J Chem Ecol (2013) 39:232–242

DOI 10.1007/s10886-013-0244-9

REVIEW ARTICLE

Plant-Soil Feedbacks and Soil Sickness: From Mechanisms

to Application in Agriculture
Li-Feng Huang & Liu-Xia Song & Xiao-Jian Xia &
Wei-Hua Mao & Kai Shi & Yan-Hong Zhou &
Jing-Quan Yu

Received: 18 November 2012 / Revised: 9 January 2013 / Accepted: 15 January 2013 / Published online: 6 February 2013
# Springer Science+Business Media New York 2013

Abstract Negative plant-soil feedbacks play an important Keywords Autotoxicity . Beneficial microbes . Detrimental
role in soil sickness, which is one of the factors limiting the microbes . Microbial community . Reactive oxygen species .
sustainable development of intensive agriculture. Various Rhizosphere . Root exudates . Soil health . Soil-borne
factors, such as the buildup of pests in the soil, disorder in pathogens . Suppressive soil . Soil-legacy effects
physico-chemical soil properties, autotoxicity, and other
unknown factors may contribute to soil sickness. A range
of autotoxins have been identified, and these exhibit their Introduction
allelopathic potential by influencing cell division, water and
ion uptake, dark respiration, ATP synthesis, redox homeo- Plant-soil legacy-effects or feedbacks, the net effects of all
stasis, gene expression, and defense responses. Meanwhile, positive and negative interactions between plant and soil
there are great interspecific and intraspecific differences in the organisms, have received increasing attention as a mecha-
uptake and accumulation of autotoxins, which contribute to the nism involved in many ecological phenomena such as plant
specific differences in growth in response to different autotox- invasion, species dominance, old-field succession, and soil
ins. Importantly, the autotoxins also influence soil microbes sickness (Kardol et al., 2006; Bever et al., 2010; van de
and vice versa, leading to an increased or decreased degree of Voorde et al., 2012). Plants can influence soil organisms via
soil sickness. In many cases, autotoxins may enhance soilborne the supply of organic matter, or rhizodeposition and soil
diseases by predisposing the roots to infection by soilborne organisms, in turn, can alter plant performance through
pathogens through a direct biochemical and physiological mutualistic interactions, nutrition availability, or pathogenic
effect. Some approaches, such as screening for low autotoxic activity, etc. In ecosystems, plants can modify the soil by
potential and disease-resistant genotypes, proper rotation and root exudation, root deposition, and susceptibility to ene-
intercropping, proper soil and plant residue management, mies and symbionts. These changes can increase or decrease
adoption of resistant plant species as rootstocks, introduction subsequent plant growth, which is usually called positive
of beneficial microbes, physical removal of phytotoxins, and and negative plant-soil feedback, respectively (Kulmatiski
soil sterilization, are proposed. We discuss the challenges that et al., 2008). Meanwhile, aboveground and belowground
we are facing and possible approaches to these. herbivores of preceding plants can induce changes in the
soil biota, which greatly influence secondary metabolite
L.-F. Huang : L.-X. Song : X.-J. Xia : W.-H. Mao : K. Shi : accumulation, biomass, and aboveground multitrophic inter-
Y.-H. Zhou : J.-Q. Yu (*) actions of succeeding plants (Kostenko et al., 2012).
Department of Horticulture, Zijingang Campus, Zhejiang
Soil sickness is a typical negative plant-soil feedback
University, Yuhangtang Road 866,
Hangzhou, Peoples Republic of China 310058 with a reduction in crop yield and a prevalence of soil borne
e-mail: jqyu@zju.edu.cn diseases when the same crop or its related species are
cultivated on the same soil successively. The problem of
L.-F. Huang
soil sickness dates to the beginning of agriculture, and in an
Center for Biomedicine and Health, Hangzhou Normal University,
Wenyi Road 222, ecological sense, to much earlier times. Theophrastus (ca.
Hangzhou 310016 Zhejiang, Peoples Republic of China 300 BC), the father of Botany, wrote of how chickpea
J Chem Ecol (2013) 39:232–242 233

“exhausts” the soil and destroys weeds in his botanical Autotoxicity and the Action Mechanism in Soil Sickness
works. In an ancient Chinese book, Jiminyaoshu (ca. 540)
gave a detailed description of the importance of a cropping Allelopathy is a biological phenomenon by which an organ-
sequencing for high crop productivity. Later, many agricul- ism releases one or more biochemicals to the environment
turists and biologists investigated the involvement of auto- that are directly or indirectly harmful or beneficial to other
toxic substances in cropping systems (See Grodzinsky, plants or microorganisms (Rice, 1984). The biochemicals
2006). However, scientific work was not initiated until the involved with beneficial or detrimental effects on the target
beginning of 20th century. Pioneering work by Schreiner organisms are known as allelochemicals. Autotoxicity is a
and Reed (1907; Schreiner and Shorey, 1909; Schreiner and type of intraspecific allelopathy where a plant species inhib-
Sullivan 1909; Russell and Petherbridge, 1912) revealed the its the growth of its own or relatives through the release of
involvement of phytotoxins and detrimental microbes in soil toxic chemicals into the environment (Singh et al., 1999; Yu
sickness (Börner, 1960). Later, many biologists and agrono- et al., 2000). Similar to other allelochemicals, autotoxins are
mists attempted to isolate phytotoxic substances from plant released into the environment through leaf volatilization,
tissues, root exudates, and soils, and this trend was especially leachation and root exudation of living plants, as well as
significant in the 1950s–60s and 1980s–2010s. Many phyto- decomposition of dead plant tissue (Singh et al., 1999).
toxic substances have now been isolated from plants, soils and Autotoxicity has been observed in both natural and ma-
rhizosphere (Table 1). nipulated ecosystems. In agroecosystems in particular, auto-
Since the 1960s, great progress has been made in agri- toxicity causes losses in crop yields, regeneration failure of
cultural science and technology. In many areas, traditional forests, and replant problem in orchards (Singh et al., 1999).
cropping systems with multi-crops have been replaced by Monocropping of annual crops, such as rice, alfalfa, cucum-
monocropping with specific crops in many intensive agro- ber, tomato, corn, wheat, sugarcane, and beans like soybean
ecosystems. The shift of cropping systems changes the and pea, is known to reduce performance and decrease
relationship of plant-soil feedbacks and ultimately influen- yields over a period of time (Chou, 1999). Autotoxicity
ces plant growth and sensitivity to soilborne pathogens. At also is prevalent in perennial plants, such as strawberry,
present, soil sickness becomes prevalent in the production of apple, peach, citrus, grapes, cherries, ginseng, and roses
many annual crops with intensive monocropping, and it also (Singh et al., 1999). Plant extracts, root exudates, and
affects trees and shrubs in orchards (apple, pear, grapes, etc.), sometimes the water or organic solvent extracts of soils
coffee and tea plantations, where it causes replant problems for after planting with these crops are usually autotoxic,
fruit trees and regeneration problems in natural forests (Rice, leading to a 20–50 % decrease in growth rate (Singh et
1984; Chou, 1999; Caboun, 2005; Canals et al., 2005). al., 1999). Interestingly, the autotoxic potential for many
Accordingly, understanding the mechanisms of plant-soil feed- plants is species-dependent. Takijima and Hayashi (1959)
backs in agroecosystems is an important step before we gain revealed that the nutrient solution after tomato culture
insight into the mechanism of soil sickness and solve the was toxic to the tomato plants but not to rice plants and
problem for the establishment of sustainable agroecosystems. vice versa. Similarly, we observed that root exudates of
The occurrence of soil sickness varies with plant species cucumber plants were toxic to the cucumber plants but
and is easily influenced by the soil type and environmental not to figleaf gourd plants (Yu et al., 2000; Ding et al.,
factors. The reasons are complicated and have not been 2007). Moreover, the release of autotoxic substances is
clearly defined. Early works were mainly focused on phy- stage-dependent. For example, cucumber and tomato
totoxins in the root exudates and litter and on an ion imbal- plants exude autotoxic substances at the reproductive
ance in the soil (Schreiner and Reed, 1907). Since the stage, while pea plants exude autotoxic substances main-
1960s, many soil-borne pathogens have been characterized ly at the vegetative stage (Yu and Matsui, 1994; Yu and
from the soils or roots, and they contribute greatly to soil Matsui, 1999). In addition, autotoxic potential also is
sickness. A survey in Japan and China revealed that soil influenced by genotypes, light, and nutrition levels in
sickness in vegetable crops is attributable to (i) soil-borne many crops (Pramanik et al., 2000).
pests followed by (ii) deterioration of soil physicochemical Many compunds have been identified as autotoxins from
properties and (iii) allelopathy/autotoxicity (Komada, 1988; plants, root exudates, and soils. These chemicals include
Ogweno and Yu, 2006). In agreement with these studies, simple water-soluble organic acids, aliphatic aldehydes, lac-
domestic rare plants experience strong negative feedback tones, long-chain fatty acids, naphthoquinones, anthraqui-
when grown in monoculture as compared to invasive plants nones, phenols, benzoic and cinnamic acids, coumarins,
(Klironomos, 2002). Klironomos (2002) concluded that the tannins, terpenoids, steroids, alkaloids, cyanohydrins, sul-
negative feedback responses are pathogen-density depen- fides, oil glycosides, purines and others (Table 1). In fact, it
dent. Others have shown the feedback is associated with is often quite difficult to isolate these substances from soils.
allelopathy (van de Voorde et al., 2012). Until now, several autotoxins have been isolated from
234 J Chem Ecol (2013) 39:232–242

Table 1 List of known autotoxins

Plants Autotoxic agents Autotoxins References

Alfalfa (Medicago sativa) roots medicarpin, 4-methoxy medicarpin, sativan, 5-methoxy Miller et al., 1988; Dornbos
sativan, coumarin, trans-cinnamic, salicylic, o-coumaric, et al., 1990; Chung et al.,
chlorogenic and hydro-cinnamic acids 2000; Chon et al., 2002
American ginseng roots phenolic acids He et al., 2009
(Panax quinquefolium)
Apple (Pyrus malus) bark phlorizin, phloretin, p-hydroxy hydrocinnamic, Börner, 1959
p-hydroxy benzoic acids, phloroglucinol
Asparagus roots ferulic, iso-ferulic, malic, citric, fumaric and caffeic acids
Hartung et al., 1990;
(Asparagus officinalis) Miller et al., 1991
Broad bean (Vicia faba) root exudates lactic, adipic, succinic, malic, benzoic, vanillic, Asaduzzaman et al., 2012;
p-hydroxybenzoic, glycolic and Asaduzzaman and Asao,
p-hydroxyphenylacetic acids 2012
Chininese fir (Cunninghamia soil coumarin, vanillin, isovanillin, p-hydroxybenzoic, vanillic, Kong et al., 2008
lanceolata) benzoic, cinnamic and ferulic acids, friedelin
Citrus (Citrus sp.) bark homovanillic acid, seselin, xanthyletin, oil Burger and Small, 1983
Coffee (Coffea arabica) plant tissue caffeine, theophylline, theobromine, paraxanthine, Chou and Waller, 1980
scopoletin, caffeic, coumaric, ferulic,
p-hydroxybenzoic, vanillic, chlorogenic acids
Cucumber (Cucumis sativus) root exudates benzoic,myristic, cinnamic, p-hydroxybenzoic, Yu and Matsui, 1994
2,5-dihydroxybenzoic, 3-phenylpropionic,
p-hydroxycinnamic, palmitic and stearic acids,
p-thiocyanatophenol, 2-hydroxybenzothiazole
Eggplant (Solanum melongena) root exudates cinnamic acid and vanillin Chen et al., 2011b
Huangqin (Scutellaria roots baicalin Zhang et al., 2010a; b; c
baicalensis)
Lettuce (Lactuca sativa) root exudates vanillic acid Asao et al., 2004a; b
Parsley (Pastinaca sativa) volatiles essential oils Gog et al., 2005
Pea (Pisum sativum) root exudates benzoic, cinnamic, vanillic, p-hydroxybenzoic, 3, Yu and Matsui, 1999
4-dihydroxybenzoic, p-coumaric and sinapic acids
Peach (Prunus persica) bark amygdalin Patrick, 1955; Patrick
and Koch, 1958
Rehmannia soils phenyl aromatic acids Li et al., 2012
(Rehmannia glutinosa)
Rice (Oryza sativa) plant decomposition p-coumaric, p-hydroxy benzoic, syringic, vanillic, Chou and Lin, 1976
ferulic and o-hydroxy phenyl acetic acids
Schrenk’s Spruce needles 3,4-dihydroxyacetophenone Ruan et al., 2011
(Picea schrenkiana)
Strawberry root exudates lactic, benzoic, succinic, adipic and Kitazawa et al., 2005
(Fragaria×ananassa) p-hydroxybenzoic acids
Taro (Colocasia esculenta) root exudates lactic, benzoic, m-hydroxybenzoic, p-hydroxybenzoic, Asao et al., 2003
vanillic, succinic and adipic acids
Tea (Camellia sinensis) soil phenolic acids Cao et al., 2011
Tomato (Solanum lycopersicum) root exudates 4-hydroxybenzoic, vanillic, phenylacetic, ferulic, Yu and Matsui, 1993
2-hydroxy-3-phenylpropanoic caffeic acids
Wheat (Triticum aestivum) straw residues ferulic, p-coumaric, p-hydroxybenzoic, syringic and Guenzi and McCalla,
vanillic acids 1966; Lodhi et al., 1987

nutrient solutions after hydroponic culture with the aid of Cell Division The normal cell-cycle mode is characterized
adsorbents such as Amberlite XAD or activated charcoal. In by a round of DNA replication (S phase) followed by
cucumber and tomato, plant growth has been improved when mitosis and cytokinesis (M phase) and separated by two
the nutrient solution was supplied with adsorbents (Yu et al., gap phases (G1 and G2). Cyclin-dependent kinases (CDKs)
1993; Yu and Matsui, 1994). From the adsorbents, several and their cyclin partners regulate the G1/S- and G2/M-phase
benzoic and cinnamic acids with growth-inhibiting activity transitions and the progression through and exit from the
have been identified (Yu and Matsui, 1993, 1994). Autotoxins cell cycle. Work in our laboratory and others has established
can impact many physiological and biochemical reactions that root exudates, water extracts of roots and the identified
(Fig. 1), a subset of which are discussed in detail below. autotoxins, such as cinnamic acids of cucumber plants,
J Chem Ecol (2013) 39:232–242 235

Fig. 1 Autotoxicity, autotoxin-

microbe interactions and the
soil sickness process.
Chemicals: inorganic fertilizers CO2
and pesticides; DRB: assimilation
deleterious rhizobacteria;
PGPR, plant growth-promoting
rhizobacteria
Stomata

Leachates

Tissue Water uptake

degradate Pathogen
PGPR
Ion uptake

Root Phytotoxins
exudates Redox
homeostasis

DRB Microbes
Cell division

Chemicals Diseases

Autotoxic Chemical-Microbe Soil sickness

agents interaction

inhibit both cell proliferation and DNA synthesis in the root assimilation (Yu et al., 2003; Ye et al., 2006). Accordingly, it
apical meristem, and this is accompanied by decreased tran- is possible that decreased PS II efficiency stems from a
scripts of cell cycle-related genes and end reduplication water-stress-induced decrease in CO2 assimilation, which
(Zhang et al., 2009, 2010a). is a down-stream regulation mechanism in photosynthesis.

Disturbed Water Relations and Ion Uptake Roots play a Interruption of Dark Respiration and ATP Synthesis In
major role in plant growth and development. Root exudates many cases, autotoxins have a more significant effect on
and the constituting autotoxins can disturb cell membrane germinating seeds than on older plants. As a metabolic
function in roots. The lipophilicity of benzoic and cinnamic process associated with the generation of ATP, respiration
acids is well correlated with the inhibition of ion uptake and is one of the prominent processes in seed germination and
subsequently root elongation in cucumber (Yu and Matsui, also is sensitive to many autotoxins and allelochemicals.
1994). Additionally, many autotoxins and allelochemicals Recently, we reported that autotoxins such as cinnamic acid,
can inhibit the membrane H+-ATPase activity that drives the which is found in the root exudates of cucumber, decreased
uptake of essential ions, other solutes and water (Ye et al., the total respiration rate but increased the KCN-resistant
2004, 2006). Accordingly, decreased transpiration rate and respiration rate, thus suggesting an adaptation mechanism
ion uptake frequently are observed in plants after exposure to avoid over-generation of reactive oxygen species (ROS)
to autotoxic agents. (Zhang et al., 2010b).

Inhibition of Photosynthesis Decreased CO2 assimilation Redox Homeostasis and Defense Response There are in-
and PSII electron transport efficiency have been observed creasing reports of ROS metabolism in plants after exposure
in plants exposed to autotoxic agents. Some allelochemicals to autotoxins and allelochemicals. In many cases, an over-
or autotoxins are inhibitors of electron transport at PS II; generation or accumulation of ROS may induce damage to
however, the effect is likely limited to the germinating seed- enzymes, lipids, DNA, proteins, and lipid peroxidation.
lings, as the autotoxins are barely transported to the shoots However, it also is possible that ROS in cells after exposure
of adult plants (Dayan, 2006). Significantly, exposure to to autotoxins functions as s signaling component in the
autotoxins usually induces stomata closure, which may de- allelopathic response. Like other stimuli, autotoxins may
crease the CO2 availability and subsequently decrease CO2 be perceived first by receptors on the cell membrane and
236 J Chem Ecol (2013) 39:232–242

then transduced downstream, resulting in a generation of Plant community may change the soil microbial commu-
secondary messages that include calcium ions (Ca2+), ROS, nity by root exudation and root deposition, etc., Microbes
and inositol phosphate (Yu et al., 2009). Accordingly, ROS may have beneficial, harmful, or neutral effects on plants
and associated changes in [Ca2+]cyt may be one part of the (Sturz and Christie, 2003). The beneficial microbes include
defense cascade in an autotoxic response. In cucumber, those that have direct or indirect positive effects on plant
cinnamic acid induces NADPH oxidase-dependent H2O2 growth, mineral availability, and the stress response. For
generation at the apoplast (Yu et al., 2009), which works example, arbuscular mycorrhizal fungi (AMF) can improve
as a secondary signal in response to many stimuli and plant resistance by improving phosphate acquisition and
induces an increase in the activity of many antioxidants, heavy metal resistance, while some microbial species can
such as Cu/Zn-superoxide dismutase (Cu/Zn-SOD), ascor- produce growth-promoting substances, such as indole-3-
bate peroxidase (APX), monodehydroascorbate reductase acetic acid and cytokinins (Khare and Arora, 2010). These
(MDAR), dehydroascorbate reductase (DHAR) and gluta- microorganisms also function to inhibit or reduce the effect
thione reductase (GR), and non-enzymatic antioxidants, of soilborne phytopathogens, which is termed disease sup-
such as ascorbate and glutathione. However, the signaling pression (Garbeva et al., 2004). These microorganisms can
role of ROS in the autotoxic response has not been well suppress soilborne phytopathogens by niche competition,
established until recently. antibiosis, induced systemic resistance (ISR), and root cam-
ouflage (Sturz and Christie, 2003). The harmful or deleteri-
ous microbes include those that are phytopathogenic and
those that produce phytotoxins. Several Pseudomonas spp.
The Role of the Soil Microbial Community in Soil in monocropped soil are known for their ability to produce
Sickness hydrogen cyanide (HCN) (Khare and Arora, 2010).
Root exudates vary with plant species, leading to changes
Soil contains a vast diversity of microorganisms, and these in the soil microbial community. Roots of sorghum and
microorganisms are critical to many of the biological, chem- maize exude strigolactones and benzoxazinoids that can
ical, and physical processes that drive terrestrial ecosystems. stimulate AM fungi and attract Pseudomonas putida, a
Microbial diversity is important for soil quality and may be competitive colonizer of the maize rhizosphere with plant-
influenced by soil type, plant history, and agricultural prac- beneficial traits, to the rhizosphere, respectively (Besserer et
tices, such as fertilization and pesticide application. Bacteria al., 2006; Neal et al., 2012). On the other hand, monocrop-
are the most abundant and diverse group of organisms in ping together with heavy applications of chemicals has been
soil (Kennedy, 1999). For many decades, microbial commu- found to be accompanied by losses of soil biota and in-
nities have been monitored through traditional culture- creased crop disease, e.g. potatoes (Carter and Sanderson,
dependent methods. Recently, culture-independent methods, 2001). Studies have shown that soil microbial communities
such as fatty acid analysis (FAME and PLFA) and nucleic are changed after monoculture with a single plant species,
acid analysis (PCR-DGGE), have been widely used to esti- e.g., peas, (Nayyar et al., 2009) and e.g., soybeans, (Li et al.,
mate bacterial diversity (Theron and Cloete, 2000; Larkin, 2010). Changes in soil biota will influence plant growth
2003; Wu et al., 2009). Some studies have shown that soil because soil biotas are involved in many processes impor-
populations of culturable bacteria and overall microbial tant for plant growth and nutrition availability. In many
activity tends to be highest following barley, canola, and cases, continuous monoculture reduces microbial competi-
sweet corn rotations, and lowest with continuous potato, tion in the root zone by lowering biodiversity among root-
which is characterized by the greatest proportion of straight associated fungi and bacteria, thus enabling pathogenic
chain saturated fatty acids in soils under continuous potato populations to develop, thus increasing disease incidence
growth (Larkin, 2003), while others have shown that soil and subsequent yield losses (Knops et al., 1999).
microbial community functional diversity and genetic diver- Monocropping also results in the simplification of microbial
sity (as indicated by RAPD markers) is decreased signifi- structure, leading to decreases in the population of fluores-
cantly by autotoxins such as cinnamic acid (Wu et al., cent Pseudomonas fluorescence, which is capable of pro-
2009). Most recently, pyrosequencing of the bacterial 16S ducing the antifungal metabolite 2,4-diacetylphloroglucinol
ribosomal RNA gene also has been used to characterize the (Mazzola et al., 2002; Weller et al., 2002; Validov et al.,
bacterial community in the soil, rhizosphere and roots 2005). For example, more than 60 % of the strains isolated
(Bulgarelli et al., 2012; Lundberg et al., 2012). Studies in from healthy soils corresponded to Pseudomonas sp., and
Arabidopsis have revealed that soil type defines the compo- 58 % of the isolates from sick soils were Bacillus sp., which
sition of root-inhabiting bacterial communities, and that host is able to produce HCN in vitro (Benizri et al., 2005).
genotype determines their ribotype profiles to a limited Accordingly, yield reductions following the monoculture
extent (Bulgarelli et al., 2012). of a single crop species also is related to the accumulation
J Chem Ecol (2013) 39:232–242 237

of nonpathogenic, deleterious rhizobacteria (Schippers et that autotoxins or allelochemicals can modify the prevalence
al., 1987). of many soilborne diseases. Like root exudates, autotoxins
However, there also are quite different responses to or allelochemicals can change soil microbial genetic diver-
monocropping. In contrast to sick soil or conducive soil, sity, biological activity, and microbial metabolic activity,
suppressive soil has a low level of disease development which alter soil microbial ecology and accordingly affect
even though a virulent pathogen and susceptible host are the growth of plants, with an accumulation of allelochem-
present (Mazzola, 2002). In tomatoes, the suppressive char- icals in the soil (Szabo and Wittenmayer, 2000; Wu et al.,
acteristics are related to the microbial community (Shiomi et 2009). Research in our laboratory and in others has shown
al., 1999). Interestingly, suppressiveness may be induced by that root exudates of cultivars susceptible to Fusarium wilt
continuous monocropping, intercropping, or short-term ro- stimulates spore germination and fungal growth, while re-
tation with some genotypes, and this characteristic is attrib- sistant genotypes inhibited spore germination (Wu et al.,
uted to the induction of specific fluorescent Pseudomonas 2006, 2010; Yu et al., unpublished). Declines in productivity
genotypes with antagonistic activities toward this pathogen in continuous monocultures of crops also are attributed to
(Mazzola and Gu, 2000; Mazzola et al., 2001; 2002; 2004; the synergistic interference of autotoxicity and soil-borne
Gu and Mazzola, 2003). However, it is unclear how the root plant pathogens (Ye et al., 2006). In asparagus, autotoxic
exudates of these plants influence the microbial community substances derived from its tissues not only depressed seed-
and how the specific Pseudomonas population is related to ling emergence and reduced seedling growth but also in-
the root exudates of these genotypes. creased Fusarium virulence (Hartung and Stephenes, 1983;
Huang et al., 2000). Ginseng saponins (ginsenosides) present
in the root exudates and the soil associated with the roots of
Interplay Between Autotoxins and Microbes in Soil American ginseng (Panax quinquefolius L.) stimulated the
Sickness growth of soilborne pathogens of American ginseng (Nicol
et al., 2003). Similarly, allelochemicals released by Scutellaria
Soil is a complicated matrix, and soil sickness may stem baicalensis negatively affected S. baicalensis directly, by
from the interaction of different factors such as autotoxins, inducing autotoxicity, and indirectly, by increasing pathogen
microbes, and others, that lead to growth inhibition and a activity in the soil (Zhang et al., 2010c). There also is evidence
prevalence of soilborne diseases. Plant-microbe interactions that exotic invasive plants accumulate native soil pathogens,
extend over time, space, and substrate. While root exudates which inhibit native plants (Mangla et al., 2008). Others,
influence the composition of microbial communities in the however, have shown that secondary metabolites, such as
root zone, rhizobacteria themselves can change the compo- flavones, phenolics, and saponins, from the invasive
sition of root exudation in plants and finally the products Solidago canadensis L. accumulate in soil and inhibit the soil
(Meharg and Killham, 1995). In addition, antagonism pathogen Pythium ultimum (Zhang et al., 2011).
also occurs between microbes. The presence of delete- Soil sickness is common in crops such as cucumber and
rious rhizobacteria (DRB) may increase plant suscepti- watermelon. Cucumber plants have autotoxic potential by
bility to other pathogens (Fredrickson and Elliott, 1985). exuding substances, such as cinnamic acid (Yu and Matsui,
In fact, both enhancement and suppressive effects of 1994). These substances significantly increase ion leakage
microbial modification of autotoxins have been observed by increasing membrane permeability (Yu and Matsui,
in many soil sickness phenomena. This interplay may 1997) and by affecting the activity of ROS scavenging
partly explain the different responses of plants to spe- enzymes, such as peroxidase and superoxide dismutase
cific autotoxins or allelochemicals in different types of (SOD) (Yu et al., 2003). Due to the sensitivity of cucumber
soils. to F. oxysporum. f. sp. cucumerinum, the pathogen of
Many plant-soil feedbacks are mediated by microbes in Fusarium wilt, and autotoxins (Yu and Matsui, 1997), it
the soils. Autotoxicity in peach plants is attributed to amyg- serves as a good experimental system to study the interac-
dalin, which is broken down in the soil by microbes into tion between a soil-borne pathogen and an autotoxin.
toxic cyanide substances, causing injury to roots of young Exposure to cinnamic acid results in enhanced membrane
peach seedlings (Patrick, 1955). A similar phenomenon also peroxidation, decreased plasma membrane ATPase activity,
has been observed in the soil sickness of walnut with and increased incidence of Fusarium wilt (Ye et al., 2004,
juglone as the autotoxin (Thevathasan et al., 1998). In 2006). Autotoxins enhance Fusarium wilt by predisposing
contrast, many allelochemicals or autotoxins are easily de- cucumber roots to infection by soilborne pathogens through
graded by microbes (Blum, 1998; Blum et al., 2000; see also an indirect biochemical and physiological effect (Ye et al.,
Weidenhamer et. al., 2013). In one study, several benzoic 2004, 2006). It is likely that soil sickness results from an
and cinnamic acids disappeared a few days after amending interaction of many factors, such as autotoxins and patho-
the soils (Blum et al., 2000). There is increasing evidence gens (Fig. 1).
238 J Chem Ecol (2013) 39:232–242

Approaches to Overcome Soil Sickness environment suitable for the survival of soilborne patho-
gens. Removal of these residues from the soils may be an
Although soil sickness is a complex phenomenon, it can at important step for overcoming soil sickness (Singh et al.,
least partially be overcome by the integrating the following 1999).
practices:
Soil Sterilization Both physical and chemical sterilization
Screening for Low Autotoxic Potential and Disease- approaches now are available. Instead of using methyl bro-
resistant Genotypes There are intraspecific variations in mide, many alternatives are being developed for soilborne
the autotoxic potential of many crops. Work on cucumber pathogen control in commercial production. Solar steriliza-
has revealed that many commercial cultivars have low auto- tion, an environmentally friendly method, is increasingly
toxic potentials, while others show strong potential (Asao T., used for the control of many soilborne diseases, although
personal communication). A series of genotypes with resis- its influence on autotoxin degradation is unknown.
tance to different soil-borne pathogens have been developed. However, soil sterilization can kill both pathogens and ben-
eficial microbes in the soils. Interestingly, the sensitivity of
Adoption of Resistant Plant Species as Rootstocks Autotoxicity soil microbes to chemicals sterilizers such as calcium cyan-
and pathogens are species–dependent in many cases. For amide varies with their species and many microbes recovery
example, root exudates of both cucumber and watermelon faster than pathogens (Shi et al., 2009).
show high autotoxicity but not toxicity to other species,
such as figleaf gourd (Yu et al., 2000). A recent study Introduction of Beneficial Microbes Biotic factors play an
revealed that there was an interspecific difference in the important role in autotoxicity and pathogenesis. Beneficial
uptake and the recognition of autotoxin(s) (Yu et al., microbes can be used to degrade phytotoxins, both autotox-
2009), which induced oxidative stress accompanied by ins and microbial toxins (Caspersen et al., 2000; Asao et al.,
root cell death in cucumber, an autotoxic plant, but not 2003, 2004b; Chen et al., 2011a). Microbes also can be
in figleaf gourd, a cucumber relative (Ding et al., 2007). developed for biological control. Many beneficial microbes
Genotypes resistant to pathogens and autotoxins can be with fungicidal capacity have been identified from sup-
developed as rootstocks for many horticultural crops pressive soil and other soil types (Berg, 2009). Similarly,
(Asao et al., 1999). many isolates from suppressive soils or others can de-
grade autotoxins in the rhizosphere of continuously
Proper Rotation and Intercropping A proper rotation can cropped plants (Asao et al., 2004b; Chen et al., 2011a).
decrease pathogen populations and also minimize the auto- We found that inoculation with Fusarium flocciferum and
toxic effects of the crops. The residues of crops like Cephalosporium acremonium alleviated the autotoxicity
Brassicaceae and marigolds also can be useful in suppress- induced by phenolic acids in cucumber (Yu,unpublished
ing soilborne pathogens and nematodes (Cohen et al., 2005). data). These beneficial microbes can be used alone or in
Furthermore, the allelopathic properties of cover, smother, combination with bioorganic fertilizers.
and green-manure crops, or crops grown in rotation can be
useful for pest management (Singh et al., 1999; Farooq et Physical Removal of Phytotoxins Activated charcoal has a
al., 2011). Many crops exude nematicides and antimicrobial strong capacity for adsorbing organic chemicals and is an
substances. For example, intercropping or rotation with ideal adsorbent for practical applications. In cucumber, to-
Chinese chive can decrease the occurrence of bacterial wilt mato, and asparagus, a 15–30 % increase in productivity has
caused by Pseudomonas solanacearum, and the root exu- been observed after using activated charcoal (Yu et al.,
dates from Chinese chive plants exhibit strong inhibitory 1993; Yu and Matsui, 1994; Asao et al., 2003). In addition,
effects on the bacterial pathogen (Yu, 1999; Zhang et. al., by applying TiO2 photocatalysis and electro-degradation in
2013). Rotation with cereal crops such as sorghum and a recycling hydroponic cultivation system, autotoxicity was
maize suppresses the incidence of nematode and other root avoided in asparagus and strawberry (Sunada et al., 2008;
diseases in tomato and cucumber (unpublished data). It Miyama et al., 2009; Asaduzzaman et al., 2012).
remains to be determined, however, that whether strigolac-
tones and benzoxazinoids in the root exudates of these crops
such as maize contribute to their beneficial effects. It is,
therefore, apparent that plant diversity is an important factor Challenges and Outlook
for successful plant growth in agroecosystems.
As discussed above, intensive agriculture is prevalent in
Proper Soil and Plant Residues Management Many crop many countries and regions due to increased food and
residues release autotoxic substances and provide an environmental concerns. This intensive approach may lead
J Chem Ecol (2013) 39:232–242 239

to soil sickness in croplands. Soil sickness is a complicated Allelochemicals or autotoxins in the rhizosphere directly
phenomenon, and the detailed mechanisms involved are not or indirectly affect soilborne pathogens or other detrimental
fully understood. In general, autotoxicity, disturbed microbial microbes. Root exudates of many plants also contain anti-
communities, and others are responsible for the observed microbial compounds; however, research in this area has
phenomenon. The interaction between allelochemicals, auto- been minimal. Biodiversity conservation with different
toxins, and microbes is important. Additionally, it seems cropping systems will be an increasingly important ap-
likely that causes may differ from plant to plant. proach for the sustainable development of agriculture pro-
There is an increasing interest in the autotoxicity of duction and pest control. It is important to reexamine the
crops, and more than 50 crops have been shown to have usefulness of traditional agricultural management methods,
autotoxic potential. GS-MS and HPLC-MS have been the and this is especially important in developing countries.
most popular instruments for the identification of autotox-
ins. However, sample preparation for the identification of Acknowledgements This work was supported by the National Basic
soil autotoxins must be conducted carefully because con- Research Program of China (2009CB119000), the National Key Tech-
tamination or artifacts from the culture or solvents, such as nology R&D Program of China (2011BAD12B04) and the National
additives. In addition, the autotoxic potential of many crops Natural Science Foundation of China (31272155).
has been established based only on the correlation of phy-
totoxicity and the dose of extracts in plant tissues, without
evidence for autotoxins in the rhizosphere. Until now, not
enough studies have followed a criterion similar to Koch’s References
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