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From yogurt to yield: Potential applications oflactic acid bacteria in plant production
Article in Soil Biology and Biochemistry · August 2017
DOI: 10.1016/j.soilbio.2017.03.015

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Soil Biology & Biochemistryjournal homepage: www.elsevier.com/locate/soilbio

From yogurt to yield: Potential applications of lactic acid bacteria inplant production€rd b, Donald L. Smith aJohn R. Lamont a, *, Olivia Wilkins a, Margaret Bywater-Ekegaab

Plant Science Department, McGill University/Macdonald Campus, Sainte-Anne-de-Bellevue, QC, Canada
Inocucor Technologies Inc., Montr
eal, QC, Canada

a r t i c l e i n f o

a b s t r a c t

Article history:
Received 27 October 2016
Received in revised form
21 March 2017
Accepted 22 March 2017

Ferments containing lactic acid bacteria (LAB) have been used for decades in agricultural systems to
improve soils, control disease and promote plant growth, however, the functional roles of LAB in thephytomicrobiome have yet to be discovered. An understanding of the symbiotic relationship between
plants and LAB could be exploited to improve agricultural plant production.
Scientiﬁc investigations to validate plant growth promoting properties of LAB are increasing in number
and scope. LAB isolated from diverse sources have been shown to be effective biofertilizers, biocontrol
agents, biostimulants. As biofertilizers, LAB can improve nutrient availability from compost and otherorganic material. In fermented food, LAB has served as an effective biocontrol agent; recently LAB havebeen shown to be effective in the control of a wide variety of fungal and bacterial phytopathogens. As
biostimulants, LAB can directly promote plant growth or seed germination, as well as alleviating various
abiotic stresses.
In this review, we discuss the history and ecology of plants and LAB, appraise the available informationon the use of LAB in improving plant production, and consider the limitations and potential new directions for the use of LAB in plant agriculture.
© 2017 Elsevier Ltd. All rights reserved.

Keywords:
Lactic acid bacteria
Effective microorganisms
Biocontrol
Biostimulant
Biofertilizer
Bioelicitor

1. Introduction
Recent advances in plant-microbe interaction research havedrawn attention to the importance of microbial communities inpromoting plant health and resilience (Smith et al., 2015a; b). Engineering the phytomicrobiome to promote plant growth is apromising strategy for maintaining crop production in the context
of a changing climate and growing population. Broadly, plant
growth promoting microorganisms (PGPM) promote plant growth
by improving nutrient acquisition, acting as biocontrol agents(BCAs), improving the ability of the host plant to withstand biotic
and abiotic stress, or by producing compounds that directly stimulate plant growth. Many PGPM promote plant growth throughmultiple mechanisms simultaneously (Avis et al., 2008).
Plants in nature interact with a diversity of beneﬁcial, pathogenic, and benign microorganisms. Most PGPM research has
focused on only a few groups of common symbiotic rhizospheremicroorganisms: rhizobia, Bacillus, Pseudomonas and mycorrhizal* Corresponding author.
E-mail address: john.lamont@mail.mcgill.ca (J.R. Lamont).
http://dx.doi.org/10.1016/j.soilbio.2017.03.015
0038-0717/© 2017 Elsevier Ltd. All rights reserved.

fungi (Vessey, 2003). However, the functional roles of other groupsof potential PGPMs, including lactic acid bacteria (LAB), have yet to
be explored. The as-yet uncharacterized phytomicrobiome is an
untapped genetic and metabolic resource that may offer a host of
biochemical solutions to pressing agricultural issues.
LAB are ubiquitous members of many plant microbiomes, butlittle is known about functional interactions between the LAB andtheir hosts. The gap in our knowledge about LAB-plant interactions
stands in contrast to our depth and breadth of knowledge of LAB infood processing. In this review, we appraise the available information on the use of LAB in improving plant production in thecontext of historical uses of LAB in agriculture and food preservation, and discuss the limitations and potential new directions forthe use of LAB in plant agriculture.
LAB are gram positive, facultative anaerobic bacteria that typically reside in substrates rich in carbohydrates, which they ferment
into organic acids. The ability of LAB to produce organic acids andother antimicrobial substances has made them indispensable in thepreservation of plant and animal-based foods as diverse as sauerkraut, cheese, sausage, sourdough bread and animal silage (deVuyst and Vandamme, 1994). Furthermore, the efﬁciency with

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J.R. Lamont et al. / Soil Biology & Biochemistry 111 (2017) 1e9

which LAB convert carbohydrates into organic acids has promptedinterest in industrial applications of LAB bioreactors used to produce organic acids; especially lactic acid, an important precursor
for biodegradable plastics (Konings et al., 2000). The beneﬁts of
Lactobacillus strains on human health also make them valuableprobiotic (Naidu et al., 1999).
The widespread use of LAB in food processing has generated agreat deal of knowledge about their physiology and the bioactive
compounds they produce (Garsa et al., 2014; de Vuyst andVandamme, 1994). This usage has also resulted in the designationof LAB as generally regarded as safe (GRAS) and would pose no risks
for applications in edible crop production, exempting it from costly
and time consuming regulatory approval processes. (Lutz et al.,2012). Moreover, the combined empirical evidence from agriculture paired with a growing body of scientiﬁc evidence makes aconvincing case for LAB as a new class of PGPM. There is great
potential to use LAB as biofertilizers, biocontrol agents and biostimulants to aid in producing food (Fig. 1).

2. History of LAB in agriculture
Proponents of holistic, ecologically-based agricultural systems
have long valued LAB, and especially Lactobacillus as an agricultural
input. Lactobacillus is ubiquitous on plants and proliferates quickly
when plant tissues are damaged and carbohydrate-rich cell contents are released. The ease of culturing wild lactobacilli without
the use of laboratory equipment or microbiological expertise,paired with its ability to preserve, and even improve, the nutritional quality and ﬂavor of foods, have contributed to the widespread use of these microbes by farmers and the general public(Katz, 2008, 2012).
Beginning in the 1930s, when the use of mechanized farmequipment and chemical pesticides and fertilizers was becoming
more prevalent, (Martin and Sauerborn, 2013), many alternative
agricultural movements, that looked to preindustrial farming
practices, were initiated around the world. Many of these alternative agricultural movements adopted LAB, and especially Lactobacillus, as an indispensable component of sustainable agriculture, tocontrol pests, condition soils, and stimulate plant growth (Higa,
1991, 2001; Somers et al., 2007; Paulsen et al., 2009).

3. Plant-LAB ecology
To harness the beneﬁts of LAB for improved agricultural production, we must ﬁrst understand the ecological relationship between plants and LAB, including the ecological niches LAB ﬁll innature. Plants interact with diverse communities of beneﬁcial,benign, and pathogenic microorganisms in the environment andmust be able to distinguish between members of these communities to optimize growth. If the plant-LAB relationship provides anadvantage to the plant, this relationship can be promoted ormanipulated to improve agricultural production.
Lactobacilli are found in the phyllosphere, endosphere andrhizosphere of many plants. Each of these niches provides distinct
challenges to the growth of the LAB. In the phyllosphere, lactobacilli
are exposed to a host of stresses including ultraviolet radiation,
extremes in water availability, scarce nutrient availability and highredox potential (Mundt and Hammer, 1968; Müller and Seyfarth,1997). LAB also live inside plants as endophytes, and can survive
in seeds (Minervini et al., 2015) and vegetative propagules (Leifert
et al., 1994). Lactobacillus has been found living as an endophyte indiverse crop plants including sweet corn, cotton, (McInroy and
Kloepper, 1991), sugar beet (Jacobs et al., 1985), strawberry fruit(de Melo Pereira et al., 2012) pepper (Shrestha et al., 2014), cucumber (Rzhevskaya et al., 2013), wheat seeds (Baffoni et al., 2015;
Minervini et al., 2015) and Lolium perenne roots (Gaggìa et al., 2013).
The ability of LAB to live in the endosphere of such a diversity ofplants suggests an intimate relationship between plants and LAB.
The rhizosphere is deﬁned as the fraction of soil under the direct
biochemical inﬂuence of root exudates. Plants devote a signiﬁcant
proportion of photosynthetically ﬁxed carbon to root exudates,
which include sugars, signaling compounds, enzymes and otherchemicals that alter the soil environment to select for particular
microbial communities (Bais et al., 2006). This carbohydrate-richenvironment would appear to be ideal for LAB, however, organic
acids break down quickly in the rhizosphere (Jones, 1998); limiting
the ability of LAB to acidify the rhizosphere to their advantage.
Although this limitation prevents LAB from being a dominantbacterial group in most soils, diverse LAB strains have been isolated
from rhizospheres (Chen et al., 2005; Yanagida et al., 2006;
Shrestha et al., 2009a; Ekundayo, 2014). Research on theFig. 1. Mechanisms by which lactic acid bacteria can mitigate stress to plants.

J.R. Lamont et al. / Soil Biology & Biochemistry 111 (2017) 1e9

3

LAB are one of the major microbial groups responsible fordecomposing a variety of organic materials for use in agriculture;they are common in compost (Partanen et al., 2010), silage(MacDonald, 1981), and methogenic anaerobic digestion systems(Li et al., 2011). These waste processing systems generally use
indigenous microbial populations, however there have been someattempts to improve these processes by inoculating waste materials
with microbial consortia, typically containing LAB.
Effective Microorganisms (EM) consortia are composed of aconsortium of yeast, mold fungi, LAB, photosynthetic bacteria, actinomycetes, and others (Higa, 1991). LAB generally becomes themost active and dominant group in mature ferments of EM consortia (Kyan et al., 1999). Analysis of three commercial EM products
found that LAB were the most abundant microbial group in the
consortia (Ahn et al., 2014).
Compost inoculated with EM have been shown to produce
greater yields and increase nutrient uptake for wheat (Hu and Qi,
2010; Hussain et al., 1999), soybean (Javaid and Mahmood, 2010),
mung bean (Javaid and Bajwa, 2011) rice (Javaid, 2011) and cotton(Khaliq et al., 2006) than plants grown with non-inoculated composts. Increased productivity in crops treated with EM-inoculated
composts versus untreated composts is likely due to hastened
decomposition of organic compounds into plant available nutrients. LAB has been shown to solubilize phosphate (Shrestha et al.,2014; Giassi et al., 2016), likely through the production of organic
acids. Three strains of LAB isolated from a sugarcane ferment can ﬁx
atmospheric nitrogen (Giassi et al., 2016). While LAB appear to havevirtually no Fe requirement and have been thought to not produce
siderophores (Pandey et al., 1994; Weinberg, 1997), Shrestha et al.
(2014) reported three plant growth promoting strains of Lactobacillus produced siderophores.
While there have been promising results in many trials with EM,
the efﬁcacy of EM has yet to be determined. Many ﬁeld trials where
EM have improved crop yield have been conducted in tropical or
subtropical regions, while most trials in temperate regions have notshown any beneﬁt from EM applications (Mayer et al., 2010).

search for safer alternatives. Numerous microorganisms have been
identiﬁed as safe and effective biocontrol agents (BCAs) for bacterial and fungal phytopathogens.
BCAs work through a variety of mechanisms (Compant et al.,2005). There are three known mechanisms by which LAB acts asa biocontrol agent; through the production of antimicrobial compounds (Kao and Frazer, 1966; Tramer, 1966; Trias et al., 2008),
reactive oxygen species (Trias et al., 2008) and bacteriocins; by
excluding pathogens by pre-emptively colonizing plant tissues
 et al.,vulnerable to infection (Visser and Holzapfel, 1992; Rosello2013), and by altering the plant immune response (Konappa
et al., 2016).
LAB produce a diversity of antimicrobial compounds including
antifungal diketopiperazines, hydroxy derivatives of fatty acids, 3phenyllactate; antibacterial bacteriocins and bacteriocin-likecompounds; and general antimicrobials such as organic acids,hydrogen peroxide, pyrrolidone-5-carboxylic acid, diacetyl andreuterin (b-OH-propionic aldehyde) (Stoyanova et al., 2012). It has
been proposed that the major mechanism of foliar bacterial pathogen control by LAB is organic acid production (Visser andHolzapfel, 1992) however, with diversity of antimicrobial compounds produced by LAB in mind, it has also been argued that LAB
barrage competitor microorganism with a variety of compoundswith multiple modes of action (Gupta and Srivastava, 2014;
Sangmanee and Hongpattarakere, 2014).
Aside from direct antagonism toward phytopathogens, LAB
treatments can alter the response of plant to pathogens, thus
improving their innate immunity. Such effect is called systemicacquired resistance (SAR). Hamed et al. (2011) suggested changes tothe morphology of tomatoes treated with various Lactobacillus
strains were evidence of an SAR response, leading to resistance tofungal pathogens. Supporting this theory, tomato seeds treatedwith Lactobacillus paracasei isolated from the tomato rhizosphere
produced seedlings that were more resistant to infection by Ralstonia solanacearum due to differential expression of defenserelated metabolites in treated seedlings (Konappa et al., 2016.
The ability of LAB to control bacterial and fungal phytopathogens of crop plants has been investigated (Table 1). Because, LAB are
so ubiquitous in the phyllosphere, LAB were ﬁrst evaluated as BCAs
for foliar phytopathogens (Visser and Holzapfel, 1992), but havebeen evaluated as BCAs for a variety of bacterial and fungal
phytopathogens.
Compost teas fermented with mixed cultures containing
Lactobacillus have been effective against powdery mildew on avariety of cucurbits (DeBacco, 2011; Naidu et al., 2012). Other
compost teas with undeﬁned microbial communities have beeneffective biocontrols of numerous fungal pathogens (Scheuerell and
Mahaffee, 2002; Martin, 2014). It is likely that many compost teaswith undeﬁned microbial populations contain a signiﬁcant proportion of LAB (Ahn et al., 2014), which may have antipathogenic
activity. Similarly, milk, whey and other dairy products have often
been used as a natural control for powdery mildew (Medeiros et al.,2012) and have been applied to various cucurbits (Ferrandino andSmith, 2007; Bettiol et al., 2008; DeBacco, 2011), grape (Crisp
et al., 2006) and greenhouse roses (Wurms et al., 2015). Milk fermented with Lactobacillus is an effective control for powdery
mildew on melon (Bettiol and Astiarraga, 1998). Furthermore, evenuninoculated milk applied to leaves is likely to ferment (Medeiros
et al., 2012), leading to a proliferation of LAB and the associatedantifungal activity.

5. LAB as biocontrol

6. Lactobacillus and stress amelioration

Concerns over the harmful effects many chemical pesticides
have on the environment and human health have prompted a

Climate change and land degradation are expected to make theenvironment more stressful for plants in many regions. Moreover,rhizosphere microbiome has shown that microbial communities in
the rhizosphere are largely shaped by plant species and age, as wellas environmental factors such as temperature and moisture(Grayston et al., 1998). For example, L. lactis subsp. lactis appears to
be a constitutive member of the mulberry microbiome where it iscommonly found in the rhizosphere, despite large geographic distances between plants (Chen et al., 2005).
While many soils do not appear to contain large numbers of LAB,
they do contain a diversity of LAB, which produce a diverse suite of
metabolites (Chen et al., 2005; Yanagida et al., 2006). LAB have beenreported to be most numerous in carbon-rich soil environments,
such as those under fruit trees or animal agriculture (Yanagida
et al., 2005, 2006; Reyes-Escogido et al., 2010), however, a richdiversity of LAB has been isolated from the rhizospheres of olives
and desert trufﬂes as well as in desert soils (Fhoula et al., 2013).
Lactobacilli can survive and grow in dry environments withwater potentials as low as 15 MPa (Focht and Martin, 1979; Skujins,1984) There are also many halotolorant LAB, as is demonstrated by
the diversity of LAB in brined fermented foods. LAB often become
dominant in mixed cultures by virtue of their ability to acidify theirenvironment to a level that many other microbes cannot survive.
4. LAB as biofertilizers

4J.R. Lamont et al. / Soil Biology & Biochemistry 111 (2017) 1e9

Table 1
Selected lactic acid bacteria biocontrol agents.
Species

StrainIsolated from

Antagonistic in vitro

Crop/Pathogen

Proposed
Mechanism

Citation

Lactobacillus
plantarum

L1515aCucumber pickle

Bean & Cucumber/
Pseudomonas
campestris

Organic acids

Visser et al., 1986

Lactobacillus sp.

KLF01

Tomatorhizosphere

Tomato/Ralstonia
solanacearum,
Pepper/Xanthomonas
campestris pv.
vesicatoria, Chinese
Cabbage/
Pectobacterium
carotovorum subsp.
carotovorum

None

Shrestha et al.,2009a; b

Unidentiﬁed LAB

KLC02

Unknown

Pepper/Xanthomonas
campestris pv.
vesicatoria

None

Shrestha et al.,2009a

Unidentiﬁed LAB

KPD03

Unknown

Pepper/Xanthomonas
campestris pv.
Vesicatoria

None

Shrestha et al.,2009aLactobacillus
plantarum

AF1

Kimchi

Xanthomonas
campestris,
Pseudomonas
campestris and
Erwinia carotova
Ralstonia
solanacearum,
Xanthomonas
axonopodis pv. citri,
X. campestris pv.
vesicatoria, Erwinia
pyrifoliae andE. carotovora subsp.
carotovora,
Pectobacterium
carotovorum subsp.
carotovorum
Ralstonia
solanacearum,
Xanthomonas
axonopodis pv. citri,
X. campestris pv.
vesicatoria, Erwinia
pyrifoliae andE. carotovora subsp.
carotovora,
Pectobacterium
carotovorum subsp.
carotovorum
Ralstonia
solanacearum,
Xanthomonas
axonopodis pv. citri,
X. campestris pv.
vesicatoria, Erwinia
pyrifoliae andE. carotovora subsp.
carotovora,
Pectobacterium
carotovorum subsp.
carotovorum
Aspergillus ﬂavus

Soybean/Aspergillus
ﬂavus

Yang and Chang,2010

Lactobacillus spp.

Unknown

Dairy products

Lactobacillus
plantarum

IMAU10014

Fermented maremilk

3,6-bis(2methylpropyl)-2,5piperazinedion
SAR, antifungal
metabolites
proteinacious andnon-proteinacious
antifungal
compounds

Lactobacillus
plantarum

C5

Durian fruit

Lactobacillus
plantarum

G7

Ginger root

Unidentiﬁed LAB

Unknown

Unknown

Lactobacillus
plantarum

ONU87

Unknown

Rhizobium
radiobacter

Lactobacillus
paracasei
Lactobacillus
plantarum

Unknown

Unknown

Unknown

Unknown

Ralstonia
solanacearum
N/A

SLG17

Unknown

Lactobacillus
plantarum

Fusarium
oxysporum
Botrytis cinerea,
Alternaria solani,
Phytophthora
drechsleri, Fusarium
oxysporum andGlomerella cingulate
Streptococcus,
Bacillus subtilis,
Protous, Klebsilla, E.
coli and S. aureous
Streptococcus,
Bacillus subtilis,
Protous, Klebsilla, E.
coli and S. aureous
Pythium ultimum

Fusariumgraminearum

Tomato/Fusarium
oxysporum
N/A

Hamed et al., 2011
Wang et al., 2011

Pepper seed/
Colletotrichum
capsidNone

Elmabrok andHussin 2012

Pepper seed/
Colletotrichum
capsidNone

Elmabrok andHussin 2012

Cucumber/Pythium
ultimum
Carrot &Kalanchoe/
Rhizobium
radiobacter
Tomato/Ralstonia
solanacearumApple & Pear/
Erwinia amylovora

None

Lutz et al., 2012

None

Korotaeva et al.,
2013

None

Murthy et al., 2012

Preemptive
colonization,
plantericin
Organic acids,
plantericin

 et al., 2013
Rosello

Wheat/Fusarium
graminearum

Baffoni et al., 2015

J.R. Lamont et al. / Soil Biology & Biochemistry 111 (2017) 1e95

Table 1 (continued )Species

StrainIsolated from

Antagonistic in vitro

Crop/Pathogen

Proposed
Mechanism

Citation

Lactobacillus
paracasei

Unknown

Unknown

N/A

Tomato/Ralstonia
solanacearum

SAR

Konappa et al.,
2016

Table 2
Selected lactic acid bacteria biostimulants.
Species

StrainIsolated from

Crop

EffectProposed
Mechanism

Citation

Lactobacillus
plantarum
Lactobacillus
acidophilus

IFO 3070

EM-4

RadishIncreased yield

None

Higa and Kinjo, 1991

Unknown

Dairy products

TomatoNone

Hamed et al., 2011

Lactobacillus sp.

Unknown

Dairy products

TomatoNone

Hamed et al., 2011

Lactobacillus
plantarum

NRRL B-4524

TomatoNone

Hamed et al., 2011

LAB

Unknown

None

Lutz et al., 2012

Lactobacillus
plantarum
Lactobacillus
plantarum

ONU 12The National Center
for Agricultural
Utilization
Research
Agricultural
rhizosphere
Grape must

Increased shootbranching, shootand root growth
Increased shootbranching, shootand root growth
Increased shootbranching, shootand root growth

Bacteriogenic
metabolites
Bacteriogenic
metabolites

Limanska et al., 2013

TomatoTomatoONU 315, 316

Oyster mushroom
surface

TomatoLactobacillus
plantarum

ONU 991

Dairy products

TomatoLactobacillus
acidophilus
Lactobacillus casei

WR2

Wheat rhizosphere

Wheat

6

Embiko® microbial
phytostimulant

Cucumber

Lactobacillus lactis

4/6

Cucumber

Lactobacillus
plantarum

20

Embiko® microbial
phytostimulant
Embiko® microbial
phytostimulant

Lactobacillus sp.

KLF01

Tomatorhizosphere

PepperUnidentiﬁed LAB

KLC02

Unknown

PepperUnidentiﬁed LAB

KPD03

Unknown

PepperLactobacillus
plantarum
Lactobacillus
plantarum

8Р-AZ

Human probiotic

Wheat

Unknown

PGPR Corp. (Korea)

Cucumber

LAB

BL06

Sugarcane ferment

Citrus seedling

Lactobacillus
plantarum

ATCC 9019

Unknown

Swertia chirayita

Cucumber

Increased
germination rate
Increased shoot androot growth
Increased
germination rate,shoot and root
growthIncreased
germination rate,
root growth
Increase height andchlorophyll content
Increased
germination rate,
inhibited seedling
growthIncreased seedling
growth rate
Increased
germination andseedling growthrate
Increased root
length, shootlength, root fresh
weight andchlorophyll content
Increased root
length, shootlength, root fresh
weight andchlorophyll content
Increased root
length, shootlength, root fresh
weight andchlorophyll content
Osmotic stressalleviation
Increased growth,
nutrient uptake andamino acid content

Increased height,
stem diameter, dryroot and shootweightSalt stressalleviation

Limanska et al., 2013

Bacteriogenic
metabolites

Limanska et al., 2013

Bacteriogenic IAA

Mohite, 2013

None

Rzhevskaya et al., 2014

None

Rzhevskaya et al., 2014

None

Rzhevskaya et al., 2014

Bacteriogenic IAA,
phosphatesolubilization

Shrestha et al., 2014

Bacteriogenic IAA,
phosphatesolubilization

Shrestha et al., 2014

Bacteriogenic IAA,
phosphatesolubilization

Shrestha et al., 2014

Bacteriogenic NO
signaling
Increased nutrient
availability via
succinic acid andlactic acidproduction
Phosphatesolubilization,
nitrogen ﬁxation

Yarullina et al., 2014

Altered plant stressresponse

Kang et al., 2015

Giassi et al., 2016

Phoboo et al., 2016

6

J.R. Lamont et al. / Soil Biology & Biochemistry 111 (2017) 1e9

increasing food, ﬁber, and energy demands from a growing population will force more agricultural production onto marginal lands,
imposing even more stress on food production globally. Stressalleviation with microbial treatments offers a low-input, lowenvironmental impact way to sustain food production in a morestressful environment.
Extremophilic microorganisms; those which live in extreme
environments, often play an important, or even essential, role in thesurvival of plants native to harsh environments (Rodriguez andRedman, 2008). The ability of symbiotic microorganisms to alleviate abiotic stresses in their host plant has been well documented.
In fact, the effects of many PGPM are only noticeable when plants
are subjected to environmental stress (Wang et al., 2012;
Subramanian, 2014; Prudent et al., 2015). PGPM can improve theability of plants to withstand stressful environments by protecting
plants from abiotic stresses or by altering the stress response of theplant, thus improving the survival of the entire phytomicrobiome.
Production of reactive oxygen species (ROS) and ethylene arealso common plant stress responses. Both aid in responding to andwithstanding stress at low concentrations, but are detrimental athigher concentrations. Increasing tissue concentrations of ROS
prompts the production of enzymatic and non-enzymatic antioxidants, which scavenge ROS; protecting plants from the harmful
oxidizing effects of ROS. Plants will often synthesize osmolytes,
such as proline, to regulate cellular osmotic potential in response toa variety of abiotic stresses.
Strains of Lactobacillus have been shown to ameliorate abiotic
stress in plants (Table 2). Phoboo et al. (2016) found that clones ofthe medicinal plant, Swertia chirayita, that were inoculated with
L. plantarum (ATCC 9019) were more resilient to salt stress. Plants
treated with L. plantarum had an altered metabolic response to salt
stress. With increasing salt concentrations, treated plants had
increased concentrations of proline and decreasing total phenolicconcentrations whereas untreated plants had consistently low
proline concentrations and consistently high phenolic concentrations across salt concentrations. Treated plants also had decreasing
antioxidant activity with increasing salt concentrations except for
guaiacol peroxidase, which increased with increasing salt
concentrations.
Strains of L. plantarum has been shown to produce a variety ofpolyamines, including putrescene, citrulline and ornithine (Arenaand Manca de Nadra, 2001). Bacterial plant growth promotion
was observed in a pot experiment in which bean plants were grownin soil inoculated with a polyamine-producing strain of Streptomyces griseoluteus (Nassar et al., 2003). While the relationship is
not yet elucidated, there appears to be a link between polyaminesand plant stress response pathways, including the NO pathway(Yamasaki and Cohen, 2006; Pang et al., 2007; Hussain et al., 2011;
Alc
azar and Tiburcio, 2014). The ability of LAB to produce polyamines, NO, or other signal molecules may contribute to plant
growth stimulation or stress alleviation.
Microbe-associated molecular patterns (MAMPs) are known tochange plant response to biotic stresses (Henry et al., 2012) andabiotic stresses and it is likely that MAMPs produced by LAB are
responsible for increases resilience of plants treated with LAB. Noneof these MAMP elicitors for LAB have yet been identiﬁed, but theidentiﬁcation of MAMP elicitor compounds could lead to a better
understanding of the plant-microbe relationship, as well as enable
to puriﬁcation of active MAMP compounds for use as bioelicitors.
Many of the intricacies of plant stress response networks have
yet to be completely understood, but it appears that treatment with
LAB can signiﬁcantly alter plant stress response to the beneﬁt of theplant.

7. LAB as biostimulant
Some plant growth promoting microorganisms produce hormones that can stimulate plant growth (Tsavkelova et al., 2006);
however, there is little evidence that bacteriogenic hormones play asigniﬁcant role in plant growth stimulation by LAB. L. acidophilus
has been reported to produce cytokinens (Lynch, 1985), and somestrains of Lactobacillus have been shown to produce indole-3-acetic
acid (IAA) (Mohite, 2013; Shrestha et al., 2014; Giassi et al., 2016)
while others do not (Kang et al., 2015).
While Lactobacillus has been shown to promote growth indiverse crops (Table 2), the underlying mechanisms of this biostimulation remain unclear. There appears to be plant and strain
speciﬁcity in Lactobacillus phytostimulation. Screens of hundreds of
Lactobacillus strains may only yield a few stimulatory strains (Lutzet al., 2012). Furthermore, different strains of the same Lactobacillus
species may produce different morphological changes in the sameplant (Hamed et al., 2011; Limanska et al., 2013; Rzhevskaya et al.,2014).
Most early EM research did not characterize the activity of individual members of the EM consortium, however, Higa and Kinjo(1991) found that radish had a dose-dependent growth response tovarying concentrations of L. plantarum cultures, with plants treatedwith the greatest concentration of culture growing larger thanuntreated plants. Treatment with the EM consortium can also affectplant growth and development directly. Applications of an EM
product containing at least ﬁve Lactobacillus strains changed themorphology of Lolium perenne, to make it less susceptible to mechanical damage associated with turf grass management (Gaggìa
et al., 2013). Axel et al. (2012) suggest elucidating the role of LAB
in EM by isolating LAB members of the EM consortia to test forbioactivity.
Kang et al. (2015) investigated the effects of three potential
members of an EM consortia, Rhodobacter sphaeroides, Saccharomyces cerevisiae and Lactobacillus plantarum on the growth anddevelopment of cucumber. All three microorganisms increased
cucumber growth, nutrient uptake and amino acid content. The
plant growth stimulation observed for R. sphaeroides was attributed
to large quantities of IAA, measured in R. sphaeroides media ﬁltrate.
There was no IAA detected in media ﬁltrate from L. plantarum,
suggesting it produced another compound that inﬂuenced plant
growth. In contrast, others have suggested IAA produced by LAB is
responsible for plant growth promotion (Mohite, 2013; Shrestha
et al., 2014). LAB likely promote plant through diverse environmental-, strain-, and host-dependant mechanisms, which have yet
to be elucidated.
8. Limitations and new directions
Some of the major limitations to widespread implementation of
PGPMs are developing effective and efﬁcient methods to screen for
PGPMs; ensuring PGPMs can survive and have the desired bioactivity in the ﬁeld environment; and developing effective and efﬁcient formulations for applying PGPMs (Le Mire et al., 2016).
Traditional methods of screening for PGPMs in vitro may not beadequate to discover all PGPMs. For example, de Melo Pereira et al.
(2012) screened strawberry fruit for potential PGPM endophytes,
and, while they found several strain of L. plantarum, the only
criteria used to identify PGPM were IAA production, N ﬁxation andsiderophore production. Along with overlooking strains that may
be effective PGPMs, in vitro screens may identify strains as good
PGPM candidates that do not preform well in the ﬁeld. In theirinvestigation of LAB as BCAs, Visser and Holzapfel (1992) foundthere is often there is little correlation between in vitro antagonism
and practical pathogen control in the ﬁeld.

J.R. Lamont et al. / Soil Biology & Biochemistry 111 (2017) 1e9

As with other PGPMs, a major limitation to the use of LAB inagricultural applications is its ability to survive and produce sufﬁcient quantities of bioactive metabolites in the required environments. Visser and Holzapfel (1992) suggested this could beovercome by isolating or engineering strains that are well suited tothe phyllosphere environment; applying cultures with essential
nutrients or protective carriers; reapplying cultures to maintainhigh numbers of viable cells; however, these methods arecumbersome, and time consuming. Using plant growth promoting
LAB selectively in environments which are more conducive to its
growth; such as fruits, ﬂowers, and highly organic soils, may be
another option. This approach has been successful in the control of
ﬂoral pathogens of rosaceous tree crops (Bonaterra et al., 2013; et al., 2013), and shows great poMartinez et al., 2008; Rosello
tential in the control of postharvest pathogens (Trias et al., 2008).
Another approach would be to produce bioactive compounds
from LAB grown under ideal conditions in bioreactors. Supernatants from LAB bioreactors, or even puriﬁed bioactive compounds
could then be applied to crops, and the survival of the LAB would
not be a concern. Furthermore, some research has shown thatexcreted metabolites are responsible for the activity of LAB (Omeret al., 2010; Limanska et al., 2015a, b). The strategy of isolating
and purifying bacteriogenic bioactive compounds has been successfully employed for the phytostimulatory bacteriocin from Bacillus thuringiensis NEB17, thuricin 17 (Gray et al., 2006); and thephytostimulatory lipo-chitooligosaccharide from Bradyrhizobium
japonicum 532C (Prithiviraj et al., 2003.
Although LAB can survive under harsh environmental conditions, they have complex nutritional requirements for growth.
There has been some research into formulating LAB media based inorganic wastes from sugar beet (Krzywonos and Eberhard, 2011)
and sweet potato processing (Hayek et al., 2013) on an industrial
scale, but a consistent LAB medium is needed to improve the sustainability of industrial LAB culture. Higa and Kinjo (1991) suggestthat LAB are not as effective as a pure culture and should be appliedin a consortium of complimentary microorganisms, such as EM. In
the EM framework, the complex nutritional requirements of LAB
are satisﬁed with metabolites from other members of the consortium. In contrast to this view, Giassi et al. (2016) found that
inoculation with a pure LAB strain promoted growth, but a mixtureof this LAB strain and other PGPBs did not promote plant growth,suggesting inhibitory competition between strains. With this inmind, PGPM consortia must be carefully designed to avoid
incompatibility.
LAB strains can improve plant production by improving nutrient
availability, acting as a BCA, alleviating biotic and biotic stresses,
and directly stimulating plant growth. These plant growth promoting characteristics paired with their long history in food science, and the GRAS status of many LAB, including all lactobacilli,
make them particularly well suited for applications in plant production. Despite being a common member of the phytomicrobiome, LAB have been largely overlooked as potential PGPBs.
Historical and current research demonstrates a clear potential for
LAB as useful, renewable and safe agricultural inputs to improve
plant growth. Re-examining uses for such ubiquitous organisms
could contribute to solving some of the issues facing food production in the 21st century.
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