Table 1
Summary of the suppressive effects of GSLs/ITCs or Brassicaceae against three soilborne fungi of sunflower: Verticillium dahliae, Sclerotinia slcerotiorum and Macrophomina phaseolina using synthetic GSLs-/-ITCs in vitro or in pot (a), Brassicaceae in vitro or in pot (b), Brassicaceae in greenhouse and in the field (c), and at the rotation scale (d).
Target pathogen/plant: fungus studied and plant from which it was isolated (when mentioned); methods: GSLs/ITCs used or destruction/incorporation mechanisms of the Brassicaceae; Brassica species (cv./var.): the Brassicaceae and the cultivar or variety (when mentioned) used for biofumigation; crop to protect: the host plant; GSL/ITC measured: compounds in the Brassicaceae; 2-PE-ITC: 2-phenylethyl-isothiocyanate; a.o.t: among other treatments; Br: Brassicaceae; M.p: Macrophomina phaseolina; MS: microsclerotia; NA: not available; NS: not significant; S.s: Sclerotinia sclerotiorum; UC: unamended/untreated control; V.d: Verticillium dahlia; VW: Verticillium wilt.
| (a) In vitro or in pot experiments using synthetic ITCs/GSLs | |||||
| Target pathogen/plant | Methods | Main results | Reference | ||
| V. dahliae/strawberry | Soil infested with MS exposed to 3 aliphatic (methyl ITC, 2-propenyl ITC, 4-methylsulfinyl-3-butenyl-ITC) and 2 aromatics (benzyl-ITC, 2-PE ITC) versus UC | All ITCs suppressed MS Aromatic ITC were more toxic than aliphatic ITC |
Neubauer et al. (2014) | ||
| V. dahliae/strawberry | 22 natural soil and sterile quartz sand infested with MS exposed to 150 nmol/g of 2-propenyl-ITC versus UC | In sterilized soil: 100% of MS suppressed In natural soil: 9% to 92% of MS suppressed |
Neubauer et al. (2014) | ||
| S. sclerotiorum/mustard and lupin | S.s and other pathogens exposed to different concentrations of 2-PE-ITC versus UC | S.s had among the lowest tolerance to 2-PE-ITC than other pathogens | Smith and Kirkegaard (2002) | ||
| S. sclerotiorum/potato | Mycelium exposed to different concentrations of pure-ITC (methyl, allyl and butyl-ITC) versus UC | Reduction of the mycelial growth 100% of inhibition at the highest concentration of methyl and allyl ITCs |
Ojaghian et al. (2012) | ||
| S. sclerotiorum/various crops | S.s exposed to different concentrations of pure aliphatic ITC (methyl, allyl, butyl and ethyl) and aromatic (ethyl, phenyl, benzyl and 2-PE) versus UC | Methyl and benzyl-ITC reduced mycelial growth Benzyl-ITC reduced sclerotia viability All ITCs (except low concentration of phenyl and 2-PE) reduced the production of apothecial |
Kurt et al. (2011)(*) | ||
| S. sclerotiorum/various crops | Infested soils transplanted with pepper seedlings exposed to synthetic ITCs (Kurt et al., 2011*) | Allyl and 2-PE ITCs reduced the incidence of S.s on pepper by 76.7% and 70% at low concentration, respectively | Kurt et al. (2011) | ||
| S. sclerotiorum/NA | Sclerotia of S.c or other pathogens exposed to different concentrations of synthetics GSLs (2-propenyl, 2-hydro-3-butenyl, benzyl, and methylsulfinylalkyl) | GSLs inhibited S.s growth Methylsulfinylalkyl was the most effective |
Manici et al. (1997) | ||
| (b) In vitro and pot experiment studies using Brassicaceae | |||||
| Target pathogen | Methods | Brassica species (cv./var.) | GSL/ITC measured | Main results | Reference |
| V. dahliae/sunflower | Mycelium or MS exposed to shoots and roots of Br sampled at mid-flowering and grinded separately versus UC | B. juncea (Etamine), S. alba (Abraham), B. rapa (Avalon), B. napus (Mosa), R. sativus (Anaconda) | Main GSL measured in shoots and roots: S. alba:4-hydroxybenzyl, B. napus: 2-PE, B. juncea: 2-propenyl, B. rapa:4-pentyl, 2-PE and 1-methoxy-3-indolylmethyl | Br reduced mycelial growth (B. juncea, the most effective) and MS germination (B. rapa, the most effective) | Seassau et al. (2016) |
| V. dahliae/eggplant and cotton | Mycelium exposed to powdered tissues of Br | B. oleracea (caulorapa) | NA | 1 g of B. oleracea reduced mycelial growth by 68.7% | Fan et al. (2008) |
| V. dahliae/NA | Mycelium exposed to macerated leaf and stem of Br sampled at flowering versus UC | 28 cv. of B. nigra and 35 cv. of B. juncea | Main ITC measured in shoots: allyl, 2-PE, benzyl, 3-butenyl | Br reduced the radial growth of V.d and reached 100% for 19 cv. of B. nigra and 20 cv. of B. juncea | Olivier et al. (1999) |
| V. dahliae/strawberry | Sterile quartz sand infested with MS amended with freeze-dried ground Br sampled at mid-flowering or non-Br species versus UC | 19 cv. of B. juncea, R. sativus and S. alba | Main GSLs measured in shoots: B. juncea: 2-propenyl, S. alba: benzyl, R. sativus: 4-methylthio-3-butenyl | Shoot of B. juncea was the most efficient to reduce viable MS (69.3 to 81.3%) than other Br or UC | Neubauer et al. (2014) |
| V. dahliae/strawberry | MS exposed to seed meals of Br or autoclaved seed meals versus UC | 16 cv. of S. alba, B. carinata, B. juncea, B. napus | Main GSL/ITC measured in seeds: S. alba: 4-hydroxybenzyl, B. napus: 3-butenyl, 4-pentenyl, 2-PE B. juncea and B. carinata: 2-propenyl-GSL |
Seed meals of B. juncea and B. carinata reduced viable MS by 92.4 to 100%. NS effects of S. alba and B. napus | Neubauer et al. (2015) |
| V. dahliae/soils naturally infested | Infested soil amended with grinded shoots of Br sampled at flowering and soils heavily watered versus UC (a.o.t) | B. juncea (ISCI-99, ISCI-20– high GSL); B. napus (Talent − low GSL) | NA | Living MS were reduced by 66% with ISCI-99, 55% with ISCI-20. NS effect of Talent | Michel et al. (2008) |
| S. sclerotiorum | S.s exposed to powder of Br (shoot, root, seeds) dried, hydrolysed and freeze versus UC | B. juncea (Cutlass), B. rapa (Parkland, Echo), B. napus (Hyola401, RGS003) | Main ITC measured in shoots: B. juncea (Cutlass): allyl | B. juncea (Cutlass) was the most effective to inhibit radial growth | Rahimi et al. (2014) |
| S. sclerotiorum/potato | Mycelium and sclerotia exposed to macerated or irradiated dried tissues of Br (shoots and roots sampled at the 10-leaf stage) versus non-Br or UC | B. napus (Mettah), B. juncea (Bresska), B. campestris (Orrega) | Main ITC measured: methyl, allyl, butyl | All Br reduced mycelial growth and sclerotia formation B. juncea was the most effective |
Ojaghian et al. (2012) |
| S. sclerotiorum/oil rape | Mycelium exposed to powdered tissues of Br | B. oleracea (Caulorapa) | NA | 1 g of B. oleracea reduced mycelial growth by ∼20% | Fan et al. (2008) |
| S. sclerotiorum/lettuce | Mycelium and sclerotia exposed to a dry powder of Br sampled at flowering versus UC (a.o.t) | B. juncea (Vittasso, Pacific Gold, Caliente 99), B. napus (Temple − low GSL control), E. sativa (Nemat), R. sativus (Terranova), S. alba (Brisant), Biofence | Main GSLs measured: B. juncea: 2-propenyl, S. alba: 4-hydroxybenzyl, R. sativus: 4-methylsulfinyl-3-butenyl, E. sativa: 4-methylthiobutyl | All Br (especially R. sativus) reduced germination of S.s B. juncea were the most effective to inhibit mycelial growth |
Warmington and Clarkson (2016) |
| M. phaseolina/NA | Infested soil amended with mustard cake versus UC (a.o.t) | B. juncea (NA) | NA | Reduction of M.p by 100% after 30 days | Sharma et al., 1995 |
| M. phaseolina | Infested soil pasteurized or non-pasteurized amended with seed meals of Br versus UC | B. juncea (Pacific Gold), B. napus (Athena), S. alba (NA) | Main GSLs measured: B. juncea: 2-propenyl, B. napus: 3-butenyl, S. alba: 4-OH-benzyl | Non-pasteurized soils: inconsistent reduction of M.p density, reduction of roots infection of strawberry Pasteurized soils: M.p density increased |
Mazzola et al. (2017) |
| (c) Field and greenhouse studies | ||||||
| Target pathogen | Methods | Brassica species (cv./var.) | Crop to protect (cv./var.) | GSL/ITC measured | Main results | Reference |
| V. dahliae | 1 field/2 years: Br chopped at early flowering, incorporated and the soil was compacted versus bare soil (UC) | B. juncea (Etamine), R. sativus (Anaconda), B. rapa (Chicon) | Sunflower (Kapllan) | Measured in shoots and roots: overall during the 2 years: B. juncea: 2-propenyl, R. sativus: 4-methylthio-3-butenyl and 1-methoxy-3-indolylmethyl, B. rapa: 2-hydro-3-butenyl and 1-methoxy-3-indolylmethyl | Br reduced VW severity both years R. sativus was the most effective (DSI = 37% and 28%) versus UC (DSI = 80% and 48%) |
Galaup et al. (pers. comm.) |
| V. dahliae | 1 greenhouse/1 year: soils infested with MS sampled from fields exposed to biofumigation (Pinkerton et al., 2000*) versus sterile soils (UC) | B. napus (Dwarf Essex) | Eggplants (Imperial Black Beauty) | NA | Br reduced eggplants biomass compared to UC | Pinkerton et al. (2000) |
| V. dahliae | 1 field/2 years: Br cut at ground level, chopped, spread and rotovated below 25 cm depth, irrigated (field capacity) compared to non-Br species and bare soil, all treatments were solarized or non-solarized (a.o.t) | B. napus (Dwarf Essex) | Norway Maple trees | NA | Br combined with solarization reduce VW severity compare to Br sole crop | Pinkerton et al. (2000)* |
| V. dahliae | 1 field/2 years: broccoli residue chopped, incorporated, and disked versus UC (a.o.t) | B. oleracea (italica) | Cauliflower (White Rock) | NA | MS densities decreased after Br compared to initial densities (50 to 75% reduction) VW severity was lower after Br compared to UC The plant height, the number of harvestable heads and the weight of total harvest increased compared to UC |
Subbarao et al. (1999) |
| V. dahliae | 6 field trials/2 years: Br flail-mowed, incorporated both years and rolled; sprinkler-irrigated the second year compared to non-Br species and bare soil (UC) (a.o.t) | B. napus (Humus), B. juncea (Pacific Gold), S. alba (Ida Gold, ISCI 20), Caliente (B. juncea × S. alba) | Tomato (Halley) | For above ground biomass during one year: B. juncea: 2-propenyl, S. alba: benzyl 4-hydroxybenzyl | NS suppressive effect on V.d in the soil Overall, no effect on tomato fruit productivity in the six field trials compared to bare soil |
Hartz et al. (2005) |
| V. dahliae | 1 field/3 years: Br chopped at flowering and incorporated into the soil versus UC (a.o.t) | B. juncea (ISCI20) | Grafted eggplants (Prosperosa) | NA | Partial results of biofumigation Biofumigation combined with grafting was more efficient |
Garibaldi et al. (2009) |
| V. dahliae | 2 fields/1 year: fresh cauliflower residues disk-incorporated twice below 25–30 cm depth and irrigated versus UC (a.o.t) | B. oleracea (Marine) | Artichoke (Blanca de Tudela) | NA | MS densities remained low compared to UC (NS) Inconsistent effects of Br residue on disease incidence, severity, and yield |
Berbegal et al. (2008) |
| V. dahliae | 2 fields/2 years: Br compared to non-Br species and UC | B. oleracea (Excelsior) | Potato (Russet Burbank) | NA | Br reduced V.d inoculum by 50% and VW by 69% at highest rate NS effect on root infection and yield compared with UC |
Ochiai et al. (2007) |
| V. dahliae | 1 field/1 year: Br incorporated at flowering with a rototiller (twice) compared to non-Br species and UC | B. juncea (ISCI-20) | Strawberry (Elsanta) | NA | Reduction of MS by 19% compared with UC | Michel et al. (2008) |
| V. dahliae | 2 farms/1 year: Br finely mulched at flowering and incorporated with a rototiller versus UC (a.o.t) | B. juncea (ISCI-20) | Sweet pepper (Red beefhorn, Somborka) | NA | Overall, reduction of MS in both farms (48% to 74%) | Michel et al. (2008) |
| V. dahliae | 1 Greenhouse/1 year: dried Br sampled at full flowering, incorporated below 20 cm depth, irrigated (35 mm), compared to non-Br and UC (a.o.t) | B. juncea (ISCI-99 and Etamine) | Tomato (Admiro) | Methylsulfinylalkyl, benzyl, 2-propenyl, and 2-hydro-3-butenyl | Short-term: NS effect on MS reduction Long-term: MS reduced by 80% |
Michel (2014) |
| V. dahliae | 1 greenhouse/1 year: biofence expanded on soil surface (250 g/m2), incorporated below 20 cm depth, irrigation (20 mm water + biofence flowable) 6 times, compared to non-Br and UC (a.o.t) | Biofence | Tomato (Admiro) | NA | NS effect of biofence and biofence FL | Michel (2014) |
| M. phaseolina | 1 field/2 years: mustard oil cake amendment or mustard residues mixed (hand spade), incorporated below 30 cm depth, irrigated or not versus UC (a.o.t) | B. juncea (Pusa bold) | Cluster bean | NA | Reduction of M.p and dry root rot Mustard oil cake was more effective by 38% than mustard residues |
Mawar and Lodha (2002) |
| M. phaseolina | 1 field/2 years: Seed meal incorporated, and plots irrigated (surface saturation) | B. juncea (Pacific Gold), B. alba (Ida Gold) | Strawberry (Camarosa) | NA | NS effect on strawberry plant biomass, total number of fruit produced and total fruit biomass | Mazzola et al. (2017) |
| (d) Rotation scale studies | ||||||
| Target pathogen | Methods | Brassica species (cv./var.) | Crop to protect | GSL/ITC measured | Main results | Reference |
| V. dahliae | 10 years of 2-year rotation with potato−Br (1 × Br−1 × P) Br was either incorporated as green manure (Dwarf Essex) or harvested without incorporation (canola) compared to non-Br Crops and continuous potato (1 × P−1 × P) |
B. napus (canola), B. napus (Dwarf Essex) | Potato (Russet Burbank) | NA | Overall, rapeseed reduced VW and canola had inconsistent effects Higher tuber yields after Canola (+6.8%) compared to continuous potato, and inconsistent effects of rapeseed |
Larkin et al. (2010) |
| V. dahliae | 7 years with potato−Br rotation (3 × Br−2 × P−1 × Br−1 × P) Br was incorporated into the soil by disking or rotovating compared to non-Br species and barre soil |
B. napus (Dwarf Essex and Bridger) | Potato (Russet Burbank) | NA | Inconsistent effects of Br on V.d population in the soil Reduction in VW NS differences of the yield compared to bare soil (see Davis et al., 1996) |
Davis et al. (2010) |
| V. dahliae | 5 years with potato−Br rotation (3 × Br−2 × P) Br was incorporated into the soil by disking or rotovating compared to non-Br species and barre soil (UC) |
B. napus (Dwarf Essex and Bridger) | Potato (Russet Burbank) | NA | Overall, NS effects on V. d and yield Reduction in VW |
Davis et al. (1996) |
| V. dahliae | 2 fields with strawberry−Br rotation compared to non-Br rotation (a.o.t) Br was harvested and residues flailed shredded, air dried on the soil surface for 48 h and incorporated into the soil below 15–20 cm depth with a rototiller |
B. oleracea (Marathon), B. oleracea (Oliver) | Strawberry (Selva) | NA | Reduction of MS density (up to 83%), and VW severity in the rotation with Br Increase of strawberry growth |
Subbarao et al. (2007) |
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