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Use of beneficial bacteria and their secondary metabolites to control grapevine pathogen diseases

TLDR
The current knowledge on new strains from the rhizo- and endosphere and their metabolites that can be used on grapevine plants to counteract pathogen attack needs to be discussed.
Abstract
Grapevine is one of the most important economic crops yielding berries, wine products as well as derivates. However, due to the large array of pathogens inducing diseases on this plant, considerable amounts of pesticides—with possible negative impact on the environment and health—have been used and are currently used in viticulture. To avoid negative impacts of such products and to ensure product quality, a substantial fraction of pesticides needs to be replaced in the near future. One solution can be related to the use of beneficial bacteria inhabiting the rhizo- and/or the endosphere of plants. These biocontrol bacteria and their secondary metabolites can reduce directly or indirectly pathogen diseases by affecting pathogen performance by antibiosis, competition for niches and nutrients, interference with pathogen signaling or by stimulation of host plant defenses. Due to the large demand for biocontrol of grapevine diseases, such biopesticides, their modes of actions and putative consequences of their uses need to be described. Moreover, the current knowledge on new strains from the rhizo- and endosphere and their metabolites that can be used on grapevine plants to counteract pathogen attack needs to be discussed. This is in particular with regard to the control of root rot, grey mould, trunk diseases, powdery and downy mildews, pierce’s disease, grapevine yellows as well as crown gall. Future prospects on specific beneficial microbes and their secondary metabolites that can be used as elicitors of plant defenses and/or as biocontrol agents with potential use in a more sustainable viticulture will be further discussed.

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Use of benecial bacteria and their secondary
metabolites to control grapevine pathogen diseases
Stéphane Compant, Günter Brader, Saima Muzammil, Angela Sessitsch,
Ahmed Lebrihi, Florence Mathieu
To cite this version:
Stéphane Compant, Günter Brader, Saima Muzammil, Angela Sessitsch, Ahmed Lebrihi, et al.. Use of
benecial bacteria and their secondary metabolites to control grapevine pathogen diseases. BioControl,
Springer Verlag, 2013, vol. 58 (n° 4), pp. 435-455. �10.1007/s10526-012-9479-6�. �hal-01177560�

Any correspondence concerning this service should be sent to the repository administrator:
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DOI:10.1007/s10526-012-9479-6
Official URL: http://dx.doi.org/10.1007/s10526-012-9479-6
This is an author-deposited version published in: http://oatao.univ-toulouse.fr/
Eprints ID: 9738
To cite this version:
Compant, Stéphane and Brader, Günter and Muzammil, Saima and Sessitsch,
Angela and Lebrihi, Ahmed and Mathieu, Florence Use of beneficial bacteria
and their secondary metabolites to control grapevine pathogen diseases. (2013)
BioControl, vol. 58 (n° 4). pp. 435-455. ISSN 1386-6141
Open Archive Toulouse Archive Ouverte (OATAO)
OATAO is an open access repository that collects the work of Toulouse researchers and
makes it freely available over the web where possible.


can be infected and colonized by a large variety of
pathogenic microorganisms such as deleterious fungi,
oomycetes and bacteria (Gouadec et al.
2007). These
vine diseases can have drastic effects on the host
plants, on berr ies, but also on wine qualities and their
sensorial and organoleptic properties (Gouadec et al.
2007), resulting in economi c losses for the wine
grower
s and producers (van Helden 2008).
Pesticides have been or are currently applied in the
vineyard to avoid the outbreak of vine pests or diseases,
to manage the surrounding flora, to increase grape yield
and to ensur e wine quality (Leroux
2003; Pezet et al.
2004). As for instance in France more than 30,000 t
year
-1
of fungicides and bactericides have been
used for grapevine production (FAOSTAT 2011).
For Europe, the International Organization of Vines
and Wine estimates that 70,000 t of fungicides are used
annually on around 3.8 million hectares of land
dedicated to viticulture (http://www.endure-network.
eu/). Worldwide, on average 35 % of all pesticides are
used for viticulture. The continuous use of phytosani-
tary products during the last decades has been, how-
ever, accompanied by an increasing awareness of the
problems arising from intensive pesticide use. Conse-
quences of intensive pesticide use include their per-
sistence in soils, contamination of the environment,
as well as appearance of resistant pathogenic strains
(Leroux 2004). Additionally, specific pesticides have
been
withdrawn from the market due to their negative
impact on human health and the environment (Amaro
and Mexia 2003). Development of new active mole-
cules
targeting vine
pests without undesired impact is
possible. However, due to increasing costs to develop
these new molecu les, other alternative solutions have
also been proposed.
To reduce the use of phytosanitary produc ts,
genetically modified (GM) plants have been propa-
gated to control vine pests and diseases (see for
examples the studies of Ferreira et al.
2004; Agu
¨
ero
et
al. 2005;
Vidal et al. 2006; The Local Monitoring
Committee et al. 2010). However, this alternative
strategy has not been and is still not widely accepted.
So far, no GM grapevine has been commercialized
(The Local Monitoring Committee et al.
2010). Many
regions, especially in Europe, are generally not in
favour of cultivation of GM crops (Marshall 2009), so
there is a need for other solutions.
One of the alternative strategies to reduce the use of
pesticides in grapevine production corresponds to the
use of beneficial bacteria as biocontrol agents (Bent
2006). Since the rhizosphere concept of Lorenz
Hiltner describing
that the soil surrounding roots is
influenced by plants and by microorganisms (Hiltner
1904; Hartmann et al. 2008), a large n umber of studies
have demonstrated that part of the rhizobacteria
inhabiting the rhizosphere can stimulate plant growth
(plant growth-promoting rhizobacteria; PGPR) as well
as protect plants against pathogen infections (biocon-
trol strains) (Berg
2009; Lugtenberg and Kamilova
2009). Plant growth promotion (e.g. achieved by
hormone
stimulation
or changed nutrient availability)
and biocontrol activities of particular rhizobacteria
strains are disti nct issues. However, in practice this
is often hard to dissect as bacteria can show both
activities. Also, particularly in field or in green-
house trials, biocontrol bacteria might promote plant
growth by reducing pathogenic pressures. Biocontrol
by beneficial bacteria might be achieved by direct
antibiosis, competition for niches and nutrients, inter-
ference with pathogen signalling or by inducing plant
resistance (Fig. 1, Berg 2009; Lugtenberg and Kamil-
ova 2009). Moreover biocontrol might be achieved by
degrad
ation of virulence factors or phytotoxins of
pathogens, thereby leading to reduction of disease
symptoms (Compant et al.
2005a). Considerable
literature information has shown that rhizobacteria
can secrete various secondary metabolites (SMs).
Both rhizobacteria and SMs produced by them can act
on pathogens by depriving the path ogens of nutrients
(competition), lysing cells and/or blocking specific
functions related to pathogen growth (antibiosis) and
act therefore as biocontrol agents (Berg 2009; Com-
pant
et al.
2005a;
Lugtenberg and Kamilova 2009).
Rhizobacteria and their SMs are also known to induce
plant defense reactions leading to a systemic resis-
tance or priming of above-ground parts to be more
resistant to subsequent pathogen infections (Berg
2009
; van Loon 2008; van Loon and Bakker 2005),
and
this can be used for grapevine protection against
phytopathogenic disease s.
Already since the nineteenth century with the
description of bacteria-like structures by Woronin
(the so-called Frankia sp.) and the work of Galippe
and di Vestea (see Compant et al. 2010a , 2012) with
bacteria
other than root nodulating strains, it has been
widely accepted that specific microsymbionts can
also colonize different host plants and plant parts.
Although sources of colonization of these endophytic

bacteria could be the anthosphere, the caulosphere,
the phyllosphere or the spermosphere, the prevailing
opinion suggests colonization of a large fraction
of the endophytic population from the rhi zosphere as
described by microscopic, genetic as well as metage-
nomic evidences (Hallmann
2001; Hallmann and Berg
2007; Compant et al. 2010a).
As rhizobacteria,
also endophytes are known to
stimulate host plant growth and can act as biocontrol
agents to alleviate infection by pathogenic strains,
in particular cases even to higher levels than root-
restricted bacteria (Welbaum et al. 2004; Hallmann
and Berg 2007).
Bacterial endophytes inhabiting plant
internal tissues are also a source of SMs that may act as
elicitors of plant defenses or as antimicrobi al agents
with potential use to control disease (Qin et al.
2011).
Different elicitors of plant defenses are known
from beneficial bacteria, both from the rhizo- and the
endosphere of plants. This includes a variety of
primary bacterial constituents such as flagella (flagel-
lin) or lipopolysaccharides (LPS) but also SMs with
high structural diversity specific for certain strains
(Qin et al. 2011; van Loon and Bakker 2005). In
additio
n, continuous research and discovery of novel
elicitors and strains from different environments,
particularly from harsh ecosy stems, will likely yield
novel strains and elicitors capable of triggering plant
defenses and enabling resistance. Th is is especially
interesting for the reduction of the use of pesticides in
viticulture, where—in Franc e—up to 50 % of the total
pesticide entry is used for only 3.3 % of cultivated
surfaces and in EU 3.5 % of the cultivated land
receives 15 % of the total pesticide entry representing
20–22 kg of pesticide per ha used for grapevine
(Compant
2011; Compant and Mathieu, 2011).
The role of both rhizobacteria and endophytes
in biocontrol of plan t diseases or for a sustainable
management of agriculture has been highlighted
(van Loon and Bakker 2005; Lugtenberg and
Kamilov
a 2009) and information on the usage of
beneficial microbes in viticulture is currently emerg-
ing. Research performed on specific strains have
moreover allowed the description of SMs secreted by
specific strains (both rhizo- and endosphere colonizing
bacteria), which may be responsible for their effects
on pathogen targets and/or on resistance mechanisms
of grapevine plants (Compant and Mathieu 2011).
Addit
ionally, new beneficial bacterial strains and SMs
to control plant diseases with potential use in viticul-
ture are continuously described (Compant
2011).
Nevert
heless, a better understanding of how and
which microorganisms or bacterial metabolite s can
Beneficial bacteria
and metabolites
Pathogens
Protection
competition for space and nutrients & colonization;
antibiosis (excretion of lytic enzymes or production of antibiotics);
interference with pathogen signaling e. g. by degrading enzymes or by
interfering metabolites;
reduction of disease symptoms by degradation or interference with pathogen
toxins or virulence factors
Induced (systemic) resistance
Fig. 1 Drawing summarizing the potential mechanisms involved in the control of grapevine pathogen diseases by beneficial bacteria
and their secondary metabolites

Citations
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Journal ArticleDOI

Advances in plant growth-promoting bacterial inoculant technology: formulations and practical perspectives (1998–2013)

TL;DR: Practical aspects of bacterial inoculants for contemporary agriculture and environmental restoration is critically evaluated from the point of view of their current technological status, current applications, and future use.
Journal ArticleDOI

Managing Grapevine Trunk Diseases With Respect to Etiology and Epidemiology: Current Strategies and Future Prospects

TL;DR: A number of areas of future prospect for effective management of GTDs worldwide, which, if addressed, will provide a positive outlook on the longevity of vineyards in the future are identified.
Journal ArticleDOI

Biotechnological Applications of Bacterial Endophytes

TL;DR: Possible traits required by these bacteria to enter the plant and live inside will be discussed and possible biotechnological applications of bacterial endophytes are focused on.
Journal ArticleDOI

Challenges for Managing Candidatus Liberibacter spp. (Huanglongbing disease pathogen): Current Control Measures and Future Directions

TL;DR: This work summarizes the greenhouse and field studies that have documented the effects and implications of chemical-based treatments and nonchemical measures for phytopathogen control and adverse impacts of broad-spectrum treatments on plant-beneficial microbiota, and potential implications on public and ecosystem health.
References
More filters
Journal ArticleDOI

Plant-growth-promoting rhizobacteria.

TL;DR: This review restricts itself to bacteria that are derived from and exert this effect on the root and generally designated as PGPR (plant-growth-promoting rhizobacteria), which can be direct or indirect in their effects on plant growth.
Journal ArticleDOI

Use of Plant Growth-Promoting Bacteria for Biocontrol of Plant Diseases: Principles, Mechanisms of Action, and Future Prospects

TL;DR: As agricultural production intensified over the past few decades, producers became more and more dependent on agrochemicals as a relatively reliable method of crop production.
Journal ArticleDOI

Plant growth-promoting bacteria in the rhizo- and endosphere of plants: Their role, colonization, mechanisms involved and prospects for utilization

TL;DR: The individual steps of plant colonization are described and the known mechanisms responsible for rhizosphere and endophytic competence are surveyed to better predict how bacteria interact with plants and whether they are likely to establish themselves in the plant environment after field application as biofertilisers or biocontrol agents.
Journal ArticleDOI

Induced Systemic Resistance and Promotion of Plant Growth by Bacillus spp.

TL;DR: Two products for commercial agriculture have been developed, one aimed mainly at plant growth promotion for transplanted vegetables and one, which has received registration from the U.S. Environmental Protection Agency, for disease protection on soybean.
Journal ArticleDOI

Plant–microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture

TL;DR: The use of microorganisms and the exploitation of beneficial plant–microbe interactions offer promising and environmentally friendly strategies for conventional and organic agriculture worldwide.
Related Papers (5)
Frequently Asked Questions (18)
Q1. What are the contributions mentioned in the paper "Use of beneficial bacteria and their secondary metabolites to control grapevine pathogen diseases" ?

In this paper, a review of the use of biocontrol agents for grapevine diseases is presented. 

Considerable information on the possibility to use biocontrol agents of bacterial origin to fight a variety of grapevine diseases affecting yield and productivity has become available. Any application of specific microbe ( s ) should lead to study its behaviour inside grape plants and also the interaction with the natural microflora. The research for mechanisms involved can be of high importance for a better understanding of the processes involved and should subsequently also lead to better applications in disease management. In case of a climate change scenario ( Compant et al. 2010b ), some strains isolated from desert soil can be promising agents as they are adapted to more extreme conditions ( unpublished results ). 

The state of plant resistance was associated with a stimulation of plant defense responses such as chitinase and b-1,3glucanase activities (with known botryticidal activities) in both leaves and berries (Magnin-Robert et al. 2007), again indicating a major contribution of enhanced plant resistance in response to the biocontrol strains. 

Additionally studying effect of new biocontrol bacteria as well as new metabolites having the abilities to control cropdisease or to stimulate plant defense reactions is of special importance for fundamental knowledge and development. 

Although the extent of disease control depends on the grape variety tested, the results suggest that there is potentially beneficial effect in using the antagonists to diminish the influence of latent rootstock infection of crown gall. 

A potential mechanism of how bacterial diseases can be controlled is by cross protection with mild or avirulent strains of the disease causing agents (Seemüller and Harries 2010). 

cyclic bacterial metabolites (tetracyclopeptides) secreted by these latter strains can induce protection directly by antibiosis or indirectly by inducing various plant defense responses leading to protective effects (Lebrihi et al. 2009a, b). 

Bacillus strains and bacterial SMs acting as bioeffectors may also have the advantage to be used in combination with synthetic or inorganic antifungal compounds. 

The syndromes are brown wood streaking of rooted cuttings, Petri disease with brown wood streaking in young vines, young esca (also recently called phaeotracheomicosis), white rot, and escaproper (addition of young esca with white rot; Gramaje and Armengol 2011; Graniti et al. 

rhamnolipids potentiated defense responses induced by chitosan elicitor and by the culture filtrate of B. cinerea (Varnier et al. 2009), suggesting that the combination of rhamnolipids with other effectors could participate in grapevine protection against the grey mould disease. 

At the moment, apart from fungicide use, various Trichoderma strains are in discussion as potential biocontrol agents for dieback (John et al. 

Since only limited means for the control of trunk disease exist, development ofbioncontrol strains will be an important factor in the future for controlling trunk disease in viticulture. 

an effective biocontrol strain against Eutypa dieback has high potential in application, especially if this strain could also control a number of other fungi causing similar symptoms/other trunk diseases. 

Such cross protection with avirulent strains has been observed with phytoplasma (Ca. Phytoplasma prunorum) infected apricots, where infections with avirulent or mild strains seem to have a pre-immunizing effect (Seemüller and Harries 2010), either competing with disease causing phytoplasmas or enhancing the resistance of colonized plants. 

With Rahnella aquatilis HX2, it has been shown in field trials that immersion of the basal ends of grape cuttings with HX2 cell suspension inhibited or evencompletely prevented crown gall formation caused by A. vitis K308 (30.8 % compared to 93.5 % in plants without HX2). 

It may be speculated that jasmonate and ethylene dependent induced resistance is important in enhanced grapevine resistance to Fusarium rot—at least after P. fluorescens treatment—since the contribution of these signal pathways in enhanced resistance in Arabidopsis after treatment with different P. fluorescens strains is well established (van der Ent et al. 2009; van Wees et al. 2008). 

In a two-year assay on cv. ‘Himrod’ in the vineyard, strain Syc86-1 (isolated from sycamore), but not strain PD-1 (derived from grapevine), was effective in limiting the development of Pierce’s disease. 

it has been further demonstrated that spraying a suspension of this strain on grape wood reduces infection with the pathogenic agent (with a 100 % reduction; Ferreira et al. 1991).