Abstract
β-aminobutyric acid (BABA) has been known as an inducer of disease-resistance since 1963, however, only in the recent two decades an increasing number of reports have been published shedding light on its spectrum of activity, physiological impacts, and mode of action. BABA has been shown to protect about 40 plant species against about 80 pathogens and pests, including a virus, protista, bacteria, oomycetes, fungi, nematodes and arthropods. Interestingly, it is also active against abiotic stress and enhances salt, heat and drought tolerance in several plant species. Although generally regarded as a xenobiotic, there are a few reports that mention its occurrence in plants. BABA-treated plants react faster and in a more robust manner to a stress situation, a phenomenon that has been termed priming. 14C BABA is highly systemic, readily taken up by roots and leaves, and translocate both acropetally and basipetally. No metabolites of BABA are known. BABA is effective as a foliar spray, soil drench and seed treatment. Seeds derived from treated plants may produce primed progeny, making BABA the first agent with transgenerational efficacy. BABA induces numerous biochemical changes in treated plants. Among them are the induction of reactive oxygen species (ROS) and glycolate oxidase (GO) that are tightly linked to defense. ROS scavengers may alleviate the activity of BABA. Interestingly, only the R but not the S enantiomer of BABA primes for resistance. Unfortunately, BABA can also impose growth stress (and phytotoxicity) in some treated plants therefore BABA analogs with reduced stress effects are highly desirable for agricultural use.
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History
Lotan and Fluhr reported in 1990 (Lotan and Fluhr 1990) that application of DL-α-aminobutyric acid (AABA) to intact tobacco leaves gave comparable levels of elicitation of PR-proteins as achieved by TMV. We applied AABA to tobacco plants with the expectation that the induced PR proteins might protect against downy mildew caused by Peronospore tabacina. Since this was not the case, we tried the two other isomers of aminobutyric acid, DL-β-aminobutyric acid (BABA) and γ-aminobutyric acid (GABA). Surprisingly, BABA (but not GABA) provided excellent protection against downy mildew in tobacco and late blight in tomato caused by Phytophthora infestans with no adverse effect on spore germination on the leaf surface or penetration of the pathogen into the leaf epidermis (Cohen 1994a, b). BABA applied to tomato plants as a foliar spray induced PR proteins and provided 92 % protection against late blight. No activity was obtained with the isomers AABA, iso-AABA, iso-BABA, or GABA (Cohen 1994b). Additionally, BABA applied as a foliar spray, petiole dip, stem injection or soil drench to tobacco plants protected against downy mildew. Foliar spray induced PR protein accumulation but not the other modes of application. Interestingly, protection achieved by SA (sodium salicylate) or INA (2,6 dichloro-isonicotinic acid) was associated with PR-protein accumulation, regardless of the mode of application (Cohen 1994b).
Subsequent search of the literature revealed that Papavizas and Davey (1963) were the first to discover the activity of BABA against the root rot oomycete pathogen Aphanomyces euteiches. During the following 30 years, 1963–1994, no research was published on BABA. By 2016, a total of 147 papers were published (Fig. 1), including five review articles (Cohen 2001, 2002; Jakab et al. 2001; Piekna-Grochala and Kepczynska 2013; Baccelli and Mauch-Mani 2016) and three patents (Cohen 2000; Cohen et al. 2004; Oka et al. 2001) describing resistance induced by BABA against about 80 biotic and 6 abiotic stresses (Fig. 2; Table 1).
Number of published articles describing abiotic and biotic stresses against which BABA induces resistance
Number of articles published per year during 1958–2016 describing abiotic and biotic resistances induced by BABA
BABA induces resistance against numerous biotic and abiotic stresses
BABA induces resistance against a large variety of foliar, fruit and root pathogens as well as against abiotic stresses [drought, senescence, acid rain, cadmium, salt and heat (Table 1)]. It may be sprayed on leaf surfaces, injected into the stem, applied to fruits, drenched to the soil or applied to seeds. The mode of application may affect its efficacy and phytotoxicity.
BABA induces resistance against root and soil-borne pathogens (Chamsai et al. 2004; Li et al. 1996) but does not interfere with the colonization of tobacco roots with the arbuscular mycorrhizal (AM) fungus Glomus intraradices (David 1997) or of tomato roots with a mixture of five AM fungi (Luna et al. 2016).
BABA protects tomato and tobacco against late blight and downy mildew, respectively, even when applied 1- day post inoculation (Cohen 1994a, b). This seemed unusual at that time, since this finding did not fit the perception of classical SAR (systemic acquired resistance) that requires a lapse period of a few days between induction treatment and challenge inoculation. BABA induced resistance against downy mildew in lettuce, even when applied as late as 4 days’ post-inoculation (dpi) (Cohen et al. 2011).
BABA induces the formation of small necrotic lesions when applied at a high concentration to leaves of tobacco, tomato, and potato (Cohen 1994a, b, 2002). No such lesions are produced when BABA is injected to the stem, applied as stem dip or petiole dip, or drenched to the soil (Cohen 1994a, b). All modes of application induced resistance but only foliar spray induced PR proteins (Cohen 2002).
The use of 14C-BABA (kindly supplied by Syngenta, Basel, Switzerland) determined the relationship between translocation of BABA and resistance. It revealed that BABA moves in both directions in the plant. The level of protection against late blight was directly proportional to the amount of BABA translocated, suggesting that resistance depends on the actual presence of BABA in the leaf tissue (Cohen and Gisi 1994).
About 96 % of the 14C-BABA applied to 6-leaf tomato plants could be re-extracted after 6 days as pure BABA from the treated leaves (number 1–6) and from the newly-developed untreated leaves (number 7–8), suggesting that BABA was not metabolized (Cohen and Gisi 1994; Jakab et al. 2001). However, about 4 % of the label remained insoluble, bound to cell walls. This insoluble BABA was released by proteinase K, cellulase or pectinase, suggesting that it has incorporated into protein-carbohydrate complexes (Cohen and Gisi 1994). The oxygen burst induced by BABA (Cohen et al. 2011) may facilitate cross-linking of BABA to the cell wall matrix.
BABA isomers, enantiomers and derivatives
BABA is a unique inducer of plant defense. It is a simple, 4-carbon, non-protein amino acid with the formula CH3-CH-(NH2)-CH2-COOH. Unlike natural amino acids whose amino group resides on carbon 2 (α position), in BABA it resides on carbon 3 (β position). This carbon is chiralic, allowing for R and S enantiomers. BABA is the only isomer of aminobutyric acid capable of inducing plant resistance. Aminobutyric acids that carry the amino group at α or γ position are inactive. The iso isomers of AABA and BABA are inactive. The R and S enantiomers of BABA (kindly synthesized by Syngenta) were tested against Peronospora tabacina in tobacco (Cohen 1994a) and against Bremia lactucae in lettuce (Cohen et al. 2011). The R, but not the S, enantiomer was active, suggesting stereospecific binding to a receptor in the plant cell. Longer β-amino acids, with a backbone of 5, 6, 8 or 10 carbons, were ineffective in inducing resistance (Cohen 2000; Oka and Cohen 2001). Substitutions made in the amino group residing at the 3 (β) position of BABA hampered its activity, indicating specific binding of the amino group to its ligand. Acid salts of BABA were as effective as BABA in inducing resistance, suggesting hydrolysis of the molecule after uptake by the plant (Cohen 2000; Oka and Cohen 2001).
Natural occurrence of BABA
There are several reports in the literature that mention a natural occurrence of BABA. For example, it was found in Spanish wines (Barrado et al. 2009) and in root exudates of tomato plants grown in solarized soil (Gamliel and Katan 1992). Pfautsch et al. (2009) also reported its occurrence in the phloem and xylem exudates of Eucalyptus regnans, Acacia dealbata and Acacia melanoxylon.
Recently, Thevenet et al. (2016) reported on a reliable method to detect and quantify BABA in plant tissues using liquid chromatography-tandem mass spectrometry (LC-MS/MS) analysis. They showed that BABA is a natural product in Arabidopsis thaliana; Chinese cabbage (Brassica rapa), maize (Zea mays), teosinte (Zea mays ssp. mexicana) and wheat (Triticum aestivum) as well as in the moss Physcomitrella patens. Interestingly, the endogenous levels of BABA rapidly increase after infection with necrotrophic, biotrophic and hemibiotrophic pathogens, as well as after salt stress and submergence. BABA was also detected in leaves of tomato plants (Cohen, Gisi, Schalberger-Diethelm and Albrecht, unpublished data).
Activity against viruses and bacteria
BABA induces resistance against TMV in tobacco (Table 1). Csikász-Krizsics et al. (2013) reported that BABA induced resistance against the virus GLRaV1 in grapevines. No other viral diseases were reported to be affected by BABA. Whether this is due the lack of activity against other viruses or the lack of studies is not known.
BABA induces resistance against numerous bacterial diseases (Table 1) including Pseudomonas syringae pv. tomato in Arabidopsis (Zimmerli et al. 2000) and Ralstonia solanacearum in tomato (Fig. 3a) (Hassan and Abo-Elyousr 2013). Remarkably, BABA was recently reported to induce resistance against the HLB bacterial disease of citrus caused by Citrus huanglongbing (citrus greening), not reported to have a cure (Li et al. 2016). This may be due to the resistance BABA induces against the vector itself or the causal bacterium, the Asian citrus psyllid, Diaphorina citri (Tiwari et al. 2013). BABA exerted no direct toxic effect on nymphs or adult D. citri.
a Resistance against Ralstonia solanacearum induced in tomato by BABA (soil drench). b Resistance against Phytophthora infestans induced in tomato by BABA (stem dip). c The R enantiomer of BABA, but not the S enantiomer, induces resistance in tomato against Phytophthora infestans (drop application). d Post-infection (1dpi) resistance induced by BABA (petiole feeding) against Phytophthora infestans in detached tomato leaves. Note heavy sporulation in the control leaves and HR in the treated leaves. For UV microscopy, leaves were clarified with ethanol and stained with calcofluor. Bar = 50 μ
Activity against oomycetes
BABA did not affect sporangial germination, zoospore release, encystment or cyst germination of Phytophthora infestans on tomato leaf tissue, nor mycelial growth on agar media (Cohen 1994b). In tomato, stem dip (Fig. 3b) or foliar spray were more effective than soil drench in protecting against late blight. R-BABA induced HR in tomato leaves when inoculated with sporangia of P. infestans whereas S-BABA allowed for abundant sporulation of the pathogen (Fig. 3c). Tomato leaves fed with 0.25 mg BABA through the petiole produced an HR upon inoculation with P. infestans while similarly-inoculated control leaves allowed for abundant sporulation of the pathogen (Fig. 3d). BABA was effective against oomycetes in NahG transgenic plants suggesting independence on salicylic acid signaling (Cohen 2002; Zimmerli et al. 2000). However, resistance against late blight in potato failed to occur in NahG plants (Eschen-Lippold et al. 2010).
Grape leaves treated with BABA show complete inhibition of sporulation of Plasmopara viticola. This is associated with a massive lignin accumulation (Cohen et al. 1999; Cohen 2002). In grape leaf discs the MIC values for R-BABA, DL-BABA and S-BABA were 4, 16 and >>32 ppm, respectively. BABA controls grape downy mildew in the field as effectively as commercial fungicides (Reuveni et al. 2001). In addition to lignin accumulation, Hamiduzzaman et al. (2005) showed that BABA protects grapevine through the potentiation of callose formation and acts via jasmonic acid signaling. It has also been shown that stilbene phytoalexins are induced by BABA leading to the protection of grapevine against downy mildew (Slaughter et al. 2008).
BABA applied to cucumber plants at 1-day before inoculation with Pseudoperonospora cubensis induces the formation of minute chlorotic lesions (Fig. 4a, b). Sporangiophore emergenge and sporangial production are suppressed in a dose-dependent manner (Fig. 4c-i) suggesting a post-penetration inhibition of the pathogen (Ovadia et al. 2000). Resistance is associated with encasement of the haustoria with callose (Fig. 4j-l). BABA applied curatively, at 1-day post inoculation, is as effective against downy mildew as when applied 1 day prior to inoculation. Lignin accumulation is associated with resistance. Similar responses are observed in detached leaves of hop plants treated with BABA and inoculated with Pseudoperonospora humuli (Fig. 4m-o).
a, b Resistance induced by BABA (foliar spray, 1 day before inoculation) against Pseudoperonospora cubensis in intact cucumber plants. c BABA (foliar spray, 1 day before inoculation) suppresses sporulation of P. cubensis in intact cucumber plants in a dose-dependent manner. d-i Microscopic observation of the resistance induced by 125–2000 ppm BABA (foliar spray, 1 day before inoculation) against P. cubensis in intact cucumber plants. Bars = 100 μm. j-l BABA (foliar spray 500 ppm) induces callose encasement of haustoria (yellow fluorescence in k and l) of P. cubensis in cucumber leaves. Bar in j and k = 50 μm; in l = 20 μm. m-o Microscopic observation of the resistance induced by BABA (foliar spray, 1 day before inoculation) against Pseudoperonospora humuli in detached leaves of hop. Bar in m and n =100 μm and in o = 50 μm
BABA protects lettuce against the biotrophic oomycete Bremia lactucae (Pajot et al. 2001) (Fig. 5a, b). It has no effect on spore germination, appressoria formation or penetration into the epidermis. BABA restricts B. lactucae soon after penetration by encasing the primary and secondary vesicles with a heavy layer of callose which prevents further growth of the pathogen (Cohen et al. 2010) (Fig. 5c). DAB staining shows that inhibition is associated with H2O2 production in the penetrated epidermal cells (Fig. 5d). Elevated activity of peroxisomal glyolate oxidase (GO) was found responsible for H2O2 production and external application of catalase as a scavenger, alleviates the protection induced by BABA (Vaknin 2016). This confirms that H2O2 is associated with BABA-induced resistance in lettuce. BABA was effective against all the tested isolates of B. lactucae in lettuce (Cohen et al. 2010) (Fig. 5e).
Microscopic observation of the resistance induced by BABA against Bremia lactucae in detached leaves of lettuce. a Sporulation in a control leaf, bar = 50 μm. b No sporulation occurs in a treated leaf, bar = 50 μm. c Callose encasement (yellow fluorescence) of the primary and secondary vesicles of the pathogen inside the epidermal cell, bar = 20 μm. Basic aniline + calcofluor staining. d H2O2 accumulation (DAB staining) in a penetrated epidermal cell, bar = 20 μm. The Spore and germ-tube fluoresce blue. e BABA applied to perlite medium in Petri dishes induces resistance against different races of B.lactucae
BABA-IR in tomato against late blight and lettuce against downy mildew is enhanced when plants are incubated in continuous light (Cohen 1994b; Vaknin 2016). The enhanced photosynthesis is associated with an elevated production of H2O2. This enhanced activity of BABA is alleviated by the photosynthesis inhibitor DCMU (Vaknin 2016), confirming the pivotal role of glycolate oxidase (GO) in BABA-induced resistance. GO was shown by Taler et al. (2004) to control resistance against downy mildew in melon.
When applied after inoculation, BABA protects against B. lactucae by inducing a range of responses, depending on application time. Application at 1 or 2 day post inoculation induces HR in the penetrated cells while application at 3 or 4 day post inoculation induces necrosis of the developing mycelium and accumulation of red (methanol-insoluble) pigment in the mesophyll (Fig. 6a-d). In both cases no sporulation occurred. However, when applied at 5 dpi, 1 day before completion of the asexual life cycle, BABA failed to prevent sporulation of the pathogen on the 6th day post inoculation (Cohen et al. 2011). Race specific resistance against B. lactucae is associated with HR while BABA-induced resistance is associated with callose encasement of the primary vesicles, regardless of the race used (Cohen et al. 2010). Unlike cultivated lettuce that responds to BABA with H2O2 accumulation in penetrated cells, the wild immune lettuce species Lactucae saligna and Lactuca serriola do not permit spore germination and/or germ-tube penetration (Fig. 6e-g) (Vaknin 2016).
Post-infection (2–4 dpi) resistance induced by BABA against Bremia lactucae in intact lettuce plants. a Heavy sporulation occurs in the control leaves. b HR develops in leaves treated with BABA at 2 dpi. c, d Necrotic hyphae are seen in leaves treated with BABA at 3dpi and 4 dpi. e-g Resistance induced by BABA in Lactuca sativa against B.lactucae is associated with H2O2 accumulation but not in the genetically-resistant wild lettuce Lactuca saligna. Bars = 20 μm
Activity against basidiomycetes
Sunflower plants sprayed with BABA are protected against rust caused by Puccinia helianthi (Amzalek and Cohen 2007) (Fig. 7a, b). BABA protects pea against rust (Uromyces pisi) by enhancing phytoalexin production (Barilli et al. 2015). Marcucci et al. (2010) reported that foliar spray or soil drench with BABA induced a high level of resistance against the necrotrophic fungal pathogen Sclerotinia sclerotiorum in artichoke plantlets. BABA applied to potted lettuce plants or to detached cotyledons of lettuce, protects against S. sclerotiorum (Fig. 7c, d) but does not affect its growth on agar medium (Vaknin 2016).
Resistance induced by BABA (foliar spray, 1 day before inoculation) against Puccinia helianthi in intact sunflower plants (a) and in floating leaf discs (b). c, d BABA applied to the soil or dropped onto detached cotyledon leaves protects lettuce against Sclerotinia sclerotiorum. e BABA injected to apple fruits protects against Alternaria alternata apple type. f The fungicide Score is fully inhibitory at 5 ppm against the pathogen in vitro. g BABA at 2000 ppm has no effect on the growth of the pathogen in vitro. h-i BABA applied to the soil protects wheat against the root knot nematode Meloidogyne marylandi. Nematode galls in the control roots stain red
Activity against ascomycetes
In the field BABA effectively protects apples from moldy-core decay (Reuveni et al. 2003) and from blotch caused by Alternaria alternata apple type (Gur et al. 2013) (Fig. 7e). No inhibition of this fungus was induced by BABA in vitro (Gur 2013) (Fig. 7f, g). BABA performed in the field as effectively as the recommended commercial fungicides against both apple diseases (Gur et al. 2013; Reuveni et al. 2003). BABA induced resistance against Alternaria brassicae in Brassica juncea (Kamble et al. 2013) and Verticillium longisporum in Brassica napus (Kamble et al. 2013). Several papers report the control of Botrytis cinerea with BABA (Zimmerli et al. 2001; Maymoune et al. 2015; Luna et al. 2016). Koen et al. (2014) showed that the protective effect induced by BABA against B. cinerea is mimicked by Fe deficiency. Wang et al. (2016) showed direct inhibition of B. cinerea at BABA of >1000 ppm. They immersed strawberry fruits in BABA for 15 min and then wound-inoculated them with B. cinerea. Fruits induced for resistance exhibited higher sucrose, fructose and glucose contents, sweetness index and sensory scores. Direct toxicity of BABA to B. cinerea in culture was also reported by Fischer et al. (2009). Vogt and Buchenauer (1997) showed that BABA protects cucumber from powdery mildew and Zeighaminejad et al. (2016) confirmed it in squash. Walz and Simon (2009) showed protection of cucumber against the biotroph P. cubensis and the necrotroph Colletotrichum lagenarium.
Activity against nematodes
Oka and associates were the first to show that BABA applied as a foliar spray or root drench protects cucumber and tomato against the root knot nematode Meloidogyne javanicum (Oka and Cohen 2001; Oka et al. 1999) and wheat against the root knot nematode Meloidogyne marylandi (Oka and Cohen 2001) (Fig. 7h, i). 14C-BABA applied to nematode-inoculated cucumber plants was shown to translocate from the treated leaves into the nematode galls (Oka et al. 1999).
BABA applied as a soil drench protects tomato against M. ingognita (Anter et al. 2014). Fatemy et al. (2012) showed that seed treatment with BABA is effective against M. javanicum in tomato. Ahmed et al. (2009) reported efficacy of BABA against M.javanica in mung bean. Mongae and Moleleki (2015) showed efficacy of BABA in protecting potato from the disease complex exerted by Meloidogyne incognita and Pectobacterium carotovorum subsp. brasiliense (Pcb). Sahebani and Hadavi (2009) concluded that the protection BABA provided to tomato against M. javanica resulted from ROS production by the enzymes SOD and POX.
Ji et al. (2015) showed that BABA induces resistance in rice against the root knot nematode M. graminicola while having no direct toxicity against the nematode. BABA applied to rice plants inhibits nematode penetration and results in delayed nematode and giant cell development. BABA-induced resistance is still functional in mutants or transgenic plants defective in salicylic acid biosynthesis and or abscisic acid (ABA) response. Pharmacological inhibition of jasmonic acid (JA) and ethylene (ET) biosynthesis indicated that BABA-IR against rice M. graminicola is independent of JA and ET. Protection resulted from the activation of basal defense mechanisms such as ROS accumulation, lignin formation, and callose deposition.
Activity against insects
Hodge et al. (2005) were the first to show that BABA induces resistance against insects. When applied as a root drench to six legume plant species it reduced the performance of the pea aphid Acyrthosiphon pisum. When applied to Brassicaceae plants, BABA suppressed the growth of the phloem-feeding insects Myzus persicae and Brevicoryne brassicae as well as chewing insects Trichoplusia ni and Plutella xylostella (Hodge et al. 2006). Tiwari et al. (2013) reported that BABA induced citrus resistance to the Asian citrus psyllid, Diaphorina citri the vector of Citrus Greening. They found no direct toxicity of BABA to this insect in leaf-dipping bioassays. BABA effectively protected soybean from Aphis glycines (Zhong et al. 2014). In contrast, Cao et al. (2014) reported that resistance of wheat to the grain aphid Sitobion avenae resulted from direct toxicity of BABA. Sitobion avenae growth rates were also reduced on artificial diet containing BABA. Philippe et al. (2016) showed that BABA protected apples against the rosy apple aphid Dysahis plantaginea with no direct toxicity to the aphid.
Seed treatment with BABA
Stirring seeds of pearl millet for 6 h in BABA of 50 mM protected emerging seedlings by up to 75 % from downy mildew caused by Sclerospora graminicola without affecting seed germination or seedling vigor (Shailasree et al. 2001). Downy mildew in BABA-protected plants was reduced by 90 % relative to control plants. Such seed treatment was long-lasting, effective against S. graminicola during the vegetative and reproductive growth periods of the plant.
In a later study, Shailasree et al. (2007) showed a close association between BABA-induced protection and increased accumulation of defense-related proteins such as phenylalanine ammonia lyase, peroxidase, β-1,3-glucanase and cell wall hydroxyproline-rich glycoproteins. Melvin et al. (2015) and Shailasree and Melvin (2015) suggested that BABA-induced resistance in pearl millet is a JA/SA mediated phenomenon. By using a proteomic approach Anup et al. (2015) revealed that the majority of the 63 differentially accumulated proteins in pearl millet seeds that were treated with BABA and inoculated with S. graminicola were associated with energy and metabolism, followed by stress and defense proteins. The over-representation of proteins pertaining to glucose metabolism suggested that seed priming ensures plant protection against disease without compromising its normal growth and development.
BABA seed priming improves drought and salinity stress tolerance potential of Vigna radiate (Jisha and Puthur 2016). These authors showed that BABA increases photosynthetic pigment content and photosynthetic and mitochondrial activities. Moreover, BABA seed priming reduces malondialdehyde content in the seedlings and enhances the accumulation of proline, total protein, total carbohydrate, nitrate reductase activity, and activities of antioxidant enzymes such as peroxidase and superoxide dismutase.
Worrall et al. (2012) showed that BABA seed treatment provided an 8 week-primed defense period against powdery mildew caused by Oidium neolycopersici. Priming responses are associated with enhanced defense gene expression during pathogen attack. No significant antagonism was seen between different forms of defense in plants grown from seeds treated with a combination of JA and BABA. Long-term defense priming by seed treatment is not accompanied by reductions in growth, and may therefore be suitable for commercial exploitation (Shailasree et al. 2001).
Luna et al. (2016) germinated tomato seeds for 1 week in BABA formulated in carboxy-methyl cellulose. Such treatment promotes seed germination efficiency, does not affect plant growth, does not affect colonization with arbuscular-mycorrhizal fungi and induces resistance against Botrytis cinerea in 4-week-old plants.
Mostek et al. (2016) soaked barley seeds in BABA for 24 h and thereafter allowed the seeds to germinate under salt stress conditions for 7 days. BABA induced the up-regulation of antioxidant enzymes (catalase, peroxidase and superoxide dismutase), PR proteins (chitinase, endo-1,3-β-glucosidase) and chaperones (cyclophilin, HSC 70). BABA induces defense and detoxification processes that may enable faster and more effective responses to salt stress, increasing the chances of plant survival under adverse environmental conditions.
The long-term protection against biotic and abiotic stresses induced by seed treatment is not derived from the actual presence of BABA in the tissues of the emerging plants but rather from a new physiological state primed by BABA.
Combination with other compounds
In field experiments, Cohen (2002) found that BABA provided significant control of late blight of potato. Baider and Cohen (2003) reported that using a mixture of BABA and mancozeb was significantly more effective in controlling late blight in potato and downy mildew in cucumber compared to BABA or mancozeb alone. Mixtures made of BABA and one or two anti-oomycete fungicides exhibited synergistic activity against late blight in potato, downy mildew in grapes and downy mildew in tobacco (Baider and Cohen 2003; Cohen et al. 1999). Liljeroth et al. (2010) showed that BABA used together with a reduced fungicide dose in the field gave the same level of late blight control as a full dose of the standard fungicide treatment. Walters et al. (2014) used a combination of three elicitors: BABA, Bion and cis-jasmonate with fungicides for the control of two barley diseases caused by Blumeria graminis f.sp. hordei and Rynchosporium commune in the field. They found that such combination provided disease control and increased yields which were equal to, and in some cases better than, that provided by the best fungicide treatment alone.
Plant stress induced by BABA
BABA applied to Arabidopsis caused female sterility due to accumulation of callose in the pistil (Jakab et al. 2001). Arabidopsis root growth is inhibited by BABA but this inhibition is alleviated by L-glutamine (Wu et al. 2010). Soil drench with BABA to 5-day Arabidopsis seedlings reduced their mass by about 60 %. However, the weight was recovered when plants were transplanted to BABA-free soil (Luna et al. 2014b). In tomato, three sprays of BABA applied to flowering plants in the field at weekly intervals resulted in a strong reduction in fruit set (Vaknin 2016). Lettuce seedlings growing on BABA-amended agar medium showed reduced growth of the main root (Fig. 8). Root growth was not restored by L-glutamine (Vaknin 2016).
The adverse effect of BABA, applied to agar medium at various doses (7.8-1000 ppm), on growth of lettuce seedlings
Luna et al. (2016) showed that BABA applied to tomato seedlings as a root drench repressed plant growth whereas seed treatment did not. Kim et al. (2013) observed that treatment of kimchi cabbage seedlings with BABA protected against Alternaria brassicicola and Colletotrichum higginsianum but significantly reduced primary root elongation and cotyledon development. BABA does not inhibit spore germination nor mycelial growth of either fungus in vitro.
Other reports showed a positive effect of BABA on yield. BABA improved tuber late blight resistance (Olivieri et al. 2009) but the degree of reduction in disease severity depended on the basic level of resistance in each cultivar. Four foliar applications of BABA increased amounts of tubers per plant and total dry matter of tubers in both the moderately resistant and the highly susceptible cultivars. Four weekly sprays of BABA applied to Carignan grapevines during flowering had no effect on yield or sugar content compared to control untreated trees (Cohen, unpublished results). According to Luna et al. (2014b) stress and defense induced by BABA are controlled by different pathways and therefore can be separated.
Toxicity to mice
BABA added to the drinking water (10 mM) of mice had no effect on their behavior during an experimental period of 4 weeks. BABA was secreted in their urine but was not detected in their brains (Y. Buganim, M. Bitton and Y. Cohen, unpublished data). These findings may encourage further studies to enable registration of BABA for agro use.
Physiological and molecular changes induced by BABA
In Arabidopsis BABA-triggered resistance to pests is associated with a major metabolic shift that includes pipecolic acid (PA) accumulation. PA is considered a critical endogenous signal for priming (Conrath et al. 2015). BABA significantly increased anthocyanin content of purple basil and its potential anti-inflammatory activity (Zlotek et al. 2015). BABA delayed senescence of sweet cherry fruits (Wang et al. 2015) due to depressed membrane permeability and malondialdehyde content, reduced activities of polygalacturonase and pectinmethylesterase, enhanced cell-wall polysaccharide content, and integrated sub epidermal cell structure. Wang et al. (2016) showed that treating strawberry fruits with BABA enhanced activity of sucrose phosphate synthase, sucrose-6-phosphate phosphatase and sucrose synthase, thus increasing sweetness of the fruits.
Sos-Hegedus et al. (2014) reported that BABA increased drought tolerance of potato. Burra et al. (2014) compared the transcriptomes induced in potato foliage by phosphite and BABA. Phosphite treatment triggered induced resistance responses at the transcriptomic level similar to that induced by BABA treatments.
Maymoune et al. (2015) provided evidence that prior exposure of tomato plants to abiotic stress (leaf wounding, water stress or nitrogen deficiency) altered the protection efficacy of BABA (and other elicitors) against B. cinerea, suggesting an antagonistic interaction between the tomato responses to abiotic stresses and BABA treatment.
BABA-treated citrus plants are characterized by significantly lower levels of iron, magnesium, phosphorus, sodium, sulphur and zinc as compared with control plants (Tiwari et al. 2013). Koen et al. (2014) showed that BABA chelates iron in vivo. They believed that Fe deficiency response caused by BABA could induce the plant to a defense ready state participating in plant resistance against the pathogens.
Molecular genetic aspects of BABA-induced resistance
Involvement of various defense pathways
By testing various defense mutants of Arabidopsis for their ability to express BABA-IR (induced resistance), it became clear that BABA-IR is not controlled by a single defense signaling pathway but by various ones, depending on the type of stress applied. For example, BABA-IR against the bacterial pathogen Pseudomonas syringae pv. tomato DC3000 and the fungal pathogen B. cinerea resembling pathogen-induced SAR, in that it requires endogenous accumulation of SA and a functional NPR1/NIM1 protein (Zimmerli et al. 2000; Zimmerli et al. 2001). BABA-IR against P. infestans in potato (Eschen-Lippold et al. 2010) and TMV infection in tobacco (Siegrist et al. 2000) has also been shown to depend on a functional SA-signaling pathway. For the protection of grapevine against downy mildew, the JA-pathway is of importance. Here, BABA treatment leads to the potentiation of JA-regulated genes such as LOX-9 and PR-4 (Hamiduzzaman et al. 2005). In drought-stressed potato pre-treated with BABA, the ethylene receptor ETR1 was expressed longer than in the corresponding controls, suggesting an involvement of the ethylene-defense pathway (Sos-Hegedus et al. 2014).
BABA-IR against Hyaloperonospora arabidopsidis, as well as the necrotrophic fungi Alternaria brassicicola and Plectosphaerella cucumerina, is fully functional in Arabidopsis genotypes impaired in SA-, JA-, and ET-dependent signaling (Zimmerli et al. 2000; Ton and Mauch-Mani 2004), whereas mutants affected in the production or sensitivity to the abiotic stress hormone abscisic acid (ABA) are unable to express BABA-IR against P. cucumerina (Ton and Mauch-Mani 2004). Similarly, BABA-induced protection against drought and salt stress is unaffected in genotypes affected in SA-, JA-, and ET-dependent signaling pathways, but blocked in genotypes impaired in ABA signaling (Jakab et al. 2005). Hence, BABA-IR functions through different defense pathways, depending on the stress applied.
Priming
BABA-IR is tightly associated with primed expression of defense mechanisms. BABA-IR against P. syringae pv. tomato and B. cinerea coincides with primed transcription of the SA-inducible PR-1 gene (Zimmerli et al. 2000, 2001). In contrast, BABA-IR against H. arabidopsidis, P. cucumerina, as well as against A. brassicicola, was found to correlate with primed accumulation of callose-containing papillae at the sites of infection (Ton and Mauch-Mani 2004) and such primed callose deposition is controlled by an ABA-dependent pathway, since ABA signaling mutants do not develop BABA-IR against P. cucumerina and concomitantly fail to express primed callose accumulation (Flors et al. 2008). ABA has also been implicated in the priming of defense during BABA-induced protection against osmotic stress. BABA-treated Arabidopsis showed a faster and higher induction of ABA-inducible marker genes upon salt stress (Jakab et al. 2005).
A screen to select Arabidopsis mutants that are impaired in BABA responsiveness (Toquin et al. 2002) yielded several ibs (impaired in BABA-induced sterility) mutants impaired in priming (Ton et al. 2005). Using subtraction suppression hybridization, a BABA-inducible gene, PRLIP1, was isolated and characterized. The predicted PRLIP1 amino acid sequence has regions of similarity to Ser hydrolases (eukaryotic lipases and esterases) similar to PAD4 (Jirage et al. 1999) and EDS1 (Falk et al. 1999). The expression profile of this lipase-like gene family has been described (Jakab et al. 2003) and it was shown to be primed in grapevine during defense against powdery mildew (Szalontai et al. 2012).
The BABA receptor
The stereospecific mode of action of BABA (see above) has long hinted to the presence of a specific receptor for this molecule. Such a receptor has been recently suggested in the form of an aspartyl-tRNA synthetase (Luna et al. 2014b). The receptor was identified in a screen of A. thaliana mutants impaired in BABA-induced immunity that yielded the mutant ibi1. Binding of R-BABA to the IBI1 protein leads to priming for non-canonical defense signaling upon pathogen attack.
Transgenerational inheritance of BABA priming
Research on the duration of BABA-IR over time revealed that the primed state in Arabidopsis thaliana is still functional in the next generation without additional treatment. When comparing the reactions of Arabidopsis plants that had been either primed with BABA or treated with water alone, it became apparent that the descendants of primed plants reacted much faster to inoculation with virulent Pseudomonads. Subjecting trans-generationally BABA-primed plants to an additional BABA-priming treatment leads to an even enhanced primed phenotype in their descendants (Slaughter et al. 2012). Interestingly, transgenerational inheritance of BABA-priming has also been observed in the weed Solanum physalifolium expressed as late blight resistance (Lankinen et al. 2016). Current evidence concerning the functioning of transgenerational priming points to epigenetic mechanisms (Luna et al. 2012).
Summary
BABA is a unique β-amino acid with major effects on plant physiology. It appears only rarely in nature. BABA moves systemically in the plant and induces resistance against soil borne, foliar and fruit pathogens belonging to different kingdoms. It also induces resistance against abiotic stresses. Of all the isomers of aminobutyric acid, BABA is the only active molecule, and of the two enantiomers, R-BABA is active. BABA is the only priming agent with long-lasting efficacy capable of causing also trans-generation resistance. It binds to a specific target in the plant cell, aspartyl-tRNA synthetase. The agro industry is seeking to develop new innovative products, such as BABA, for plant defense based on induced resistance.
References
Ahmed, N., Abbasi, M. W., Shaukat, S. S., & Zaki, M. J. (2009). Induced systemic resistance in mung bean plant against root-knot nematode Meloidogyne javanica by dl-β-amino butyric acid. Nematologia Mediterranea, 37, 67–72.
Altamiranda, E. A. G., Andreu, A. B., Daleo, G. R., & Olivieri, F. P. (2008). Effect of β-aminobutyric acid (BABA) on protection against Phytophthora infestans throughout the potato crop cycle. Australasian Plant Pathology, 37(4), 421–427. doi:10.1071/ap08033.
Amzalek, E., & Cohen, Y. (2007). Comparative efficacy of systemic acquired resistance-inducing compounds against rust infection in sunflower plants. Phytopathology, 97(2), 179–186. doi:10.1094/phyto-97-2-0179.
Andreu, A. B., Guevara, M. G., Wolski, E. A., Daleol, G. R., & Caldiz, D. O. (2006). Enhancement of natural disease resistance in potatoes by chemicals. Pest Management Science, 62(2), 162–170.
Anter, A. A., Amin, A. W., Ashoub, A. H., & El-Nuby, A. S. (2014). Evaluation of some chemical substances as inducers for tomato resistance against root-knot nematode, Meloidogyne incognita. Egyptian Journal of Agronematology, 13, 124–145.
Anup, C. P., Melvin, P., Shilpa, N., Gandhi, M. N., Jadhav, M., Ali, H., et al. (2015). Proteomic analysis of elicitation of downy mildew disease resistance in pearl millet by seed priming with β-aminobutyric acid and Pseudomonas fluorescens. Journal of Proteomics, 120, 58–74. doi:10.1016/j.jprot.2015.02.013.
Baccelli, I., & Mauch-Mani, B. (2016). β -aminobutyric acid priming of plant defense: the role of ABA and other hormones. Plant Molecular Biology, 91(6), 703–711. doi:10.1007/s11103-015-0406-y.
Baider, A., & Cohen, Y. (2003). Synergistic interaction between BABA and mancozeb in controlling Phytophthora infestans in potato and tomato and Pseudoperonospora cubensis in cucumber. Phytoparasitica, 31(4), 399–409.
Barilli, E., Sillero, J. C., & Rubiales, D. (2010). Induction of systemic acquired resistance in pea against rust (Uromyces pisi) by exogenous application of biotic and abiotici nducers. Journal of Phytopathology, 158(1), 30–34. doi:10.1111/j.1439-0434.2009.01571.x.
Barilli, E., Rubiales, D., Amalfitano, C., Evidente, A., & Prats, E. (2015). BTH and BABA induce resistance in pea against rust (Uromyces pisi) involving differential phytoalexin accumulation. Planta, 242(5), 1095–1106. doi:10.1007/s00425-015-2339-8.
Barrado, E., Rodriguez, J. A., & Castrillejo, Y. (2009). Determination of primary amino acids in wines by high performance liquid magneto-chromatography. Talanta, 78(3), 672–675. doi:10.1016/j.talanta.2008.12.023.
Baysal, O., Ziya Gursoy, Y., Ornek, H., & Duru, A. (2005). Induction of oxidants in tomato leaves with DL- β-aminobutyric acid (BABA) and infected with Clavibacter michiganensis subp. michiganensis. European Journal of Plant Pathology, 112, 361–369.
Baysal, O., Gursoy, Y. Z., Ornek, H., Cetinel, B., & da Silva, J. A. T. (2007). Enhanced systemic resistance to bacterial speck disease caused by Pseudomonas syringae pv. tomato by DL- β -aminobutyric acid under salt stress. Physiologia Plantarum, 129(3), 493–506.
Bengtsson, T., Weighill, D., Proux-Wera, E., Levander, F., Resjo, S., Burra, D. D., et al. (2014). Proteomics and transcriptomics of the BABA-induced resistance response in potato using a novel functional annotation approach. Bmc Genomics, 15. doi:10.1186/1471-2164-15-315.
Burra, D. D., Berkowitz, O., Hedley, P. E., Morris, J., Resjo, S., Levander, F., et al. (2014). Phosphite-induced changes of the transcriptome and secretome in Solanum tuberosum leading to resistance against Phytophthora infestans. Bmc Plant Biology, 14. doi:10.1186/s12870-014-0254-y.
Cao, S. Q., Ren, G., Jiang, L., Yuan, H. B., & Ma, G. H. (2009). The role of β-aminobutyric acid in enhancing cadmium tolerance in Arabidopsis thaliana. Russian Journal of Plant Physiology, 56(4), 575–579. doi:10.1134/s1021443709040190.
Cao, J. K., Yan, J. Q., Zhao, Y. M., & Jiang, W. B. (2013). Effects of four pre-harvest foliar sprays with β-aminobutyric acid or salicylic acid on the incidence of post-harvest disease and induced defence responses in jujube (Zizyphus jujuba Mill.) fruit after storage. Journal of Horticultural Science & Biotechnology, 88(3), 338–344.
Cao, H. H., Zhang, M., Zhao, H., Zhang, Y., Wang, X. X., Guo, S. S., et al. (2014). Deciphering the mechanism of β-aminobutyric acid-Induced resistance in wheat to the grain aphid, Sitobion avenae. Plos One, 9(3). doi:10.1371/journal.pone.0091768.
Castaño Monsalve, J., Ramirez Gil, J. G., Patino Hoyos, L. F., & Gonzalo Morales Osorio, J. (2015). Management alternative for Phytophthora infestans (Mont.) de Bary in Solanum betaceun Cav. mediante by resistance inducers. Revista de Proteccion Vegetal, 30, 204–212.
Chamsai, J., Buchenauer, H., Orober, M., & Siegrist, J. (1998). DL-3-aminobutyric acid induces localized cell death, salicylic acid, PR proteins and resistance in tomato and tobacco. In Aussois, France, 1998: 5th International Workshop on Pathogenesis-Related Proteins in Plants Signaling Pathways and Biological Activities.
Chamsai, J., Siegrist, J., & Buchenauer, H. (2004). Mode of action of the resistance-inducing 3-aminobutyric acid in tomato roots against Fusarium wilt. Zeitschrift fur Pflanzenkrankheiten und Pflanzenschutz-Journal of Plant Diseases and Protection, 111(3), 273–291.
Chavan, V., & Kamble, A. (2014). Induction of total phenolics and defence-related enzymes during β-aminobutyric acid-induced resistance in Brassica carinata against Alternaria blight. Archives of Phytopathology and Plant Protection, 47, 2200–2212.
Chinnasri, B., Sipes, B. S., & Schmitt, D. P. (2006). Effects of inducers of systemic acquired resistance on reproduction of Meloidogyne javanica and Rotylenchulus reniformis in pineapple. Journal of Nematology, 38(3), 319–325.
Cohen, Y. (1994a). 3-Aminobutyric acid induces systemic resistance against Peronospora tabacina Physiol. Molecular Plant Pathology, 44, 273–288.
Cohen, Y. (1994b). Local and systemic control of Phytophthora infestans in tomato plants by DL-3-amino-n-butanoic acids. Phytopathology, 84, 55–59.
Cohen, Y. (2000). Methods for protecting plants from fungal infection. US Patent 6,075,051.
Cohen, Y. (2001). The BABA story of induced resistance. Phytoparasitica, 29(5), 375–378.
Cohen, Y. (2002). β-aminobutyric acid-induced resistance against plant pathogens. Plant Disease, 86, 448–457.
Cohen, Y., & Gisi, U. (1994). Systemic translocation of 14C-DL-3-aminobutyric acid in tomato plants in relation to induced resistance against Phytophthora infestans. Physiological Molecular Plant Pathology, 45, 441–456.
Cohen, Y., Niderman, T., Mosinger, E., & Fluhr, R. (1994). β-aminobutyric acid induces the accumulation of pathogenesis-related proteins in tomato (Lycopersicon esculentum Mill.) plants and resistance to late blight infection caused by Phytophthora infestans. Plant Physiology, 104, 59–66.
Cohen, Y., Reuveni, M., & Baider, A. (1999). Local and systemic activity of BABA (DL-3-aminobutyric acid) against Plasmopara viticola in grapevines. European Journal of Plant Pathology, 105, 351–361.
Cohen, Y., Korat, M., & Zvi-Tov, D. (2004). Method to protect plants from fungal infection. US Patent 6,692,774 B2.
Cohen, Y., Baider, A., Gotlieb, D., & Rubin, A. E. (2007). Control of Bremia lactucae in field-grown lettuce by DL-3-amino-n-butanoic acid (BABA). In U. Niggli, C. Leifert, T. Alfoldi, L. Luck, & H. Willer (Eds.), Improving sustainability in organic and low input food production systems. University of Hohenheim, Germany: Proc. 3rd Intn. Cong. European integrated project ‘Quality Low Input Food’ (QLIF).
Cohen, Y., Rubin, A. E., & Kilfin, G. (2010). Mechanisms of induced resistance in lettuce against Bremia lactucae by DL-β-amino-butyric acid (BABA). European Journal of Plant Pathology, 126(4), 553–573. doi:10.1007/s10658-009-9564-6.
Cohen, Y., Rubin, A. E., & Vaknin, M. (2011). Post infection application of DL-3-amino-butyric acid (BABA) induces multiple forms of resistance against Bremia lactucae in lettuce. European Journal of Plant Pathology, 130(1), 13–27. doi:10.1007/s10658-010-9724-8.
Cohen, Y., Vaknin, M., & Ben Naim, Y. (2015). Chemical control of downy mildew in basil caused by Peronospora belbahrii. Phytoparasitica, 43, 381.
Conrath, U., Beckers, G. J. M., Langenbach, C. J. G., & Jaskiewicz, M. R. (2015). Priming for enhanced defense. In N. K. VanAlfen (Ed.), Annual Review of Phytopathology, 53, 97–119.
Csikász-Krizsics, A., Mátai, A., Nagy, Á., Kovács, S., Végh, B., Werner, J., et al. (2013). BABA (β-aminobutyric acid) induced resistance against grey mould and virus infection in grapevine. IOBC-WPRS Bulletin, 89, 429–432.
David, R. (1997). The influence of activated plant defense reaction on colonization of Glomus intraradices in tobacco roots. Thesis submitted to Bar-Ilan University,Israel.
Du, Y. L., Wang, Z. Y., Fan, J. W., Turner, N. C., Wang, T., & Li, F. M. (2012). β-Aminobutyric acid increases abscisic acid accumulation and desiccation tolerance and decreases water use but fails to improve grain yield in two spring wheat cultivars under soil drying. Journal of Experimental Botany, 63(13), 4849–4860. doi:10.1093/jxb/ers164.
EL-Metwally, M. A., Tarabih, M. E., & El-Eryan, E. E. (2014). Effect of application of β -aminobutyric acid on maintaining quality of crimson seedless grape and controlling postharvest diseases under cold storage condition. Plant Pathology Journal, 3, 139–151.
Eschen-Lippold, L., Altmann, S., & Rosahl, S. (2010). DL-β-aminobutyric acid-induced resistance of potato against Phytophthora infestans requires salicylic acid but not oxylipins. Molecular Plant-Microbe Interactions, 23(5), 585–592. doi:10.1094/mpmi-23-5-0585.
Falk, A., Feys, B. J., Frost, L. N., Jones, J. D. G., Daniels, M. J., & Parker, J. E. (1999). EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic lipases. Proceedings of the National Academy of Sciences of the United States of America, 96(6), 3292–3297. doi:10.1073/pnas.96.6.3292.
Farahani, A. S., Taghavi, S. M., Afsharifar, A., & Niazi, A. (2016). Effect of β-aminobutyric acid on resistance of tomato against Pectobacteriumcarotovorum subsp. carotovorum. Journal of Plant Diseases and Protection, 123, 155–161.
Fatemy, S., Moslemi, F., & Bernard, F. (2012). Seed treatment and soil drench with dl-β-amino butyric acid for the suppression of Meloidogyne javanica on tomato. Acta Physiologiae Plantarum, 34(6), 2311–2317. doi:10.1007/s11738-012-1032-9.
Fischer, M. J. C., Farine, S., Chong, J., Guerlain, P., & Bertsch, C. (2009). The direct toxicity of BABA against grapevine ecosystem organisms. Crop Protection, 28(8), 710–712. doi:10.1016/j.cropro.2009.03.014.
Flors, V., Ton, J., van Doorn, R., Jakab, G., Garcia-Agustin, P., & Mauch-Mani, B. (2008). Interplay between JA, SA and ABA signalling during basal and induced resistance against Pseudomonas syringae and Alternaria brassicicola. Plant Journal, 54(1), 81–92.
Gamliel, A., & Katan, J. (1992). Influence of seed and root exudates on fluorescent pseudomonas and fungi in solarized soil. Phytopathology, 82, 320–327.
Greyerbiehl, J. A., & Hammerschmidt, R. (1998). Induced resistance against Fusarium sambucinum in potato tuber tissue. Phytopathology, 88, S34.
Gur, L. (2013). Etiology and control of Alternaria blotch caused by Alternaria alternata apple pathotype on Cripps Pink apple fruits. M.SC Thesis submitted to Bar-Ilan University, Israel.
Gur, L., Reuveni, M., Stern, R., & Cohen, Y. (2013). Integrated control of Alternaria blotch on cv. ‘Cripps Pink’ apple fruits. Phytoparasitica, 41, 458–459.
Hamiduzzaman, M. M., Jakab, G., Barnavon, L., Neuhaus, J. M., & Mauch-Mani, B. (2005). β-Aminobutyric acid-induced resistance against downy mildew in grapevine acts through the potentiation of callose formation and jasmonic acid signaling. Molecular Plant-Microbe Interactions, 18(8), 819–829. doi:10.1094/Mpmi-18-0819.
Hassan, M. A. E., & Abo-Elyousr, K. A. M. (2013). Activation of tomato plant defence responses against bacterial wilt caused by Ralstonia solanacearum using DL-3-aminobutyric acid (BABA). European Journal of Plant Pathology, 136(1), 145–157. doi:10.1007/s10658-012-0149-4.
Hassan, M. A. E., & Buchenauer, H. (2007). Induction of resistance to fire blight in apple by acibenzolar-S-methyl and DL-3-aminobutyric acid. Journal of Plant Diseases and Protection, 114(4), 151–158.
Hodge, S., Thompson, G. A., & Powell, G. (2005). Application of DL-β-aminobutyric acid (BABA) as a root drench to legumes inhibits the growth and reproduction of the pea aphid Acyrthosiphon pisum (Hemiptera: Aphididae). Bulletin of Entomological Research, 95(5), 449–455.
Hodge, S., Pope, T. W., Holaschke, M., & Powell, G. (2006). The effect of b-aminobutyric acid on the growth of herbivorous insects feeding on Brassicaceae. Annals of Applied Biology, 148(3), 223–229.
Hodge, S., Ward, J. L., Galster, A. M., Beale, M. H., & Powell, G. (2011). The effects of a plant defence priming compound, β-aminobutyric acid, on multitrophic interactions with an insect herbivore and a hymenopterous parasitoid. Biocontrol, 56(5), 699–711. doi:10.1007/s10526-011-9344-z.
Hong, J. K., Hwang, B. K., & Kim, C. H. (1999). Induction of local and systemic resistance to Colletotrichum coccodes in pepper plants by DL-β-amino-n-butyric acid. Journal of Phytopathology, 147(4), 193–198.
Hossain, Z., Makino, T., & Komatsu, S. (2012). Proteomic study of β-aminobutyric acid-mediated cadmium stress alleviation in soybean. Journal of Proteomics, 75, 4151–4164.
Hwang, B. K., Sunwoo, J. Y., Kim, Y. J., & Kim, B. S. (1997). Accumulation of β-1,3-glucanase and chitinase isoforms, and salicylic acid in the DL-β-amino-n-butyric acid-induced resistance response of pepper stems to Phytophthora capsici. Physiological and Molecular Plant Pathology, 51(5), 305–322.
Jakab, G., Cottier, V., Toquin, V., Rigoli, G., Zimmerli, L., Metraux, J. P., et al. (2001). β -aminobutyric acid-induced resistance in plants. European Journal of Plant Pathology, 107, 29–37.
Jakab, G., Manrique, A., Zimmerli, L., Metraux, J. P., & Mauch-Mani, B. (2003). Molecular characterization of a novel lipase-like pathogen-inducible gene family of Arabidopsis. Plant Physiology, 132(4), 2230–2239. doi:10.1104/pp.103.025312.
Jakab, G., Ton, J., Flors, V., Zimmerli, L., Metraux, J. P., & Mauch-Mani, B. (2005). Enhancing Arabidopsis salt and drought stress tolerance by chemical priming for its abscisic acid responses. Plant Physiology, 139(1), 267–274.
Jeun, Y. C., & Buchenauer, H. (2001). Infection structures and localization of the pathogenesis- related protein AP24 in leaves of tomato plants exhibiting systemic acquired resistance against Phytophthora infestans after pre-treatment with 3-aminobutyric acid or tobacco necrosis virus. Journal of Phytopathology, 149(3–4), 141–153.
Jeun, Y. C., & Park, E. W. (2003). Ultrastructures of the loaves of cucumber plane treated with DL-3-aminobutyric acid at the vascular bundle and the penetration sites after inoculation with Colletotrichum orbiculare. Korean Society of Plant Pathology, 19, 85–91.
Jeun, Y. C., Siegrist, J., & Buchenauer, H. (2000). Biochemical and cytological studies on mechanisms of systemically induced resistance to Phytophthora infestans in tomato plants. Journal of Phytopathology, 148(6), 129–140.
Jeun, Y. C., Park, K. S., Kim, C. H., Fowler, W. D., & Kloepper, J. W. (2004). Cytological observations of cucumber plants during induced resistance elicited by rhizobacteria. Biological Control, 29(1), 34–42. doi:10.1016/s1049-9644(03)00082-3.
Ji, H. L., Kyndt, T., He, W., Vanholme, B., & Gheysen, G. (2015). β-Aminobutyric acid-induced resistance against root-knot nematodes in rice is based on increased basal defense. Molecular Plant-Microbe Interactions, 28(5), 519–533. doi:10.1094/mpmi-09-14-0260-r.
Jirage, D., Tootle, T. L., Reuber, T. L., Frost, L. N., Feys, B. J., Parker, J. E., et al. (1999). Arabidopsis thaliana PAD4 encodes a lipase-like gene that is important for salicylic acid signaling. Proceedings of the National Academy of Sciences of the United States of America, 96(23), 13583–13588. doi:10.1073/pnas.96.23.13583.
Jisha, K. C., & Puthur, J. T. (2016). Seed priming with BABA (β-amino butyric acid): a cost-effective method of abiotic stress tolerance in Vigna radiata (L.) Wilczek. Protoplasma, 253(2), 277–289. doi:10.1007/s00709-015-0804-7.
Kamble, A., & Bhargava, S. (2007). β-aminobutyric acid-induced resistance in Brassica juncea against the necrotrophic pathogen Alternaria brassicae. Journal of Phytopathology, 155(4), 255.
Kamble, A., Koopmann, B., & von Tiedemann, A. (2013). Induced resistance to Verticillium longisporum in Brassica napus by β-aminobutyric acid. Plant Pathology, 62(3), 552–561. doi:10.1111/j.1365-3059.2012.02669.x.
Karmakar, N. C., Ghosh, R., & Purkayastha, R. P. (2003). Plant defence activators inducing systemic resistance in Zingiber officinale Rosc. against Pythium aphanidermatum (Edson) Fitz. Indian Journal of Biotechnology, 2, 591–595.
Kim, Y. C., Kim, Y. H., Lee, Y. H., Lee, S. W., Chae, Y. S., Kang, H. K., et al. (2013). β-Amino-n-butyric acid regulates seedling growth and disease resistance of kimchi cabbage. Plant Pathology Journal, 29(3), 305–316. doi:10.5423/ppj.oa.12.2012.0191.
Koen, E., Trapet, P., Brule, D., Kulik, A., Klinguer, A., Atauri-Miranda, L., et al. (2014). β-Aminobutyric acid (BABA)-induced resistance in Arabidopsis thaliana: link with iron homeostasis. Molecular Plant-Microbe Interactions, 27(11), 1226–1240. doi:10.1094/mpmi-05-14-0142-r.
Lankinen, A., Abreha, K. B., Alexandersson, E., Andersson, S., & Andreasson, E. (2016). Nongenetic inheritance of induced resistance in a wild annual plant. Phytopathology, in press.
Lee, Y. K., Hong, J. K., Hippe-Sanwald, S., & Hwang, B. K. (2000). Histological and ultrastructural comparisons of compatible, incompatible and DL-β-amino-n-butyric acid-induced resistance responses of pepper stems to Phytophthora capsici. Physiological and Molecular Plant Pathology, 57(6), 269–280.
Li, J. J., Zingen-Sell, I., & Buchenauer, H. (1996). Induction of resistance of cotton plants to Verticillium wilt and of tomato plants to Fusarium wilt by 3-aminobutyric acid and methyl jasmonate. Zeitschrift fur Pflanzenkrankheiten und Pflanzenschutz-Journal of Plant Diseases and Protection, 103(3), 288–299.
Li, J. Y., Trivedi, P., & Wang, N. (2016). Field evaluation of plant defense inducers for the control of citrus huanglongbing. Phytopathology, 106(1), 37–46. doi:10.1094/phyto-08-15-0196-r.
Liljeroth, E., Bengtsson, T., Wiik, L., & Andreasson, E. (2010). Induced resistance in potato to Phytphthora infestans- effects of BABA in greenhouse and field tests with different potato varieties. European Journal of Plant Pathology, 127(2), 171–183. doi:10.1007/s10658-010-9582-4.
Liu, T. W., Jiang, X. W., Shi, W. L., Chen, J., Pei, Z. M., & Zheng, H. L. (2011). Comparative proteomic analysis of differentially expressed proteins in β-aminobutyric acid enhanced Arabidopsis thaliana tolerance to simulated acid rain. Proteomics, 11(10), 2079–2094. doi:10.1002/pmic.201000307.
Lotan, T., & Fluhr, R. (1990). Xylanase, a novel elicitor of pathogenesis-related proteins in tobacco, uses a non-ethylene pathway for induction. Plant Physiology, 93, 811–817.
Luna, E., Bruce, T. J. A., Roberts, M. R., Flors, V., & Ton, J. (2012). Next-generation systemic acquired resistance. Plant Physiology, 158(2), 844–853. doi:10.1104/pp.111.187468.
Luna, E., van Hulten, M., Zhang, Y. H., Berkowitz, O., Lopez, A., Petriacq, P., et al. (2014a). Plant perception of β-aminobutyric acid is mediated by an aspartyl-tRNA synthetase. Nature Chemical Biology, 10(6), 450–456. doi:10.1038/nchembio.1520.
Luna, E., Lopez, A., Kooiman, J., & Ton, J. (2014a). Role of NPR1 and KYP in long-lasting induced resistance by β-aminobutyric acid. Frontiers in Plant Science, 5. doi:10.3389/fpls.2014.00184.
Luna, E., Beardon, E., Ravnskov, S., Scholes, J., & Ton, J. (2016). Optimizing chemically induced resistance in tomato against Botrytis cinerea. Plant Disease, 100(4), 704–710. doi:10.1094/pdis-03-15-0347-re.
Macarisin, D., Wisniewski, M. E., Bassett, C., & Thannhauser, T. W. (2009). Proteomic analysis of β-aminobutyric acid priming and abscisic acid - induction of drought resistance in crabapple (Malus pumila): effect on general metabolism, the phenylpropanoid pathway and cell wall enzymes. Plant, Cell and Environment, 32(11), 1612–1631. doi:10.1111/j.1365-3040.2009.02025.x.
MacLennan, D. H., Kuc, J., & Williams, E. B. (1963). Chemotherapy of the apple scab disease with butyric acid derivatives. Phytopathology, 53(11), 1261–1266.
Maldonado, M. L. H., Falloon, R. E., Butler, R. C., Conner, A. J., & Bulman, S. R. (2015). Resistance to Spongospora subterranea induced in potato by the elicitor β-aminobutyric acid. Australasian Plant Pathology, 44, 445–453.
Marcucci, E., Aleandri, M. P., Chilosi, G., & Magro, P. (2010). Induced resistance by β-Aminobutyric acid in artichoke against white mould caused by Sclerotinia sclerotiorum. Journal of Phytopathology, 158(10), 659–667. doi:10.1111/j.1439-0434.2010.01677.x.
Martinez-Aguilar, K., Ramirez-Carrasco, G., Hernandez-Chavez, J. L., Barraza, A., & Alvarez-Venegas, R. (2016). Use of BABA and INA as activators of a primed state in the common bean (Phaseolus vulgaris L.). Frontiers in Plant Science, 7. doi:10.3389/fpls.2016.00653.
Maymoune, A., Adeline, P., Marie, T., Sophie, G., Sophie, C., Catherine, L., et al. (2015). Impact of abiotic stresses on the protection efficacy of defence elicitors and on metabolic regulation in tomato leaves infected by Botrytis cinerea. European Journal of Plant Pathology, 142(2), 223–237. doi:10.1007/s10658-015-0606-y.
Melvin, P., Prabhu, S. A., Veena, M., Shailasree, S., Petersen, M., Mundy, J., et al. (2015). The pearl millet mitogen-activated protein kinase PgMPK4 is involved in responses to downy mildew infection and in jasmonic- and salicylic acid-mediated defense. Plant Molecular Biology, 87(3), 287–302. doi:10.1007/s11103-014-0276-8.
Mersha, Z., Zhang, S., Fu, Y., Mo, X., Raid, R. N., & Hau, B. (2013). Efficacy of acibenzolar-S-methyl and β-aminobutyric acid for control of downy mildew in greenhouse grown basil and peroxidase activity in response to treatment with these compounds. Journal of Phytopathology, 161(3), 154–164. doi:10.1111/jph.12045.
Mongae, A., & Moleleki, L. (2015). The effect of β-aminobutyric acid (BABA) on root knot nematode and soft rot pathogen disease complexes in Solanum tuberosum plants. European Journal of Plant Pathology, 142(1), 117–124. doi:10.1007/s10658-015-0596-9.
Moricova, P., Stary, T., Pecinkova, M., Lochman, J., Kubienova, L., Mieslerova, B., et al. (2014). Oligandrin and β-aminobutyric acid-induced resistance to Oidium neolycopersici in tomato plants. Febs Journal, 281, 753–754.
Mostek, A., Borner, A., & Weidner, S. (2016). Comparative proteomic analysis of β-aminobutyric acid-mediated alleviation of salt stress in barley. Plant Physiology and Biochemistry, 99, 150–161. doi:10.1016/j.plaphy.2015.12.007.
Oka, Y., & Cohen, Y. (2001). Induced resistance to cyst and root-knot nematodes in cereals by DL-b-amino-n-butyric acid. European Journal of Plant Pathology, 107(2), 219–227.
Oka, Y., Cohen, Y., & Spiegel, Y. (1999). Local and systemic induced resistance to the root-knot nematode in tomato by DL- β-amino-n-butyric acid. Phytopathology, 89, 1138–1143.
Oka, Y., Spiegel, Y., & Cohen, Y. (2001). Methods and compositions to protect crops against plant parasitic nematodes. US Patent 6,201,023 B1.
Olivieri, F. P., Lobato, M. C., Altamiranda, E., Daleo, G. R., Huarte, M., Guevara, M. G., et al. (2009). BABA effects on the behaviour of potato cultivars infected by Phytophthora infestans and Fusarium solani. European Journal of Plant Pathology, 123(1), 47–56. doi:10.1007/s10658-008-9340-z.
Ovadia, A., Biton, R., Cohen, Y., Katzir, N., & Paris, H. S. (2000). Induced resistance to downy mildew and Fusarium wilt in cucurbits. In Proceedings of CUCURBITACEAE 2000. The 7 th EUCARPIA Meeting on Cucurbit Genetics and Breeding (pp. 55–59). Acta Horticulture.
Pajot, E., & Silue, D. (2005). Evidence that DL-3-aminobutyric acid and acibenzolar-S-methyl induce resistance against bacterial head rot disease of broccoli. Pest Management Science, 61(11), 1110–1114. doi:10.1002/ps.1103.
Pajot, E., Le Corre, D., & Silue, D. (2001). Phytogard(R) and DL- β-amino butyric acid (BABA) induce resistance to downy mildew (Bremia lactucae) in lettuce (Lactuca sativa L). European Journal of Plant Pathology, 107(9), 861–869.
Panebianco, S., Vitale, A., Platania, C., Restuccia, C., Polizzi, G., & Cirvilleri, G. (2014). Postharvest efficacy of resistance inducers for the control of green mold on important Sicilian citrus varieties. Journal of Plant Diseases and Protection, 121(4), 177–183.
Papavizas, G. C., & Davey, C. B. (1963). Effect of amino compounds and related substances lacking sulfur on Aphanomyces root rot of peas. Phytopathology, 53, 116–122.
Pastor, V., Luna, E., Ton, J., Cerezo, M., Garcia-Agustin, P., & Flors, V. (2013). Fine tuning of reactive oxygen species homeostasis regulates primed immune responses in Arabidopsis. Molecular Plant-Microbe Interactions, 26(11), 1334–1344. doi:10.1094/mpmi-04-13-0117-r.
Pfautsch, S., Gessler, A., Adams, M. A., & Rennenberg, H. (2009). Using amino-nitrogen pools and fluxes to identify contributions of understory Acacia spp. to overstory Eucalyptus regnans and stand nitrogen uptake in temperate Australia. New Phytologist, 183(4), 1097–1113. doi:10.1111/j.1469-8137.2009.02909.x.
Philippe, R., Ferreol, B., Sophie, A., & Marie-Noelle, B. (2016). DL- β -aminobutyric acid application negatively affects reproduction and larval development of the rosy apple aphid, Dysaphis plantaginea, on apple. Entomologia Experimentalis et Applicata, 159, 46–53.
Piekna-Grochala, J., & Kepczynska, E. (2013). Induction of resistance against pathogens by β -aminobutyric acid. Acta Physiologiae Plantarum, 35, 1735–1748.
Polyakovskii, S. A., Kravchuk, Z. N., & Dmitriev, A. P. (2008). Mechanism of action of the plant resistance inducer β-aminobutyric acid in Allium cepa. Cytology and Genetics, 42(6), 369–372. doi:10.3103/s0095452708060029.
Porat, R., Vinokur, V., Weiss, B., Cohen, L., Daus, A., Goldschmidt, E. E., et al. (2003). Induction of resistance to Penicillium digitatum in grapefruit by b-aminobutyric acid. European Journal of Plant Pathology, 109(9), 901–907.
Po-Wen, C., Singh, P., & Zimmerli, L. (2013). Priming of the Arabidopsis pattern-triggered immunity response upon infection by necrotrophic Pectobacterium carotovorum bacteria. Molecular Plant Pathology, 14, 58–70. doi:10.1111/j.1364-3703.2012.00827.x.
Quero, A., Fliniaux, O., Elboutachfaiti, R., Petit, E., Guillot, X., Hawkins, S., et al. (2015). β-Aminobutyric acid increases drought tolerance and reorganizes solute content and water homeostasis in flax (Linum usitatissimum). Metabolomics, 11(5), 1363–1375. doi:10.1007/s11306-015-0792-9.
Rajaei, P., & Mohamadi, N. (2013). Effect of β-aminobutyric acid (BABA) on enzymatic and non-enzymatic antioxidants of Brassica napus L. under drought stress. International Journal of Biosciences, 3, 41–47.
Reuveni, M., Zahavi, T., & Cohen, Y. (2001). Controlling downy mildew (Plasmopara viticola) in field-grown grapevine with b-aminobutyric acid (BABA). Phytoparasitica, 29(2), 125–133.
Reuveni, M., Sheglov, D., & Cohen, Y. (2003). Control of moldy-core decay in apple fruits by β-aminobutyric acids and potassium phosphites. Plant Disease, 87(8), 933–936.
Roylawar, P., Panda, S., & Kamble, A. (2015). Comparative analysis of BABA and Piriformospora indica mediated priming of defence-related genes in tomato against early blight. Physiological and Molecular Plant Pathology, 91, 88–95. doi:10.1016/j.pmpp.2015.06.004.
Sahebani, N., & Hadavi, N. (2009). Induction of H2O2 and related enzymes in tomato roots infected with root knot nematode (M. javanica) by several chemical and microbial elicitors. Biocontrol Science and Technology, 19(3), 301–313. doi:10.1080/09583150902752012.
Sahebani, N., Hadavi, N. S., & Zade, F. O. (2011). The effects of β-amino-butyric acid on resistance of cucumber against root-knot nematode, Meloidogyne javanica. Acta Physiologiae Plantarum, 33(2), 443–450. doi:10.1007/s11738-010-0564-0.
Sang, M. K., Kim, E. N., Han, G. D., Kwack, M. S., Jeun, Y. C., & Kim, K. D. (2014). Priming-mediated systemic resistance in cucumber induced by Pseudomonas azotoformans GC-B19 and Paenibacillus elgii MM-B22 against Colletotrichum orbiculare. Phytopathology, 104(8), 834–842. doi:10.1094/phyto-11-13-0305-r.
Sasek, V., Novakova, M., Dobrev, P. I., Valentova, O., & Burketova, L. (2012). β-aminobutyric acid protects Brassica napus plants from infection by Leptosphaeria maculans. Resistance induction or a direct antifungal effect? European Journal of Plant Pathology, 133(1), 279–289. doi:10.1007/s10658-011-9897-9.
Shailasree, S., & Melvin, P. (2015). β-amino butyric acid - resistance inducing agent in pearl millet. Plant Biochemistry & Physiology Journal, 2, 144–147.
Shailasree, S., Sarosh, B. R., Vasanthi, N. S., & Shetty, H. S. (2001). Seed treatment with β-aminobutyric acid protects Pennisetum glaucum systemically from Sclerospora graminicola. Pest Management Science, 57(8), 721–728.
Shailasree, S., Ramachandra, K. K., & Shetty, S. H. (2007). β-amino butyric acid-induced resistance in pearl millet to downy mildew is associated with accumulation of defence-related proteins. Australasian Plant Pathology, 36(2), 204–211. doi:10.1071/ap06093.
Sharifi-Sirchi, G. R., Beheshti, B., Hosseinipour, A., & Mansouri, M. (2011). Priming against Asiatic citrus canker and monitoring of PR genes expression during resistance induction. African Journal of Biotechnology, 10(19), 3818–3823.
Shaw, A. K., Bhardwaj, P. K., Supriya, G., Sankhajit, R., Suman, S., Sherpa, A. R., et al. (2016). β-aminobutyric acid mediated drought stress alleviation in maize (Zea mays L.). Environmental Science and Pollution Research, 23, 2437–2453.
Siegrist, J., Orober, M., & Buchenauer, H. (2000). β-aminobutyric acid-mediated enhancement of resistance in tobacco to tobacco mosaic virus depends on the accumulation of salicylic acid. Physiological and Molecular Plant Pathology, 56(3), 95–106.
Silue, D., Pajot, E., & Cohen, Y. (2002). Induction of resistance to downy mildew (Peronospora parasitica) in cauliflower by DL- β -amino-n-butanoic acid (BABA). Plant Pathology, 51(1), 97–102.
Slaughter, A. R., Hamiduzzaman, M. M., Gindro, K., Neuhaus, J. M., & Mauch-Mani, B. (2008). β-aminobutyric acid-induced resistance in grapevine against downy mildew: involvement of pterostilbene. European Journal of Plant Pathology, 122(1), 185–195. doi:10.1007/s10658-008-9285-2.
Slaughter, A., Daniel, X., Flors, V., Luna, E., Hohn, B., & Mauch-Mani, B. (2012). Descendants of primed Arabidopsis plants exhibit resistance to biotic stress. Plant Physiology, 158, 835–843.
Sos-Hegedus, A., Juhasz, Z., Poor, P., Kondrak, M., Antal, F., Tari, I., et al. (2014). Soil drench treatment with β-aminobutyric acid increases drought tolerance of potato. Plos One, 9(12). doi:10.1371/journal.pone.0114297.
Stamler, R. A., Holguin, O., Dungan, B., Schaub, T., Sanogo, S., Goldberg, N., et al. (2015). BABA and Phytophthora nicotianae induce resistance to Phytophthora capsici in chile pepper (Capsicum annuum). Plos One, 10(5). doi:10.1371/journal.pone.0128327.
Sunwoo, J. Y., Lee, Y. K., & Hwang, B. K. (1996). Induced resistance against Phytophthora capsici in pepper plants in response to DL-b-amino-n-butyric acid. European Journal of Plant Pathology, 102, 663–670.
Szalontai, B., Stranczinger, S., Palfalvi, G., Mauch-Mani, B., & Jakab, G. (2012). The taxon-specific paralogs of grapevine PRLIP genes are highly induced upon powdery mildew infection. Journal of Plant Physiology, 169(17), 1767–1775. doi:10.1016/j.jplph.2012.07.010.
Taler, D., Galperin, M., Benjamin, I., Cohen, Y., & Kenigsbuch, D. (2004). Plant eR genes that encode photorespiratory enzymes confer resistance against disease. Plant Cell, 16(1), 172–184.
Tavallali, V., Karimi, S., Mohammadi, S., & Hojati, S. (2008). Effects of β -aminobutyric acid on the induction of resistance to Penicillium italicum. World Applied Sciences Journal, (5), 345–351.
Thevenet, D., Pastor, V., Baccelli, I., Balmer, A., Vallat, A., Neier, R., Glauser, G., & Mauch-Mani, B. (2016). The priming molecule β-aminobutyric acid is naturally present in plants 1 and is induced by stress. New Phytologist, (accepted).
Tiwari, S., Meyer, W. L., & Stelinski, L. L. (2013). Induced resistance against the Asian citrus psyllid, Diaphorina citri, by β-aminobutyric acid in citrus. Bulletin of Entomological Research, 103(5), 592–600. doi:10.1017/s0007485313000229.
Ton, J., & Mauch-Mani, B. (2004). b-amino-butyric acid-induced resistance against necrotrophic pathogens is based on ABA-dependent priming for callose. Plant Journal, 38(1), 119–130.
Ton, J., Jakab, G., Toquin, V., Flors, V., Iavicoli, A., Maeder, M. N., et al. (2005). Dissecting the b-aminobutyric acid-induced priming phenomenon in arabidopsis. Plant Cell, 17(3), 987–999.
Toquin, V., Jakab, G., Maeder, M. N., & Mauch-Mani, B. (2002). β-aminobutyric acid as a useful tool to dissect the priming phenomenon in induced resistance. In B. Mauch-Mani, & A. Schmitt (Eds.), Induced Resistance in Plants against Insects and Diseases (Vol. 2002.). IOBC/wprs Bulletin.
Tosi, L., Luigetti, R., & Zazzerini, A. (1998). Induced resistance against Plasmopara helianthi in sunflower plants by DL-β-amino-n-butyric acid. Journal of Phytopathology, 146(5–6), 295–299.
Tworkoski, T., Wisniewski, M., & Artlip, T. (2009). Application of BABA and s-ABA for drought resistance in apple. Journal of Applied Horticulture (Lucknow), 13, 85–90.
Vaknin, M. (2016). Genetic resistance and induced resistance against Bremia lactucae in lettuce: microscopy and mechanism. PhD Thesis submitted to Bar-Ilan University, Israel.
Van Andel, O. M. (1958). Investigations on plant chemotherapy II. Influence of amino acids on the relation plant-pathogen. Tijdschrift der Planteziekten, 64, 307–327.
Van der Ent, S., Van Hulten, M., Pozo, M. J., Czechowski, T., Udvardi, M. K., Pieterse, C. M. J., et al. (2009). Priming of plant innate immunity by rhizobacteria and β-aminobutyric acid: differences and similarities in regulation. New Phytologist, 183(2), 419–431. doi:10.1111/j.1469-8137.2009.02851.x.
Vogt, W., & Buchenauer, H. (1997). Enhancement of biological control by combination of antagonistic fluorescent Pseudomonas strains and resistance inducers against damping off and powdery mildew in cucumber. Zeitschrift fur Pflanzenkrankheiten und Pflanzenschutz-Journal of Plant Diseases and Protection, 104(3), 272–280.
Walters, D. R., Havis, N. D., Paterson, L., Taylor, J., Walsh, D. J., & Sablou, C. (2014). Control of foliar pathogens of spring barley using a combination of resistance elicitors. Frontiers in Plant Science, 5. doi:10.3389/fpls.2014.00241.
Walz, A., & Simon, O. (2009). β-Aminobutyric acid-induced resistance in cucumber against biotrophic and necrotrophic pathogens. J. Phytopathol., 157(6), 356–361. doi:10.1111/j.1439-0434.2008.01502.x.
Wang, L., Jin, P., Wang, J., Jiang, L. L., Shan, T. M., & Zheng, Y. H. (2015). Effect of β-aminobutyric acid on cell wall modification and senescence in sweet cherry during storage at 20 degrees C. Food Chemistry, 175, 471–477. doi:10.1016/j.foodchem.2014.12.011.
Wang, K., Liao, Y., Xiong, Q., Kan, J., Cao, S., & Zheng, Y. (2016). Induction of direct or priming resistance against Botrytis cinerea in strawberries by β-aminobutyric acid and their effects on sucrose metabolism. Journal of Agricultural and Food Chemistry, 64(29), 5855–5865. doi:10.1021/acs.jafc.6b00947.
Worrall, D., Holroyd, G. H., Moore, J. P., Glowacz, M., Croft, P., Taylor, J. E., et al. (2012). Treating seeds with activators of plant defence generates long-lasting priming of resistance to pests and pathogens. New Phytologist, 193(3), 770–778. doi:10.1111/j.1469-8137.2011.03987.x.
Wu, C. C., Singh, P., Chen, M. C., & Zimmerli, L. (2010). L-Glutamine inhibits β -aminobutyric acid-induced stress resistance and priming in Arabidopsis. Journal of Experimental Botany, 61, 995–1002.
Yan, J., Yuan, S., Wang, C., Yue, D., Xin, Y., Cao, J., et al. (2015). Enhanced resistance of jujube (Zizyphus jujuba Mill. cv. Dongzao) fruit against postharvest Alternaria rot by β -aminobutyric acid dipping. Scientia Horticulturae, 186, 108–114.
Yin, Y., Li, Y. C., Bi, Y., Chen, S. J., Li, Y. C., Yuan, L., et al. (2010). Postharvest Treatment with β-Aminobutyric acid induces resistance against dry rot caused by Fusarium sulphureum in potato tuber. Agricultural Sciences in China, 9(9), 1372–1380. doi:10.1016/s1671-2927(09)60228-5.
Yun, H. K., Yi, S. Y., Yu, S. H., & Choi, D. (1999). Cloning of a pathogenesis-related protein-1 gene from Nicotiana glutinosa L and its salicylic acid-independent induction by copper and β-aminobutyric acid. Journal of Plant Physiology, 154(3), 327–333.
Zeighaminejad, R., Sharifi-Sirchi, G. R., Mohamadi, H., & Aminai, M. M. (2016). Induction of resistance against powdery mildew by β-aminobutyric acid in squash. Journal of Applied Botany and Food Quality, 89, 176–182. doi:10.5073/jabfq.2016.089.022.
Zhang, S., Reddy, M. S., Kokalis-Burelle, N., Wells, L. W., Nightengale, S. P., & Kloepper, J. W. (2001). Lack of induced systemic resistance in peanut to late leaf spot disease by plant growth-promoting rhizobacteria and chemical elicitors. Plant Disease, 85(8), 879–884.
Zhang, C. W., Jiamin, Z., Jiaguo, H., & Chengjie, W. G. (2011). Effects of β -aminobutyric acid on control of postharvest blue mould of apple fruit and its possible mechanisms of action. Postharvest Biology and Technology, 61, 145–151.
Zhang, W., Zhou, H., Yuan, Z., Zhang, C., & Wen, X. (2013a). Control effects and mechanisms of β-aminobutyric acid and chitosan on postharvest blue mold of red Fuji apple. [Chinese]. Journal of Northwest A & F University - Natural Science Edition, 41, 149–156.
Zhang, Z., Yang, D., Yang, B., Gao, Z., Li, M., Jiang, Y., et al. (2013b). β-aminobutyric acid induces resistance of mango fruit to postharvest anthracnose caused by Colletotrichum gloeosporioides and enhances activity of fruit defense mechanisms. Scientia Horticulturae, 160, 78–84.
Zhong, Y. P., Wang, B., Yan, J. H., Cheng, L. J., Yao, L. M., Xiao, L., et al. (2014). DL-β-Aminobutyric acid-induced resistance in soybean against Aphis glycines Matsumura (Hemiptera: Aphididae). Plos One, 9(1). doi:10.1371/journal.pone.0085142.
Zimmerli, L., Jakab, C., Metraux, J. P., & Mauch-Mani, B. (2000). Potentiation of pathogen-specific defense mechanisms in Arabidopsis by β-aminobutyric acid. Proceedings of the National Academy of Sciences of the United States of America, 97(23), 12920–12925.
Zimmerli, L., Metraux, J. P., & Mauch-Mani, B. (2001). β-aminobutyric acid-induced protection of Arabidopsis against the necrotrophic fungus Botrytis cinerea. Plant Physiology, 126(2), 517–523.
Zimmerli, L., Hou, B. H., Tsai, C. H., Jakab, G., Mauch-Mani, B., & Somerville, S. (2008). The xenobiotic β-aminobutyric acid enhances Arabidopsis thermotolerance. Plant Journal, 53(1), 144–156.
Zlotek, U., Szymanowska, U., Karas, M., & Swieca, M. (2015). Antioxidative and anti-inflammatory potential of phenolics from purple basil (Ocimum basilicum L.) leaves induced by jasmonic, arachidonic and β -aminobutyric acid elicitation. Food Science & Technology, 51, 163–170.
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Cohen, Y., Vaknin, M. & Mauch-Mani, B. BABA-induced resistance: milestones along a 55-year journey. Phytoparasitica 44, 513–538 (2016). https://doi.org/10.1007/s12600-016-0546-x
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DOI: https://doi.org/10.1007/s12600-016-0546-x