The rhizosphere: a playground

and battlefield for soilborne

pathogens and beneficial
microorganisms

Jos M. Raaijm akers & Timothy C. Paulit z &

Christi an Steinberg & Cla ude Alabou vette &
Yvan M oënne-Loccoz
• The rhizosphere is a hot spot of microbial interactions as exudates
released by plant roots are a main food source for microorganisms
and a driving force of their population density and activities.
• The rhizosphere harbors many organisms that have a neutral effect on
the plant , but also attracts organisms that exert deleterious or
beneficial effects on the plant.
• Microorganisms that adversely affect plant growth and health are the
pathogenic, oomycetes, bacteria and nematodes.
• Most of the soilborne pathogens are adapted to grow and survive in
the bulk soil, but the rhizosphere is the playground and infection
court where the pathogen establishes a parasitic relationship with the
plant.
• The rhizosphere is also a battlefield where the complex rhizosphere
community, both microflora and microfauna, interact with pathogens
and influence the outcome of pathogen infection. A wide range of
microorganisms are beneficial to the plant and include nitrogen-fixing
bacteria, endo-and ectomycorrhizal fungi, and plant growth-
promoting bacteria and fungi.
• The rhizosphere is an environment that the plant itself helps to create
and where pathogenic and beneficial microorganisms constitute a
major influential force on plant growth and health (Lynch 1990 ).
• Microbial groups and other agents found in the rhizosphere include
bacteria, fungi, nematodes, protozoa, algae and microarthropods
(Lynch 1990 ; Raaijmakers 2001 ).
• Many members of this community have a neutral effect on the plant,
but are part of the complex food web that utilizes the large a mount
of carbon that is fixed by the plant and released into the rhizosphere
(i.e. rhizodeposits).
• The microbial community in the rhizosphere also harbors members that
exert deleterious or beneficial effects on the plant.
• Microorganisms that adversely affect plant growth and health are the
pathogenic fungi, oomycetes, bacteria and nematodes, whereas
microorganisms that are beneficial include nitrogen fixing bacteria,
endo and ectomycorrhizal fungi, and plant growth-promoting
rhizobacteria (PGPR) and fungi.
• The number and diversity of deleterious and beneficial microorganisms
are related to the quantity and quality of the rhizodeposits and to the
outcome of the microbial interactions that occur in the rhizosphere
• There are four main groups of plant pathogens (Agrios 2005 ), but
only two of them are major players in the soil : fungi (true fungi and
oomycetes) and nematodes.
• Only a few groups of bacteria are considered to be soilborne,
probably because non-spore forming bacteria cannot survive well in
soil for long periods.
• Bacteria also require a wound or natural opening to penetrate into
the plant and cause infection.
• Examples are Ralstonia solanacearum, cause of bacterial wilt of
tomato, and Agrobacterium tumefaciens, the well-studied causal
agent of crown gall.
• Some filamentous bacteria (Streptomyces) can also infect plants and
are better adapted to survive in the soil.
• Only a few viruses can infect roots. Like bacteria, they require a
wound to infect the plant and are mostly transmitted by vectors.
• In soil, they can be transmitted by nematodes (Nepoviruses or by
zoosporic fungi such as Olpidium and Polymyxa)
• Nematodes are complex, worm-like eukaryotic invertebrate animals
and probably among the most numerous animals on the planet.
• Most nematodes in soil are free-living, consuming bacteria, fungi, and
other nematodes, but some can parasitize plants.
• Some feed on the outside of the root (migratory ectoparasitic), some
penetrate and move in the interior of the root (migratory
endoparasitic), and some set up a feeding site in the interior of the
root and remain there for reproduction (sedentary endoparasites).
• Fungi and oomycetes are the most important soilborne pathogens.
• Fungi are eukaryotic, filamentous, multicellular, heterotrophic
organisms that produce a network of hyphae called the mycelium and
absorb nutrients from the surrounding substrate.
• Oomycetes have a morphology similar to fungi , but are
phylogenetically more closely related to brown algae. They produce
swimming spores (zoospores) and contain cellulose in their cell walls
as opposed to chitin in true fungi .
• Almost all soilborne fungi are necrotrophic, meaning they kill host
tissue with enzymes and toxins in advance of the hyphae and do not
require a living cell to obtain nutrients .
• Most of the biotrophic pathogens, such as rusts and powdery
mildews, occur on the above-ground portions of the plants and
require a living cell to obtain nutrients.
• A few root pathogens such as Phytophthora sojae are semibiotrophic.
• Surprisingly few root pathogens are biotrophic. Some examples are
lower zoosporic fungi and Oomycetes, such as Plasmodiophora
brassicae and Plasmopara halstedii.
• Most necrotrophic pathogens are generalists with a wide host range,
as opposed to biotrophic pathogens with narrow host ranges that
have co-evolved with the plant.
• Environmental conditions in the soil are generally not favorable for
fungal growth, due to high or low temperatures (frozen ground) or
extremely dry conditions.
• Pathogens survive in the soil as resistant propagules, such as
chlamydospores, sclerotia, thick-walled conidia or hyphae, or survive
in plant roots and crop residues.
• When conditions are favorable and when a seed or root approaches
the dormant propagule, the fungus is stimulated to germinate by root
or seed exudates and chemotactically grows toward the plant .
• The germ tube or zoospore can attach to the surface of the root,
penetrate and infect the epidermal cells of the root tips, secondary
roots , and root hairs, or attack the emerging shoots and radicles of
seedlings.
• Some fast-growing pathogens, such as Pythium species, can attack
seeds and embryos before they emerge.
• Fungi penetrate through intact cell walls via cell wall-degrading
enzymes and mechanical turgor pressure, and colonize the root
cortex.
• Most soil borne fungi attack young, juvenile roots as opposed to
secondary woody roots . After the roots have been killed and the
fungus ramifies through the cortex, it reproduces and forms spores
within the root tissue.
• Mycelium can continue to spread up the root, internally or externally,
or can spread to other roots in close proximity.
• A specialized group of pathogens that cause wilt diseases (e.g.
Fusarium oxysporum , Verticillium dahliae ) can penetrate through the
endodermis into the vascular tissue and move up the xylem to above-
ground parts of the plant , impeding the flow of water.
• A number of diseases and symptoms can be manifested by plants
infected with fungal soilborne pathogens.
• However, these diseases can be difficult to diagnose, because most of
the symptoms occur below ground, and the above-ground symptoms
may be non-distinct or similar to those caused by abiotic factors such
as drought, stress, and lack of nutrients.
• Soilborne pathogens can cause seed decay, damping-off (both pre- and
post- emergence), and can also move into the base of the stem, causing
crown rot and wilt.
• In perennial trees, fungi can move into the collar of the tree, girdling
the tree, or inoculum can splash onto the fruit, causing decay and rot.
• However, the primary disease is root rot.
• By killing root tips, root growth on that axis is eliminated.
• By destroying fine feeder roots and root hairs, the ability of the plant to
absorb water and nutrients is diminished. This leads to reduced plant
size, stunting, drought stress and nutrient deficiencies.