Abstract:
Reactive oxygen species are important signaling molecules that influence
many aspects of plant biology. One way in which ROS influence plant
growth and development is by modifying intercellular trafficking through
plasmodesmata (PD). Viruses have evolved to use plasmodesmata for their
local cell-to-cell spread between plant cells, so it is therefore not
surprising that they have found ways to modulate ROS and redox signaling
to optimize plasmodesmata function for their benefit. This review
examines how intracellular signaling via ROS and redox pathways regulate
intercellular trafficking via PD during development and stress. The
relationship between viruses and ROS-redox systems, and the strategies
viruses employ to control PD function by interfering with ROS-redox in
plants is also discussed.
Introduction
Reactive oxygen species (ROS) are oxygen-containing molecules that are
highly reactive due to the presence of unpaired electrons. In plant
cells, ROS are produced as natural byproducts of various metabolic
processes (Mittler, 2017). While ROS are important for various signaling
and regulatory processes in plants, excessive ROS levels can cause
oxidative stress, leading to damage in cellular components such as DNA,
proteins, and lipids (Mittler et al., 2022). Some common types of ROS
include the superoxide radical (O2•-), hydrogen peroxide
(H2O2), the hydroxyl radical (•OH), and
singlet oxygen (1O2). Nitric oxide
(NO˙) and peroxynitrite (ONOO−) are classified as reactive nitrogen
species (RNS) and are capable of exacerbating oxidative stress (del Río
and López-Huertas, 2016; Mittler, 2017).
To protect against oxidative stress, plants have evolved elaborate
antioxidant defense systems that include thioredoxins (TRX) and enzymes
like superoxide dismutase (SOD), catalase, peroxidases, and various
non-enzymatic antioxidants like ascorbate and glutathione. These
antioxidants help neutralize and regulate ROS levels, maintaining
cellular redox balance and protecting the plant from oxidative damage
(Mittler et al., 2022). Redox state, short for reduction-oxidation
state, refers to the balance of electrons in a chemical reaction. It
involves two processes: reduction (gain of electrons) and oxidation
(loss of electrons). The connection between redox (reduction-oxidation)
reactions and ROS lies in the transfer of electrons during chemical
processes. Redox reactions involve the exchange of electrons between
molecules, leading to the reduction and oxidation of species. When
electrons escape from this redox process, particularly in the electron
transport chains of photosynthesis or cellular respiration, they can
interact with molecular oxygen, giving rise to ROS (Foyer and Hanke,
2022). Disruptions in redox balance can lead to cellular dysfunction and
contribute to diseases (Mittler, 2017) (Mittler et al., 2022).
Each cell in a plant is surrounded by a cellulosic wall which hampers
communication between plant cells that involves direct plasma membrane
contacts or plasma membrane-facilitated ligand-receptor interactions
that are commonly found in animals. Plants have instead evolved
intercellular connections called plasmodesmata (PD) that permeate the
cell wall to allow direct trafficking of metabolite and signaling
molecules between connected cells (Azim and Burch-Smith, 2020). Beyond
their roles in trafficking endogenous plant molecules, PD also provide a
route for direct cell-to-cell conveyance of viruses during infection
(Heinlein, 2015; Reagan and Burch-Smith, 2020). PD are not only routes
for direct cell-to-cell signaling, but they also connect individual
cells to the vasculature for systemic or long-distance transport in the
plant. The last few years have seen an exciting resurgence in interest
in the role of PD in long-distance signaling. There is accumulating
evidence that many mRNA molecules can travel long distances in the plant
from their sites of synthesis (transcription) to their sites of action
to regulate developmental processes (Thieme et al., 2015). The role of
PD in long-distance signaling via propagation of ROS and calcium signals
is also garnering attention (Toyota et al., 2018; Fichman et al., 2021),
although the role of PD is these processes may not be as straightforward
as thought (Bellandi et al., 2022). This review focuses on local
cell-to-cell movement and explore how ROS and redox impacts cell-to-cell
communication. It also discusses how redox signaling is modified by
plant viruses to manipulate PD for their local cell-to-cell movement
during infection as one illustration of how redox mechanisms contribute
to plant responses to biotic stress.
Organelles as ROS production sites
ROS are generated within plant cells in response to various stimuli,
including biotic and abiotic stresses, hormone signaling, and
developmental cues. Chloroplasts, the hub of photosynthesis in plant
cells, play a crucial role in the generation of ROS. As part of
photosynthesis, electrons can escape from the electron transport chain,
leading to the formation of O2·− and
H2O2. The production of ROS in
chloroplasts involves both photosystems I and II, leveraging the surplus
of photons harnessed by PSII and directing electrons towards molecular
oxygen via PSI, (Foyer and Hanke, 2022; Li and Kim, 2022). In
photosynthesizing cells, peroxisomes are required for photorespiration
that occurs when ribulose-1,5-bisphosphate carboxylase/oxygenase
(RubiscCO) favors O2 as a substrate instead of
CO2. The phosphoglycolate produced by this reaction is
transported from chloroplasts to peroxisomes where it is broken down and
H2O2 is produced (Tripathy and
Oelmuller, 2012). Peroxisomes are also involved in other metabolic
processes, including fatty acid and polyamines breakdown and
detoxification of harmful substances. Peroxisomal ROS are also produced
as by-products during these processes (del Río and López-Huertas, 2016;
Corpas et al., 2020). Thus, in photosynthesizing cells, the chloroplasts
and peroxisomes together account for approximately a significant
proportion of ROS production. Glyoxysomes, specialized peroxisomes in
germinating plant cells, participate in ROS production while converting
stored lipids to carbohydrates (Janku et al., 2019; De Bellis et al.,
2020). As in all eukaryotes, mitochondria are the respiratory organelles
in plant cells. Mitochondrial ROS (mtROS) are produced by electron
leakage occurring within the electron transport system, which is
influenced by the inhibition of particular sites within the electron
transport chain (ETC) or the reduction state of ETC components, as
substrates are metabolized (Moller, 2001; Huang et al., 2016). Together,
chloroplasts, peroxisomes and mitochondria account for the bulk of ROS
production in plant cells (Tripathy and Oelmuller, 2012).
Apart from these main sources or ROS, the plasma membrane (PM),
endoplasmic reticulum (ER) and apoplast also produce ROS. The
Respiratory Burst Oxidase Homologs (RBOHs), are transmembrane PM
proteins that transfer electrons from cytosolic NADPH to molecular
oxygen, leading to superoxide radicals’ production and their
transformation into other ROS. RBOHs can also be regulated by protein
kinases, such as calcium-dependent protein kinases (CDPKs) and
mitogen-activated protein kinases (MAPKs), which can phosphorylate and
activate RBOHs (Chapman et al., 2019) (Zandalinas and Mittler, 2018).
The ER generates ROS during oxidative protein folding, driven by the
formation of ROS due to the occasional incorrect formation of disulfide
bonds and the NAD(P)H-dependent electron transport system using
Cytochrome P450 (Cyt P450) (Sharma et al., 2012; Cao and Kaufman, 2014).
The apoplast and cell wall are additional sources of ROS production,
involving various factors, such as the respiratory burst, cell wall
peroxidases, polyamine oxidases, and processes like cell wall remodeling
and lignification. RBOHs release superoxide radicals into the apoplast,
notably during stress responses or immune reactions (Schmidt et al.,
2018).