyed. The literature is published mainly in Finnish. In this study, the Literature survey pathogen names were changed to common names recommended by Species Fungorum (2010). Based on the literature study, 57 plant pathogens In the second part, we studied the incidence and causing cereal diseases in Finland have been reported distribution of cereal leaf spot diseases in spring to date (Table 1). In 25 cases, the data for collection barley, spring wheat and oats in Finland in 2009. year were not available. Reports were published 64 65 AGRICULTURAL AND FOOD SCIENCE AGRICULTURAL AND FOOD SCIENCE

Jalli, M. et al. The emergence and incidence of cereal fungal diseases in Finland Vol. 20(2011): 62–73. - Liro 1917 Liro 1917 Liro 1917 Liro 1917*, Koponen and Mäkelä 1975** Liro 1917*, Mäkelä 1972** Mäkelä 1975b First reference of the oc curence of the pathogen in Finland Liro 1917 Liro 1917 Liro 1917 1966 Talvia Mäkelä 1971 Mäkelä 1971 Lindroth 1898b Lindroth 1898b Liro 1917 Liro 1917 Liro 1917 Oxley et al. 2010 Lindroth 1898b Lindroth 1898b Lindroth 1898b Mäkelä 1972 Mäkelä 1972 Kurtto 1998 Rainio 1930 Jamalainen 1943a Jamalainen 1943a - 1972 1971** Collection year for the first reported oc curence in Finland 1965 1967-1970 1967-1970 2001 1970-1971 1970-1971 1938 1938 1928 (Fuckel) J. Schröt. Speg. (Died.) Drechsler f.sp. avenaria O.E. Erikss.** (S. Ito & Kurib.) Drechsler ex Dastur (Fr.) Sacc. (Fr.) (Schwein.:Fr.) Petch (Schwein.:Fr.) Mycosphaerella graminicola Mycosphaerella Phaeosphaeria avenaria Phaeosphaeria nodorum (E. Müll.) Hedjar.** Teleomorph chaetomioides Pyrenophora graminea S. Ito & Kurib. Pyrenophora Drechsler f. teres teres Pyrenophora Cochliobolus sativus tritici-repentis Pyrenophora Pyrenophora teres f. maculata Smed.-Pet. teres Pyrenophora Gibberella zeae Gibberella pulicaris Gibberella Causal agent (Oudem.) Davis B. Sutton & J.M. Waller B. Sutton & J.M. (Sacc.) Shoemaker Westend (De Not.) Crous & U. Braun Dietel & Holw. (Eidam) Scharif Pers. (Petr.) R. Sprague & Aar.G. Johnson Aar.G. R. Sprague & (Petr.) Prill. & Delacr Roberge in Desmaz Roberge avenae Fr. alopecuri (Fr.) Septoria tritici Stagonospora avenae (A.B. Frank) Bissett* Stagonospora nodorum (Berk.) E. Castell. & Germano* Septoria secalis avenae Anamorph graminea (Rabenh. ex Schltdl.) Ito Drechslera (Sacc.) Shoemaker f. teres teres Drechslera Rhynchosporium secalis Bipolaris sorokiniana (Died.) Shoemaker tritici-repentis Drechslera Hara Ascochyta hordei Puccinia striiformis Blumeria graminis (DC.) Speer Davidiella tassiana Fusarium sp. Fusarium culmorum (Wm. G. Smith) Sacc. Corda Puccinia coronata Puccinia graminis G.H. Otth Puccinia hordei Puccinia recondita f. maculata Smed.-Pet. teres Drechslera Ellis & Everh. Hymenula cerealis Ramularia collo-cygni Fusarium graminearum Schwabe Fusarium sambucinum Fuckel Leaf spot diseases Ascochyta leaf spot Dilophospora leaf spot Septoria tritici leaf blotch Stagonospora leaf blotch Stagonospora leaf blotch Septoria leaf blotch of rye Oat leaf spot Table 1. Cereal fungal pathogens reported in Finland. Table Plant disease Barley stripe Barley net blotch (net type) Scald Spot blotch Tan spot Tan Ascochyta leaf spot Stripe rust Powdery mildew Black head mold Root, stem and head diseases, snow molds Head blight/root and stem diseases Rusts and mildew Oat crown rust Stem rust Leaf rust of barley Leaf rust of wheat Barley net blotch (spot type) Cephalosporium stripe Ramularia leaf spot Head blight/root and stem diseases Head blight/root and stem diseases 64 65 AGRICULTURAL AND FOOD SCIENCE AGRICULTURAL AND FOOD SCIENCE

Jalli, M. et al. The emergence and incidence of cereal fungal diseases in Finland Vol. 20(2011): 62–73. - Jamalainen 1943b Jamalainen 1943b Jamalainen 1943b First reference of the oc curence of the pathogen in Finland Jamalainen 1943b Jamalainen 1943b Jamalainen 1944 Jamalainen 1944 Jamalainen 1944 Hårdh 1953 Ylimäki 1972 Korpinen and Uoti and Ylimäki 1974 Uoti and Yli-Mattila et al. 2004 Reuter 1912 Hårdh 1953 Mäkelä and Mäki 1980 Talvia 1970 Talvia Mäkelä 1979 Hannukkala 1985 Karsten 1868 Liro 1917 Liro 1917 Maatalouskoelaitos 1951 Lindroth 1899 Mäkelä and Parikka 1980 Lindroth 1898a Liro 1914 Liro 1914 Liro 1915 Liro 1915 Liro 1915 Liro 1915 - 1938 1938 1938 Collection year for the first reported oc curence in Finland 1938 1938 1938 1938 1946-1953 1938 1966-1968 1910 1946-1953 2001 1975-1978 1963-1968 1975-1977 1979-1983 1938 1975-1978 1887 (Berk. & Broome) Samuels D.J. Politis D.I. Murray & Burpee (Wallwork & Spooner) Crous (Wallwork (Schaffnit) E. Müll. (Schaffnit) R.J. Cook Wollenw Wollenw El-Gholl, McRitchie, Schoult. & Gibberella avenacea Gibberella Gibberella tricincta Gibberella Ridings Teleomorph Haematonectria haematococca & Rossman Gibberella intricans Gibberella (Sawada) Wollenw. Wollenw. (Sawada) fujikuroi Gibberella (Sacc.) Arx & D.L. Olivier Gaeumannomyces graminis (Sacc.) Oculimacula yallundae Gams W. Thanatephorus cucumeris (A.B. Frank) Donk cereale Monographella nivalis (Fr.) Tul. Tul. (Fr.) Claviceps purpurea graminicola Glomerella

Causal agent (Fron) Deighton (Ces.) G.W. Wilson (Ces.) G.W. Sherb. Schaffnit (Fr.:Fr.) Samuels & I.C. Hallet (Fr.:Fr.) Torp & Nirenberg Torp (Corda) Sacc. Typhula ishikariensis / Typhula Remsberg Lasch J.G.Kühn Lév. (Corda) Sacc. (Wallr.) Rabenh. (Wallr.) Sacc (Pers.) Rostr. (DC.) Tul. & C. Tul. & C. Tul. (DC.) J.G. Kühn (Fr.:Fr.) Sacc. Fusarium avenaceum (Fr.:Fr.) Wollenw Fusarium poae (Peck) Sherb. Fusarium arthrosporioides Fusarium tricinctum Anamorph Fusarium solani (Mart.) Sacc. Fusarium sporotrichioides Fusarium detonianum Sacc. Fusarium oxysporum Schltdl Fusarium equiseti Fusarium moniliforme J. Sheld & Reinking Wollenw. Fusarium chlamydosporum Fusarium incarnatum (Desm.) Sacc. Phialophora sp. herpotrichoides Pseudocercosporella solani Fusarium langsethiae Wojnowicia hirta Wojnowicia E.P. Hoeven E.P. Rhizoctonia cerealis idahoensis Typhula S. Imai nivale Microdochium incarnata Typhula Vleugel Bubák & borealis Sclerotinia Sphacelia segetum Colletotrichum graminicola occulta Urocystis Tilletia caries Tilletia laevis Tilletia Ustilago avenae (Pers.) Lagerh. Ustilago hordei Schaffnit Ustilago nuda f.sp. hordei Ustilago nuda f.sp. tritici Table 1. continuing Table Plant disease Head blight/root and stem diseases Head blight/root and stem diseases Head blight/root and stem diseases Head blight/root and stem diseases Head blight/root and stem diseases Head blight/root and stem diseases Head blight/root and stem diseases Head blight/root and stem diseases Head blight/root and stem diseases Head blight/root and stem diseases Head blight/root and stem diseases Head blight/root and stem diseases Take-all Take-all Eyespot Rhizoctonia root rot Head blight/root and stem diseases Root rot Rhizoctonia root rot blight Typhula Snow mold blight Typhula Sclerotinia snow mold Ergot Anthracnose Smuts stalk smut Rye Common bunt Common bunt Oat loose smut Covered smut in barley and oats Barley loose smut Wheat loose smut 66 67 AGRICULTURAL AND FOOD SCIENCE AGRICULTURAL AND FOOD SCIENCE

Jalli, M. et al. The emergence and incidence of cereal fungal diseases in Finland Vol. 20(2011): 62–73. between 1917 and 2010 for cereal leaf spot diseases. sativus in 25% (Fig. 3b), and S. avenae in 3% of - The most recent report is on Ramularia collo- the investigated fields. cygni. The rusts, powdery mildew and smuts were all reported between 1898 and 1917. The reports on the occurrence of different root, stem and head diseases, and snow moulds, originate from 1868 Discussion Jamalainen 1943b Jamalainen 1943b Jamalainen 1943b First reference of the oc curence of the pathogen in Finland Jamalainen 1943b Jamalainen 1943b Jamalainen 1944 Jamalainen 1944 Jamalainen 1944 Hårdh 1953 Ylimäki 1972 Korpinen and Uoti and Ylimäki 1974 Uoti and Yli-Mattila et al. 2004 Reuter 1912 Hårdh 1953 Mäkelä and Mäki 1980 Talvia 1970 Talvia Mäkelä 1979 Hannukkala 1985 Karsten 1868 Liro 1917 Liro 1917 Maatalouskoelaitos 1951 Lindroth 1899 Mäkelä and Parikka 1980 Lindroth 1898a Liro 1914 Liro 1914 Liro 1915 Liro 1915 Liro 1915 Liro 1915 to 2004. The most recent pathogens to emerge are

- Fusarium langsethiae and Ramularia collo-cygni. The main outcome of the literature study was the list of plant pathogens identified on cereals in Field survey Finland. Mention of the first report is missing in most cases, except for the most recently identified 1938 1938 1938 Collection year for the first reported oc curence in Finland 1938 1938 1938 1938 1946-1953 1938 1966-1968 1910 1946-1953 2001 1975-1978 1963-1968 1975-1977 1979-1983 1938 1975-1978 1887 diseases, Fusarium langsethiae and Ramularia The causal agents of fungal leaf spot diseases identi- collo-cygni. Some of the papers reported the first fied in the 2009 field survey were:Pyrenophora teres observation of the sexual stage of the pathogen, (net blotch), Cochliobolus sativus (spot blotch) and including Phaeosphaeria avenaria f.sp. avenaria Rhynchosporium secalis (scald) in barley, Stagono- and Phaeosphaeria nodorum. spora nodorum, Pyrenophora tritici-repentis and The most recently identified cereal pathogens Mycosphaerella graminicola in spring wheat and in Finland, F. langsethiae on barley and oats, and R. (Berk. & Broome) Samuels Pyrenophora chaetomioides (oat leaf spot), Coch- collo-cygni on barley, are considered to be emerg- D.J. Politis D.I. Murray & Burpee

(Wallwork & Spooner) Crous (Wallwork liobolus sativus, and Stagonospora avenae in oats. ing pathogens also in Europe (Walters et al. 2008; (Schaffnit) E. Müll. (Schaffnit) R.J. Cook Wollenw Wollenw El-Gholl, McRitchie, Schoult. & Minor powdery mildew infections were identified Torp and Nirenberg 2004). F. langsethiae may on wheat and barley, and yellow rust infection was cause serious problems, mainly because of its tox- observed in one wheat field. in production. Since 2004, it has been detected in Two of the 107 barley fields studied had no Finnish barley and oat fields annually (Parikka, P., identified plant pathogens on the sampled leaves, MTT, personal communication). In contrast, even Gibberella avenacea Gibberella Gibberella tricincta Gibberella Ridings Teleomorph Haematonectria haematococca & Rossman Gibberella intricans Gibberella (Sawada) Wollenw. Wollenw. (Sawada) fujikuroi Gibberella (Sacc.) Arx & D.L. Olivier Gaeumannomyces graminis (Sacc.) Oculimacula yallundae Gams W. Thanatephorus cucumeris (A.B. Frank) Donk Ceratobasidium cereale Monographella nivalis (Fr.) Tul. Tul. (Fr.) Claviceps purpurea graminicola Glomerella and 46 fields carried all three barley pathogens. though R. collo-cygni is recognized as an important

Causal agent Disease symptoms were observed on 95% of the pathogen of barley in Northern Europe and New collected leaves. P. teres was present in 86 % (Fig. Zealand (Walters et al. 2008), and has been identi- 3a), C. sativus in 90% (Fig. 3b) and R. secalis in fied in Finnish barley field already since 2001, it 52% (Fig. 3c) of the investigated fields. has not yet caused any epidemics in Finland (Jalli, (Fron) Deighton Based on the PCR-test, only one of the studied unpublished data). 84 spring wheat fields had none of the tested patho- As Mäkelä (1975b) concluded, the time of (Ces.) G.W. Wilson (Ces.) G.W. Sherb. Schaffnit gens. No visual symptoms were observed in that identification of a pathogen on cereals does not (Fr.:Fr.) Samuels & I.C. Hallet (Fr.:Fr.) Torp & Nirenberg Torp

(Corda) Sacc. field either. A positive PCR-result was obtained correlate with its history on wild plants in Fin- Typhula ishikariensis / Typhula Remsberg Lasch J.G.Kühn Lév. (Corda) Sacc. (Wallr.) Rabenh. (Wallr.) Sacc

(Pers.) Rostr. from 15% of the samples that had no clear visual land. Most of the leaf spot disease causal agents, (DC.) Tul. & C. Tul. & C. Tul. (DC.) J.G. Kühn symptoms. Five of the fields were infected by all like Stagonospora species and R. secalis, have three pathogens. Disease symptoms were observed been isolated from numerous cultivated and wild on 92% of the collected leaves. S. nodorum was grass species (Mäkelä 1974; Mäkelä 1975b). Plant (Fr.:Fr.) Sacc. Fusarium avenaceum (Fr.:Fr.) Wollenw Fusarium poae (Peck) Sherb. Fusarium arthrosporioides Fusarium tricinctum Anamorph Fusarium solani (Mart.) Sacc. Fusarium sporotrichioides Fusarium detonianum Sacc. Fusarium oxysporum Schltdl Fusarium equiseti Fusarium moniliforme J. Sheld & Reinking Wollenw. Fusarium chlamydosporum Fusarium incarnatum (Desm.) Sacc. Phialophora sp. herpotrichoides Pseudocercosporella Rhizoctonia solani Fusarium langsethiae Wojnowicia hirta Wojnowicia E.P. Hoeven E.P. Rhizoctonia cerealis idahoensis Typhula S. Imai nivale Microdochium incarnata Typhula Vleugel Bubák & borealis Sclerotinia Sphacelia segetum Colletotrichum graminicola occulta Urocystis Tilletia caries Tilletia laevis Tilletia Ustilago avenae (Pers.) Lagerh. Ustilago hordei Schaffnit Ustilago nuda f.sp. hordei Ustilago nuda f.sp. tritici present in 98% (Fig. 3d), P. tritici-repentis in 94% pathogens are assumed to have co-evolved from (Fig. 3e) and M. graminicola in 6% (Fig. 3f) of the their original host to their modern hosts during do- investigated fields. mestication thousands of years ago. This is shown, Oat fields had the fewest fungal diseases. 26% for example, with M. graminicola (Stukenbrock et of the tested fields had no fungal infection. 27% of al. 2007) and R. secalis (Zaffarano et al. 2008). the studied oat leaves were totally symptomless. Therefore, caution is needed when drawing conclu- P. chaetomioides was present in 63% (Fig. 3g), C. sions on emergence of a specific pathogen. Instead, based on the literature, we can estimate which plant Table 1. continuing Table Plant disease Head blight/root and stem diseases Head blight/root and stem diseases Head blight/root and stem diseases Head blight/root and stem diseases Head blight/root and stem diseases Head blight/root and stem diseases Head blight/root and stem diseases Head blight/root and stem diseases Head blight/root and stem diseases Head blight/root and stem diseases Head blight/root and stem diseases Head blight/root and stem diseases Take-all Take-all Eyespot Rhizoctonia root rot Head blight/root and stem diseases Root rot Rhizoctonia root rot blight Typhula Snow mold blight Typhula Sclerotinia snow mold Ergot Anthracnose Smuts stalk smut Rye Common bunt Common bunt Oat loose smut Covered smut in barley and oats Barley loose smut Wheat loose smut 66 67 AGRICULTURAL AND FOOD SCIENCE AGRICULTURAL AND FOOD SCIENCE

Jalli, M. et al. The emergence and incidence of cereal fungal diseases in Finland Vol. 20(2011): 62–73.

Fig. 2. The area for the cereal leaf spot disease survey conducted in Finland.

a) b) c)

d) e) f)

Fig. 3. The locations of the cereal fields investigated in 2009. Red areas represent positive incidence and blue ab- sence of the specific pathogen in the field. The incidence of a) P. teres in barley fields, b)C. sativus in barley and oat fields, c)R. secalis in barley fields, d)S. nodorum in spring wheat fields, e)P. tritici-repentis in spring wheat fields, f)M. graminicola in spring wheat fields, g)P. ave- g) nae in oat fields. 68 69 AGRICULTURAL AND FOOD SCIENCE AGRICULTURAL AND FOOD SCIENCE

Jalli, M. et al. The emergence and incidence of cereal fungal diseases in Finland Vol. 20(2011): 62–73.

pathogens have been significant in Finnish cereal or dressed seed (Mathre 1997). During the past production at different times. 40 years, the barley growing area has increased Even though the year of emergence of differ- 50% from 403 500 ha to 600 700 ha. At the same ent fungal species on cereals in Finland is usually time, the total cultivated area has decreased from missing, the significance of different diseases at 2 526 400 ha to 2 026 800 ha (Matilda 2010a), various times is illustrated in an interesting way in which means that the possibilities for crop rotation the literature. In the early 20th century, the litera- have lessened. Barley monoculture together with ture concentrated on smut and rust diseases while the increase in no- or reduced tillage cultivation towards the end of the century the focus was more area in Finland (MAVI 2009) represent a risk for on leaf spot diseases. In general, the earliest pub- increase in straw-borne pathogen incidence. How- lications reported most about identification and ever, the data presented in this paper illustrate only of fungi while the later ones informed the incidence, not the severity of different patho- on applied research results on the importance and gens. control methods of the diseases. Some of the pa- Efficient control methods, the active use of pers published already at the beginning of the 20th fungicides (Mäenpää 2010) and the moderate re- century are relevant today, such as that published sistance level of Finnish barley cultivars (Kangas by Pesola (1927) on the resistance of spring wheat et al. 2009), all play a role in keeping the level of cultivars to yellow rust. Currently yellow rust and yield losses to a minimum. However, at the same host-plant resistance are again subjects of special time, large effective population sizes pose a risk of interest in Europe and other parts of the world cancelling out efficient control methods (McDon- (Hovmøller 2008). There is a similar phenomenon ald and Linde 2002). There is evidence that sexual with stem rust. After the heavy stem rust epidemics recombination may also be influenced by climate in Northern Europe in 1951 (Jamalainen 1953) this change and milder winters (Garret et al. 2006). A disease was rare or of minor importance in Finnish recombinant pathogen can rapidly assemble new cereal fields until recent years (Jalli, unpublished combinations of virulence alleles (McDonald and data). Linde 2002). In addition to surveys on the inci- The disease survey, made on spring cereals in dence of plant pathogens, surveys on virulence 2009, represents an opportunity to compare the are needed when studying the emergence of plant changes in incidence and distribution of leaf spot pathogens. In Finland, no change in the virulence diseases in Finland. Forty years ago, in 1971–1973, of P. teres f. teres has been observed during the last a similar type of survey was made for cereals 15 years (Jalli 2010). (Mäkelä 1974; Mäkelä 1975a: Mäkelä 1975b). The In spring wheat, the frequency of both S. no- surveys were made on the same crops covering the dorum and P. tritici-repentis infected fields has in- same cultivation areas. In barley and in oats, the creased over 40 years. The number of S. nodorum causal agents were identified with methods com- infected fields has risen from 60–70 to 98% and parable to each others. P. tritici-repentis infected fields from 30 to 94%. For barley, the frequency of fields infected In the study by Mäkelä (1975b), M. graminicola by leaf spot diseases increased during the last 40 was only observed in winter wheat. In this study, years. The incidence of P. teres infected fields M. graminicola was identified on spring wheat in has increased from 60 to 86%, C. sativus infected Finland for the first time. The positive samples fields from 30 to 90%, and in R. secalis infected originated from South-West and Southern Finland. fields from 30 to 52%. In contrast, Pyrenophora During the last 40 years, the wheat cultivation graminea that was found in 30% of the fields in area has increased by 25%, spring wheat covering 1971–1973 was absent in the fields studied in 2009. 90% of the wheat growing area (Matilda 2010a). P. teres, C. sativus and R. secalis survive in S. nodorum was considered the main wheat patho- straw debris and are favoured by barley monocul- gen in Finland till 2004 when the first epidemics ture, while P. graminea is controlled using healthy of P. tritici-repentis were observed (Laine and 68 69 AGRICULTURAL AND FOOD SCIENCE AGRICULTURAL AND FOOD SCIENCE

Jalli, M. et al. The emergence and incidence of cereal fungal diseases in Finland Vol. 20(2011): 62–73.

Jalli 2005). There is evidence that one reason for Also C. sativus was moderately common in oats rapid increase of P. tritici-repentis is the practice already in the previous study. In contrast to wheat of wheat monoculture combined with no-tillage and barley, the cultivation of oat has decreased cultivation (Huusela-Veistola et al. 2008). Moreo- 35% since 1970s (Matilda 2010a). ver, P. tritici-repentis has been recorded in 50% The information on the incidence of cereal leaf of the studied Finnish Agropyron (Elymus) repens diseases in Finland is based on a survey made in samples (Mäkelä 1971), a weed present in 30% of one cropping season and reflects the situation under the spring cereal fields in Finland (Salonen et al. that season’s environmental conditions. The PCR- 2011). P. tritici-repentis is a that became based diagnostic method to identify wheat patho- pathogenic on wheat only recently in comparison gen species is very sensitive compared with the with other leaf spot diseases. Friesen et al. (2006) agar-plate method used by Mäkelä (1975b). How- provided evidence that a gene encoding a virulence ever, it is evident that the cereal leaf spot diseases factor was transferred from S. nodorum to P. tritici- have more importance today than they had 40 years repentis probably in the beginning of 1950s. This ago. In Mäkelä’s studies both S. nodorum and M. horizontal gene transfer significantly enhanced graminicola were considered to be of minimum virulence and led to the emergence of a new dis- importance and were observed most commonly ease of wheat. in the southern parts of the country, while in our M. graminicola has been relatively common on studies S. nodorum and P. tritici-repentis were winter wheat tillers in early spring, but the disease common at all locations. P. teres, C. sativus and R. has rarely developed further under Finnish condi- secalis were of minor significance in barley until tions (Kurtto et al. 2005). However, since 2006, M. the early 1970s while the seed-borne pathogen P. graminicola has also been observed on the upper graminea was dominant in barley fields (Mäkelä leaves of winter wheat later in the growing season 1972). Now the situation has become reversed. (Jalli et al. 2007). Furthermore, in other parts of The low incidence of P. graminea is related to the Europe, the importance of Septoria tritici blotch, increase in barley seed treatment. In 2009, 46% of caused by M. graminicola, has increased particu- the cereal seed was fungicide treated in Finland. larly during the last decade, being currently the Approximately 75% of the farmers use fungicide most important wheat disease in Europe (Kema et treated barley seed (Markkula, A., Syngenta, per- al. 2008). Contrary to P. tritici-repentis, M. gramin- sonal communication). icola is an ancient pathogen of wheat. The genetic As a plant disease is an interaction of several data provide evidence that the domestication of an components, the role of different factors in the agricultural crop was accompanied by the domes- complex function may only be discussed. A com- tication of a wheat-adapted fungal pathogen from mon factor affecting the plant pathogens’ environ- a population infecting wild grasses in the Middle ment, besides climatic conditions, is the increased East approximately 10,500 years ago (Stukenbrock cultivation of susceptible host plants. Huusela- et al. 2007). The recent growth in the incidence Veistola and Jauhiainen (2006) concluded that the of M. graminicola may partly be explained by the risk of pea moth infestation increases if regional changes in climate as well as the increase in wheat cropping area and frequency of pea cropping in- growing area. Similar phenomenon has been ob- creases. Planting large areas of susceptible culti- served with potato late blight epidemics in Finland. vars would increase the infection pressure exerted Earlier outbreaks of the potato late blight epidem- on other cultivars (Bingham et al. 2008). The wheat ics were associated with a climate more conducive cultivars grown in Finland are only moderately tol- to the disease and the lack of rotation (Hannukkala erant (Kangas et al. 2009) to leaf spot diseases and et al. 2007). the resistance level of barley has increased only In oats, the incidence of P. avenae (observed in during the last 15 years (Jalli 2010). about 60% of the oat fields both in 1971–1973 and Our field study concentrated on fungal leaf spot 2009) has remained stable during the past 40 years. diseases of cereals. However, there is evidence for 70 71 AGRICULTURAL AND FOOD SCIENCE AGRICULTURAL AND FOOD SCIENCE

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Travers, S.E. 2006. Climate change effects on plant dis- the increased importance of Fusarium head blight ease: genomes to ecosystems. Annual Review of Phy- (Parikka et al. 2010) and rusts (Jalli, unpublished topathology 44: 489–509. data) on wheat, barley and oats. Stem diseases are Giraud, T., Gladieux, P. & Gavrilets, S. 2010. Linking the emergence of fungal plant diseases with ecological spe- important cereal pathogens in Finland (Hannukkala ciation. Trends in Ecology and Evolution 25: 387–395. 1985). Also, the insect-transmitted virus diseases Gregory, P.J., Johnson, S.N., Newton, A.C. & Ingram, J.S.I. are becoming increasing relevant in Finnish ce- 2009. Integrating pests and pathogens into the climate change / food security debate. Journal of Experimental real production. A recently emerged virus disease Botany 60: 2827–2838. is wheat yellow dwarf virus (WYDV) on winter Grotenfelt, G. 1922. Suomalainen peltokasviviljelys, jälkim- wheat (Lemmetty and Huusela-Veistola 2005). mäinen osa. In: Arola, T. et al. (ed.), Maatalouden tieto- kirja. Helsinki: Otava 509 p. (In Finnish). Even though novel pathogen species emerge rare- Hannukkala, A. 1985. Inverkan av ensidig spannmålsod- ly, the existing hosts and pathogens continuously ling på stråbassjukdomar. Växtskyddsnotiser 49: 75– interact, which may lead to novel virulence if no 78. (In Swedish). Hannukkala, A.O., Kaukoranta, T., Lehtinen, A. & Rahko- precautions are taken. Research on pathogen-host nen, A. 2007. Late-blight epidemics on potato in Fin- interactions, monitoring, risk assessments, multi- land, 1933–2002; increased and earlier occurrence of protection using cultural practices, crop rotation, epidemics associated with climate change and lack of rotation. Plant Pathology 56: 167–176. durable resistant plants, fungicide used only when Hovmoller, M.S., Yahyaoui, A.H., Milus, E.A. & Just- needed, and global cooperation among researchers esen, A.F. 2008. Rapid global spread of two aggres- and breeders, are the main strategies to avoid, or sive strains of a wheat rust fungus. Molecular Ecology 17: 3818–3826. to minimize the impact of plant diseases in cereal Huusela-Veistola, E., Jalli, H., Jalli, M. & Salonen, J. 2008. production. Plant protection in direct drilling - needs and solutions. In: NJF Seminar 418: New insights into sustainable cul- Acknowledgements: KASMO-team, ProAgria and EVIRA tivation methods in agriculture, Piikkiö, Finland, 17–19 September 2008. NJF Report 4, 3: 14. seed health are greatly acknowledged for their thorough Huusela-Veistola, E. & Jauhiainen, L. 2006. Expansion of collection of the leaf samples. 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