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Allelopathy in Poaceae species present in Brazil. A review

  • Adriana FavarettoEmail author
  • Simone M. Scheffer-Basso
  • Naylor B. Perez
Review Article

Abstract

Allelopathy is an important ecological mechanism in natural and managed ecosystems. Its study is critical to understand natural plant behaviors, to isolate allelochemicals with herbicide potential, and to use the allelopathic genes in transgenic studies. Poaceae is an ecologically dominant plant family and it is economically important worldwide because its chemical diversity represents an important source to discover new molecules. From this viewpoint, Brazil is an interesting place to study, encompassing 197 genera of the Poaceae family, many of them being dominant in various biomes and some being native to Brazil. Here, we review the literature describing allelopathic activities involving grasses of the Poaceae family. We evaluate the experimental conditions used in these studies, we identify the allelochemicals involved, and, finally, we assess the applicability of allelopathy. Our main findings are (1) among the 47 Brazilian species studied for their allelopathic effects, only Bothriochloa barbinodis, Bothriochloa laguroides, Paspalum notatum, and Paspalum urvillei are native to Brazil; (2) 51% of the reviewed studies prepared extracts from the leaves and used lettuce as the target plant; and (3) 64% of the papers identified allelochemicals, of which 67% were phenolic acids. This first bibliographical survey on allelopathy in Poaceae species present in Brazil shows that less than 3% of the Brazilian species have been studied, suggesting it is an incipient research subject. Since this plant family is a valuable source of unknown natural products, refining such studies should contribute to a better understanding of the ecosystem relationships. Identification and isolation of grass allelochemicals should promote environmentally safer compounds with bioherbicide properties, in sustainable agriculture.

Keywords

Allelochemicals Bioprospecting Grasses Native resources 

1 Introduction

The influence of some plant species on the growth of others in their vicinity remained an unexplained phenomenon (Rodrigues et al. 1992) until Theophrastus (300 B.C.) conceptualized it as allelopathy (Reigosa et al. 2013). In 1974, Elroy L. Rice defined allelopathy as the effect of one plant on another via the release of chemical compounds into the environment (Rice 1984). Currently, the most accepted concept of allelopathy is as “any process involving secondary metabolites produced by plants, algae, bacteria, and fungi that influence the growth and development of agriculture and biological systems” (Ias 1996).

Allelopathy is an important ecological mechanism in the natural and managed ecosystems. It is a phenomenon that influences the primary and secondary plant succession, encompassing all successional stages (Reigosa et al. 1999); the structure and composition of plant communities and the dynamics between different formations (Rizvi et al. 1992); the dominance of certain plant species that affect the local biodiversity (Reigosa et al. 1999); and agriculture, which is the target of most studies (Chou 1989). Considering the importance of allelopathy, several studies have been conducted on the subject, a great majority of which focused on species of economic interest. Allelopathic studies in Brazil also focused on agroecosystems, especially with cultivated and weedy plants. On the other hand, considering the territorial extent and the diversity of the Brazilian flora, studies on the allelopathic potential of native species are scarce (Ferreira et al. 1992).

The Poaceae family is ecologically the most dominant and economically the most important family in the world (Heywood 1978), with approximately 793 genera and 8,000–9,000 species (Sánchez-Moreiras et al. 2004). In Brazil, this family is represented by 197 genera and 1,368 species, many of which are native and dominant in several Brazilian biomes. However, despite the representativeness of this family, the knowledge about allelopathy and the allelochemicals present in these species is limited (Fig. 1).
Fig. 1

Grasses with allelopathic effect, native to Brazil. a Bothriochloa laguroides. b Paspalum urvillei. Photos from University of Passo Fundo, Passo Fundo, RS, Brazil

In order to investigate works related to the allelopathic potential of Poaceae species present in Brazil, research literature were searched in the databases of Science Direct, the Portal of Periodicals of Capes (Coordination for the Improvement of Higher Education Personnel), and the Academic Google. For the search purpose, the following keywords were used: “allelopathy,” “allelochemicals,” “phytochemistry,” “chemical compounds,” and “bioprospecting,” besides the genera of Poaceae species present in Brazil, as described by Boldrini et al. (2010) and Pillar et al. (2009).

2 Poaceae genera native to Brazil with allelopathic effect

A total of 44 papers referring to 47 species were found for works related to the allelopathic effect of grasses present in Brazil (Table 1). Of these, 31 species occur in Brazil, but only four are native to the country, which include Bothriochloa barbinodis, Bothriochloa laguroides, Paspalum notatum, and Paspalum urvillei. The fact that only 2.56% of the Brazilian species have been studied in terms of their allelopathic potential shows that this area is still incipient for the Poaceae, especially, for the species native to the country.
Table 1

General characteristics of allelopathic works conducted with grasses present in Brazil

Species

Plant organ

Target species

Effect

Reference

Aristida junciformis

Leaves and roots

Lactuca sativa

Germination, root and shoot length

Ghebrehiwot et al. (2014)

Arundo donax a

Leaves

Lens culinaris

Germination and initial growth

Abu-Romman and Ammari (2015)

Avena fatua a

Whole plant

Triticum aestivum

Germination, root and shoot length

Ahmad et al. (2014)

Axonopus compressus a

Leaves

Asystasia gangetica, Pennisetum polystachion

Hypocotyl and shoot length, mean germination time

Samedani et al. (2013)

Brachiaria brizantha a

Seeds, shoot, and roots

Desmodium adscendens, Sida rhombifolia, Vernonia polyanthes, Stylosanthes guianensis, Lepidium sativum, Lactuca sativa, Phleum pratense, Lolium multiflorum

Germination, root and shoot length

Souza Filho et al. (1997); Carvalho et al. (1993); Kato-Noguchi et al. (2014)

Brachiaria decumbens a

Seeds, shoot, and roots

Desmodium adscendens, Sida rhombifolia, Vernonia polyanthes

Germination and root length

Souza Filho et al. (1997)

Brachiaria humidicola a

Seeds, shoot, and roots

Desmodium adscendens, Sida rhombifolia, Vernonia polyanthes

Germination and root length

Souza Filho et al. (1997)

Bothriochloa barbinodis b

Roots, stem, and leaves

Lactuca sativa, Zea mays, Eragrostis curvula, Paspalum guenoarum

Germination, root and shoot length

Scrivanti et al. (2011)

Bothriochloa edwardsiana

Roots, stem, and leaves

Lactuca sativa, Zea mays, Eragrostis curvula, Paspalum guenoarum

Germination, root and shoot length

Scrivanti et al. (2011)

Bothriochloa laguroides b

Roots, stem, and leaves

Lactuca sativa, Zea mays, Eragrostis curvula, Paspalum guenoarum

Germination, root, and shoot length

Scrivanti (2010)

Bothriochloa perforata

Roots, stem, and leaves

Lactuca sativa, Zea mays, Eragrostis curvula, Paspalum guenoarum

Germination, root and shoot length

Scrivanti et al. (2011)

Bothriochloa pertusa a

Inflorescence, roots, stem, and leaves

Pennisetum americanum, Setaria italica, Lactuca sativa

Germination, root and shoot length

Hussain et al. (2010)

Bothriochloa saccharoides a

Roots, stem, and leaves

Lactuca sativa, Zea mays, Eragrostis curvula, Paspalum guenoarum

Germination, root and shoot length

Scrivanti et al. (2011)

Bothriochloa springfieldii

Roots, stem, and leaves

Lactuca sativa, Zea mays, Eragrostis curvula, Paspalum guenoarum

Germination, root and shoot length

Scrivanti et al. (2011)

Cenchrus ciliaris a

Inflorescence, roots, stem, and leaves

Pennisetum americanum, Setaria italica, Lactuca sativa

Germination, root length

Hussain et al. (2010)

Cenchrus echinatus a

Shoot and roots

Panicum maximum, Amaranthus hypochondriacus, Physalis ixocarpa, Trifolium alexandrinum, Lolium perenne

Germination, root and shoot length

Nascimento et al. (2009)

Chloris gayana a

Leaves

Lactuca sativa

Germination

Chou and Young (1975)

Cynodon dactylon a

Shoot, roots, stem, and leaves

Ocimum basilicum, Portulaca oleracea, Triticum aestivum, Phaseolus vulgaris, Pisum sativum, Vicia faba, Thymus vulgaris, Melissa officinalis, Mentha spicata, Avena fatua, Sorghum halepense, Oryza sativa, Zea mays

Length and weight of coleoptile and root germination, dry and fresh weight

Golpavar et al. (2015); Mahmoodzadeh and Mahmoodzadeh (2013); Mahmoodzadeh and Mahmoodzadeh (2014); Novo et al. (2009)

Dactylis glomerata

Shoot

Phleum subulatum

Germination, root and shoot length

Scognamiglio et al. (2012)

Danthonia richardsonii

Leaves and stem

Trifolium subterraneum

Germination

Slater et al. (1996)

Digitaria decumbens a

Leaves

Lactuca sativa

Germination

Chou and Young (1975)

Festuca arundinacea a

Shoot

Lactuca sativa

Germination and hypocotyl length

Bertoldi et al. (2012)

Festuca paniculata

Leaves

Bromus erectus, Raphanus sativus, Lactuca sativa, Centaurea uniflora, Dactylis glomerata

Germination, dry mass of leaf and root

Mold (2005)

Festuca rubra

Shoot

Dactyilis glomerata, Lolium perenne, Poa pratensis

Protein content

Bostan et al. (2013)

Hordeum spontaneum a

Shoot and seeds

Triticum aestivum

Germination, dry and fresh mass of root and shoot

Hamidi et al. (2006)

Hordeum vulgare a

Leaves

Brassica juncea, Setaria viridis

Germination, root and shoot length

Asghari and Tewari (2007)

Imperata cylindrica a

Shoot, leaves, and roots

Andropogon arctatus, Aristida stricta, Lyonia ferruginea, Pinus elliottii, Echinochloa crus-galli, Cynodon dactylon

Shoot weight, germination, root and coleoptile length

Hagan et al. (2013); Koger and Bryson (2004)

Lolium rigidum a

Shoot, leaves, and roots

Triticum aestivum, Lolium multiflorum, Dactylis glomerata, Medicago sativa

Root and shoot length

Amini et al. (2009); Emeterio et al. (2004)

Melinis minutiflora a

Leaves

Lactuca sativa

Germination

Bomediano et al. (2013)

Merostachys multiramea a

Leaves

Araucaria angustifolia

Germination

Fernandes et al. (2007)

Merostachys pluriflora a

Leaves, stem, and rhizome

Lycopersicum esculentum, Oryza sativa

Germination and root and hypocotyl growth

Faria and Guaratini (2011)

Miscanthus transmorrisonensis

Leaves, stem, and roots

Lactuca sativa, Brassica oleracea, Festuca arundinacea, Lolium perenne

Germination and root and hypocotyl growth

Chou and Lee (1991); Ma et al. (2014)

Oryza sativa a

Shoot, glumes, and exocarp

Echinochloa crus-galli, Lactuca sativa, Triticum aestivum, Oryza sativa

Germination, dry mass

Jung et al. (2004)

Panicum maximum a

Shoot, leaves, and roots

Lactuca sativa, Leucaena leucocephala, Cajanus cajan e Sesbania sesban, Amaranthus viridis

Germination, germination speed index, root length, leaves chlorosis and necrosis

Chou and Young (1975); De Almeida et al. (2000); Santos et al. (2002)

Panicum virgatum a

Shoot and roots

Lolium perenne, Medicago sativa

Germination, root and coleoptile length

Shui et al. (2010)

Paspalum notatum b

Leaves, stem, and roots

Medicago sativa

Germination and seedling growth

Martin and Smith (1994)

Paspalum urvillei b

Leaves

Cucumis sativus, Solanum lycopersicum

dry mass, leaves number

Ishimine et al. (1987)

Pennisetum purpureum a

Leaves, shoot

Cyperus iria, Hedyotis verticillata, Leptochloa chinensis

Germination, root and shoot length, fresh mass

Tan et al. (2011); Zain et al. (2013)

Phleum pratense a

Pollen

Agropyron repens, Bromus inermis, Danthonia compressa, Poa compressa

Germination

Murphy and Aarssen (1995)

Phyllostachys edulis a

Shoot

Castanopsis sclerophylla, Cyclobalanopsis glaunca

Germination, root length

Bai et al. (2013)

Poa pratensis a

Leaves

Lolium perenne, Dactylis glomerata, Festuca rubra

Root and coleoptile length

Bostan et al. (2010)

Saccharum spontaneum a

Leaves, stem

Lactuca sativa

Germination

Tantiado and Saylo (2012)

Setaria faberi

Leaves, stem, and roots

Medicago sativa

Germination and seedling growth

Martin and Smith (1994)

Setaria glauca

Leaves, stem, and roots

Medicago sativa

Germination and seedling growth

Martin and Smith (1994)

Setaria viridis a

Leaves, stem, and roots

Medicago sativa

Germination and seedling growth

Martin and Smith (1994)

Vulpia bromoides

Shoot

Triticum aestivum

Germination, coleoptile length and seminal roots

An et al. (1996)

Vulpia myuros a

Shoot

Triticum aestivum

Germination, coleoptile length and seminal roots

An et al. (1996)

aSpecies present in Brazil

bSpecies native to Brazil

Despite the popular belief of several authors that scientific studies on allelopathy has been successful in recent years (Reigosa et al. 2013), most studies so far refer to the interaction between crops and weeds and only few to the grasses native to Brazil.

Among the genera studied, Bothriochloa stands out as the most studied in relation to the allelopathic effect of its species, for which seven works were found (Table 1). Allelopathy in species of this genus is attributed to the production and release of essential oils and richness in sesquiterpenes and monoterpenes (Scrivanti 2010).

3 Experimental conditions

3.1 Plant organs used to prepare extracts

We found that most of the studies have investigated the allelopathic properties of the leaves of the Poaceae species. Only a small minority investigated seeds, inflorescences, and pollen (Fig. 2). These data are in agreement with those reported by Reigosa et al. (2013), who investigated the works of allelopathy in Brazil. According to them, the preference for leaves may reflect the fact that it is certainly easier to collect leaves than other parts and that leaves represent a large part of the litter produced by the vegetation biomass that directly impacts the growth of the seedling.
Fig. 2

Plant organs used for the preparation of extracts in allelopathy studies of Poaceae species present in Brazil

The leaves are considered to be the most metabolically active organ of a plant and, therefore, it is reasonable that they present greater diversity of allelochemicals and, consequently, greater allelopathic effect (Ribeiro et al. 2009). However, it is known that allelochemicals can be produced in different organs of a plant, including the stems, roots, flowers, and seeds (Parvez et al. 2003; Weston and Duke 2003), with varying concentrations from one organ to another (Hong et al. 2004). However, for grasses, the evidence indicates that the aerial part, followed by the roots and seeds, are the main sources of potentially allelopathic substances (Souza Filho 1995).

In seed allelopathy, it is worth considering that the seeds of several forage grass that contain phytotoxic compounds may inhibit the germination of other seeds in their vicinity, compromising the germination and establishment of one or more species in the mixture, which in turn compromises the performance of the pasture (Souza Filho and Alves 1998).

3.2 Target species

The effect of grass extracts was tested in different target species, including lettuce (Lactuca sativa) (Table 2), followed by cultivated species such as maize (Zea mays), wheat (Triticum aestivum), and alfalfa (Medicago sativa). Lettuce is considered as a bioindicator plant and has been used in several allelopathy researches because it presents with rapid germination and uniform initial growth, which are desirable attributes for experiments that compare the effects of different treatments (Reigosa et al. 2013).
Table 2

Target species used in allelopathy studies of Poaceae species present in Brazil

Target species

Number

Percent

Lactuca sativa

19

15.08

Triticum aestivum

7

5.56

Zea mays

7

5.56

Medicago sativa

6

4.76

Eragrostis curvula

6

4.76

Paspalum guenoarum

6

4.76

Lolium perene

5

3.97

Oryza sativa

3

2.38

Vernonia polyanthes

3

2.38

Sida rhombifolia

3

2.38

Desmodium adscendens

3

2.38

Others (with fewer than 5 mentions)

58

46.03

Most of the past studies have evaluated the allelopathic effect of grasses on cultivated species, followed by native, forages, and invasive plants (Fig. 3). In the ecological context, once the allelopathy of a species is verified, this effect can be tested in species that live together in the field, as only then can the applicability of allelopathy and the interaction with neighboring plants be inferred. As pastures are constituted of several types of grasses, it is interesting to examine the allelopathic effect in other forage plants or in weeds.
Fig. 3

Classification according to the use of target species in Poaceae allelopathy bioassays

3.3 Evaluation of allelopathic effect

The most common physiological parameters used to identify the allelopathic effects of grasses were germination (41.35%), followed by the root length (27.89%) and shoot length (15.38%) (Table 3). Although germination is largely considered to be less sensitive to the presence of allelochemicals (Oliveira et al. 2012), it is the most commonly used attribute in evaluations of allelopathy. As for the vegetative structures, the allelopathic effect is most observed in the root system (Yamagushi et al. 2011). However, the allelopathic effect is often not evident in the germination process or during the initial growth of the seedlings; therefore, the evaluation of the appearance of abnormalities becomes a valuable tool to study allelopathy (Ferreira and Aquila 2000). However, of all the studies evaluated, only 0.96% studies analyzed the presence of abnormalities in the target species, which may have underestimated the allelopathic effect of the tested plants.
Table 3

Most commonly reported physiological effects in allelopathic studies conducted with Poaceae species present in Brazil

Effects

Number

Percent

Germination

43

41.35

Root length

29

27.89

Shoot length

16

15.38

Hypocotyl length

4

3.85

Coleoptile length

5

4.81

Dry mass of leave and root

6

5.77

Abnormalities (chlorosis and necrosis)

1

0.96

Most of the research reported so far has been conducted under laboratory conditions or under controlled conditions. Although such studies are important for isolating variables and identifying the true factors involved in plant interactions, there is a need for further studies to describe the allelopathic properties of plants under natural conditions.

Based on this requirement, the type of research on allelopathy can be divided into two main categories: (i) the one that follows the concepts of an ecological approach, corresponding to studies on phenomena occurring in natural ecosystems (allelopathy sensu stricto) and (ii) the other one that follows the criteria and commercial and economic interests corresponding to studies based on interactions between cultivated species that do not occur naturally in the same habitat (applied allelopathy). In the first category, preliminary or complementary laboratory studies could replicate, under controlled conditions, the expected effects of rain or dew on substance leaching, mimicking the events in natural environment. In fact, the species under study should coexist in the same habitat (Reigosa et al. 2013).

Due to the complexity of this kind of study, only limited studies have successfully “completed the cycle” or, in other words, have shown the production of a specific metabolite by the allelopathic (donor) plant, its journey through the environment (soil, water, or atmosphere), its arrival at the target, and its influence on the affected (recipient) plant (Reigosa et al. 2013).

4 Allelochemicals in Poaceae genera native to Brazil

For the successful application of allelopathic properties of a plant, the identification of allelochemicals is required (Bhadoria 2011). In this bibliographical survey review, only thirty (30) papers were found on the identification of allelochemicals in 23 genera and thirty (30) species of Poaceae present in Brazil (Table 4). Among the species studied, 22 occur in Brazil and only one is native to this country, namely, Merostachys riedeliana (Table 4).
Table 4

Allelochemicals in Poaceae species present in Brazil

Specie

Allelochemical

Reference

Andropogon nodosum

Syringic, vanillic, o-hydroxyphenyl acetic, ferulic, trans-p-coumaric, cis-p-coumaric, and o-coumaric acids

Chou and Young (1975)

Anthoxanthum odoratum

Coumarin

Yamamoto and Fugii (1997)

Arundo donax

Donaxine, donaxaridine, arundinine

Khuzhaev (2004)

Axonopus compressus

Alkaloids, saponins, tannins, flavonoids, terpenes

Bartholomew et al. (2013); Ogie-Odia et al. (2010)

Brachiaria brizantha

(6R,9R)-3-Oxo-α-ionol, (6R,9S)-3-oxo-α-ionol, 4-ketopinoresinol

Kato-Noguchi et al. (2014)

Brachiaria humidicola

p-Coumaric acid

Souza Filho et al. (2005)

Brachiaria mutica

Ferulic, 2,4-dihydroxybenzoic, vanillic, p-hydroxybenzoic, p-Hydroxyphenyl acetic, trans-p-coumaric, and cis-p-coumaric

Chou (1989); Chou and Young (1975)

Cenchrus ciliaris

Phenols, flavonoids, saponins, alkaloids

Kannan and Priyal (2015)

Chloris gayana

Ferulic, p-coumaric, syringic, vanillic, o-hydroxyphenyl acetic, p-hydroxyphenyl acetic, trans-p-coumaric, and cis-p-coumaric acids

Chou and Young (1975)

Cynodon dactylon

p-Coumaric, syringic, vanillic, o-hydroxyphenyl acetic, p-hydroxyphenyl acetic, trans-p-coumaric, and cis-p-coumaric acids; alkaloids; terpenoids; saponins; flavonoids; tannins

Chou and Young (1975); Abdullah et al. (2012)

Dactylis glomerata

Polygonocinol, 5-alkylresorcinols, 5-alkyl-2-methylresorcinols, 5-alkylresorcinol-3-methyl ethers, 5-eicosanoyl-2-methylresorcinol

Scognamiglio et al. (2012)

Digitaria decumbens

Ferulic, syringic, vanillic, p-hydroxyphenylacetic, trans-p-coumaric, and cis-p-coumaric acids

Chou and Young (1975)

Festuca arundinacea

E/Z-thesinine-O-40-α-rhamnoside, E/Z-thesinine, quercetin-3-O-xylosylglucoside, isorhamnetin 3-O-glucoside, quercetin 3-O-rutinoside, isorhamnetin 3-O-xylosylglucoside, kaempferol 3-O-rutinoside

Bertoldi et al. (2012)

Festuca paniculata

Caffeic and ferulic acids

Mold (2005)

Festuca rubra

N-Formyl loline, N-acetyl loline, ergovaline

Bostan et al. (2013)

Hemarthria altissima

Benzoic, phenylacetic, hydroxycinnamic, cinnamic, syringic, ferulic, and synaptic acids

Tang and Young (1982)

Hordeum vulgare

Gramine, hordenine, benzoic, caffeic, chlorogenic, m-coumaric, o-coumaric, p-coumaric, ferulic, synaptic, cinnamic, vanillic and gentisic acids, coumarin, apigenin, lutonarin, catechin, saponarin, cyanadin, isovitexin, heterodendrin, epidermin, sutherlandin, osmaronin, hordatine, DIBOA, butyronitrile

Hoult and Lovett (1993); Kremer and Ben-Hammouda (2009)

Imperata cylindrica

Gallic, caffeic, salicylic, synaptic, benzoic, cinnamic, ferulic, chlorogenic, linoleic, vanillic, p-coumaric, o-coumaric, gentisic, and p-hydroxybenzoic acids; emodin; resorcinol; 4-acethyl-2-methoxyphenol

Hagan et al. (2013); Xuan et al. (2009); Eussen and Niemann (1981)

Melinis minutiflora

1,8-Cineole, limonene, α-pinene

Mbuthia (1997)

Merostachys riedeliana a

p-Hydroxybenzoic, benzoic, benzeneacetic, 3,4-metylenedioxymandelic, salicylic, p-hydroxyphenylacetic, isovanillic, m-anisic, p-coumaric, protocatechuic, syringic, gallic, ferulic, m-coumaric, vanillylmandelic, and 4-metylmandelic acids; orientine; isovitexine

Torres et al. (2014)

Miscanthus sinensis

Caffeic, p-coumaric, and ferulic acids

Parveen et al. (2013)

Miscanthus sacchariflorus

Syringic, p-coumaric, ferulic, dihydroxybenzoic, and vanillic acids

Parveen et al. (2013)

Miscanthus transmorrisonensis

Caffeic, gallic, p-hydroxybenzoic, ferulic, m-hydroxybenzoic, and o-hydroxybenzoic acids; floridzine

Chou and Lee (1991)

Oryza sativa

Salicylic, p-coumaric, o-hydroxyphenyl acetic, syringic, ferulic, benzoic, p-hydroxybenzoic, octacosanoic, m-coumaric, and o-coumaric acids; hentriacontane; 1-tetratriacontanol; β-sitosterol; momilactone A; momilactone B; tricin; 3,7-dimethyl-n-octan-1-yl benzoate; β-sitosterol-3-O-β-D-glucoside; n-tritriacont-4,12-diene; n-pentacosane; stigmastanol-3beta-p-glyceroxydihydrocoumaroate; stigmastanol-3beta-p-butanoxydihydrocoumaroate; lanast-7; 9(11)-dien-3α,15α-diol-3α-D-glucofuranoside; 1-phenyl-2-hydroxy-3,7-dimethyl-11-aldehydictetradecane-2-β-D-glucopyranoside

Chung et al. (2015); Chung et al. (2006)

Panicum maximum

p-Hydroxyphenyl acetic, trans-p-coumaric, and cis-p-coumaric acids

Chou and Young (1975)

Setaria sphacelata

Ferulic, p-coumaric, syringic, vanillic, o-hydroxyphenyl acetic, and o-coumaric acids

Chou and Young (1975)

Setaria verticilllata

Alkaloids, flavonoids, saponins, tannins, terpenoides, phenols

Shivakoti et al. (2015)

Spartina alterniflora

Adipic acid, isohexyl methyl ester, hexadecanoic, dibutyl phthalato, and octadecanoic acids

Zheng et al. (2011)

Sporobolus pyramidalis

Ferulic and p-coumaric acids

Rasmussen and Rice (1971)

Vulpia myuros

Salicylic, benzoic, protocatechuic, succinic, 3,4-dymetoxyphenol, syringic, hydrocaffeic, p-hydroxybenzoic, vanillic, p-hydroxyphenyl acetic, gentisic, p-coumaric, ferulic, and hydrocinamic acids; coniferyl alcohol; hydroquinone; catechol

An et al. (2001)

aSpecie native to Brazil

Chemicals that establish allelopathic influence are called allelochemicals and they are divided into classes, viz., water-soluble organic acids; simple unsaturated lactones; long-chain fatty acids and polyacetylenes; naphthoquinones, anthraquinones, and complex quinines; simple phenols; benzoic acid and derivatives; cinnamic acid derivatives; coumarins; flavonoids; condensed and hydrolysable tannins; terpenoids and steroids; amino acids and polypeptides; alkaloids and cyanohydrins; sulphides and glycosides; and purines and nucleosides (Rice 1984). Although allelochemicals may belong to any of these classes, they generally belong to the terpenoids (Llusià et al. 1996), phenolic compounds (Li et al. 2010), and alkaloids (Levitt and Lovett 1985), which are mainly responsible for allelopathy (Trezzi 2002; Taiz and Zeiger 2013).

The allelochemicals present in the Poaceae are diverse, ranging from phenols to quinones. The most clearly identified compounds of these can be broadly divided into four groups: phenolic acids, hydroxamic acids, alkaloids, and quinones (Sánchez-Moreiras et al. 2004). In this review, despite the great diversity of compounds (Table 4), the main allelochemicals were found to belong to the group of phenolic acids, flavonoids, alkaloids, and terpenoids, with a predominance of phenolic acids (67%) (Fig. 4) probably due to the methodological facility adopted to identify these compounds.
Fig. 4

Allelochemicals identified in Poaceae species present in Brazil

The plant that releases allelochemicals is known as the donor plant, whereas the plant that is influenced by the release of the allelochemicals is termed as the target plant or a recipient plant (Inderjit and Duke 2003). The release of the allelochemicals by the donor plant can happen through leaching, volatilization, and decomposition of the plant material or by release from the roots (Bhadoria 2011).

From the release process of the allelochemical by the donor plant to the effect in the recipient plant, several factors can influence the allelopathic activity. However, for the optimal use of allelopathy under field conditions, the influence of environmental factors needs to be investigated. In this context, the soil factor can be said to be the most important (Bhadoria 2011).

Understanding the effect of the relationships as well as the release form of the allelochemicals is crucial for designing alternatives for possible applications of these compounds. The first step is to know the potential of the species as well as to identify the compounds responsible for allelopathy. In this sense, a positive aspect observed in the last decades was that there was an increase both in the number of studies related to Brazilian Poaceae allelopathy and in those that isolated and identified allelochemicals from these species. In a review of allelopathy surveys conducted in Brazil, Reigosa et al. (2013) reached the same conclusion, that is, the last two decades has witnessed a proliferation of studies on the allelopathic properties of species introduced or cultivated in Brazil. These authors reported an evident increase in the number of publications, attributing it to the growing interest not only in allelopathic interactions in natural ecosystems and agroecosystems but also in products that can be derived from allelochemicals, such as natural herbicides and growth regulators.

The studies referring to the simple allelopathic activity of Brazilian Poaceae outnumber those that identify the allelochemicals (Fig. 5) owing to the comparatively greater ease, practicality, and lower costs of operations involved. In addition, bioprospecting for secondary metabolites in plants requires prior knowledge of biochemistry and molecular signaling among organisms, making them lengthier and more difficult to execute.
Fig. 5

The number of articles published quoting the terms associated with allelopathic studies from Poaceae species present in Brazil

Although the search was made only for grasses present in Brazil, few of the works found in the survey performed the researches in this country. With respect to the allelopathy experiments, only 20% of the studies were performed in Brazil and a smaller percent (2%) of the allelochemical studies were developed in the country. This observation indicates that allelopathy in Brazil is an area of recent knowledge with much scope to expand.

5 Allelopathy and its applicability

Considering that Brazilian Poaceae can be found mainly in natural fields and cultivated pastures, it should be emphasized that allelopathy may play two extremely important roles in the pasture areas: (1) act as a management tool and (2) act as a supplier of basic structures for the production of bioherbicides (Souza Filho and Alves 1998).

Bioherbicides are environmentally safe alternatives, sources of new mechanisms of action, and have a structural diversity that has been attracting the attention of companies and researchers. Although research in the field of allelopathy, which aims at the search for bioherbicides, is only a recent process, some examples of natural compounds with potential use for weed control has already been established. For instance, in the case of Poaceae, the products 2-benzoxazolinone (BOA) and 6-methoxy-2,3-benzoxazolinone (MBOA) can be highlighted (Macías et al. 2007). In addition, we highlight sorgoleone—a lipid benzoquinone exuded from sorghum roots (Sorghum bicolor L.)—that reduces weed growth through its action on the PSII (Hejl and Koster 2004) by inhibiting the enzyme H+-ATPase in the roots. Sorgoleone affects the absorption of ions and the water balance of the plant, reducing its water absorption capacity (Soltys et al. 2013). It acts in a similar way to herbicides of the triazine class such as atrazine (Gniazdowska and Bogatek 2005).

On the other hand, allelopathy is important for the use of plants that control certain undesirable species (Resende et al. 2003). In this context, the identification of allelopathic forages and the knowledge of the mechanisms by which they exert their effects on the environment are of great importance as they provide a more adequate management of these plants in order to increase productivity and the persistence of pastures (Resende et al. 2003).

The reductions affected by forage grasses on the germination and development of the weeds assume an important aspect from the ecological perspective, because, with the decrease in the germination of the seeds, a reduction in the number of undesirable plants in the area were noted, thus reducing the competition power of these plants for water, light, and nutrients. Moreover, with the reduction in the development of the root system, the weeds have reduced their aggressive capacity. As a consequence of these two aspects, there is a greater possibility of establishing denser stands of desirable plants in cultivated pasture areas (Souza Filho and Alves 1998).

In the last few years, some studies involving the analysis of allelopathic activity have been developed with different species of forage grasses (Souza Filho et al. 2005). Studies involving forage grasses Brachiaria humidicola, Brachiaria decumbens, and Brachiaria brizantha cv. Marandu showed potentially allelopathic effects on the desmodium pastures (Desmodium adscendens), arrowleaf sida (Sida rhombifolia), and assa-fish (Vernonia polyanthes) (Souza Filho et al. 1997). The use of cover crops for the control of weeds is one of the earliest examples of the economic use of allelopathy. In addition to the suppressive effect of weeds, mulching has important effects on soil conservation and the maintenance of soil moisture (Medeiros 1989).

Considering these points, allelopathy assumes an important aspect from the point of view of pasture management as it allows not only the identification of forage species that can exert a certain level of control of certain undesirable species but also the establishment of grasses and legumes that are not strongly allelopathic to each other and which can compose more balanced pastures, with extremely favorable effects on their productivity and longevity (Wardle 1987). The difficulty in managing these two groups of physiologically different plants is one of the factors that prevent the establishment of intercropped pastures in several places across Brazil. Therefore, before recommending consortia with known species, it would be advisable to evaluate the allelopathic potential of the species considered (Rodrigues et al. 1992), considering that the allelopathic potential of the grasses can compromise the persistence of a legume in a consortium (Souza Filho and Alves 1998).

Another important role that allelopathy may play in terms of pasture management strategies and other crops is the possibility of obtaining pest- and disease-resistant species of plants. This bias opens up from the perspective of genetic transfer—through the manipulation of DNA—of this ability of a plant without major agronomic interests to a forage species of great interest to livestock, in which this characteristic was absent. The current phase of global research presents with practically no results in this regard. However, given the importance of this line of research, it is essential that studies be conducted in this sense (Souza Filho and Alves 1998).

The main problem in allelopathy works is to probe this phenomenon. It often happens due to the difficulty in separating allelopathy from competition. According to Duke (2015), most articles that claim to demonstrate allelopathy do not prove that it occurs. They only demonstrate that a crude extract of a plant species suspected to be allelopathic, or one or more compounds from such a plant, are phytotoxic in unrealistic bioassays that maximize the effects of the phytotoxin. This can be a first step in the proof of allelopathy, but all plants produce compounds that are weakly phytotoxic in simple bioassays conducted in the absence of soil. A successful demonstration of an allelopathic interaction has three components: (1) an ecological component—a demonstration that it exists in nature; (2) a chemical component—isolation, identification, and characterization of allelochemicals involved; and (3) a physiological component—identification of the interference mechanism at the biochemical, physiological, cellular, and molecular level (Inderjit and Weston 2000). Besides the difficulty of proving allelopathy, the studies that have been developed do not have an adequate standard methodology, which makes it difficult to compare them.

6 Conclusion

The allelopathic properties of Poaceae species present in Brazil are poorly studied. Moreover, most of the species described in studies as belonging to the genera native to Brazil are not actually native to the country. Most of the reported work was performed only under laboratory conditions with leaf extracts, using lettuce as a target plant and by evaluating simple growth characters such as germination. The number of papers that identified or isolated allelochemicals in Poaceae is lower than those that simply tested the allelopathic effect. Among the species studied, the great majority of identified allelochemicals belong to a group of phenolic acids. A fewer number of studies identified compounds responsible for allelopathy, reflecting the complexity and costs of this type of study.

Despite the increase in the number of studies on allelopathy in recent years, the fact that only a minority of these works have been performed in Brazil is worrisome as the information about the chemical composition and biological properties of native Poaceae is limited. Allelopathy is important to explain interactions both in the composition of natural ecosystems and in the interaction between cultivated and invasive plants. Therefore, to understand this phenomenon and to identify allelochemicals, it is fundamental to understand the natural behavior of plants and managed pastures, besides bioprospecting for allelochemicals with potential herbicide value. In addition, there is a need for further genetic and molecular studies of allelopathic plants toward increasing their protection against competitors as well as to identify allelopathic genes that can be used in transgeny.

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Copyright information

© INRA and Springer-Verlag France SAS, part of Springer Nature 2018

Authors and Affiliations

  • Adriana Favaretto
    • 1
    Email author
  • Simone M. Scheffer-Basso
    • 1
  • Naylor B. Perez
    • 2
  1. 1.Universidade de Passo FundoPasso FundoBrazil
  2. 2.Embrapa Pecuária SulBagéBrazil

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