Introduction
Since several chemical pesticides have been shown to be detrimental on
human health and ecosystems, considerable research has been done to find
more environment-friendly plant protection solutions (Gay, 2012;
Hernández et al. , 2013; Wang et al. , 2013; Carvalho,
2017). Elicitors, defined as molecules able to stimulate defence
responses in a host plant, are one of the emerging alternatives (Paréet al. , 2005; Henry et al. , 2012; Thakur and Sohal, 2013).
They
can be derived from plants (termed as Damage-Associated Molecular
Patterns (DAMPs)) or microorganisms (referred as Microbe-Associated
Molecular Patterns (MAMPs) or Pathogen-Associated Molecular Patterns
(PAMPs)) (Yu et al. , 2017; Malik et al. , 2020). For
example, flagellin (flg22) or cryptogein are a bacterial and a fungal
elicitor respectively (Gómez-Gómez and Boller, 2002; Gerbeau-Pissotet al. , 2014), or chemically synthesized molecules like
rhamnolipids (RLs) or COS-OGA also act as elicitors (Clinckemaillieet al. , 2017; Luzuriaga-Loaiza et al. , 2018). They can
hence be of different chemical natures like carbohydrate polymers,
lipids, peptides or proteins (Boller and Felix, 2009; Thakur and Sohal,
2013; Jogaiah et al. , 2019; Pršić and Ongena, 2020). Recognition
of elicitors by the plant cells first triggers early defence responses
among which the release of reactive oxygen species (ROS) (superoxide
anion (O2●¯), hydrogen peroxide
(H2O2) and hydroxyl radical
(●OH)), also known as the oxidative burst (Mittler,
2017; Camejo et al. , 2019; Wang et al. , 2019; Zaid and
Wani, 2019). The perception of elicitors by plant cells further results
in protection based on the activation of signalling cascades and defence
mechanisms leading to the induction of plant immunity, like the systemic
acquired resistance (SAR) and the induced systemic resistance (ISR)
(Malik et al. , 2020; Pršić and Ongena, 2020).
In addition to be a selective barrier between the cell and the
extracellular medium, the plasma membrane is a sensor for modification
of cellular environment and plays thus a key role in the recognition
process of bioactive molecules.
While most of elicitors are
perceived by membrane proteic receptors, the involvement of the lipid
part of the cell membrane has not been ruled out (Nimchuk et al. ,
2003; Deleu et al. , 2018). Indeed, many danger signals or
invasion patterns are recognized by specific pattern recognition
receptors within PPM (Schellenberger et al. , 2019; Pršić and
Ongena, 2020), and some amphiphilic elicitors, like surfactin fromBacillus and RLs from Pseudomonas , have been strongly
suggested to be perceived by the lipid fraction of PPM (Henry et
al. , 2011; Gerbeau-Pissot et al. , 2014; Haba et al. ,
2014; Luzuriaga-Loaiza et al. , 2018; Monnier et al. , 2018;
Herzog et al. , 2020; Come et al. , 2021). Vey recently, it
was demonstrated that the RL-triggered immune response is affected by
the sphingolipid composition of the plasma membrane and thus independent
of a receptor (Schellenberger et al. , 2021).
Fatty acid hydroperoxides (HPOs) are amphiphilic molecules naturally
produced by plants in response to (a)biotic stresses by the oxidative
catabolism of polyunsaturated fatty acids. They belong to the large
family of plant oxylipins (Blée, 2002; Wasternack and Feussner, 2018;
Genva et al. , 2019). Oxylipins are ubiquitous in the plant
kingdom and can either be esterified, notably in biological membranes,
or be found in free form. Among them, the best known are the jasmonates,
a family of molecules including jasmonic acid (JA), its derivatives and
some JA precursors such as 12-oxo-phytodienoic acid (OPDA) and
12-dinor-oxo-phytodienoic acid (dnOPDA) (Wasternack and Strnad, 2018).
JA is obtained from 13-hydroperoxy-9,11,15-octadecatrienoic acid
(13-HPOT) following the successive action of various enzymes
(lipoxygenase, etc.) (Deboever et al. , 2020a ). 13-HPOT and
its dienoic equivalent, 13-hydroperoxy-9,11-octadecadienoic acid
(13-HPOD), are key intermediates in the synthesis of jasmonates and
other oxylipins, and have been extensively studied for their signalling
properties (Deboever et al. , 2020b ).
In
the recent years, HPOs have emerged as a promising plant defence
solution and their exogenous application to protect plants against
phytopathogens has been considered (Granér et al. , 2003; Prostet al. , 2005; Deboever et al. , 2020a ). However,
their biological activities in plant defence and hence their potential
as elicitors still remain elusive.
In addition, in our previous study
(Deleu et al. , 2019), we have shown that HPOs are able to
interact with PPM lipids inducing a perturbation of their lateral
organization. We have suggested that, by this interaction, HPOs could
activate cellular signaling involved in plant defense mechanisms.
In the present study, we first explored the potential of exogenously
applied HPOs to protect Arabidopsis thaliana plants againstBotrytis cinerea by a systemic signalling mechanism. Their
eliciting activity was evaluated by measuring ROS production byArabidopsis thaliana cells in their presence. In a second part,
the molecular mechanism of HPO perception by the PPM was further
investigated on plant biomimetic lipid systems by using a panel of
complementary biophysical tools. More particularly, we analysed the
effects of HPOs on the transversal organization and on the structure of
the PPM bilayer.
The relationship between the results of biological assays and the effect
of HPOs on model plant plasma membrane suggests that their action on the
lipids might trigger early plant defence events.