Cropping systems to mediate biologically based soil suppressiveness

Several modifications to crop production systems have been employed as a means to control soilborne plant diseases. The most common and effective scheme has been the use of crop rotations, with disease control believed to be achieved as the absence of a suitable plant host results in diminished viability of the pathogen. Attempts to develop specific cropping models to manage the resident soil microbiota for disease suppression have been few. It has been reasoned that as increased plant diversity can enhance micro-bial community biomass (Zak et al., 2003) mixed cropping systems will generate a more diverse microbial community and thus should be more resilient to pathogen invasion (Workneh and van Bruggen, 1994; Hiddink et al., 2005). However, the preponderance of examples of induced suppressive soils come from crop monoculture systems (Chet and Baker, 1980; Cook and Weller, 1987), and limited attempts to compare mixed crop systems with single crop systems indicate that mixed systems may not enhance micro-bial diversity or disease suppressiveness (Hiddink et al., 2005).

Plant root systems and their release of a complement of root exudates serve as a dominant driving force in determining soil microbial community diversity and density (Lemanceau et al., 1995; Dalmastri et al., 1999; Miethling et al., 2000; Marschner et al., 2001; Berg et al., 2002; Mazzola and Gu, 2002), particularly in conventional crop production systems where organic matter and substrate availability is typically nominal. As noted above, certain crop monoculture systems express the ability to select for microbial communities that over time lead to the development of soils suppressive to specific soilborne pathogens (Larkin et al., 1993; Weller et al., 2002). Alternatively, previous cropping systems may inadvertently yield a soil suppressive to a pathosystem of a subsequent unrelated crop. For example a soil cropped to a continuous wheat monoculture was shown to be biologically suppressive to Rhizoctonia root rot of apple incited by R. solani AG-5 (Mazzola, 1999). Once planted to apple, soil suppressiveness towards this pathogen diminished over time and loss of disease suppression corresponded with specific changes in composition of the fluorescent Pseudomonas spp. population and reduced densities of Burkholderia cepacia recovered from orchard soils. Interestingly, soil suppressiveness towards Rhizoctonia root rot of both apple and wheat could be restored in greenhouse trials through repeated cultivation of these soils with wheat (Mazzola and Gu, 2000, 2002). Restoration of soil suppressiveness was associated with a transformation of the fluorescent pseudomonad community to one that more closely resembled that initially recovered from the field suppressive soil.

Although extended cultivation of apple selected for a microbial community lacking apparent inhibitory activity towards soil-borne fungal pathogens (Mazzola, 1999), this does not appear to be a universal response in perennial plant production systems. Long-term grapevine monoculture enriched the soil with fluorescent pseudomonad genotypes that produce 2,4-DAPG and hydrogen cyanide (HCN) (Svercel et al., 2009), bacterial characteristics which have been repeatedly associated with disease suppressive soils (Haas and Défago, 2005). While the duration of grapevine monoculture examined in this study was excessive, with certain sites planted since the first millennium without interruption, this example does demonstrate again the capacity of crop monoculture to selectively enhance microbial communities functional in the development of disease suppressive soils.

In an evaluation of organic cropping systems, Postma et al. (2008) reported significant differences in soil suppressive-ness towards multiple pathogens, including R. solani AG 2.2IIIB, which is an important pathogen of sugarbeet. Disease suppression was elevated in systems that employed a grass-clover sequence within the rotation cycle, and suppressiveness lasted 2 years beyond this sequence but disappeared after 3 years. The development of soil suppres-siveness in this system was correlated with a significant increase in Lysobacter spp. populations. Lysobacter spp. produce a number of lytic enzymes and antibiotics that account for their capacity to provide biological control of various fungi and oomycetes (Kobayashi et al., 2005). The association of Rhizoctonia suppressiveness and Lysobacter was restricted to clay soils and was not detected in sandy soils (Postma et al., 2008).

Multiple aspects of a production system have the capacity to limit or enhance the adoption of plant-mediated induction of soil suppressiveness as a viable practice for the management of soilborne plant diseases. Foremost among these is the time frame, perceived or actual, required to bring about the disease suppressive state. Different plant species or genotypes have inherently differential abilities to select for microbial communities with the capacity to yield disease suppression (Smith et al., 1999; Mazzola and Gu, 2002; Mazzola et al., 2004; Berg et al., 2005). Thus, plant species or genotype evaluation will be instrumental to optimizing densities of the functional microbial population and reducing the time necessary to yield a disease suppressive soil. 2,4-DAPG-producing fluorescent pseudomonads have a demonstrable role in the development of soils suppressive to take-all of wheat (Weller et al., 2002) and also have been isolated from soils that naturally suppress black root rot of tobacco (Keel et al., 1996; Ramette et al., 2003) or Fusarium wilt disease (Landa et al., 2002). Development of a take-all suppres-sive soil requires a threshold population of these bacteria (Raaijmakers et al., 1997) and certain bacterial genotypes possess a superior capacity to limit disease development (Raaijmakers and Weller, 2001).

Plant genotypes were shown to differ in both the ability to enrich for populations of indigenous 2,4-DAPG-producing fluorescent pseudomonads and the dominant bacterial genotype that was supported in the rhizosphere (Mazzola et al., 2004; Picard et al., 2008). In addition, expression of 2,4-DAPG biosynthetic genes in the rhizosphere is influenced by plant genotype (Notz et al., 2001; Jamali et al., 2009). Thus, effort to select for plant genotypes that possess a greater capacity to stimulate resident populations of effective 2,4-DAPG-producing fluorescent pseudomonad genotypes, or other functional genotypes, should be of benefit in systems that seek to utilize cropping systems as a means to induce disease suppressive soils.

The importance of plant genotype in determining the development of a biologically suppressive soil has been demonstrated in multiple systems. The capacity of continuous cropping of watermelon to induce soil suppressiveness to Fusarium wilt was cultivar dependent (Larkin et al., 1993). Furthermore, plant genotype was shown to be a significant factor in the capacity of wheat cultivation to yield a soil microbial community suppressive towards Rhizoctonia root rot of wheat and apple (Mazzola and Gu, 2002). Among five genotypes evaluated, only two were shown to consistently generate a soil biologically suppressive towards Rhizoctonia root rot in response to successive wheat growth cycles

(Mazzola and Gu, 2002). The two effective wheat cultivars, 'Lewjain' and 'Penawawa', altered the genetic and species composition of the fluorescent pseudomonad community resident in the wheat-cropped orchard soils (Mazzola and Gu, 2002; Gu and Mazzola, 2003). The fluorescent Pseudomonas spp. population from the resulting suppressive soils demonstrated a significantly greater degree of antagonism towards R. solani than did the population from non-treated control soil or soils cultivated with wheat genotypes that were ineffective in the induction of soil suppressiveness.

In subsequent studies, the capacity of continuous wheat cropping as a means to effectively control Rhizoctonia root rot of apple was demonstrated in field trials (Mazzola and Mullinix, 2005). In this system, a three-cultivar seed mixture was used in the cropping of wheat on a replant apple orchard site with three successive 10-week growth cycles. At the end of each growth cycle plant biomass was removed prior to replanting the site, and at the end of the third wheat cycle the orchard was planted to Gala/M26 apple. Under this practice, Rhizoctonia root infection was significantly reduced (Fig. 11.4) and the wheat cropping

Control MeBr Fallow Wheat Cgm Cgm Cgm Cgm (3 years) (1 year) (1 year) (2 years) (3 years) (2 years)

Soil treatment

Fig. 11.4. Effect of soil treatments on incidence of Rhizoctonia solani infection of Gala/M26 apple roots at CV orchard, Orondo, Washington state (Mazzola and Mullinix, 2005). Bars designated with the same letter do not differ significantly (P > 0.05). MeBr, pre-plant methyl bromide soil fumigation; Wheat (1 year), mixed cultivar cover crop grown for three successive 10-week plantings followed by removal of plant biomass; Cgm, canola green manure with soil incorporation of plant biomass.

procedure was more effective than a 1- or 2-year canola green manure in suppressing this root disease. The 3-year canola green manure was as effective as the wheat-cropping scheme in limiting apple root infection by Rhizoctonia spp.

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