Review Article

Symbiotic Root-Endophytic Soil Microbes Improve Crop Productivity and Provide Environmental Benefits

Table 1

Examples of the abilities of endophytic symbiotic microorganisms and their SAMPs to increase plants’ productivity and yield.

Symbiotic microbesCropEffects

RhizobiaceaeSoybeanMeta-analysis showed −6 to 176% increase in soybean yields across 28 studies [43].

Commercial Rhizobium inoculantsSoybeanOn farmer fields in Michigan, yields were increased by 23–45% where inoculants had not been used previously. Average yield increased 2-3% where inoculants had previously been used [44]. In Indiana, yield increases were ∼1.5–2% [45].

RhizobiumCommon beanIncreases of 2–3.5 t/ha under dry conditions [16].
R. leguminosarum bv. trifoliiRice, wheat, and corn [17, 19, 46]Increases in yield were seen under field conditions. With corn, not all plant genotype-microbial combinations increased yield.

AMFNumerous cropsAcross numerous studies in the literature, AMF inoculation has resulted in increases in yield but not statistically different from zero. In grasses, the combination of aerially applied endophytic fungi and AMF gave greater than expected results than from either alone [47, 48].

AMF (Glomus versiforme)WatermelonIncreased shoot and root growth seen compared to untreated controls in drought but not well-watered conditions. Inactivation of reactive oxygen species (ROS) by gene expression changes was required [49, 50].

Piriformaspora indicaOver 150 plant speciesVarious studies have identified plant growth-promoting activities of plants whose roots were colonized by P. indica, as reviewed [8]. Improvements in plant performance include better seed germination under temperature [8], improved resistance of plantlets during micropropagation [31], and stress resistance.

P. indicaBarleyP. indica reduced effects of stresses and pathogens, inducing reprogramming of plant gene expression, which resulted in increased plant biomass and resistance to abiotic stresses [51]. These include upregulation of enzymes that inactivate toxic levels of reactive oxygen species (ROS) that are formed in plants under stress [50, 5254].

Trichoderma afroharzianum, T. virens, T. viride, and other speciesNumerous plant speciesInoculation with the organism induced increased growth responses in numerous vegetable species [55], greenhouse ornamental plants [6, 7], and cereal crops [6, 7, 56, 57].

T. afroharzianumTomato, cornSeed treatments applied to corn or tomato resulted in endophytic colonization of plant roots. This colonization is associated with increased resistance to stresses and is causally associated with higher levels of expression of enzymes that inactivate ROS [5860].

T. afroharzianumGrapesApplication, even to the soil, increased fruit yield and increased total amount of polyphenols [61].

SAMPSDerived from:

Chitooligosaccharides (COs) and lipochitooligosaccharides (LCOs)Rhizobiaceae and AMF [62, 63]Increased seedling growth of roots; increased yields of corn and other crops including leaf area, shoot mass, and root mass; root branching; increased photosynthesis; changes in plant gene expression; induced resistance to plant diseases. LCOs are produced by the bacteria, but COs may elicit similar plant responses. These compounds added to plants of many kinds result in season-long disease resistance and plant yield increases [34, 36].

6-Pentyl-α-pyrone (6PP)T. afroharzianumApplication of this volatile unsaturated lactone molecule, even to the soil, increased fruit yield and increased the total amount of polyphenols as effectively as did treatments with the organism [61].

1-Octen-3-ol (1o3)Various Trichoderma spp.Seed treatments with picoliter quantities of this volatile metabolite resulted in season-long improvements to shoot and root growth in corn as effectively as did treatments with the fungus itself [56].

Harzianic acid (HzA)Various Trichoderma spp.This has both antifungal and growth promotive activities and acts as a siderophore to chelate iron [39].

Peptabiols (Pb)Various Trichoderma spp.These induced plant defense responses and are inhibitory to soil microflora. These are peptides, and hundreds of separate compounds have been identified [40].

Hydrophobins and other hydrophobin-like proteins (Hp)Various Trichoderma spp.These hydrophobic proteins induce plant resistance and increase plant growth [41, 64]. There is great variability between these proteins, and only a few have beneficial activity.

Plant response-like proteinT. formosaInduces immunity to a virus, a fungus, a bacterium, and an oomycete plant pathogen [65].