Plant sulphur metabolism and plant diseases

IX. International Symposium on Plant Biotechnology, St. Clara, 20 - 22 April 2010

Plant sulphur metabolism and plant diseases

Silvia Haneklaus, Elke Bloem and Ewald Schnug

Institute for Crop and Soil Science, Julius Kühn-Institut, Federal Research Centre for Cultivated Plants (JKI) Braunschweig, Germany www.jki.bund.de


Severe sulphur deficiency

Macroscopic sulphur deficiency in oilseed rape, wheat and sugar beet on production fields


Interactions between performance of Brassica crops and gradation of pests in relation to anthropogenic and environmental factors (Defence metabolites: -N = N-free; +N and +S = N and S-containing compounds).


Sulphur and insects

Sulphur fertilisation promotes specialist insects (Haneklaus et al., 2008).

Pollen beetle (Meligethes spp.)

Severe S-deficiency coinicides with a reduced number of visiting honeybees because the major attractants scent, color and petal morphology alter significantly (Schnug and Haneklaus, 2005).

Honeybees mistake S-deficient for pollinated flowers


Sulphur and plant diseases Disease Verticillium wilt Downy mildew Stripe rust Leaf blight Fusarium wilt Verticillium wilt Club root Downy mildew Powdery mildew

Pathogen Verticillium dahliae Sclerophthora macrospora Puccinia striiformis Bipolaris maydis Fusarium oxysporum Verticillium dahliae Plasmodiophora brassicae Phomopsis viticola Uncinular necator

Host Cacao Cereals Cereals Corn Cotton Cotton Crucifers Grape Grapes

Stewart’s wilt Light leaf spot

Erwinia stewartii Pyrenopeziza brassicae

Maize Oilseed rape

Scleroteria stem rot Alternaria black spot Black leg

Sclerotinia sclerotiorum

Oilseed rape

Alternaria brassicae

Oilseed rape

Leptosphaeria maculans

Oilseed rape

Wilt Pea root rot Leaf spot Needle blight Late blight

Verticillium dahliae Aphanomyces euteiches Cercospora arachidicola Dothistroma Phytophthora infestans

Oilseed rape Pea Peanut Pine Potato

Stem canker Common scab

Rhizoctonia solani Streptomyces scabies

Potato Potato

Black leg Bud death Root rot Leaf spot Mosaic Wilt Wilt

Erwinia carotovera Pycnostysanus agaleae Rhizoctonia solani Ramularia beticola Tobacco mosaic virus Fusarium oxysporum Verticillium dahliae

Potato Rhododendron Soybean Sugar beet Tobacco Tomato Tomato

Patch Sharp eyespot Stem rust

Fusarium nivale Rhizoctonia cerealis Puccinia graminis

Turfgrass Wheat Wheat

Powdery mildew

Erysiphe graminis

Wheat

Mites Bud mite

General Cecidophyopsis ribis

Currant

Reference Cooper et al. 1996; Williams et al. 2002 Hoy 1987 McNew 1953 Wang et al. 2003 Wang et al. 2003 Wang et al. 2003 Pryer 1940 Beffa 1993 Bourbos et al. 2000; Coleno 1987; Girolami and Duso 1984; Kassenmeyer 2003; Schmid et al. 1980 Spencer and McNew 1938 Coleno 1987; Bloem et al. 2004; Schnug 1988; Schnug et al. 1995 Dornberger et al. 1975; Mithen et al. 1986; Wang et al. 2003 Anon 1988; Koch 1989 HCGA 2003; Gladders et al 1998; Pedras et al. 1997; Salac et al. 2004 Burandt et al. 2001 van Andel 1966 Campbell et al. 1988 Lambert 1986 Campbell et al. 1988; Doke and Tomiyama 1978 Klikocka et al. 2005 Chester 1942; Funakoshi and Matsuura 1983; Hooker 1957; Keinath and Loria 1989; Vlitos and Mortvedt et al. 1963 DeLacy Costillo et al. 1999 Schmalscheidt, 1985 Castano and Kernkemp, 1956 Tolman and Stoker 1941 Chessin and Scott 1955 Jones and Woltz 1969 Resende et al. 1996; Williams et al. 2002 Goss and Gould, 1996 Wang et al. 2003 Coleno 1987; Cook 1987; Hoy 1987; McNew 1953; Reuveni 2001 Coleno 1987; Cook 1987; Hoy 1987; McNew 1953; Reuveni 2001; Vidhyasekaran, 2000 Hoy 1987 Korchagin 1983


William Forsyth (1802) discovered the fungicidal effect of S0


Influence of foliar S0 application and inoculation with F. culmorum on infection rate (%) of winter barley with Fusarium head blight three and four weeks after inoculation and yield parameters.

Weekly S0 application1

Inoculation with F.

culmorum

Infection Rate (%)

BBCH 73 BBCH 77 without without 35 48 without with 34 58 with without 28 37 with with 19 38 1 first S0 application one week before inoculation Source: Haneklaus et al. (2007)

Grain yield (dt ha-1)

Straw yield (dt ha-1)

72.9 65.2 76.6 74.6

43.4 36.4 43.4 47.2


Interactions between sulphate-based soilapplied S and disease index have been found since the early 1990s.


S Cycling in Plants (De Kok, 2001)


Influence of sulphur application rates in pot experiments to the resistance of crops against certain diseases (Wang et al., 2003)


Influence of the sulphur rate and sulphur form on soil pH, yield and infection rate and severity with Rhizoctonia solani in a field experiment in Poland Rhizoctonia solani S rate

S form

Soil pH

Tuber yield

Infection rate

(dt ha-1)

(%)

5.9

239

33.3

4.7

(kg ha-1) 0

Infection severity

25

SO4

5.8

202

32.8

4.9

25

S0

5.4

207

26.2

4.8

50

SO4

5.8

262

25.2

5.2

50

S0

5.3

270

19.7

6.6

LSD5%

S rate

0.08

1.9

0.5

0.07

S form

0.06

1.5

0.4

0.06

Note: Infection severity: 9 = none; 1 = >25% small and big sclerotia; source: Klikocka et al. 2005; photo: LFL, Bavaria


The term Sulphur Induced Resistance (SIR) denotes the reinforcement of the natural resistance of plants against fungal pathogens through triggering the stimulation of metabolic processes involving sulphur by targeted soil-applied fertiliser strategies.


S status / soil SO4 pool

S nutritional demand / determent

Interacting components involved in plant disease

feedback


Sulphur metabolites and pathways putatively involved in SIR in Brassica species


Influence of sulphur source on fungal growth of agar cultures Main effect: S source Control (KCl) K2SO4 Control (MgCl2) MgSO4 Control (PDA) S0 Cysteine Glutathione Methionine

Main effect: S source Control (KCl) K2SO4 Control (MgCl2) MgSO4 Control (PDA) S0 Cysteine Glutathione Methionine

Mean diameter (mm)

Std. Error

55.7 60.0 56.2 57.8 64.4 46.0 58.1 40.1 65.7

.61 .25 .61 .25 .30 .25 .25 .25 .25

Sclerotinia sclerotiorum

Mean diameter (mm)

Std. Error

33.5 33.9 26.5 29.2 23.1 27.6 13.6 10.7 25.5

.15 .06 .15 .06 .07 .06 .06 .06 .06

GSH and S0 were most efficient.

95% Confidence Interval Lower Bound

Upper Bound

54.5 59.5 55.0 57.3 63.8 45.5 57.6 39.6 65.2

56.8 60.5 57.4 58.3 65.0 46.5 58.5 40.6 66.2

Rhizoctonia solani 95% Confidence Interval Lower Bound

Upper Bound

33.3 33.8 26.2 29.1 23.0 27.5 13.4 10.6 25.4

33.8 34.1 26.8 29.3 23.3 27.7 13.7 10.9 25.6

GSH and cys reduced growth strongly. S0 had no significant effect.

GSH and cys were most efficient. S0 promoted growth.

Mean diameter (mm)

Fusarium culmorum Main effect: S source

Control (KCl) K2SO4 Control (MgCl2) MgSO4 Control (PDA) S0 Cysteine Glutathione Methionine

52.6 55.0 21.9 29.9 65.9 65.9 37.0 23.6 54.9

Std. Error .22 .09 .22 .09 .11 .09 .09 .09 .09

95% Confidence Interval Lower Bound

Upper Bound

52.2 54.9 21.4 29.7 65.7 65.8 36.8 23.4 54.8

53.0 55.2 22.3 30.1 66.1 66.1 37.2 23.8 55.1


Influence of 250 mg S plate-1 on mean growth (mm) of different pathogens in relation to sulphur source at full plate coverage D. teres Period under review (d)

F. culmorum

R. solani

S. Sclerotiorum

23

19

24

7

KCl

27.0

77.4

80.0

85.0

K2SO4

41.6

85.0

73.2

85.0

MgCl2

15.0

33.8

51.0

85.0

MgSO4

43.2

85.0

85.0

85.0

PDA

85.0

85.0

45.4

85.0

S0

31.4

85.0

72.0

31.6

Cysteine

7.0

53.8

18.0

85.0

Glutathione

7.0

15.0

7.0

7.0

Methionine

85.0

85.0

55.2

85.0

S source


SIR is one constituent of the complex phenomenon of Induced Resistence. So far it is not possible to trigger SIR consistently by fertiliser practices.

100 kg ha-1 S

Control


Influence of infection with P. brassicae and S fertilisation on the cysteine content in leaf discs of two varieties of oilseed rape

The strongest increase in cysteine was determined in infected, S-fertilised plots.

(Experimental sites: Braunschweig 2002, Aberdeen 2002 and 2003; n=384) (data from Salac, 2005)


Influence of infection with P. brassicae of two oilseed rape varieties on enzyme activities, cysteine and glutathione content (data derived from Bloem et al. 2004).


H2S is fungitoxic! Börner (1975) Pflanzenkrankheiten und Pflanzenschutz. UTB, Stuttgart Sekiya et al. (1982) Plant Physiol. 70: 430-436 Beauchamp et al. (1984) Crit. Rev. Toxicol. 13: 25-48 Carlile et al. (2004) The Fungi. Elsevier Academic Press, Amsterdam

Is H2S fungitoxic?


Relative growth of S. scabies in relation to H2S concentration in the growth medium Sources: Vlitos and Hooker (1951)


H2S – systemic or local response?

Emission of H2S by grape plants in relation to infection with U. necator and sulphur application


Influence of rated H2S concentrations on fungal growth of S. sclerotiorum and Rhizoctonia solani (Yang et al. 2006, Haneklaus et al. 2007)


Emission of H2S by field-grown oilseed rape plants in relation to infection with V. dahliae and sulphur application


Influence of extremely high concentration of H2S on R. solani


Indicator kriging – an alternative approach for the interpretation of data from field experiments

Small-scale spatial variability of the glutathione, glucosinolate, total sulphur content and the probability of severe infections of oilseed rape with L. maculans (Salac et al. 2004)


Potential efficacy of SIR Reduction of disease index (%) Greenhouse experiments

Field experiments

5-50%

17-35%


Conclusions  Controlling the triggers, which prompt SIR is important to promote natural resistance against diseases by crop-specific S fertilisation.  Mechanisms of SIR are host/pathogen-specific.  Cysteine and glutathione are major players in SIR.  H2S emissions seem to affect fungal growth strongest during the initial phase of pathogenesis.  H2S may yield a fungitoxic/fungistatic effect only if released locally.  The plant available S pool in the soil needs to satisfy an elevated crop demand after infection, which may exceed the physiological need.



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