REVIEW
\npublished: 17 November 2015
\ndoi: 10.3389\/fpls.2015.01020
\nEdited by:
\nRichard Sayre,
\nNew Mexico Consortium at Los
\nAlamos National Labs, USA
\nReviewed by:
\nShan Lu,
\nNanjing University, China
\nBala Rathinasabapathi,
\nUniversity of Florida, USA
\n*Correspondence:
\nZhihui Cheng
\nchengzh@nwsuaf.edu.cn
\nSpecialty section:
\nThis article was submitted to
\nPlant Physiology,
\na section of the journal
\nFrontiers in Plant Science
\nReceived: 14 July 2015
\nAccepted: 04 November 2015
\nPublished: 17 November 2015
\nCitation:
\nCheng F and Cheng Z (2015)
\nResearch Progress on the use
\nof Plant Allelopathy in Agriculture
\nand the Physiological and Ecological
\nMechanisms of Allelopathy.
\nFront. Plant Sci. 6:1020.
\ndoi: 10.3389\/fpls.2015.01020
\nResearch Progress on the use
\nof Plant Allelopathy in Agriculture
\nand the Physiological and Ecological
\nMechanisms of Allelopathy
\nFang Cheng and Zhihui Cheng*
\nCollege of Horticulture, Northwest A&F University, Yangling, China
\nAllelopathy is a common biological phenomenon by which one organism produces
\nbiochemicals that influence the growth, survival, development, and reproduction of
\nother organisms. These biochemicals are known as allelochemicals and have beneficial
\nor detrimental effects on target organisms. Plant allelopathy is one of the modes of
\ninteraction between receptor and donor plants and may exert either positive effects
\n(e.g., for agricultural management, such as weed control, crop protection, or crop reestablishment) or negative effects (e.g., autotoxicity, soil sickness, or biological invasion).
\nTo ensure sustainable agricultural development, it is important to exploit cultivation
\nsystems that take advantage of the stimulatory\/inhibitory influence of allelopathic
\nplants to regulate plant growth and development and to avoid allelopathic autotoxicity.
\nAllelochemicals can potentially be used as growth regulators, herbicides, insecticides,
\nand antimicrobial crop protection products. Here, we reviewed the plant allelopathy
\nmanagement practices applied in agriculture and the underlying allelopathic mechanisms
\ndescribed in the literature. The major points addressed are as follows: (1) Description
\nof management practices related to allelopathy and allelochemicals in agriculture. (2)
\nDiscussion of the progress regarding the mode of action of allelochemicals and the
\nphysiological mechanisms of allelopathy, consisting of the influence on cell microand ultra-structure, cell division and elongation, membrane permeability, oxidative and
\nantioxidant systems, growth regulation systems, respiration, enzyme synthesis and
\nmetabolism, photosynthesis, mineral ion uptake, protein and nucleic acid synthesis.
\n(3) Assessment of the effect of ecological mechanisms exerted by allelopathy on
\nmicroorganisms and the ecological environment. (4) Discussion of existing problems and
\nproposal for future research directions in this field to provide a useful reference for future
\nstudies on plant allelopathy.
\nKeywords: allelochemical, allelopathy, agriculture practice, physiological mechanism, ecological mechanism,
\nmicroorganism, agricultural sustainable development
\nINTRODUCTION
\nAllelopathy is a sub-discipline of chemical ecology that is concerned with the effects of chemicals
\nproduced by plants or microorganisms on the growth, development and distribution of other plants
\nand microorganisms in natural communities or agricultural systems (Einhellig, 1995). The study
\nof allelopathy increased in the 1970s and has undergone rapid development since the mid-1990s,
\nFrontiers in Plant Science | www.frontiersin.org 1 November 2015 | Volume 6 | Article 1020
\nCheng and Cheng Plant Allelopathy Application and Mechanisms
\nbecoming a popular topic (sample nursing essay examples by the best nursing assignment writing service) in botany, ecology, agronomy, soil
\nscience, horticulture, and other areas of inquiry in recent
\nyears. The allelopathic interaction can be one of the significant
\nfactors contributing to species distribution and abundance within
\nplant communities and can be important in the success of
\ninvasive plants (Chou, 1999; Mallik, 2003; Field et al., 2006;
\nInderjit et al., 2006; Zheng et al., 2015), such as water hyacinth
\n(Eichhornia crassipes Mart. Solms) (Jin et al., 2003; Gao and Li,
\n2004), spotted knapweed (Centaurea stoebe L. ssp. micranthos)
\n(Broeckling and Vivanco, 2008) and garlic mustard (Alliaria
\npetiolata M. Bieb) (Vaughn and Berhow, 1999). Allelopathy is
\nalso thought to be one of the indirect causes of continuous
\ncropping obstacles in agriculture. As a result of the in-depth
\nstudy of allelopathy, strategies for the management of agricultural
\nproduction and ecological restoration involving the application
\nof allelopathy and allelochemicals are improving. The main
\npurposes of this review are to present conclusions regarding
\nthe application of allelopathy in agricultural production, to
\nhighlight the physiological and ecological mechanisms underlying
\nplant allelopathy, to illustrate the effect of allelopathy on
\nsoil microorganisms and to discuss key points for further
\nresearch.
\nALLELOPATHY AND ALLELOCHEMICALS
\nThe definition of allelopathy was first used by Molish in 1937 to
\nindicate all of the effects that directly and indirectly result from
\nbiochemical substances transferred from one plant to another
\n(Molisch, 1937). Almost half a century later, the accepted targets
\nof allelochemicals in the plant kingdom include algae, fungi
\nand various microorganisms. The term was refined by Rice
\n(1984) to define \u201cany direct or indirect harmful or beneficial
\neffect by one plant (including microorganisms) on another
\nthrough production of chemical compounds that escape into the
\nenvironment\u201d (Rice, 1984). In 1996, the International Allelopathy
\nSociety broadened its definition of allelopathy to refer to any
\nprocess involving secondary metabolites produced by plants,
\nmicroorganisms, viruses and fungi that influence the growth and
\ndevelopment of agricultural and biological systems. In addition,
\nthe allelopathic donor and receiver should include animals (Kong
\nand Hu, 2001).
\nAllelochemicals, which are non-nutritive substances mainly
\nproduced as plant secondary metabolites or decomposition
\nproducts of microbes, are the active media of allelopathy.
\nAllelochemicals consist of various chemical families and are
\nclassified into the following 14 categories based on chemical
\nsimilarity (Rice, 1974): water-soluble organic acids, straightchain alcohols, aliphatic aldehydes, and ketones; simple
\nunsaturated lactones; long-chain fatty acids and polyacetylenes;
\nAbbreviations: APX, ascorbic acid peroxidase; BNI, biological nitrification inhibition; BNIS, biological nitrification inhibition substances; BOA, 2(3H)-
\nbenzoxazolinone; C4H, cinnamate-4-hydroxylase; CAT, catalase; COMT, caffeic acid O-methyltransferases; DEP, diethyl phthalate; DIBOA, 4-dihydroxy1,4(2H)-benzoxazin-3-one; DTD, [4, 7-dimethyl-1-(propan-2-ylidene)-1, 4, 4a, 8a-tetrahydronaphthalene-2, 6(1H, 7H)-dione]; F5H, ferulic acid 5-hydroxylase;
\nGR, glutathione reductase; GS, glutamine synthetase; HHO, [6-hydroxyl-5-isopropyl-3, 8-dimethyl-4a, 5, 6, 7, 8, 8a-hexahydronaphthalen-2(1H)-one]; ISR,
\ninduced systemic resistance; MDA, malondialdehyde; NiR, nitrate reductase; NIS, nitrification-inhibiting substances; PA, pyrogallic acid; PAL, phenylalanine
\nammonialyase; PDMS, polydimethylsiloxane; PGPR, plant growth-promoting rhizobacteria; POD, peroxidase; PPO, polyphenol oxidase; QTL, quantitative trait
\nlocus; RAPD, random amplification of polymorphic DNA; ROS, reactive oxygen species; SDH, succinodehydrogenase; SOD, superoxide dismutase; STEM,
\nsilicone tubing microextraction.
\nbenzoquinone, anthraquinone and complex quinones; simple
\nphenols, benzoic acid and its derivatives; cinnamic acid and
\nits derivatives; coumarin; flavonoids; tannins; terpenoids and
\nsteroids; amino acids and peptides; alkaloids and cyanohydrins;
\nsulfide and glucosinolates; and purines and nucleosides. Plant
\ngrowth regulators, including salicylic acid, gibberellic acid and
\nethylene, are also considered to be allelochemicals. The rapid
\nprogress of analysis technology in recent years has made it possible
\nto isolate and identify even minute amounts of allelochemicals and
\nto perform sophisticated structural analyses of these molecules.
\nThe structures of some allelochemicals produced by plants are
\nshown in Figure 1.
\nMANAGEMENT OF PLANT ALLELOPATHY
\nIN AGRICULTURE
\nAllelopathy is a natural ecological phenomenon. It has been
\nknown and used in agriculture since ancient times (Zeng, 2008,
\n2014). Allelochemicals can stimulate or inhibit plant germination
\nand growth, and permit the development of crops with low
\nphytotoxic residue amounts in water and soil, thus facilitating
\nwastewater treatment and recycling (Macias et al., 2003; Zeng
\net al., 2008). They are a suitable substitute for synthetic herbicides
\nbecause allelochemicals do not have residual or toxic effects,
\nalthough the efficacy and specificity of many allelochemicals
\nare limited (Bhadoria, 2011). The main purposes of research on
\nallelopathy include the application of the observed allelopathic
\neffects to agricultural production, reduction of the input of
\nchemical pesticides and consequent environmental pollution, and
\nprovision of effective methods for the sustainable development
\nof agricultural production and ecological systems (Macias et al.,
\n2003; Li et al., 2010; Han et al., 2013; Jabran et al., 2015).
\nThe use of allelopathic crops in agriculture is currently being
\nrealized, e.g., as components of crop rotations, for intercropping,
\nas cover crops or as green manure (Cheema and Khaliq, 2000;
\nSingh et al., 2003; Cheema et al., 2004; Khanh et al., 2005;
\nReeves et al., 2005; Yildirim and Guvenc, 2005; Iqbal et al.,
\n2007; Mahmood et al., 2013; Wortman et al., 2013; Farooq
\net al., 2014; Silva et al., 2014; Wezel et al., 2014; Haider
\net al., 2015). The applications of allelopathy in crop production
\nin Pakistan are successful examples in recent years (Cheema
\net al., 2013). The suitable application of allelopathy toward the
\nimprovement of crop productivity and environmental protection
\nthrough environmentally friendly control of weeds, insect pests,
\ncrop diseases, conservation of nitrogen in crop lands, and the
\nsynthesis of novel agrochemicals based on allelochemicals has
\nattracted much attention from scientists engaged in allelopathic
\nresearch.
\nFrontiers in Plant Science | www.frontiersin.org 2 November 2015 | Volume 6 | Article 1020
\nCheng and Cheng Plant Allelopathy Application and Mechanisms
\nFIGURE 1 | Structures of some of the allelochemicals produced by
\nplants.
\nARRANGEMENT OF CROPPING SYSTEMS
\nCompetition is one of the main modes of interaction between
\ncultivated crops and their neighboring plants (Inderjit and Moral,
\n1997; Xiong et al., 2005; He et al., 2012b; An et al., 2013).
\nAllelopathy is a chemical mechanism that provides plants with
\nan advantage for competing for limited resources (Singh et al.,
\n1999; He et al., 2012b; Gioria and Osborne, 2014). The ability of
\nplants to suppress weeds is thus determined by crop allelopathy
\nand competitiveness. Crop allelopathy can be effectively used to
\ncontrol weeds in the field, to alleviate allelopathic autotoxicity
\nand reduce inhibitory influence among allelopathic crops (Iqbal
\net al., 2007; John et al., 2010; Farooq et al., 2013; Andrew et al.,
\n2015), to improve the utilization rate of land and to increase the
\nannual output of the soil by establishing reasonable crop rotation
\nand intercropping systems. For example, Odeyemi et al. (2013)
\nreported relative abundance and population suppression of plant
\nparasitic nematodes under Chromolaena odorata (L.) (Asteraceae)
\nfallow in a field study conducted over 2 years, and suggested
\nthat the use of bush fallow with C. odorata might become an
\nintegrated management practice in the management of nematode
\npests in crop production in south-western Nigeria. Intercropping
\nis a common practice among farmers in developing countries
\nfor maximizing land resources and reducing the risks of single
\ncrop failure. Weed population density and biomass production
\ncan be markedly reduced using crop rotation and intercropping
\nsystems (Liebman and Dyck, 1993; Narwal, 2000; Nawaz et al.,
\n2014; Jabran et al., 2015). Intercropping of sorghum (Sorghum
\nbicolor L.), sesame (Sesamum indicum L.) and soybean (Glycine
\nmax L.) in a cotton (Gossypium hirsutum L.) field produced
\ngreater net benefits and a significant inhibition on purple nutsedge
\n(Cyperus rotundus L.) in comparison with the cotton alone in a 2-
\nyear experiment (Iqbal et al., 2007). Recently, Wang et al. (2015)
\nreported that eggplant\/garlic relay intercropping is a beneficial
\ncultivation practice to maintain stronger eggplant growth and
\nhigher yield. However, the allelopathy between different species
\nmay cause promontory or inhibitory effects. Farooq et al. (2014)
\nreported that when grown in rotation with tobacco (Nicotiana
\ntabacum L.), the stand establishment and growth of maize
\n(Zea mays L.) were improved compared to mung bean (Vigna
\nradiata L.), whereas mungbean stand establishment and growth
\nwere suppressed. Therefore, the allelopathic nature of crops
\nmust be considered in crop rotation, intercropping and stalk
\nmulching (Xuan et al., 2005; Cheng et al., 2011; Cheng and Xu,
\n2013).
\nSTRAW MULCHING
\nIn conventional agriculture, weed control using herbicides is
\nnot only an expensive practice; it is also harmful to the
\nenvironment. Allelopathic applications, such as straw mulching,
\nprovide sustainable weed management (Jabran et al., 2015),
\nfurther reducing the negative impact of agriculture on the
\nenvironment (Cheema and Khaliq, 2000; Cheema et al., 2004).
\nUsing allelopathic plants as ground cover species provides an
\nenvironmental friendly option (Dhima et al., 2006; Moraes
\net al., 2009; Wang et al., 2013a). The allelochemicals from
\ndecomposed straw can suppress weed growth in farmlands, and
\nreduce the incidence of pests and diseases. Moreover, straw
\nmulch can improve the soil organic matter content and increase
\nsoil fertility. However, it may also have negative effects by
\nincreasing the C: N ratio of the soil. Research has shown that
\ngreen wheat (Triticum aestivum L.) straw inhibits the growth
\nof Ipomoea weeds in corn (Zea mays L.) and soybean fields,
\nthereby reducing the need for herbicide application. Rye (Secale
\ncereale L.) mulch significantly reduced the germination and
\ngrowth of several problematic agronomic grass and broadleaf
\nweeds (Figure 2; Schulz et al., 2013). The transformation reactions
\nof rye allelochemicals, i.e., benzoxazinoids, in soil led primarily
\nto the production of phenoxazinones, which can be degraded by
\nseveral specialized fungi via the Fenton reaction. Because of their
\nselectivity, specific activity, and presumably limited persistence
\nin the soil, benzoxazinoids or rye residues are suitable means for
\nweed control (Schulz et al., 2013). Furthermore, Tabaglio et al.
\n(2008) found that the allelopathic inhibition effects on weeds
\ndiffer between different cultivars of rye straw used for mulching.
\nXuan et al. (2005) concluded that the application of allelopathic
\nFrontiers in Plant Science | www.frontiersin.org 3 November 2015 | Volume 6 | Article 1020
\nCheng and Cheng Plant Allelopathy Application and Mechanisms
\nFIGURE 2 | Field trial on rye mulch preceding a tomato crop in a biological farm (Schulz et al., 2013). Left, test plot with rye mulch left on the soil surface,
\nshowing the good weed suppression ability. Right, control plot without rye mulch, split into two treatments: left side, untreated sub-plot in which tomato plants are
\nalmost completely overgrown by weeds; right side, sub-plot with mechanical control by cultivation, in which tomato plants grow as well as those in the test plot.
\nplant materials at 1\u20132 tons ha\u22121
\ncould reduce weed biomass by
\napproximately 70%, and increase rice (Oryza sativa L.) yield by
\napproximately 20% in paddy fields (1998\u20132003) compared with
\nthe respective controls. In the southeastern region of Brazil, coffee
\n(Coffea arabica) fruit peels, which contain allelochemicals such
\nas phenols, flavonoids and caffeine, are often used as an organic
\namendment in agricultural practice to control weeds (Silva et al.,
\n2013). An et al. (2013) found that switchgrass (Panicum virgatum
\nL.) plants and residues reduced the biomass and density of
\nassociated weeds, and their research provided weed management
\nstrategies in agroecosystems and important information for the
\nintroduction of switchgrass into new ecosystems. Water extracts
\nof Conyza bonariensis (L.) Cronquist, Trianthema portulacastrum
\nL., and Pulicaria undulata (L.) C. A. Mey. can be applied at a
\nconcentration of 10 g L\u22121
\nto manage the weed Brassica tournefortii
\nGouan by inhibiting germination and seedling growth (Abd ElGawad, 2014). Moreover, some soybeans induce the germination
\nof sunflower broomrape (Orobanche spp.), a noxious parasitic
\nweed, which suggests that soybean has the potential to be used as a
\ntrap crop to reduce the seed bank of sunflower broomrape (Zhang
\net al., 2013b).
\nDEVELOPING ENVIRONMENTALLY
\nFRIENDLY AGROCHEMICAL AND
\nMICROBIAL PESTICIDES
\nAllelochemicals with negative allelopathic effects are important
\ncomponents of plant defense mechanisms against weeds and
\nherbivory. The technology that modifies allelochemicals for the
\nproduction of environmentally friendly pesticides and plant
\ngrowth regulators allows the effective management of agricultural
\nproduction and confers few environmental problems in the soil
\ndue to the fairly high degradability of allelochemicals (Bhadoria,
\n2011; Ihsan et al., 2015). Uddin et al. (2014) revealed that
\nsorgoleone, a hydrophobic compound found in Sorghum bicolor
\n(L.) root exudates, was more effective in inhibiting weed growth
\nafter formulation as a wettable powder, while crop species
\nwere tolerant to it. Some microorganisms are capable of using
\nsorgoleone as a carbon source. Sorgoleone can be mineralized
\nvia complete degradation to CO2 in soil, although the different
\nchemical groups of the molecule were not mineralized equally
\n(Gimsing et al., 2009). The strong weed-suppressive ability of
\nformulated sorgoleone raised interest as an effective, natural,
\nenvironmentally friendly approach for weed management. Plant
\ngrowth-promoting rhizobacteria (PGPR) include a wide range
\nof beneficial bacteria that confer positive effects on plants, such
\nas eliciting induced systemic resistance (ISR), promoting plant
\ngrowth and reducing susceptibility to diseases caused by plant
\npathogens (Kloepper et al., 1980, 2004). Allelopathic bacteria can
\nachieve the same function in mixtures of bacteria that exhibit
\nPGPR attributes and activity against allelopathic weeds, which
\nreduces the inhibitory effect on susceptible plants caused by
\nallelopathic weeds (Kremer, 2006; Mishra and Nautiyal, 2012).
\nThere are some organic herbicides or plant growth inhibitors
\nthat have been manufactured from allelopathic plant materials
\nto inhibit weed growth in fields (Guillon, 2003; Ogata et al.,
\n2008; Miyake, 2009). Ogata et al. (2008) manufactured a type
\nof herbicide comprised of a mixture of components extracted
\nfrom pine (Pinus L.), hinoki (Chamaecyparis obtusa Endl.), or
\nJapanese cedar (Cryptomeria japonica D. Don) and bamboo
\n(Bambusoideae; Poaceae) vinegar, which provided a practical
\nmethod of utilizing plant allelopathy in paddy fields.
\nREDUCTION OF NITROGEN LEACHING
\nAND ENVIRONMENTAL POLLUTION
\nNitrogen leaching is a severe ecological problem due to water
\npollution. Mineralization of soil organic nitrogen, especially
\nthe nitrification of nitrogen fertilizer, is one of the main
\nreasons for the enrichment of nitrogen in the soil. Biological
\nFrontiers in Plant Science | www.frontiersin.org 4 November 2015 | Volume 6 | Article 1020
\nCheng and Cheng Plant Allelopathy Application and Mechanisms
\nnitrification inhibition (BNI) has gradually become the main
\ntarget in investigating the effect of plants on soil nitrification.
\nIn recent years, studies have proven that nitrification-inhibiting
\nsubstances (NIS) produced by plants are the first choice for soil
\nnitrification management. For example, biological nitrification
\ninhibition substances (BNIS) are allelochemicals that are able to
\ninhibit soil nitrification. Wheat allelochemicals, such as ferulic
\nacid, p-hydroxybenzoic acid and hydroxamic acid, can act on
\nsoil microbes to inhibit soil nitrification, reduce the emission
\nof N2O, improve the utilization rate of nitrogen fertilizer and
\nreduce pollution to the environment (Ma, 2005). Dietz et al.
\n(2013) found that the allelopathic plantain (Plantago lanceolata
\nL.) plant has inhibitory effects on soil nitrogen mineralization,
\nsuggesting that plantain could be utilized to reduce soil nitrogen
\nleaching.
\nBREEDING OF ALLELOPATHIC CULTIVARS
\nAllelopathic cultivars, which have great potential to minimize
\nthe introduction of refractory chemicals and effectively control
\nweeds in farmland ecosystems, represent the most promising
\napplication of allelopathy (Mahmoud and Croteau, 2002; Weston
\nand Duke, 2003; Fragasso et al., 2013). Both conventional breeding
\nmethods and those developed using transgenic technology can
\nbe applied in the breeding of allelopathic cultivars. Successful
\ncultivars must also combine a weed suppression ability with high
\nyield potential, disease resistance, early maturity and quality traits
\n(Gealy and Yan, 2012). Rondo, a rice cultivar that combines
\na high yield potential with rice blast resistance and weed
\nsuppression ability, has been grown in a commercial organic
\nrice production operation in Texas and its weed-suppressive
\nability is superior to that of many commercial cultivars (Yan and
\nMcClung, 2010; Gealy and Yan, 2012). Huagan 3, a particularly
\npromising F8 generation line derived from crosses between the
\nlocal rice cultivars N9S and PI 312777, is considered to be
\nthe first commercially acceptable weed-suppressive cultivar in
\nChina (Kong et al., 2011). Bertholdsson (2010) bred spring wheat
\nfor improved allelopathic potential by conventional breeding.
\nThe material used originated from a cross between a Swedish
\ncultivar with low allelopathic activity and a Tunisian cultivar
\nwith high allelopathic activity. The result from the field study
\nwas a 19% average reduction in weed biomass for the high
\nallelopathic lines. However, a negative effect was that the grain
\nyield was reduced by 9% in the high allelopathic lines. In
\nthis research, the high allelopathic lines showed a lower early
\nbiomass compared with the control. If the early biomass of the
\nallelopathic wheat had also been improved, the weed biomass
\nshould have been much lower (Bertholdsson, 2004). Putative
\ngenes related to the weed competition ability of wheat have been
\nfound on chromosomes 1A, 2B, and 5D via quantitative trait locus
\n(QTL) identification, which might be helpful for the breeding
\nof allelopathic wheat (Zuo et al., 2012a). However, until now, a
\nsuccessful allelopathic wheat cultivar has not been obtained. To
\nincrease crop resistance to continuous cropping obstacles and
\nautotoxicity and in the selection of crop successions, species\u2019
\ndetoxification potential should be considered as an important
\nindicator of breeding.
\nMECHANISMS UNDERLYING
\nALLELOPATHY
\nAllelopathy has been studied for quite some time, and many
\naspects of plant physiological and biochemical processes have
\nbeen proved to be affected by allelochemicals (Zeng et al., 2001;
\nGniazdowska and Bogatek, 2005). A series of physiological and
\nbiochemical changes in plants induced by allelochemicals are
\ndetailed as follows.
\nCHANGES IN THE MICRO- AND
\nULTRA-STRUCTURE OF CELLS
\nThe shape and structure of plant cells are affected by
\nallelochemicals. Volatile monoterpenes, eucalyptol and camphor
\ncan widen and shorten root cells, in addition to inducing nuclear
\nabnormalities and increasing vacuole numbers (Bakkali et al.,
\n2008; Pawlowski et al., 2012). Cruz Ortega et al. (1988) found that
\na corn pollen extract reduced mitotic activity by more than 50%,
\ninduced nuclear irregularities and pyknotic nuclei, and inhibited
\nradicle and hypocotyl growth in watermelon (Citrullus lanatus
\nvar. lanatus). Upon exposure to hordenine and gramine, which
\nare allelochemicals from barley (Hordeum vulgare) roots, the
\nradicle tips of white mustard (Sinapis alba L.) exhibited damaged
\ncell walls, increases in both the size and number of vacuoles,
\ndisorganization of organelles, and cell autophagy (Liu and
\nLovett, 1993). Likewise, cinnamic acid significantly deformed the
\nultrastructure of cucumber chloroplasts and mitochondria (Wu
\net al., 2004). After treatment with benzoic acid, mustard (Brassica
\njuncea L.) roots displayed irregularly shaped cells arranged in a
\ndisorganized manner and disruption of cell organelles (Kaur et al.,
\n2005). Allelochemicals from Convolvulus arvensis L. and catmint
\n(Nepeta meyeri Benth.) can alter the random amplification of
\npolymorphic DNA (RAPD) profiles of receiver plants (Kekec
\net al., 2013; Sunar et al., 2013). Citral is a volatile essential oil
\ncomponent of lemongrass (Cymbopogon citrates) and other
\naromatic plants that has been suggested to have allelopathic
\ntraits (Dudai et al., 1999). It was reported that citral can cause
\ndisruption of microtubules in wheat and Arabidopsis thaliana L.
\nroots, where the mitotic microtubules were more strongly affected
\nthan the cortical microtubules (Chaimovitsh et al., 2010, 2012).
\nMoreover, citral has a strong long-term disorganizing effect
\non the cell ultra-structure of A. thaliana seedlings, thickening
\nthe cell wall and reducing intercellular communication and the
\nformation of root hairs (Grana et al., 2013).
\nINHIBITION OF CELL DIVISION
\nAND ELONGATION
\nAllelochemical monoterpenoids (camphor, 1,8-cineole, betapinene, alpha-pinene, and camphene) affected cell proliferation
\nand DNA synthesis in plant meristems (Nishida et al., 2005);
\n2(3H)-benzoxazolinone (BOA) inhibited the mitotic process,
\nespecially the G2-M checkpoint of lettuce (Sanchez-Moreiras
\net al., 2008); and sorgoleone reduced the number of cells in
\neach cell division period, damaging tubulins and resulting in
\npolyploid nuclei (Hallak et al., 1999). Burgos et al. (2004)
\nFrontiers in Plant Science | www.frontiersin.org 5 November 2015 | Volume 6 | Article 1020
\nCheng and Cheng Plant Allelopathy Application and Mechanisms
\nargued that the rye allelochemicals BOA and 2, 4-dihydroxy1,4(2H)-benzoxazin-3-one (DIBOA) significantly inhibited the
\nregeneration of cucumber root cap cells and thus inhibited
\ngrowth. Following the treatment of soybean with aqueous leaf
\nextracts from Datura stramonium L., Cai and Mu (2012) found
\nthat higher concentrations of the extracts inhibited primary
\nroot elongation and lateral root development, decreased root
\nhair length and density, inhibited cell division in root tips and
\nincreased the chromosomal aberration index and micronucleus
\nindex. Teerarak et al. (2012) suggested that the ethyl acetate
\nfraction of Aglaia odorata Lour. leaves inhibited mitosis and
\ninduced mitotic abnormalities in Allium cepa roots by damaging
\nchromatin organization and the mitotic spindle in roots exposed
\nto the allelochemicals.
\nIMBALANCES IN THE ANTIOXIDANT
\nSYSTEM
\nThe generation and clearing of reactive oxygen species (ROS)
\nand the balance of the redox state in the cell play an important
\nrole in allelopathic effects. After exposure to allelochemicals,
\nthe recipient plants may rapidly produce ROS in the contact
\narea (Bais et al., 2003; Ding et al., 2007), and alter the activity
\nof antioxidant enzymes such as superoxide dismutase (SOD),
\nperoxidase (POD; Zeng et al., 2001; Yu et al., 2003) and
\nascorbic acid peroxidase (APX; Zuo et al., 2012b) to resist
\noxidative stress. Batish et al. (2008) argued that caffeic acid
\ninduces significant changes in the activities of proteases, PODs,
\nand polyphenol oxidases (PPOs) during root development and
\ndecreases the content of total endogenous phenolics in hypocotyl
\ncuttings from mung bean (Phaseolus aureus). Shearer et al.
\n(2012) found that allelopathic interactions led to changes in
\nsignal transduction and an imbalance between the production
\nof reactive oxidant species and antioxidant capabilities within a
\ncoral holobiont. This oxidative imbalance resulted in rapid protein
\ndegradation and ultimately, apoptosis or necrosis of the coral
\nAcropora millepora when compensatory transcriptional action by
\nthe coral holobiont insufficiently mitigated the damage caused
\nby allelochemicals produced by Chlorodesmis fastigiata (Shearer
\net al., 2012).
\nINCREASES IN CELL MEMBRANE
\nPERMEABILITY
\nMany studies have shown that allelochemicals significantly inhibit
\nthe activity of antioxidant enzymes and increase free radical
\nlevels, resulting in greater membrane lipid peroxidation and
\nmembrane potential alteration, which diminish the scavenging
\neffect on activated oxygen and damage the whole membrane
\nsystem of plants (Lin et al., 2000; Zeng et al., 2001; Lin, 2010;
\nHarun et al., 2014; Sunmonu and Van Staden, 2014). The
\ngrowth of Hordeum spontaneum, Avena ludoviciana, and wild
\nmustard seedlings were found to be inhibited by an aqueous
\nextract of barley aerial parts through increasing lipid peroxidation
\n(Farhoudi et al., 2012; Farhoudi and Lee, 2013). Zuo et al.
\n(2012b) argued that the combination of non-sterile shoots of
\nwheat and Alopecurus aequalis weeds led to the accumulation of
\noxygen radical species, such as the superoxide radical O2
\n\u2212 anion,
\nH2O2 and malondialdehyde (MDA) in the leaves of transgenic
\n(with Cu\/ZnSOD and APX genes) and non-transgenic potato
\n(Solanum tuberosum L.) seedlings, in addition to increasing
\nmembrane permeability and altering the activities of SOD and
\nAPX. Poonpaiboonpipat et al. (2013) found that lemongrass
\n(Cymbopogon citratus) essential oil damages the membrane
\nsystem of barnyard grass (Echinochloa crus-galli L.), causing lipid
\nperoxidation and electrolyte leakage. Sun et al. (2014) investigated
\nthe generation of ROS induced by pyrogallic acid (PA) in
\nMicrocystis aeruginosa. They found O2
\n\u2212 to be the precursor of
\nH2O2 and showed that the hydroxyl radical OH\u00b7was generated at
\nsignificant levels, demonstrating that PA caused oxidative stress
\nin M. aeruginosa and that futile redox cycling of PA was the main
\nsource of excessive intracellular O2
\n\u2212 and consequent H2O2 and
\nOH\u00b7production.
\nEFFECT ON THE PLANT GROWTH
\nREGULATOR SYSTEM
\nAllelochemicals can alter the contents of plant growth regulators
\nor induce imbalances in various phytohormones, which inhibits
\nthe growth and development of plants, for example, with
\nrespect to seed germination and seedling growth. Most phenolic
\nallelochemicals can stimulate IAA oxidase activity and inhibit
\nthe reaction of POD with IAA, bound GA or IAA to influence
\nendogenous hormone levels (Yang et al., 2005).
\nLeslie and Romani (1988) found that salicylic acid inhibited
\nthe synthesis of ethylene in cell suspension cultures of pear
\n(Pyrus communis). Through treatment of wheat seedlings with
\nhigh concentrations of ferulic acid (2.50 mM), Liu and Hu
\n(2001) found that the growth of wheat seedlings was inhibited by
\nthe accumulation of IAA, GA3, and CTK, with a simultaneous
\nincrease in ABA. An aqueous extract from rice was shown
\nto significantly stimulate IAA oxidase activity in barnyard
\ngrass and reduce IAA levels, thereby damaging the growth
\nregulation system and inhibiting seedling growth (Lin et al.,
\n2001). Yang et al. (2008) investigated the mechanisms of
\ntwo allelochemicals: DTD [4, 7-dimethyl-1-(propan-2-ylidene)-
\n1, 4, 4a, 8a-tetrahydronaphthalene-2, 6(1H, 7H)-dione] and
\nHHO [6-hydroxyl-5-isopropyl-3, 8-dimethyl-4a, 5, 6, 7, 8,
\n8a-hexahydronaphthalen-2(1H)-one], isolated from Ageratina
\nadenophora Sprengel weeds. DTD at a higher concentration
\n(1.5 mM), significantly increased the ABA content in the roots of
\nrice seedlings, but this decreased sharply after 96 h of treatment.
\nHHO also significantly enhanced the ABA content for 48 and
\n96 h. However, the application of DTD or HHO decreased
\nthe IAA and ZR contents in rice roots. The IAA\/ABA and
\nZR\/ABA ratios decreased quantitatively in response to higher
\nconcentrations of DTO or HHO. These results suggest that
\nthe endogenous hormones might have dependent as well as
\ninteractive effects on the responses of rice seedlings and their
\nadaptability to DTD or HHO stress. Moreover, the results from
\nanother study indicated that cyanamide (1.2 mM) caused an
\nimbalance of plant hormone (ethylene and auxin) homeostasis
\nin tomato (Solanum lycopersicum L.) roots (Soltys et al.,
\n2012).
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\nCheng and Cheng Plant Allelopathy Application and Mechanisms
\nEFFECT ON THE FUNCTIONS AND
\nACTIVITIES OF VARIOUS ENZYMES
\nAllelochemicals exert different effects on the synthesis, functions,
\ncontents and activities of various enzymes. Previous studies
\nhave shown that the key enzyme \u03bb-phosphorylase involved in
\nseed germination might be inhibited by chlorogenic acid, caffeic
\nacid and catechol (Rice, 1984; Einhellig, 1995). Additionally,
\nPOD, CAT, and cellulase can be suppressed by tannic acid,
\nwhich can also reduce the synthesis of amylase and acidphosphatase in the endosperm. Phenolic acids can increase
\nthe activity of phenylalanine ammonialyase (PAL) and \u03b2glucosidase, while reducing the activity of phenol-\u03b2-glucose
\ntransferase, thus inhibiting root growth. In addition, protease,
\ninvertase and succinodehydrogenase (SDH) can be suppressed by
\nallelochemicals.
\nLin et al. (2001) argued that caffeic acid, gallic acid and phenols
\nregulate phenylalanine metabolism by suppressing the activities
\nof PAL and cinnamic acid-4-hydroxylase. An aquatic extract of
\nthe above-ground parts and rhizospheric soil of chrysanthemum
\n(Chrysanthemum indicum L.) inhibited the activities of root
\ndehydrogenase and nitrate reductase (NiR), reduced the contents
\nof soluble sugar and soluble protein, and inhibited the root growth
\nof stem cuttings of the same species (Zhou et al., 2010). Cheng
\n(2012) investigated the effects of diethyl phthalate (DEP) on
\nthe enzyme activity and polypeptide accumulation of glutamine
\nsynthetase (GS) in greater duckweed (Spirodela polyrhiza L.) and
\nfound that DEP is toxic to this species due to the inhibition of GS
\nisoenzymes in nitrogen assimilation and antioxidant enzymes.
\nINFLUENCE ON RESPIRATION
\nAllelochemicals affect plant growth by influencing different stages
\nof respiration, such as electron transfer in the mitochondria,
\noxidative phosphorylation, CO2 generation and ATP enzyme
\nactivity. These chemicals can reduce oxygen intake, which
\nprevents NADH oxidation, inhibits ATP synthesis enzyme
\nactivity, reduces ATP formation in mitochondria, disturbs plant
\noxidative phosphorylation and ultimately inhibits respiration; on
\nthe other hand, they can stimulate the release of CO2, which
\npromotes respiration.
\nCruz Ortega et al. (1988) found that an ethanol extract from
\ncorn pollen acted as an inhibitor of the electron pathway and
\ndecreased oxygen consumption; the specific inhibition site was
\nmost likely located upstream of cytochrome c. Rasmussen et al.
\n(1992) found that sorgoleone interfered with the function of
\nmitochondria isolated from etiolated soybean and corn seedlings
\nby blocking electron transport at the b-c1 complex. Moreover,
\nHejl and Koster (2004b) observed that juglone could reach the
\nmitochondria in the root cells of corn and soybean seedlings,
\nthereby disrupting root oxygen uptake. Alpha-pinene, camphor,
\nlimonene and other monoterpenes significantly affect radicle
\nand hypocotyl mitochondrial respiration in soybean and corn,
\nbut their targets are different. Alpha-pinene acts under at least
\ntwo mechanisms: uncoupling of oxidative phosphorylation and
\ninhibition of electron transfer. Alpha-pinene strongly inhibits
\nmitochondrial ATP production, decreases the mitochondrial
\ntransmembrane potential and impairs mitochondrial energy
\nmetabolism. Camphor causes uncoupling of mitochondria.
\nLimonene inhibits coupled respiration but does not affect basal
\nrespiration, and inhibits ATP synthetase and the activities of
\nadenine nucleotide translocase complexes at concentrations of 1.0
\nand 5.0 mM (Abrahim et al., 2003a,b).
\nEFFECT ON PLANT PHOTOSYNTHESIS
\nThe impacts of allelochemicals on plant photosynthesis mainly
\ninvolve inhibition of or damage to the synthesis machinery and
\nacceleration of the decomposition of photosynthetic pigments.
\nConsequently, photosynthetic pigment contents are decreased,
\nwhich blocks energy and electron transfer, reduces ATP synthesis
\nenzyme activity, inhibits the synthesis of ATP, and affects stomatal
\nconductance and transpiration, which inhibit the photosynthetic
\nprocess (Meazza et al., 2002; Yu et al., 2003, 2006; Wu et al., 2004).
\nAllelochemicals affect photosynthesis mainly by influencing the
\nfunction of PS II (Weir et al., 2004; Wang et al., 2014). For example,
\nsorgoleone inhibits the decay of variable fluorescence, blocks
\nthe oxidation of the PSII-reduced primary electron acceptor,
\nQ
\n\u2212
\nA, by the PSII secondary electron acceptor and that of QB by
\ndisplacing QB from the D1 protein, thus inhibiting photochemical
\neffects (Gonzalez et al., 1997). Similarly, Shao et al. (2009)
\ndemonstrated that the D1 protein is an important target in the
\ndamage caused to Microcystis by pyrogallol. Moreover, Uddin
\net al. (2012) found that sorgoleone reduced the Fv\/Fm of weeds
\nand inhibited weed growth. By studying the inhibitory effect
\nof the dried macroalga Gracilaria tenuistipitata (Rhodophyta)
\non the microalga Phaeodactylum tricornutum, Ye et al. (2013)
\nfound a decrease in the number of active reaction centers and
\nblockade of the electron transport chain. Poonpaiboonpipat et al.
\n(2013) observed that a high concentration of essential oil from
\nlemongrass (Cymbopogon citratus) leaves significantly decreased
\nthe chlorophyll a and b and carotenoid contents of barnyard
\ngrass and affected alpha-amylase activity in seeds, indicating that
\nessential oil interferes with photosynthetic metabolism. However,
\naqueous extracts of leaves from Trema micrantha (Ulmaceae), an
\nallelopathic plant, did not lead to inhibition of the synthesis of
\nphotosynthetic pigments in radish (Raphanus sativus L.) (Borella
\net al., 2014).
\nINFLUENCE ON WATER AND NUTRIENT
\nUPTAKE
\nMany allelochemicals affect nutrient absorption in plant roots
\nor induce water stress through long-term inhibition of water
\nutilization. Allelochemicals can inhibit the activities of Na+\/K+-
\nATPase involved in the absorption and transport of ions at the
\ncell plasma membrane, which suppresses the cellular absorption
\nof K+, Na+, or other ions.
\nBergmark et al. (1992) found that ferulic acid (250 \u00b5M)
\ninhibited ammonium and NO3
\n\u2212 uptake in corn seedlings,
\nalthough ammonium uptake was less sensitive to this treatment
\nthan NO3
\n\u2212. Ferulic acid also inhibits Cl\u2212 uptake and increases
\nthe initial net K+ loss from roots exposed to a low K ammonium
\nnitrate solution and delays recovery that results in a positive
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\nCheng and Cheng Plant Allelopathy Application and Mechanisms
\nnet uptake. Yuan et al. (1998) showed that the effects of
\nallelochemicals, such as ferulic acid, benzaldehyde and 4-tertbutylbenzoic acid, on nitrogen absorption in wheat seedlings
\nare negatively correlated, but the negative effects of NH4
\n+-N
\non nitrogen absorption were stronger than those of NO3
\n\u2212-
\nN. Yu and Matsui (1997) observed that cinnamic acid and
\nthe root exudates of cucumber inhibited the uptake of NO3
\n\u2212,
\nSO4
\n2\u2212, K+, Ca2+, Mg2+, and Fe2+ by cucumber seedlings.
\nThrough further study, Lv et al. (2002) found that cinnamic
\nacid and p-hydroxybenzoic, the main allelochemicals found in
\ncucumber root exudates, strongly inhibited the activities of root
\ndehydrogenase, root-combined ATPase and nitrate reductase in
\ncucumber, thus inhibiting the root uptake of K+, NO3
\n\u2212, and
\nH2PO4
\n\u2212. Sorgoleone and juglone significantly inhibited H+-
\nATPase activity and the proton-pumping function across the root
\ncell plasmalemma, which affected solute and water uptake in
\npeas (Pisum sativum L.), soybeans and corn (Hejl and Koster,
\n2004a,b). Abenavoli et al. (2010) found that the allelochemicals
\ntrans-cinnamic, ferulic acid and p-coumaric acid inhibited net
\nnitrate uptake and plasma membrane H+-ATPase activity in
\nmaize seedlings, while umbelliferone and caffeic acid had no
\neffect on H+-ATPase activity. Sunflower (Helianthus annus L.)
\nresidues negatively affected plant development, the efficiency of
\ntranslocation of assimilates and nutrient accumulation in radish
\nplants (Barros de Morais et al., 2014).
\nThe effects of allelochemicals on ion uptake are closely related
\nto allelochemical concentrations and classifications. For example,
\na low concentration of dibutyl phthalate increases the absorption
\nof N but decreases that of P and K. However, a high concentration
\nof this chemical inhibits the absorption of N, P and K. Similarly, a
\nlow concentration of diphenylamine stimulates the absorption of
\nN and K but inhibits the absorption of P by tomato roots (Geng
\net al., 2009).
\nINFLUENCE ON PROTEIN AND NUCLEIC
\nACID SYNTHESIS AND METABOLISM
\nMost alkaloids show allelopathic potential. Some can closely
\nintegrate with DNA and increase the temperature of DNA
\ncleavage, while some can inhibit DNA polymerase I and prevent
\nthe transcription and translation of DNA, whereas others can
\ninhibit protein biosynthesis (Wink and Latzbruning, 1995).
\nAllelochemicals can also inhibit amino acid absorption, in
\naddition to transport, thus interfering with protein synthesis,
\nwhich affects cell growth (Abenavoli et al., 2003). All phenolic
\nacids can affect the integrity of DNA and RNA. Ferulic acid
\nand cinnamic acid as well as many phenols and alkaloids can
\nalso inhibit protein synthesis (Baziramakenga et al., 1997; Zeng
\net al., 2001; Li et al., 2010). This suggests that the observed
\nallelopathic phenomenon is partly a result of the interaction of
\nthe allelochemicals with these basic targets, such as DNA, RNA,
\nprotein biosynthesis and related processes.
\nBy analyzing the gene expression profile of A. thaliana after
\ntreatment with fagomine, gallic acid, and rutin, which are
\nallelochemicals found in buckwheat (Fagopyrum esculentum
\nMoench), Golisz et al. (2008) observed that genes that reacted to
\nthe allelochemicals mainly fell into several functional categories:
\ninteraction with the environment, subcellular localization,
\nproteins with a binding function or cofactor requirement, cell
\nrescue, defense and virulence, or metabolism. The plant response
\nto allelochemicals was similar to the response to biotic or abiotic
\nstress. This indicated that allelochemicals might have relevant
\nfunctions in the cross-talk between biotic and abiotic stress
\nsignaling, as they generate ROS (Bais et al., 2003; Baerson et al.,
\n2005; Golisz et al., 2008, 2011). Shao et al. (2009) found that
\nthe allelochemical pyrogallol affects the expression of psbA,
\nmcyB, prx, and faab( in Microcystis aeruginosa, and indicated
\nthat membranes are the first target in the damage of Microcystis
\ncaused by pyrogallol. Guo et al. (2011) showed that HHO affected
\nthe expression of CHS, which is associated with the synthesis
\nof various amino acids in Eupatorium adenophorum roots.
\nCyanamide alters the expression of the expansin genes, LeEXPA9
\nand LeEXPA18, which are responsible for cell wall remodeling
\nafter cytokinesis, thereby inhibiting the formation of tomato root
\n(Soltys et al., 2012). In a recent study, Fang et al. (2015) found
\nthat the expression levels of miRNAs relevant to plant hormone
\nsignal transduction, p53 signaling pathways, nucleotide excision
\nrepair and the peroxisome proliferator-activated receptor were
\nenhanced in barnyard grass co-cultured with allelopathic rice or
\ntreated with rice-produced phenolic acids. Kato-Noguchi et al.
\n(2013) reported that the rice allelochemicals momilactone A and
\nB might inhibit the germination of Arabidopsis seeds by inhibiting
\nthe degradation process of the storage proteins cruciferin and
\ncruciferina.
\nAllelochemicals produced by donor plants act on receiver
\nplants, while the receiver plants will react to the donor
\nplants by inducing changes in gene expressions. The upregulated expression of PAL, cinnamate-4-hydroxylase
\n(C4H), ferulic acid 5-hydroxylase (F5H), and caffeic acid
\nO-methyltransferases (COMT), which are involved in the
\nbiosynthesis of phenolic compounds in rice, is consistent with
\ntheir inhibitory effects on barnyard grass, while barnyard grass
\ninduces the expression of genes related to the synthesis of
\nphenolic compounds in allelopathic rice (He et al., 2012a).
\nEFFECTS OF ALLELOCHEMICALS ON
\nMICROORGANISMS AND THE
\nECOLOGICAL ENVIRONMENT
\nResearchers have found that there are significant relationships
\nbetween crop growth and soil microbes under the application of
\nallelochemicals or in the presence of allelopathic plants (Figure 3;
\nBarazani and Friedman, 1999; Bais et al., 2006; Mishra et al., 2013).
\nRecent studies demonstrated that indirect effects of allelopathy as
\na mediator of plant\u2013plant interactions were more important than
\nthe direct effects of an inhibitor (Zeng, 2014). Chemical-specific
\nchanges in soil microbes could generate negative feedbacks in soil
\nsickness and plant growth (Stinson et al., 2006; Huang et al., 2013;
\nZhou et al., 2013; Li et al., 2014). Meanwhile, the rhizosphere soil
\nmicrobes contribute to the allelopathic potential of plants through
\npositive feedback (Inderjit et al., 2011; Zuo et al., 2014; Wu et al.,
\n2015). Bacteria can help to increase inhibition by activating a
\nnon-toxic form of an allelochemical (Macias et al., 2003). For
\nexample, non-glycosylated compounds may be modified after
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\nCheng and Cheng Plant Allelopathy Application and Mechanisms
\nFIGURE 3 | A schematic diagram showing the various roles of microbes in modulating the interaction of allelopathic donor-receiver species
\n(Barazani and Friedman, 1999; Bais et al., 2006; Mishra et al., 2013). Red arrows with double lines indicate the phenomenon of allelopathy, and blue arrows
\nwith single lines indicate the involvement of various microbial processes in reducing\/enhancing allelopathic inhibition by soil microorganisms. This figure explains that
\nbeneficial rhizobacteria can minimize the phytotoxicity of the allelopathic donor toward the allelopathic receiver by using various rhizospheric processes such as
\nrhizosphere colonization, biofilm formation, and degradation\/transformation of toxic allelochemicals or modulation of the defense mechanism in receiver species by
\ninducing the expression of stress responsive genes or the activity of antioxidant enzymes. Furthermore, microbes also can play an important role in the activation of
\nallelochemicals, e.g., through the release of non-toxic glycosides followed by microbial degradation to release the active allelochemical.
\nrelease from plants and become more toxic (Tanrisever et al.,
\n1987; Macias et al., 2005a). However, bacteria can also help
\nsusceptible plants to tolerate biotic stress associated with weeds,
\nand to decrease the allelopathic inhibition of weeds by causing
\nalterations in the expression patterns of some genes that might
\nbe responsible for different functions but ultimately lead to a
\nself-defense process (Mishra and Nautiyal, 2012). In addition,
\nthe microbial degradation\/transformation of allelochemicals in
\nsoil affects the effective dose of allelochemicals that can cause
\nplant inhibition (Mishra et al., 2013; Li et al., 2015). Bacterial
\nbiofilms in rhizospheric regions can protect colonization sites
\nfrom phytotoxic allelochemicals and can reduce the toxicity of
\nthese chemicals by degrading them (Mishra and Nautiyal, 2012;
\nMishra et al., 2012). Microorganisms have the ability to alter
\nthe components of allelochemicals released into an ecosystem,
\nhighlighting their key role in chemical plant\u2013plant interactions
\nand suggesting that allelopathy is likely to shape the vegetation
\ncomposition and participate in the control of biodiversity in
\necology (Fernandez et al., 2013). Some sesquiterpenoid lactones
\nand sulfides are antimicrobial and can disrupt the cell walls
\nof fungi and invasive bacteria, while others can protect plants
\nfrom environmental stresses that would otherwise cause oxidative
\ndamage (Khan et al., 2011; Chadwick et al., 2013). Zhang et al.
\n(2013a) found that antifungal volatiles released from Chinese
\nFrontiers in Plant Science | www.frontiersin.org 9 November 2015 | Volume 6 | Article 1020
\nCheng and Cheng Plant Allelopathy Application and Mechanisms
\nchive (Allium Tuberosum Rottler) helped to control Panama
\ndisease (Fusarium wilt) in banana (Musa spp.) and showed
\nthat intercropping\/rotation of banana with Chinese chive could
\ncontrol Panama disease and increase cropland biodiversity.
\nWang et al. (2013b) indicated that the shift in the microbial
\ncommunity composition induced by barnyard grass infestation
\nmight generate a positive feedback in rice growth and
\nreproduction in a given paddy system. The relative abundance
\nand population of plant parasitic nematodes were significantly
\nreduced in the presence of Chromolaena odorata (Asteraceae)
\nfallow (Odeyemi et al., 2013). Pearse et al. (2014) found that
\nradish soils had a net positive effect on Lupinus nanus biomass
\nand explained that radish might alter the mutualistic\/parasitic
\nrelationship between L. nanus and its rhizobial associates, with a
\nnet benefit to L. nanus. Fang et al. (2013) indicated that inhibiting
\nthe expression of the rice PAL gene reduced the allelopathic
\npotential of rice and the diversity of the rhizosphere microflora.
\nThese findings suggested that PAL functions as a positive
\nregulator of the rice allelopathic potential.
\nPGPR, such as root-colonizing Pseudomonas, Paenibacillus
\npolymyxa, endophytes and Chryseobacterium balustinum Aur9,
\nhave been shown to alter plant gene expression and regulate
\nplant allelochemical synthesis and signaling pathways to enhance
\ndisease resistance, adaptability and defense capabilities in
\nresponse to biotic and abiotic stresses in plants (van Loon, 2007;
\nDardanelli et al., 2010; Mishra and Nautiyal, 2012).
\nPROBLEMS AND FUTURE RESEARCH
\nDIRECTIONS
\nAllelochemicals mainly consist of secondary metabolites that are
\nreleased into the environment through natural pathways, such as
\nvolatilization, leaf leaching, residue decomposition, and\/or root
\nexudation. Therefore, it should first be noted how allelochemicals
\nare released into the environment (Inderjit and Nilsen, 2003).
\nThe activity of allelochemicals varies with research techniques
\nand operational processes (Peng et al., 2004). The natural state of
\nallelochemicals may be changed somewhat during the process of
\nextraction (Li et al., 2002). Therefore, researchers must be careful
\nto determine whether a plant has allelopathic potential or separate
\nand identify allelochemicals using organic solvents and aqueous
\nextracts from plant tissues.
\nAn allelochemical released into the environment is usually not
\na single substance, and the amounts of allelochemicals released
\nunder different conditions vary. Therefore, both the type and
\namount of allelochemicals released by plants should be considered
\nwhen their allelopathic potential is investigated. Interactions such
\nas synergy, antagonism and incremental effects between different
\nallelochemicals should be evaluated because one allelochemical
\nmay not show allelopathic activity as a single component in a
\ncertain situation, but might increase allelopathy in association
\nwith other allelochemicals (Albuquerque et al., 2010).
\nThe type and amount of allelochemicals released into the
\nenvironment depend on the combined effects of the plant itself
\n(plant factors) and environmental factors, as shown in Figure 4
\n(Albuquerque et al., 2010). The plant factors include the species,
\nvariety, growth stage and different tissues (Belz, 2007; Leao et al.,
\nFIGURE 4 | Induction of allelochemical production by the plant itself
\nand environmental factors (Part of this figure was modified from
\nAlbuquerque; Albuquerque et al., 2010). The plant factors include species,
\nvariety, growth stage, tissue type, etc. Environmental factors include abiotic
\nfactors (irradiation, temperature, nutrient limitation, moisture, pH) and biotic
\nfactors (plant competition, diseases, insects, animal attack and receptor
\nfeedback regulation).
\n2012; Iannucci et al., 2013). Allelopathic effects vary between
\nvarieties or genotypes (Li and Shen, 2006; Zhou et al., 2011;
\nLeao et al., 2012). Plants from the same environment or with
\nclose taxonomic proximity do not necessarily display similar
\nproduction of secondary metabolites, and they may therefore
\nnot secrete the same quantity and quality of allelochemicals
\nor have similar allelopathic effects (Chon and Nelson, 2010;
\nHagan et al., 2013; Imatomi et al., 2013). Lin et al. (2000)
\nfound that varietal differences in the allelopathic potential of
\nrice were related to the genetic background. Environmental
\nfactors include both abiotic factors (e.g., irradiation, temperature,
\nnutrient limitation, moisture, pH) and biotic factors (e.g., plant
\ncompetition, diseases, insects, animal invasion, receptor feedback
\nregulation; Anaya, 1999). In a recent study, endogenous levels of
\nallelochemicals were used as indices of abiotic stress resistance.
\nMeanwhile, the exogenous application of allelochemicals has
\nbeen found to increase the endogenous level of the receivers,
\nwith a simultaneous increase in growth and resistance against
\nabiotic stresses (Maqbool et al., 2013); consequently, appropriate
\nenvironmental conditions are necessary for allelopathic studies. It
\nhas been noted that a stress environment can increase the release
\nof allelochemicals from allelopathic plants (Albuquerque et al.,
\n2010). Through studying the dynamic release of allelochemicals
\nunder different stress environments, we can clarify the release
\ncharacteristics of allelochemicals and determine the conditions
\nrequired for allelochemical release, thereby revealing the nature
\nof allelochemicals.
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\nCheng and Cheng Plant Allelopathy Application and Mechanisms
\nAllelochemicals can be degraded after they have been released
\ninto the soil; the half-life of allelochemicals varies from a few hours
\nto a few months (Demuner et al., 2005; Macias et al., 2005b; Wang
\net al., 2007; Barto and Cipollini, 2009; Bertin et al., 2009), and
\nthis is mainly associated with the allelochemical concentration,
\nsoil type, soil enzymes, and soil microbial population and
\ncommunity structure (Macias et al., 2004; Understrup et al.,
\n2005; Kong et al., 2008; Gu et al., 2009). Previous studies
\nindicated that some allelochemicals had tremendous spatial and
\ntemporal heterogeneity (Weidenhamer, 2005; Dayan et al., 2009;
\nMohney et al., 2009; Weidenhamer et al., 2009, 2014), but these
\ncharacteristics of most allelochemicals have not been confirmed.
\nIt was reported that polydimethylsiloxane (PDMS) microtubing
\n(silicone tubing microextraction, or STME) could be used as a
\ntool to provide a more finely resolved picture of allelochemical
\ndynamics in the root zone (Weidenhamer, 2005; Mohney et al.,
\n2009; Weidenhamer et al., 2009, 2014). Until now, much remains
\nunknown about the fate or persistence of allelochemicals in the
\nsoil or their effects on soil chemistry or microflora (Belz, 2007).
\nExplaining how allelochemicals function is complicated due
\nto the many classes of chemicals and different structures that
\nhave been identified as agents in allelopathy. There is no generic
\nallelochemical, and we should certainly anticipate different
\nmechanisms of action among allelopathic chemicals. Moreover, it
\nshould be investigated in future studies whether allelochemicals
\nare absorbed through transport proteins or whether different
\nallelochemicals have the same molecular targets in different
\nspecies (Weston and Mathesius, 2013). The systematic study of
\nallelochemical detoxification mechanisms in different species will
\nhelp reveal the differences in detoxification mechanisms between
\nplants and microbes.
\nAllelopathy is a complex process. Many allelochemicals
\nhave been identified to date. Due to the different sensitivities
\nof different receptors to the same allelochemical and the
\nvarious allelopathic activities of different allelochemicals,
\nconsiderable further work is required in the field of allelochemical
\nresearch. Very little is known about the transportation and
\nbiodegradation of allelochemicals in soil or the population
\ngenetics of allelopathic species, the establishment of practical ways
\nof using allelochemicals in the field, the rapid adaptation of weeds
\nto avoid them, the diversity of the soil microbial community that
\nis maintained in their presence or the role of signal transduction
\nin herbivore defense. These areas should be the focus of future
\ninvestigations.
\nConsiderable research has showed that allelopathy has good
\napplication potential in agricultural production. Until now, many
\nallelopathic crops have been used in agricultural production, but
\nthe applications are limited to small-scale and regional areas. The
\nstructure and mode of action of many allelochemicals have been
\ndeeply revealed in recent years, and this has laid a good foundation
\nfor project ( help with nursing paper writing from experts with MSN & DNP degrees)s where allelochemicals are used to obtain the basic
\nstructures or templates for developing new synthetic herbicides.
\nThe commonly used methods of weed control (herbicide
\napplication, mechanical weeding and hand weeding) are
\neffective in agricultural production. However, there are many
\ndisadvantages associated with these methods, for example, the
\nevolution of herbicide resistance in weeds, the negative impacts
\nof herbicides on environmental, human and animal health,
\nthe expense of herbicides, the losses in soil structure and the
\nenormous labor requirements. Many of the above problems can
\nbe allayed by creating diversity in weed control practices with
\nthe application of allelopathy. The combination of more than
\none weed control method has been proved to be effective in
\nreducing the probability of herbicide resistance development in
\nweeds. Moreover, the combined application of reduced synthetic
\nherbicides dose and allelopathic extracts can provide control that
\nis as effective as that obtained from the standard dose of herbicides
\n(Farooq et al., 2011). Further, using diverse weed management
\npractices in certain fields can ensure sustainable and effective
\nweed control.
\nCONCLUSION
\nAllelopathy has been known and used in agriculture since
\nancient times; however, its recognition and use in modern
\nagriculture are very limited. Allelopathy plays an important
\nrole in investigations of appropriate farming systems as well as
\nin the control of weeds, diseases and insects, the alleviation of
\ncontinuous cropping obstacles, and allelopathic cultivar breeding.
\nFurthermore, allelochemicals can act as environmentally friendly
\nherbicides, fungicides, insecticides and plant growth regulators,
\nand can have great value in sustainable agriculture. Although
\nallelochemicals used as environmentally friendly herbicides has
\nbeen tried for decades, there are very few natural herbicides on
\nthe market that are derived from an allelochemical. However,
\nthere are a few research investigations testing natural-product
\nherbicides. With increasing emphasis on organic agriculture and
\nenvironmental protection, increasing attention has been paid
\nto allelopathy research, and the physiological and ecological
\nmechanisms of allelopathy are gradually being elucidated.
\nMoreover, progress has been made in research on the associated
\nmolecular mechanisms. It is obvious that allelopathy requires
\nfurther research for widespread application in agricultural
\nproduction worldwide.
\nACKNOWLEDGMENTS
\nThe authors acknowledge the editors for providing us with this
\nopportunity to share our understanding of the practices of plant
\nallelopathy in agriculture and the physiological and ecological
\nmechanisms of allelopathy. This research and the writing of this
\nreview were supported by a project ( help with nursing paper writing from experts with MSN & DNP degrees) of the National Natural Science
\nFoundation of China (No. 31471865).
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\nConflict of Interest Statement: The authors declare that the research was
\nconducted in the absence of any commercial or financial relationships that could
\nbe construed as a potential conflict of interest.
\nCopyright \u00a9 2015 Cheng and Cheng. This is an open-access article distributed under
\nthe terms of the Creative Commons Attribution License (CC BY). The use, distribution
\nor reproduction in other forums is permitted, provided the original author(s) or
\nlicensor are credited and that the original publication in this journal is cited, in
\naccordance with accepted academic practice. No use, distribution or reproduction is
\npermitted which does not comply with these terms.
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