\documentclass[10pt]{article}

\usepackage{fullpage}
\usepackage{setspace}
\usepackage{parskip}
\usepackage{titlesec}
\usepackage[section]{placeins}
\usepackage{xcolor}
\usepackage{breakcites}
\usepackage{lineno}
\usepackage{hyphenat}





\PassOptionsToPackage{hyphens}{url}
\usepackage[colorlinks = true,
            linkcolor = blue,
            urlcolor  = blue,
            citecolor = blue,
            anchorcolor = blue]{hyperref}
\usepackage{etoolbox}
\makeatletter
\patchcmd\@combinedblfloats{\box\@outputbox}{\unvbox\@outputbox}{}{%
  \errmessage{\noexpand\@combinedblfloats could not be patched}%
}%
\makeatother


\usepackage{natbib}




\renewenvironment{abstract}
  {{\bfseries\noindent{\abstractname}\par\nobreak}\footnotesize}
  {\bigskip}

\titlespacing{\section}{0pt}{*3}{*1}
\titlespacing{\subsection}{0pt}{*2}{*0.5}
\titlespacing{\subsubsection}{0pt}{*1.5}{0pt}


\usepackage{authblk}


\usepackage{graphicx}
\usepackage[space]{grffile}
\usepackage{latexsym}
\usepackage{textcomp}
\usepackage{longtable}
\usepackage{tabulary}
\usepackage{booktabs,array,multirow}
\usepackage{amsfonts,amsmath,amssymb}
\providecommand\citet{\cite}
\providecommand\citep{\cite}
\providecommand\citealt{\cite}
% You can conditionalize code for latexml or normal latex using this.
\newif\iflatexml\latexmlfalse
\providecommand{\tightlist}{\setlength{\itemsep}{0pt}\setlength{\parskip}{0pt}}%

\AtBeginDocument{\DeclareGraphicsExtensions{.pdf,.PDF,.eps,.EPS,.png,.PNG,.tif,.TIF,.jpg,.JPG,.jpeg,.JPEG}}

\usepackage[utf8]{inputenc}
\usepackage[T2A]{fontenc}
\usepackage[ngerman,greek,polish,english]{babel}



\usepackage{float}








\begin{document}

\title{Hot Topic: Thermosensing in Plants}



\author[1]{Scott Hayes}%
\author[2]{Joëlle Schachtschabel}%
\author[3]{Michael Mishkind}%
\author[4]{Teun Munnik}%
\author[2]{Steven Arisz}%
\affil[1]{Wageningen University \& Research}%
\affil[2]{University of Amsterdam}%
\affil[3]{National Science Foundation Directorate for Biological Sciences}%
\affil[4]{Swammerdam Institute for Life Sciences}%


\vspace{-1em}



  
  \date{May 04, 2024}


\begingroup
\let\center\flushleft
\let\endcenter\endflushleft
\maketitle
\endgroup





\selectlanguage{english}
\begin{abstract}
Plants alter their morphology and cellular homeostasis to promote
resilience under a variety of heat regimes. Molecular processes that
underlie these responses have been intensively studied and found to
encompass diverse mechanisms operating across a broad range of cellular
components, timescales and temperatures. This review explores recent
progress throughout this landscape with a particular focus on
thermosensing in plants. Direct temperature sensors include the
photosensors phytochrome B and phototropin, the clock component ELF3 and
an RNA switch. In addition, there are heat-regulated processes mediated
by ion channels, lipids and lipid-modifying enzymes taking place at the
plasma membrane and the chloroplast. In some cases the mechanism of
temperature perception is well understood but in others this remains an
open question. Potential novel thermosensing mechanisms are based on
lipid and liquid phase separation. Finally, future research directions
of high temperature perception and signalling pathways are discussed.%
\end{abstract}%



\sloppy


\textbf{1. Introduction}

Heat stress is an increasingly prevalent environmental constraint for
plants. Rising average global temperatures, and more frequent
temperature extremes have a negative impact on world crop yield (Kang et
al., 2009; Lobell \& Field, 2007). Warm temperatures can impair plant
growth, fertility, development, metabolism, photosynthesis and immunity
(Hatfield \& Prueger, 2015; Howarth \& Ougham, 1993; Janda et al., 2019;
Wolf et al., 1991; Xu et al., 1995). In natural environments, plants
experience daily and seasonal temperature fluctuations that vary in
range, rate and duration. Whether a temperature becomes stressful
depends on these variables, as well as coincident stress factors such as
drought and salinity. At the cellular level, heat stress perturbs
protein folding, membrane fluidity, cytoskeletal organization,
transport, and enzymatic reactions, which leads to metabolic imbalances
and pernicious accumulation of by-products such as reactive oxygen
species (ROS). It is therefore of primary interest for plants to sense
temperature alterations and initiate timely adaptive strategies to
preserve cell function and viability. Plants respond to different
temperature ranges with widely divergent physiological and developmental
responses. However much less is known about the sensing mechanisms
involved.

At temperatures above the optimum ambient growth temperature, but still
within the physiological range (i.e. up to around 28\selectlanguage{ngerman}°C for Arabidopsis),
many plants undergo a process known as thermomorphogenesis, in which
they alter morphology and development (for example, through expanded
leaf structure, deeper roots and early flowering) to reduce exposure to
potentially damaging temperatures (Fig. 1) (Casal \& Balasubramanian,
2019; Crawford et al., 2012; Park \& Park, 2019). At higher
temperatures, i.e 28-37°C for Arabidopsis, there is still some growth,
but several adverse effects become visible. Reproductive development and
photosynthesis are affected, and root and shoot growth rates are
compromised. At these temperatures, plants employ a variety of
acclimation strategies to enhance temperature tolerance, including the
production of molecular chaperones within minutes, and modulating the
composition of cell membranes over a period of days. As temperatures
rise above 40°C, severe heat stress is experienced, which can result in
global injury, malfunction and ultimately, cell death (Fig. 1).

Molecular plant scientists have long questioned how heat is actually
perceived and converted into a cellular signal. Since macromolecules are
generally affected by heat, many have the potential to serve as
thermosensors. The concept of thermosensor needs to incorporate
processes akin to ligand-receptor binding coupled to downstream
signaling, but also include less well-demarcated processes such as
heat-induced increases in membrane fluidity followed by changes in
membrane structure and function. This makes it difficult to identify
macromolecules that actually perceive temperature and elicit specific
signalling events. In recent years, several potential thermosensors and
sensing mechanisms have emerged, both of ambient warm and stressful hot
temperatures. Here, we summarize that knowledge, focussing on their mode
of action, and provide a perspective for future research in this
exciting field.

\textbf{2. Sensing mechanisms of warm ambient temperatures}

\textbf{2.1. Phytochrome B (phyB) as temperature sensor}

In recent years, there has been a growing realization that certain
molecules originally characterized as photosensors moonlight as
thermosensors, fine tuning growth and differentiation in response to
moderate temperature changes. Here, the photo/thermo sensor acts as a
receptor for a change in temperature, and in doing so initiates
downstream signaling processes.

There is extensive crosstalk between light and temperature signalling in
plants (Hayes, 2020). Plants perceive light conditions with at least
five types of photoreceptors, i.e. (1) phytochromes, (2) cryptochromes,
(3) phototropins, (4) zeitlupes and (5) UVR8 (Voitsekhovskaja, 2019). Of
these photoreceptors, the temperature sensitive activity of phytochromes
is the most well characterised, in particular phytochrome B (phyB).
Phytochromes control many aspects of thermomorphogenesis, especially
architectural changes, accelerated flowering and senescence (Jung et
al., 2016; C. Kim, 2020; Quint et al., 2016).

Phytochromes are red/far red (R/FR) sensitive photoreceptors that absorb
light through a phytochromobilin chromophore. The absorption of light by
phytochromobilin induces its isomerisation, and this translates to
conformational changes in phytochrome structure. R light promotes a
shift to the active form of phytochrome (Pfr) whereas FR light promotes
reversion to the inactive form (Pr) (Hayes, 2020). Importantly, Pfr can
also spontaneously revert to Pr, and this process is temperature
dependent. The rate of thermal reversion from Pfr to Pr is accelerated
at warm temperatures (Legris et al., 2016), resulting in a reduced pool
of active phytochrome (Fig. 2).

When activated by R light and cool temperatures, phytochromes promote
the degradation of a family of bHLH transcription factors known as
PHYTOCHROME INTERACTING FACTORS (PIFs).When phytochrome function is
reduced by FR light or warm temperatures, PIFs accumulate and promote
hypocotyl elongation through the enhanced expression of auxin
biosynthesis genes (Jung et al., 2016; Koini et al., 2009; Legris et
al., 2016). Hypocotyl elongation at warm temperatures is largely driven
by \emph{PIF4} , \emph{PIF7} and to some extent \emph{PIF5} (Chung et
al., 2020; Fiorucci et al., 2020; Koini et al., 2009). PIF-mediated
elongation and hyponasty at warm temperatures results in an open
architecture and enhances leaf cooling (Crawford et al., 2012; Park \&
Park, 2019).

\textbf{2.2. Other photosensors: phototropin, cryptochrome and UVR8}

Phytochrome B is not the only plant photosensor with the ability to
perceive temperature. The phototropin of liverwort (\emph{Marchantia
polymorpha} ) (Mp\emph{PHOT} ) is also temperature sensitive (Fujii et
al., 2017). Phototropins are membrane bound blue light receptors that
respond to positional light cues. They regulate phototropism, leaf
flattening and chloroplast positioning. In \emph{Marchantia} , an
important phototropin regulated process is the cold avoidance response.
At 22°C, blue light induces the movement of chloroplasts to the cell
surface, in order to maximise photosynthesis. In contrast, at 5°C blue
light induces the movement of chloroplasts to the periclinal cell walls.
This process is known as cold avoidance and is thought to protect the
photosynthetic machinery in suboptimal temperature conditions (Fujii et
al., 2017).

\emph{MpPHOT} contains two LOV (light, oxygen or voltage) domains that
are responsible for light sensing. In darkness, each LOV domain contains
a non-covalently bound flavin mononucleotide (FMN) chromophore. Blue
light absorption by FMN triggers its covalent attachment to the LOV
domain. This in turn causes structural re-arrangement of the phototropin
molecule into its active form. Importantly, the covalent bond that links
FMN and the LOV domain spontaneously degrades over time, resulting in
inactivation of \emph{MpPHOT} . This degradation rate increases with
temperature, meaning that MpPHOT remains more active at cooler
temperatures. As a result, MpPHOT promotes the relocation of
chloroplasts to the cell periphery when temperatures are too low for
efficient photosynthesis (Fujii et al., 2017). The phototropins of
Arabidopsis were also recently implicated in temperature signalling
(Kostaki et al., 2020). Warm temperatures promote guard cell opening in
a cell autonomous manner. Curiously, this process is dependent on blue
light and phototropins (Kostaki et al., 2020). This would seem to imply
that in contrast to MpPHOT (Fujii et al., 2017), the activity of
phototropin in Arabidopsis guard cells is actually enhanced at warm
temperatures. Further investigation into the potential temperature
sensitivity of Arabidopsis phototropins should help to resolve this
point.

Zeitlupes are another class of blue light photoreceptor, which act to
accelerate the pace of the circadian clock. Zeitlupes contain a LOV
domain with a similar activation mechanism to phototropins (Pudasaini et
al., 2017). If the rate of zeitlupe inactivation is increased at warm
temperatures, this could potentially reduce the pace of the clock at
warm temperatures (a process known as temperature compensation) (Hayes,
2020). Several years ago, zeitlupe was identified as a quantitative
trait locus for natural variation in temperature compensation in
Arabidopsis (Edwards et al., 2005) and so it would be interesting to
experimentally test this hypothesis. Other plant photosensors, such as
the blue light sensing cryptochrome (cry) and UV-B sensing UV Resistance
Locus 8 (UVR8), could potentially also function as thermosensors (Figure
2). Cryptochromes undergo thermal reversion in a similar manner to
phytochromes and phototropins. If cryptochrome thermal reversion is
enhanced at warm temperatures, it is feasible that cryptochrome would
also exhibit higher activity at cool temperatures (Hayes, 2020). UVR8
exists as a homodimer in the dark, but undergoes monomerization after
absorbing UV-B. The active UVR8 monomer then reverts back to the
inactive dimer, in a process that is mediated by Repressor of UV-B
Photomorphogenesis 1 (RUP1) and RUP2. The RUP-mediated reversion of the
UVR8 monomer to the UVR8 dimer seems to be influenced by temperature
(Findlay \& Jenkins, 2016), but the details of this process are
currently unclear. Whether zeitlupe, cryptochrome and UVR8 functions are
truly temperature sensitive remains to be investigated.

\textbf{2.3. RNA thermosensors}

Temperature sensing through RNA structure has earlier been shown in
bacteria and animals (Vu et al., 2019). Recently, an RNA based
temperature `switch' was also identified in plants. Chung \emph{et
al.}(2020) used ribosome profiling to identify genes that show an
increase in translational efficiency at warm temperatures.
Interestingly, one of the genes that showed enhanced translation was
\emph{PIF7} . \emph{PIF7}mRNA contains a hairpin structure in its 5'-UTR
and the structure of this hairpin is temperature dependent (Fig. 2). It
has been proposed that at low temperatures the hairpin forms and blocks
\emph{PIF7} mRNA translation. At warm temperatures, the hairpin can no
longer form and PIF7 can be translated (Chung et al., 2020; Fiorucci et
al., 2020). As PIF7 is one of the key transcription factors regulating
hypocotyl and petiole elongation at warm temperatures, the
temperature-dependent folding of its mRNA can be considered a
temperature sensor.

\textbf{2.4. Temperature-dependent action of the Evening Complex}

A large proportion of the genome is regulated by the circadian clock. To
ensure robust rhythmicity, the clock is entrained to daily cycles of
light and temperature. The evening complex (EC) is a group of core clock
components that show peak expression in the early evening. In recent
years it has become apparent that the EC is one of the key points at
which light and temperature signals enter the clock (Ezer et al., 2017).
The EC consists of three components, the scaffold protein EARLY
FLOWERING 3 (ELF3), the transcription factor LUX ARRYTHMO (LUX), and a
protein of unknown function, ELF4. Together they act as a
transcriptional repressor that directly binds DNA (Ezer et al., 2017;
Huang et al., 2016; Nusinow et al., 2011). Besides its function in the
clock, the EC also represses the expression of thermomorphogenesis
promoting genes such as \emph{PIF4} , limiting the period of
temperature-induced growth (Box et al., 2015).

Consistent with its importance in conveying temperature information to
the clock, binding of the EC to DNA is temperature dependent. At cool
temperatures, the EC binds to DNA much more strongly than at warm
temperatures (Ezer et al., 2017). Phytochromes play an important role in
regulating the EC (Ezer et al., 2017; Huang et al., 2016) and so
temperature sensitivity of DNA binding could potentially be ascribed to
increased thermal reversion of phyB (Legris et al., 2016). Intriguingly
however, EC DNA binding is also temperature dependent \emph{in vitro} ,
implying that EC activity is directly modulated by temperature (Silva et
al., 2020).

ELF3 contains a prion-like domain (PrD) with a high proportion of
glutamine residues (Jung et al., 2020). The PrD shows variable length
between species, with \emph{Arabidopsis thaliana} ELF3 (AtELF3)
containing a much longer PrD than \emph{Brachypodium distachyon} ELF3
(BdELF3). Replacing the PrD of AtELF3 with the corresponding region from
BdELF3 abolished the temperature-dependent DNA binding of AtELF3 (Jung
et al., 2020). At high temperatures, AtELF3 forms speckles within the
nucleus and this is also dependent on the PrD. Importantly, these
PrD-dependent speckles also form at high temperatures when AtELF3 is
expressed in yeast cells, in the absence of other evening complex
components. Furthermore, the purified PrD from AtELF3 spontaneously and
reversibly forms liquid droplets when in solution, in a
temperature-dependent manner (Jung et al., 2020). Warm
temperature-dependent self-coalescence of ELF3 through its PrD domain
therefore likely constitutes a temperature sensing mechanism in plants
(Fig. 2).

Direct temperature sensing by ELF3 may help to explain a curious
observation about phyB at warm temperatures. Under R light, active phyB
accumulates in several large sub-nuclear foci known as photobodies (Hahm
et al., 2020). In R + FR light, phyB is inactivated and disperses to
numerous smaller foci. Warm temperature also inactivates phyB and so we
might expect it to lead to a similar change in phyB photobodies.
However, in direct contrast to FR light, warm temperature appears to
promote the aggregation of phyB into fewer, larger photobodies (Hahm et
al., 2020). Whether there is a link between phyB aggregation and ELF3
PrD-mediated condensation at warm temperatures remains to be
investigated. However if this is the case, it presents an attractive
mechanism whereby plant cells could distinguish between FR and warm
temperature signals, based on the inactivation of phyB alone or the
inactivation of phyB \emph{and} ELF3 in conjunction.

\textbf{2.5. Epigenetic regulation of thermomorphogenesis}

In a screen for mutants with enhanced temperature response, Kumar \&
Wigge (2010) discovered ARP6, a component of a chromatin remodelling
complex. Mutants lacking ARP6 show constitutive warm temperature
phenotypes. ARP6 is required for the deposition of a specific histone
variant H2A.Z. It was shown that at warm temperatures, there is a
reduction in H2A.Z occupancy at the promoters of warm-temperature
induced genes and it was initially proposed that H2A.Z could play a role
in temperature sensing (Kumar \& Wigge, 2010). More recent evidence has
however cast doubt on this hypothesis. It was shown that at warm
temperatures, the binding of HSFA1a to heat responsive genes precedes
the H2A.Z eviction and the activation of transcription (Cortijo et al.,
2017). The eviction of H2A.Z is facilitated by HISTONE DEACETYLASE 9
(HDAC9), and is required for the full transcriptional response to
elevated temperatures (van der Woude et al., 2019), but it appears that
this occurs mostly downstream of temperature perception.

\textbf{3. Sensing mechanisms of moderate to severe heat stress}

\textbf{3.1. The heat stress response is partly based on unfolded
protein sensing}

Heat stress triggers adaptive responses which protect macromolecular
structures, restore cellular homeostasis and prevent damage. The
composite response likely involves the action of multiple parallel
sensors that activate signaling pathways in different cellular
compartments with different dynamics. Cellular defense mechanisms are
activated by monitoring protein, DNA and membrane damage (Balogh et al.,
2013; Ding et al., 2020; Niu \& Xiang, 2018). The expression of Heat
Shock Proteins (HSPs) is induced by elevated temperatures in a large
variety of eukaryotes. HSPs act as molecular chaperones to promote the
correct folding of proteins in the cell and are crucial for tolerance to
high temperatures in plants. HSPs can also contribute to the
thermomorphogenic response. For example, HSP90 promotes the stability of
the auxin receptor TIR1 and in doing so, promotes root and shoot
elongation at warm temperatures (R. Wang et al., 2016).

Studies in yeast have suggested a mechanism by which HSPs are induced at
warm temperatures. HSPs bind to a class of transcription factors known
as Heat Shock Factors (HSF), which are thus kept in an inactive state.
At warm temperatures, the binding of HSPs to HSFs is disrupted. HSFs are
then free to travel to the nucleus to induce the expression of HSPs and
other heat stress genes. This increased abundance of HSPs then
sequesters the free HSFs, thus reaching another equilibrium.

Currently it is unclear whether the HSP:HSF module functions in the same
manner in plants, but similar mechanisms are known to activate the
unfolded protein response (UPR). When a plant experiences heat stress,
unfolded and misfolded proteins can accumulate to such levels that they
overload the protein quality control system, leading to ER stress. When
unfolded proteins accumulate in the ER, they are bound by binding
protein (BiP), an HSP70 chaperone. In the absence of unfolded proteins,
BiP binds to the ER membrane-tethered transcription factors (MTTFs)
bZIP17 and bZIP28. When unfolded proteins sequester BiP, bZIP17 and
bZIP28 are activated by translocation and proteolytic cleavage of their
membrane anchors at the Golgi. These transcription factors then travel
to the nucleus to promote the expression of chaperones and foldases to
assist in protein folding, a process known as the unfolded protein
response (UPR). Unfolded proteins also interact with the lumenal domain
of the transmembrane sensor IRE1b (inositol-requiring enzyme1), inducing
unconventional splicing of bZIP60, which then activates the ER stress
response genes. IRE1b splicing activity is induced by heat (Deng et al.,
2011). Moreover, IRE1 was found to be inducible by lipid bilayer stress
in yeast (Ernst et al., 2018; Halbleib et al., 2017), and to regulate
the degradation of specific mRNA's, shaping the stress transcriptome.
Interestingly, the transcription factor ELONGATED HYPOCOTYL 5 (HY5) was
recently found to compete with bZIP17 and bZIP28 to repress the UPR
(Nawkar et al., 2017). HY5 abundance is reduced at warm temperatures
(Park et al., 2017), potentially through the photo/thermo sensing
mechanism described above. Reduced HY5 abundance may help to promote the
UPR under heat stress.

High temperature and light conditions can also activate UPR responses
through a signal from the chloroplast, methyl-D-erythritol
2,4-cyclodiphosphate (MEcPP, Fig. 3), a retrograde signaling metabolite
(Rivasseau et al., 2009; Walley et al., 2015). This intermediate of the
methylerythritol-4-phosphate (MEP) pathway of isoprenoid synthesis
accumulates as a direct consequence of a heat stress-induced metabolic
bottleneck, and induces CAMTA3-dependent transcription of IRE1a and
bZIP60 and other genes with a \emph{rapid stress response element} (Benn
et al., 2016). Hence, the MEP pathway is considered an important stress
sensor (Xiao et al., 2012). The functions of retrograde signals in heat
stress have been reviewed elsewhere (Sun \& Guo, 2016). Clearly,
different sensory modules feed into the UPR response.

Under heat stress, unfolded proteins also accumulate in chloroplasts.
The small heat shock protein (sHSP) of Chlamydomonas, HSP22E/F, forms
high-molecular weight complexes with them to prevent proteotoxicity
(Rütgers, Muranaka, Mühlhaus, et al., 2017). Heat-inactivation of
specific thermolabile proteins in the chloroplast, and their
sequestration into complexes with sHSP, is considered an adaptive
mechanism to directly regulate metabolism and signaling processes in
response to heat.

AtNTL4 and OsNTL3, which are MTTFs of the NTL (NAC transmembrane
transcription factor-like) group, also appear critical in regulating
heat stress responses. The basis for their thermosensitive proteolytic
activation remains however, unresolved (Lee et al., 2014; X. Liu et al.,
2020). Evidence of their ER localization (Liang et al., 2015) and
partial convergence with ER-stress responses (Yang et al., 2014),
suggests that they could signal heat-induced protein and lipid
perturbations at the ER.

\textbf{3.2. Regulation based on physical changes in the membrane}

The membrane is the most thermally sensitive macromolecular structure in
the cell (Balogh et al., 2013; Niu \& Xiang, 2018). With increasing
temperature, the rotational motion, lateral diffusion, and fatty acid
disorder of the lipid bilayer increase, while the headgroup packing
density decreases. These four parameters are different aspects of the
commonly used term 'membrane fluidity'. Changes in membrane fluidity
affect the folding, mobility, and activity of membrane proteins. These
changes can have deleterious effects on cell functions, but at moderate
levels can also serve as a basis for thermosensing. Plants, like other
non-homeothermic organisms, actively maintain an almost constant
membrane fluidity upon shifts in temperature (Higashi et al., 2015; Los
\& Murata, 2004). The increased fluidity under heat stress is
counteracted by the incorporation of fluidity-decreasing saturated fatty
acids, a process known as homeoviscous adaptation. In bacteria, membrane
thickness is measured through the membrane protein DesK and in yeast,
lipid packing density is measured by Mga2. These sensors support
membrane homeostasis by the transcriptional activation of lipid
desaturases when temperature drops (Ballweg et al., 2020; Covino et al.,
2016; Cybulski et al., 2010).

In plants, such membrane property sensors have not been identified.
Instead, heat was found to directly inhibit the activity of critical
desaturases, simply by virtue of their heat-instability. The plastidial
FAD8 enzyme is responsible for the synthesis of \selectlanguage{greek}α-\selectlanguage{english}linolenic acid (18:3),
a component of the main thylakoid lipid, monogalacosyldiacylglycerol
(MGDG). FAD8 contains a labile autoregulatory domain, that destabilizes
the protein upon a temperature shift from 22\selectlanguage{ngerman}°C to 27°C (Matsuda et al.,
2005) (Fig. 3). Reduced FAD8 stability resulted in decreased
accumulation of 18:3 and reduced membrane fluidity. The importance of
this is clear from the finding that mutants with low 18:3 content in
their MGDG showed improved heat tolerance (Murakami, 2000). This may be
because 18:3-MGDG is prone to oxidative damage and perturbs membranes.
The ER desaturases FAD2 and FAD3 also display thermolability. Upon
transfer to warm temperatures, FAD2 and FAD3 are targeted for
ubiquitin-mediated or ER-associated degradation, respectively (O'Quin et
al., 2010; Tang et al., 2005). Currently the mechanism by which these
desaturases are inactivated upon heat stress is unknown; they may either
be direct thermosensors or act downstream of temperature perception.

Adjustment of membrane fluidity through changes in membrane desaturation
is a slow process and can take several takes days (Falcone et al.,
2004). In the case of acute heat stress, alternative mechanisms are
employed to secure bilayer integrity. These sense-and-respond mechanisms
are based on heat-induced, biophysical changes in membrane properties.
In thylakoid membranes, heat induces packing defects in the lipid
headgroups. These defects provide a spatial cue for docking of proteins
with membrane-protecting functions, such as sHSP (Heckathorn et al.,
1998) and vesicle-inducing protein in plastids 1 (VIPP1, Fig. 3) (Theis
et al., 2019; L. Zhang et al., 2016). The inducible association of these
proteins with membranes likely follows the sensing of the membrane
status through their amphipathic \selectlanguage{greek}α-\selectlanguage{english}helices.

Acute heat also induces the aggregation of light-harvesting complex II
(LHCII) proteins in the thylakoid membranes. MGDG is normally associated
with LHCII, and upon aggregation of LHCII, excess MGDG gets extruded to
the lumen (Jahns et al., 2009; Schaller et al., 2010) (Fig. 3). Due to
MGDG's non-bilayer propensity, extruded MGDG forms a so-called inverted
hexagonal phase (HII) (Garab et al., 2017; Krumova et al., 2008).
Thylakoid membranes are always close to HII phase transition and, as HII
phases emerge, they must be controlled to avoid damage. HII phases are
however key to chloroplast heat acclimation because when they emerge
under stress, they recruit and activate the xanthophyll cycle enzyme,
violaxanthin de-epoxidase (VDE). VDE synthesizes zeaxanthin which
quenches excess excitation energy and enhances membrane stability. The
HII phases serve the sequestering of excess MGDG and promote the
diffusion of xanthophylls (Latowski et al., 2002) (Fig. 3).

Another membrane feature that can undergo rapid stress-induced
modification are microdomains. Most lipids within a membrane exist in
liquid-disordered phase, often envisioned as a two-dimensional fluid.
Lipids can however also exist in the liquid-ordered phase known as nano-
and microdomains (Jaillais \& Ott, 2020; Saenz et al., 2012).
Microdomains form coherent, dynamic platforms for proteins with
functions in sensing, signaling, membrane integrity maintenance and
transport. Even mild changes in temperature can result in altered
microdomain fluidity and consequently, redistribution and modified
activity of these proteins (T\selectlanguage{ngerman}örök et al., 2014). Based on studies of
membranes and Molecular Dynamics simulation, microdomains are speculated
to act as dynamic reservoirs of fluidity-decreasing lipids. Heat may
trigger increased partitioning of these lipids from microdomains to the
bulk fluid phase (Nickels et al., 2019). This simple buffering effect
that can occur in complex membranes is based on thermodynamics of phase
separation and could be far more responsive than the metabolic responses
of homeoviscous adaptation (Ernst et al., 2018).

Some plasma membrane microdomains are tethered to the underlying
cortical ER at so-called ER-plasma membrane contact sites (EPCSs)
through synaptotagmins (SYT1 and SYT3) (Ruiz-Lopez et al., 2020). SYT1/3
are ER proteins that bind (via C2-domains) to
phosphatidylinositolphosphate (PIP)-containing microdomains of the
plasma membrane (Fig. 4). The close proximity of the two membranes
allows for exchange/removal of detrimental lipids, e.g. diacylglycerol
that is formed at the plasma membrane during phospholipase C (PLC)
signaling (\emph{see below} ). In yeast, EPCSs are important for plasma
membrane integrity maintenance under heat stress (Collado et al., 2019),
and they appear to function similarly under stresses in plants
(Ruiz-Lopez et al., 2020; Yan et al., 2017).

The biophysical changes in membranes under heat stress can be sensed by
altered protein activity and/or location. Moreover, the alternative
lipid phases allow for prompt, thermosensitive responses, and thereby
provide structural and functional flexibility that is of vital
importance under heat stress. Notably, this suggests that homeoviscous
adaptation does not necessarily involve a sensor of membrane fluidity.
Whether fluidity sensing underlies other heat stress responses remains
unknown. Many studies have attempted to probe the effect of membrane
fluidization using pharmacological and genetic interventions, but it is
becoming clear that these techniques have indirect effects on proteins
and gene expression (Rütgers, Muranaka, Schulz-Raffelt, et al., 2017; Vu
et al., 2019).

\textbf{3.3. The primary roles of Ca\textsuperscript{2+} and
H\textsubscript{2}O\textsubscript{2} signaling}

Intracellular Ca\textsuperscript{2+} increases are a feature of all
plant stress responses, and heat stress is no exception (Finka et al.,
2012; Saidi et al., 2011). Ca\textsuperscript{2+} increases were found
to be required for the induction of HSPs through
Ca\textsuperscript{2+}/calmodulin-dependent kinases and for the
acquisition of heat tolerance (H.-T. Liu et al., 2003, 2007). It has
been reasoned that Ca\textsuperscript{2+} channels could function as
thermosensors at moderate temperature elevations and many attempts have
been made to identify such channels (Ding et al., 2020; Horvath et al.,
1998; Saidi et al., 2011).

Using Arabidopsis seedlings expressing the
Ca\textsuperscript{2+}reporter aequorin, Lenzoni and Knight (2019) were
unable to detect a heat-induced cytosolic Ca\textsuperscript{2+}
response. Instead, they found a Ca\textsuperscript{2+} increase in the
chloroplast stroma (Lenzoni \& Knight, 2019). Temperatures of
\textgreater{}35°C induced rapid Ca\textsuperscript{2+} responses, with
higher temperatures provoking higher and faster peaks. The response was
not influenced by the rate of warming, but was determined by the
absolute temperature. The thylakoid membrane Ca\textsuperscript{2+}
sensor CAS was required for full induction of stromal
Ca\textsuperscript{2+} in response to heat (Fig. 3). CAS amplified the
Ca\textsuperscript{2+} signal, but what governs the initial signal is
still unknown.

Cyclic nucleotide-gated channels (CNGCs) have also been shown to mediate
heat-induced cytosolic Ca\textsuperscript{2+} increases
in\emph{Physcomitrella} \emph{patens} and in Arabidopsis. A temperature
increase from 22°C to 28°C in moss quickly triggered a transient inward
electrical current, likely reflecting Ca\textsuperscript{2+} influx
through PpCNGCb (Finka et al., 2012; Saidi et al., 2009). Based on the
use of channel blockers and chelators, the heat-activated
Ca\textsuperscript{2+} current was attributed to CNGC6 in Arabidopsis
(Finka et al., 2012; F. Gao et al., 2012) (Fig. 4). CNGC6 is activated
by cAMP, which also increases upon heat stress. This has led to the
suggestion that an, as yet unidentified, adenylyl cyclase activity could
act as membrane-associated temperature sensor (Thomas et al., 2013).
Research on CNGC functions is complicated by the fact that CNGC subunits
make various combinations to form heterotetrameric channels. These
channels differ in ion conductance, physiological function and mode of
regulation, and mutations in CNGC subunit genes often lead to pleotropic
mutant phenotypes (Dietrich et al., 2020).

Identifying the primary heat-activated Ca\textsuperscript{2+} channel
remains a challenge. The animal heat-activated Transient Receptor
Potential channel, TRPV1, is a mechanosensitive and voltage-gated cation
channel (Benítez-Angeles et al., 2020). It likely responds to forces
transmitted via microtubules (Bavi et al., 2017; Prager-Khoutorsky et
al., 2014). Plants lack TRP channel homologs, but possess other
mechanosensitive channel types that may function in heat signaling,
including OSCA1 (reduced hyperosmolality-induced
{[}Ca\textsuperscript{2+}{]} increase1), MCA (Mid1-complementing
activity), which was implicated in cold sensing (Mori et al., 2018), and
Small Conductance Mechanosensitive Ion Channel (MscS)-Like (MSL)
proteins (Ackermann \& Stanislas, 2020).

Annexins are another class of membrane proteins that may play a role in
heat-induced Ca\textsuperscript{2+} signaling. Proteomic and forward
genetic approaches identified several Arabidopsis annexins that enhanced
heat- and oxidative stress-induced Ca\textsuperscript{2+} responses and
the expression of HSPs and HSFs (Liao et al., 2017; X. Wang et al.,
2015). In the presence of Ca\textsuperscript{2+}, annexins bind to
anionic lipids, such as phosphatidic acid (PA) and phosphatidylserine
(PS) in the plasma membrane (Yadav et al., 2018). Heat stress rapidly
induces ANNEXIN1 (ANN1) membrane association, but this may be a
downstream effect of Ca\textsuperscript{2+} and/or PA accumulation (see
below), rather than a direct effect of temperature on ANN1.

In addition to Ca\textsuperscript{2+},
H\textsubscript{2}O\textsubscript{2} levels at the plasma membrane also
rise quickly in response to heat stress, a process catalyzed by the
NADPH oxidase, RbohD . The plasma membrane
H\textsubscript{2}O\textsubscript{2} signal is required for the heat
stress gene expression and the enhancement of heat tolerance (Suzuki et
al., 2012; Volkov et al., 2006). There is also accumulation of
H\textsubscript{2}O\textsubscript{2} in chloroplasts and mitochondria
and this may provide additional priming signals (Sun \& Guo, 2016). ANN1
is activated by H\textsubscript{2}O\textsubscript{2} (Richards et al.,
2014) and so it may be that annexins function to co-ordinate
H\textsubscript{2}O\textsubscript{2} and Ca\textsuperscript{2+} signals
under heat stress (Fig. 4).

RbhoD-derived H\textsubscript{2}O\textsubscript{2} has also been shown
to accumulate in the apoplastic space in a self-propagating manner. This
results in an extracellular ROS wave travelling through the plant at a
speed of 8.4 cm/min (Miller et al., 2009; Suzuki et al., 2012). Local
heat stress triggered accumulation of
H\textsubscript{2}O\textsubscript{2} can thereby lead to acclimation of
systemic tissues (Miller et al., 2009).
H\textsubscript{2}O\textsubscript{2} and Ca\textsuperscript{2+} signals
are not unique to heat stress and it is presently unclear how these
signals lead to particular stress responses. It has been proposed that
the relative intensity or timing of these signals confers specificity to
the response (Gilroy et al., 2016).

\textbf{3.4. Heat sensing is mediated by lipid signals}

Lipids are the primary structural components of membranes, but also have
signaling and regulatory functions, coupling perception of environmental
cues to cellular responses (Hou et al., 2015). Lipids such as PA and
phosphatidylinositol 4,5-bisphosphate (PIP\textsubscript{2}), and their
metabolic enzymes, i.e. phospholipases C and D (PLC/PLD), and lipid
kinases, diacylglycerol (DAG) kinase (DGK) and
phosphatidylinositol-4-phosphate 5-kinase (PIP5K) have a wide range of
cellular regulatory functions in environmental stress responses. In
Arabidopsis seedlings, heat stress (40°C) triggers increases in PA and
PIP\textsubscript{2} abundance within 2 min (Mishkind et al., 2009).

This extremely rapid response suggests that the synthesis of these
signaling lipids is closely tied to thermosensing, but as of yet it is
unknown how increases in temperature activate these lipid modifying
enzymes (Fig. 4). High-temperature induction of PA is largely dependent
on membrane lipid hydrolysis by PLD (Mishkind et al., 2009; Shiva et
al., 2020) (Fig. 4). The PLD enzyme is localized at the plasma membrane
and associated with microtubules, where it regulates their
membrane-anchorage (Andreeva et al., 2009). In heat-stressed stomatal
cells, apoplastic H\textsubscript{2}O\textsubscript{2} enters the
cytosol through aquaporins. H\textsubscript{2}O\textsubscript{2}oxidizes
cysteine residues in the C2 domain of PLD\selectlanguage{greek}δ. \selectlanguage{english}The modified cysteine
residues promoted Ca\textsuperscript{2+} binding to PLD\selectlanguage{greek}δ, \selectlanguage{english}which resulted
in depolymerization of microtubules (Song et al., 2020; S.-S. Zhang et
al., 2017). Blocking microtubule depolymerization by chemical
stabilizers inhibited the upregulation of HSP70 and the induction of
MAPK activity under heat stress (Sangwan et al., 2002; Suri \& Dhindsa,
2007), which suggests that this pathway acts to promote thermal
acclimation. Curiously though, mutants lacking \selectlanguage{greek}\emph{PLDδ} \selectlanguage{english}were more
tolerant to heat stress, which suggests the opposite. The fact that PLD\selectlanguage{greek}δ
\selectlanguage{english}requires Ca\textsuperscript{2+} and
H\textsubscript{2}O\textsubscript{2}for its activation hints that,
despite its rapid activation, phospholipid signaling occurs downstream
of primary thermosensing.

Glyceraldehyde-3-phosphate dehydrogenase (GAPC) may also play a role in
heat stress signaling. GAPC was shown to translocate to the nucleus
under heat stress, where it activates the transcription factor NF-YC10.
Activated NF-YC10 then promotes the expression of genes that confer
thermotolerance (S.-C. Kim et al., 2020). The mechanism the promotes
GAPC nuclear translocation is as yet unresolved. When in the cytosol,
GAPC can directly bind PLD\selectlanguage{greek}δ \selectlanguage{english}and positively promote its activity (Guo et
al., 2012). It has also been shown to bind PA (McLoughlin et al., 2013)
but it is unclear how or if these attributes contribute to temperature
regulation of GAPC. The involvement of GAPC in PLD/PA signaling raises
the possibility that the heat stress response is coordinated with basal
cell metabolism.

PLC also appears to have a function in the heat stress response, because
PLC9 and PLC3 knock-out seedlings show severely impaired basal and/or
acquired heat tolerance, while overexpression improved this (K. Gao et
al., 2014; Zheng et al., 2012) (Fig. 4). PLC hydrolyzes PIP and
PIP\textsubscript{2} to generate DAG and inositolphosphates. The latter
could eventually result in the activation of a
Ca\textsuperscript{2+}channel (Munnik, 2014). PLC9 and PLC3, both
localized at the plasma membrane, were required for the induction of
cytosolic Ca\textsuperscript{2+} and enhanced expression of sHSPs under
heat stress.

The heat stress-induced accumulation of PIP\textsubscript{2} displayed
interesting dynamics. During heat exposure,
PIP\textsubscript{2}accumulated first at the plasma membrane, after
which it appeared in cytoplasmic punctate structures, followed by
accumulation at the nuclear envelope (Mishkind et al., 2009).
PIP\textsubscript{2} can function in endocytosis and associates with
membrane microdomains (Furt et al., 2010). Microdomains are considered
critical in the regulation of early stress signaling, as they contain
signaling proteins such as RbohD, HSPs, and CNGCs (Dietrich et al.,
2020; Horvath et al., 1998; Niu \& Xiang, 2018). Acting very early in
the response pathway, PLC3 and PLC9 may be physically close to the
thermosensor. Regulation of PLCs is complex, involving calcium,
G-proteins and post-translational modifications (Munnik, 2014).
Potential protein interactors of PLC3 and PLC9, including two
receptor-like kinases, could provide interesting clues as to their
heat-responsive mode of activation (Pokotylo et al., 2013).

\textbf{4.. Conclusions and future challenges}

Clearly, our knowledge of thermosensory systems of plants has greatly
expanded in the past decade. Important discoveries in ambient
temperature signaling include the identification of photo/thermal
sensors, an RNA switch and self-coalescence of ELF3 through its
prion-like domain. These three systems unambiguously translate high
ambient temperatures into altered gene expression. The reprogramming of
development by these factors assists plants to avoid damaging high
temperatures. In Arabidopsis, the inhibition of phyB activity by warm
temperatures has been shown in detail. It is however still unknown if
other photoreceptors function in a similar way. Phototropin plays a role
in low temperature signalling in Physcomitrella but it is not known
whether this temperature-dependent activity also stretches to warm
temperatures. Other photoreceptors undergo thermal reversion and so
could conceptually also function in warm temperature sensing, but this
remains to be demonstrated. The finding that \emph{PIF7} RNA translation
is enhanced at warm temperatures opens the possibility that other RNAs
act in a similar way. Indeed, the authors of the PIF7 study also show
that \emph{HSF2} RNA may also be regulated through a comparable
mechanism (Chung et al., 2020). The finding that ELF3 contains a
prion-like domain that undergoes temperature-dependent coalescence
likely has effects beyond just evening complex transcriptional
repression. ELF3 acts as a scaffold protein for large protein complexes
(Huang et al., 2016) and directly binds to PIF4 to inhibit its
transcriptional activity (Nieto et al., 2015). Both of these functions
are likely inhibited at warm temperatures.

Upon moderate temperature increases, plants trigger a heat stress
response for acclimation, but the sensing mechanism is still largely
unknown. Rather than unfolded proteins, the increased membrane fluidity
at high temperatures is speculated to be a molecular basis of sensing.
While no fluidity sensor has been found in plants, evidence is
accumulating for thermosensory mechanisms based on heat-induced phase
changes in lipids and proteins.

Under heat stress, thylakoid membranes locally undergo transition to
non-bilayer, HII phases, which are essential for heat acclimation, since
they compartmentalize and activate the enzymes of the xanthophyll cycle.
At the plasma membrane, microdomains are formed containing lipids in a
liquid-ordered phase. These domains harbor potential signaling lipids
and proteins, including RbohD, which is activated in response to heat
stress. Formation of microdomains and HII phases could constitute a
basis for thermosensitive regulation of enzymes. Simultaneously, they
provide potential avenues for the rapid trafficking of lipids between
phases, in order to preserve membrane integrity under heat stress. For
the latter function, a membrane fluidity sensor would thus not be
required.

The regulation of ELF3 has unveiled a novel type of ambient temperature
sensing mechanism, based on liquid-liquid phase separation (Jung et al.,
2020). Under heat stress, the formation of spherical, condensed liquid
phases within a bulk dilute phase can be triggered by the coalescence of
proteins through their intrinsically disordered, prion-like domains. The
resulting liquid droplets, also called membraneless organelles,
constitute compartments that can contain proteins with associated
regulatory functions. The reversible process of droplet formation is
highly temperature sensitive. Could liquid-liquid phase separation also
function, at higher temperatures, in the activation of the heat stress
response? Such a function was recently proposed for the yeast
RNA-binding protein, Pab1 (poly(A)-binding protein), which displayed
self-coalescence and phase separation upon a shift to a temperature that
induces the heat-shock response (Riback et al., 2017). The extreme
thermosensitivity of this process was quantified using the temperature
coefficient \emph{Q} 10, the ratio of biological properties measured
10\selectlanguage{ngerman}°C apart. With a \emph{Q} 10 of 350, it exceeds by far any other known
biological thermosensory process. This indicates the potential of
liquid-liquid phase separation of proteins as a thermosensing mechanism.
The sharp threshold temperature above which phase separation is
triggered, which is determined by the amino acid side chains in the
prion-like domain, allows for precise temperature-dependent regulation
of responses. Pab1 was speculated to activate the heat stress response
by sequestering a negative regulator of HSF in liquid droplets, calling
into question the requirement of unfolded proteins for activation
(Riback et al., 2017). It seems plausible that similar regulation
governs heat stress responses in plants.

The stress-induced clustering of proteins into membrane microdomains
could trigger liquid-liquid phase separation in the adjacent cytosol.
This could result in coupled lipid and liquid compartments, that
assemble selected response components, allowing for specific channeling
of sensory signals to downstream responses (Jaillais \& Ott, 2020).
Similarly, plasma membrane organization could respond to changes in the
cell wall, which may also adopt different biophysical states dependent
on temperature (Wu et al., 2018). As yet, such potential interactions
are unexplored territory.

Identifying plant proteins that could act as thermosensors through
liquid-liquid phase separation will be challenging. Previously, heat
stress was found to induce relocalization of splicing factors with
disordered domains, e.g. serine/arginine-rich protein SR45, into
enlarged nuclear speckles (Ali et al., 2003; Reddy et al., 2012), which
could underlie alternative splicing of pre-mRNAs. Many of the,
approximately, 500 proteins in plants with predicted prion-like domains
are transcription factors with potential roles in temperature
signalling. There are prion-like domains in HSFA1b, and several PIFs,
auxin response factors and ABRE-binding factors (Chakrabortee et al.,
2016). Investigating the effect of temperature on the coalescence of
these factors \emph{in vitro} could yield interesting results.

Thermosensing appears to be a highly distributed capacity, based on a
range of mechanisms which are only just beginning to come to light. Most
strikingly, the temperature-dependent behavior of phyB, the PIF7 RNA
hairpin, and both lipid and liquid phase separations, provides an
impressive spectrum of potential heat sensing and responding modes,
essential for plants to acclimate and survive.

\textbf{Figure legends}

\textbf{Figure 1. Schematic overview of responses in different warm
temperature ranges.}

Plants display a wide array of responses when they experience above
optimal temperatures. At warm ambient temperatures, up to 30°C,
Arabidopsis responds by changes in morphology and development, called
thermomorphogenesis, which could aid in avoidance of future heat stress.
Thermomorphogenesis features the temperature-sensitive function of phyB.
Also in this temperature range, there is thermosensitive regulation of
PIF7 mRNA translation. Warm temperatures lead to the loss of a hairpin
structure of PIF7 mRNA, which allows for its translation. ELF3 undergoes
temperature-dependent phase separation. High temperatures promote the
coalescence of ELF3, and the inhibition of ELF3-DNS binding, At
temperatures up to 38°C, Arabidopsis initiates acclimation responses
that counteract damage to proteins and membranes, and maintain cellular
homeostasis. This process involves the activity of HSFA1 master
transcriptional factors (H. Liu \& Charng, 2013). HSPs/sHSP accumulate
to limit misfolding of proteins. and the membrane's lipid composition is
adjusted so as to prevent disruption of the bilayer structure due to
uncontrolled increases in membrane fluidity. The heat sensors that
activate acclimation are unknown. The accumulation, within the first ±15
min of heat stress, of putative signaling components, such as
Ca\textsuperscript{2+}, H\textsubscript{2}O\textsubscript{2},
PIP\textsubscript{2}, PA and cAMP suggests their function in heat
perception, closely tied to the sensor. Temperatures above 40°C are
damaging to Arabidopsis, and all responses in this range are devoted to
immediate protection of cellular structures. Mechanisms of clearance and
rescue of unfolded proteins, including the UPR, are important for
survival of severe heat stress. These heat stress responses rely on the
recognition of unfolded proteins in the ER, the cytosol, and diverse
organelles.

\textbf{Figure 2. Schematic overview of thermomorphogenic pathways in
arabidopsis.}1. Under red light, phyB is converted to a Pfr homodimer
that is translocated to the nucleus where it blocks PIF4 and PIF7
activity. High temperatures promote the reversion of phyB back to its
inactive state, leaving PIF4 and PIF7 free to transcribe
thermomorphogenesis promoting genes. 2. \emph{PIF7} mRNA contains a
hairpin near its 5'-UTR sequence. Upon an increase in temperature, this
hairpin structure becomes more relaxed. In the relaxed state,
\emph{PIF7} mRNA is more easily translated and PIF7 protein levels are
increased. 3. At cooler temperatures, ELF3 (as part of the evening
complex) represses the expression of \emph{PIF4} . As temperatures rise,
a prion like domain in ELF3 promotes its aggregation, thus relieving the
transcriptional repression of \emph{PIF4} .

\textbf{Figure 3. Sensing and signaling of heat stress at the
chloroplast.}

Exposure to moderate heat has various direct consequences for
chloroplast proteins and membranes, which trigger rescue pathways. In
the thylakoidal membrane, LHCII proteins aggregate, which leads to an
excess of its major constituent, the non-bilayer prone glycerolipid
MGDG. As a consequence, a non-bilayer structure (the HII phase) emerges,
which consists of MGDG organized in hexagonal, stacked tubules. The
xanthophyll cycle enzyme, violaxanthin de-epoxidase (VDE), recruits
specifically to the HII phase in the thylakoid lumen, catalyzing the
synthesis of zeaxanthin (ZEA) from its precursors, violaxanthin (VIO)
and antheraxanthin (ANT). The HII phase remains attached, which allows
for free diffusion of the photoprotective xanthophylls to the thylakoid.
VIPP1 and sHSP recruit to the thylakoid membrane under heat stress, as
they recognize membrane packing defects. They protect thylakoid membrane
and PSII integrity. Heat stress is signalled in the chloroplast by a
rapid Ca\textsuperscript{2+} increase in the stroma which depends on the
activity of the calcium sensor CAS. Furthermore, heat induces breakdown
of the envelope desaturase FAD8, responsible for synthesis of
polyunsaturated fatty acids. This causes an adaptive decrease in
membrane desaturation. The isoprenoid biosynthesis intermediate MEcPP
accumulates due to a heat-induced bottleneck in the pathway. MEcPP,
together with H\textsubscript{2}O\textsubscript{2} resulting from excess
excitation energy, and other stress-induced molecules, serve as
retrograde signals to regulate heat stress genes in the nucleus.

\textbf{Figure 4. Sensing and primary signalling events of heat stress
at the plasma membrane.}

In response to heat stress, several plasma membrane-linked protein
activities are triggered which lead to intracellular signals that
collectively regulate the heat stress response in plants. 1. Heat
perception gives rise to increases in Ca\textsuperscript{2+}, which can
enter the cytosol from the apoplast through channels such as CNGC6. This
channel might be activated by cAMP, which is generated by a
transmembrane adenylyl cyclase (tmAC) perhaps activated under heat
stress as membrane fluidity increases. Through association with
calmodulin (CaM), Ca\textsuperscript{2+} can negatively regulate CNGC6,
and promote the function of HSFs. HSFs are the primary regulators of the
heat response leading to transcriptional induction of HSPs and other
genes. Apart from CNGC6, Annexin 1 (ANN1) is required for cytosolic
increases in Ca\textsuperscript{2+}. 2. The second major factor in the
heat stress response is H\textsubscript{2}O\textsubscript{2}, which is
generated by the plasma membrane microdomain NADPH oxidase, RBOHD, whose
activity is modulated by several factors, including
Ca\textsuperscript{2+} and PA. After
H\textsubscript{2}O\textsubscript{2} enters the cell, it modifies the
PLD\selectlanguage{greek}δ \selectlanguage{english}protein such that it becomes sensitive to activation by
Ca\textsuperscript{2+}. 3. PLD\selectlanguage{greek}δ \selectlanguage{english}generates PA, which has a myriad of
signaling functions which are mediated by its interaction with cytosolic
target proteins. PLD\selectlanguage{greek}δ \selectlanguage{english}is attached to microtubules and its activity leads
to microtubule depolymerization. Moreover,
H\textsubscript{2}O\textsubscript{2} can activate HSFs through MAPK
signaling. 4. PLC3 and PLC9 are required for sHSP induction and
thermotolerance. Most likely, they hydrolyze PIP to generate DAG,
releasing the inositol-bisphosphate (IP\textsubscript{2}) headgroup. DAG
can be phosphorylated to PA by diacylglycerol kinase (DGK). In plants,
rather than IP\textsubscript{2} or IP\textsubscript{3}, inositol's more
highly phosphorylated derivatives are the likely inducers of cytosolic
release of Ca\textsuperscript{2+}. DAG could associate with
synaptotagmin (SYT) in the ER at ER-PM contact sites, which may function
to stabilize the plasma membrane under stress, and facilitate the
exchange of lipids between the plasma membrane and the cortical ER. 5.
Besides PA, also PIP\textsubscript{2} accumulates under heat stress,
through PIP kinase (PIPK) activity, first only in the plasma membrane,
later also in internal membranes, including the nuclear envelope.
PIP\textsubscript{2} regulates effector proteins through specific
lipid-binding domains.

\textbf{Literature:}

Ackermann, F., \& Stanislas, T. (2020). The Plasma Membrane---An
Integrating Compartment for Mechano-Signaling. \emph{Plants} ,\emph{9}
(4), 505. https://doi.org/10.3390/plants9040505

Ali, G. S., Golovkin, M., \& Reddy, A. S. N. (2003). Nuclear
localization and \emph{in vivo} dynamics of a plant-specific
serine/arginine-rich protein. \emph{The Plant Journal} , \emph{36} (6),
883--893. https://doi.org/10.1046/j.1365-313X.2003.01932.x

Andreeva, Z., Ho, A. Y. Y., Barthet, M. M., Potock\selectlanguage{ngerman}ý, M., Bezvoda, R.,
\selectlanguage{polish}Ž\selectlanguage{ngerman}árský, V., \& Marc, J. (2009). Phospholipase D family interactions with
the cytoskeleton: Isoform delta promotes plasma membrane anchoring of
cortical microtubules. \emph{Functional Plant Biology} , \emph{36} (7),
600. https://doi.org/10.1071/FP09024

Ballweg, S., Sezgin, E., Doktorova, M., Covino, R., Reinhard, J.,
Wunnicke, D., Hänelt, I., Levental, I., Hummer, G., \& Ernst, R. (2020).
Regulation of lipid saturation without sensing membrane
fluidity.\emph{Nature Communications} , \emph{11} (1).
https://doi.org/10.1038/s41467-020-14528-1

Balogh, G., Péter, M., Glatz, A., Gombos, I., Török, Z., Horváth, I.,
Harwood, J. L., \& Vígh, L. (2013). Key role of lipids in heat stress
management. \emph{FEBS Letters} , \emph{587} (13), 1970--1980.
https://doi.org/10.1016/j.febslet.2013.05.016

Bavi, N., Nikolaev, Y. A., Bavi, O., Ridone, P., Martinac, A. D.,
Nakayama, Y., Cox, C. D., \& Martinac, B. (2017). Principles of
Mechanosensing at the Membrane Interface. In R. M. Epand \& J.-M.
Ruysschaert (Eds.), \emph{The Biophysics of Cell Membranes} (Vol. 19,
pp. 85--119). Springer Singapore.
https://doi.org/10.1007/978-981-10-6244-5\_4

Benítez-Angeles, M., Morales-Lázaro, S. L., Juárez-González, E., \&
Rosenbaum, T. (2020). TRPV1: Structure, Endogenous Agonists, and
Mechanisms. \emph{International Journal of Molecular Sciences}
,\emph{21} (10), 3421. https://doi.org/10.3390/ijms21103421

Benn, G., Bjornson, M., Ke, H., De Souza, A., Balmond, E. I., Shaw, J.
T., \& Dehesh, K. (2016). Plastidial metabolite MEcPP induces a
transcriptionally centered stress-response hub via the transcription
factor CAMTA3. \emph{Proceedings of the National Academy of Sciences}
,\emph{113} (31), 8855--8860. https://doi.org/10.1073/pnas.1602582113

Box, M. S., Huang, B. E., Domijan, M., Jaeger, K. E., Khattak, A. K.,
Yoo, S. J., Sedivy, E. L., Jones, D. M., Hearn, T. J., Webb, A. A. R.,
Grant, A., Locke, J. C. W., \& Wigge, P. A. (2015). ELF3 Controls
Thermoresponsive Growth in Arabidopsis. \emph{Current Biology}
,\emph{25} (2), 194--199. https://doi.org/10.1016/j.cub.2014.10.076

Casal, J. J., \& Balasubramanian, S. (2019).
Thermomorphogenesis.\emph{Annual Review of Plant Biology} , \emph{70}
(1), 321--346. https://doi.org/10.1146/annurev-arplant-050718-095919

Chakrabortee, S., Kayatekin, C., Newby, G. A., Mendillo, M. L.,
Lancaster, A., \& Lindquist, S. (2016). Luminidependens (LD) is an
Arabidopsis protein with prion behavior. \emph{Proceedings of the
National Academy of Sciences} , \emph{113} (21), 6065--6070.
https://doi.org/10.1073/pnas.1604478113

Chung, B. Y. W., Balcerowicz, M., Di Antonio, M., Jaeger, K. E., Geng,
F., Franaszek, K., Marriott, P., Brierley, I., Firth, A. E., \& Wigge,
P. A. (2020). An RNA thermoswitch regulates daytime growth in
Arabidopsis. \emph{Nature Plants} .
https://doi.org/10.1038/s41477-020-0633-3

Collado, J., Kalemanov, M., Campelo, F., Bourgoint, C., Thomas, F.,
Loewith, R., Martínez-Sánchez, A., Baumeister, W., Stefan, C. J., \&
Fernández-Busnadiego, R. (2019). Tricalbin-Mediated Contact Sites
Control ER Curvature to Maintain Plasma Membrane
Integrity.\emph{Developmental Cell} , \emph{51} (4), 476-487.e7.
https://doi.org/10.1016/j.devcel.2019.10.018

Cortijo, S., Charoensawan, V., Brestovitsky, A., Buning, R., Ravarani,
C., Rhodes, D., van Noort, J., Jaeger, K. E., \& Wigge, P. A. (2017).
Transcriptional Regulation of the Ambient Temperature Response by H2A.Z
Nucleosomes and HSF1 Transcription Factors in
Arabidopsis.\emph{Molecular Plant} , \emph{10} (10), 1258--1273.
https://doi.org/10.1016/j.molp.2017.08.014

Covino, R., Ballweg, S., Stordeur, C., Michaelis, J. B., Puth, K.,
Wernig, F., Bahrami, A., Ernst, A. M., Hummer, G., \& Ernst, R. (2016).
A Eukaryotic Sensor for Membrane Lipid Saturation. \emph{Molecular Cell}
, \emph{63} (1), 49--59. https://doi.org/10.1016/j.molcel.2016.05.015

Crawford, A. J., McLachlan, D. H., Hetherington, A. M., \& Franklin, K.
A. (2012). High temperature exposure increases plant cooling
capacity.\emph{Current Biology} , \emph{22} (10), R396--R397.
https://doi.org/10.1016/j.cub.2012.03.044

Cybulski, L. E., Martín, M., Mansilla, M. C., Fernández, A., \& de
Mendoza, D. (2010). Membrane Thickness Cue for Cold Sensing in a
Bacterium. \emph{Current Biology} , \emph{20} (17), 1539--1544.
https://doi.org/10.1016/j.cub.2010.06.074

Deng, Y., Humbert, S., Liu, J.-X., Srivastava, R., Rothstein, S. J., \&
Howell, S. H. (2011). Heat induces the splicing by IRE1 of a mRNA
encoding a transcription factor involved in the unfolded protein
response in Arabidopsis. \emph{Proceedings of the National Academy of
Sciences} , \emph{108} (17), 7247--7252.
https://doi.org/10.1073/pnas.1102117108

Dietrich, P., Moeder, W., \& Yoshioka, K. (2020). Plant Cyclic
Nucleotide-Gated Channels: New Insights on their Functions and
Regulation. \emph{Plant Physiology} , pp.00425.2020.
https://doi.org/10.1104/pp.20.00425

Ding, Y., Shi, Y., \& Yang, S. (2020). Molecular Regulation of Plant
Responses to Environmental Temperatures. \emph{Molecular Plant}
,\emph{13} (4), 544--564. https://doi.org/10.1016/j.molp.2020.02.004

Edwards, K. D., Lynn, J. R., Gyula, P., Nagy, F., \& Millar, A. J.
(2005). Natural Allelic Variation in the Temperature-Compensation
Mechanisms of the \emph{Arabidopsis thaliana} Circadian
Clock.\emph{Genetics} , \emph{170} (1), 387--400.
https://doi.org/10.1534/genetics.104.035238

Ernst, R., Ballweg, S., \& Levental, I. (2018). Cellular mechanisms of
physicochemical membrane homeostasis. \emph{Current Opinion in Cell
Biology} , \emph{53} , 44--51. https://doi.org/10.1016/j.ceb.2018.04.013

Ezer, D., Jung, J.-H., Lan, H., Biswas, S., Gregoire, L., Box, M. S.,
Charoensawan, V., Cortijo, S., Lai, X., Stöckle, D., Zubieta, C.,
Jaeger, K. E., \& Wigge, P. A. (2017). The evening complex coordinates
environmental and endogenous signals in Arabidopsis. \emph{Nature
Plants} , \emph{3} (7). https://doi.org/10.1038/nplants.2017.87

Falcone, D. L., Ogas, J. P., \& Somerville, C. R. (2004). Regulation of
membrane fatty acid composition by temperature in mutants of Arabidopsis
with alterations in membrane lipid composition. \emph{BMC Plant Biology}
, \emph{4} (1), 17. https://doi.org/10.1186/1471-2229-4-17

Findlay, K. M. W., \& Jenkins, G. I. (2016). Regulation of UVR8
photoreceptor dimer/monomer photo-equilibrium in Arabidopsis plants
grown under photoperiodic conditions: UVR8
photo-equilibrium.\emph{Plant, Cell \& Environment} , \emph{39} (8),
1706--1714. https://doi.org/10.1111/pce.12724

Finka, A., Cuendet, A. F. H., Maathuis, F. J. M., Saidi, Y., \&
Goloubinoff, P. (2012). Plasma Membrane Cyclic Nucleotide Gated Calcium
Channels Control Land Plant Thermal Sensing and Acquired
Thermotolerance. \emph{The Plant Cell} , \emph{24} (8), 3333--3348.
https://doi.org/10.1105/tpc.112.095844

Fiorucci, A.-S., Galvão, V. C., Ince, Y. Ç., Boccaccini, A., Goyal, A.,
Allenbach Petrolati, L., Trevisan, M., \& Fankhauser, C. (2020).
PHYTOCHROME INTERACTING FACTOR 7 is important for early responses to
elevated temperature in Arabidopsis seedlings. \emph{New Phytologist}
,\emph{226} (1), 50--58. https://doi.org/10.1111/nph.16316

Fujii, Y., Tanaka, H., Konno, N., Ogasawara, Y., Hamashima, N., Tamura,
S., Hasegawa, S., Hayasaki, Y., Okajima, K., \& Kodama, Y. (2017).
Phototropin perceives temperature based on the lifetime of its
photoactivated state. \emph{Proceedings of the National Academy of
Sciences} , \emph{114} (34), 9206--9211.
https://doi.org/10.1073/pnas.1704462114

Furt, F., König, S., Bessoule, J.-J., Sargueil, F., Zallot, R.,
Stanislas, T., Noirot, E., Lherminier, J., Simon-Plas, F., Heilmann, I.,
\& Mongrand, S. (2010). Polyphosphoinositides Are Enriched in Plant
Membrane Rafts and Form Microdomains in the Plasma Membrane. \emph{Plant
Physiology} , \emph{152} (4), 2173--2187.
https://doi.org/10.1104/pp.109.149823

Gao, F., Han, X., Wu, J., Zheng, S., Shang, Z., Sun, D., Zhou, R., \&
Li, B. (2012). A heat-activated calcium-permeable channel - Arabidopsis
cyclic nucleotide-gated ion channel 6 - is involved in heat shock
responses: CNGC6 is a heat-activated calcium channel. \emph{The Plant
Journal} , \emph{70} (6), 1056--1069.
https://doi.org/10.1111/j.1365-313X.2012.04969.x

Gao, K., Liu, Y.-L., Li, B., Zhou, R.-G., Sun, D.-Y., \& Zheng, S.-Z.
(2014). Arabidopsis thaliana Phosphoinositide-Specific Phospholipase C
Isoform 3 (AtPLC3) and AtPLC9 have an Additive Effect on
Thermotolerance. \emph{Plant and Cell Physiology} , \emph{55} (11),
1873--1883. https://doi.org/10.1093/pcp/pcu116

Garab, G., Ughy, B., Waard, P. de, Akhtar, P., Javornik, U., Kotakis,
C., \selectlanguage{polish}Š\selectlanguage{english}ket, P., Karlick\selectlanguage{ngerman}ý, V., Materová, Z., \selectlanguage{polish}Š\selectlanguage{english}punda, V., Plavec, J., van
Amerongen, H., V\selectlanguage{ngerman}ígh, L., As, H. V., \& Lambrev, P. H. (2017). Lipid
polymorphism in chloroplast thylakoid membranes -- as revealed by
31P-NMR and time-resolved merocyanine fluorescence
spectroscopy.\emph{Scientific Reports} , \emph{7} (1).
https://doi.org/10.1038/s41598-017-13574-y

Gilroy, S., Bia\selectlanguage{polish}ł\selectlanguage{english}asek, M., Suzuki, N., G\selectlanguage{ngerman}órecka, M., Devireddy, A. R.,
Karpi\selectlanguage{polish}ń\selectlanguage{english}ski, S., \& Mittler, R. (2016). ROS, Calcium, and Electric
Signals: Key Mediators of Rapid Systemic Signaling in Plants.\emph{Plant
Physiology} , \emph{171} (3), 1606--1615.
https://doi.org/10.1104/pp.16.00434

Guo, L., Devaiah, S. P., Narasimhan, R., Pan, X., Zhang, Y., Zhang, W.,
\& Wang, X. (2012). Cytosolic Glyceraldehyde-3-Phosphate Dehydrogenases
Interact with Phospholipase D\selectlanguage{greek}δ \selectlanguage{english}to Transduce Hydrogen Peroxide Signals in
the \emph{Arabidopsis} Response to Stress. \emph{The Plant Cell}
,\emph{24} (5), 2200--2212. https://doi.org/10.1105/tpc.111.094946

Hahm, J., Kim, K., Qiu, Y., \& Chen, M. (2020). Increasing ambient
temperature progressively disassembles Arabidopsis phytochrome B from
individual photobodies with distinct thermostabilities. \emph{Nature
Communications} , \emph{11} (1).
https://doi.org/10.1038/s41467-020-15526-z

Halbleib, K., Pesek, K., Covino, R., Hofbauer, H. F., Wunnicke, D.,
H\selectlanguage{ngerman}änelt, I., Hummer, G., \& Ernst, R. (2017). Activation of the Unfolded
Protein Response by Lipid Bilayer Stress. \emph{Molecular Cell}
,\emph{67} (4), 673-684.e8. https://doi.org/10.1016/j.molcel.2017.06.012

Hatfield, J. L., \& Prueger, J. H. (2015). Temperature extremes: Effect
on plant growth and development. \emph{Weather and Climate Extremes}
,\emph{10} , 4--10. https://doi.org/10.1016/j.wace.2015.08.001

Hayes, S. (2020). Interaction of Light and Temperature Signalling in
Plants. In \emph{ELS} (1st ed.). Wiley.
https://doi.org/10.1002/047001590X

Heckathorn, S. A., Downs, C. A., Sharkey, T. D., \& Coleman, J. S.
(1998). The Small, Methionine-Rich Chloroplast Heat-Shock Protein
Protects Photosystem II Electron Transport during Heat
Stress.\emph{Plant Physiology} , \emph{116} (1), 439--444.
https://doi.org/10.1104/pp.116.1.439

Higashi, Y., Okazaki, Y., Myouga, F., Shinozaki, K., \& Saito, K.
(2015). Landscape of the lipidome and transcriptome under heat stress in
Arabidopsis thaliana. \emph{Scientific Reports} , \emph{5} (1).
https://doi.org/10.1038/srep10533

Horvath, I., Glatz, A., Varvasovszki, V., Torok, Z., Pali, T., Balogh,
G., Kovacs, E., Nadasdi, L., Benko, S., Joo, F., \& Vigh, L. (1998).
Membrane physical state controls the signaling mechanism of the heat
shock response in Synechocystis PCC 6803: Identification of hsp17 as a
``fluidity gene.'' \emph{Proceedings of the National Academy of
Sciences} , \emph{95} (7), 3513--3518.
https://doi.org/10.1073/pnas.95.7.3513

Hou, Q., Ufer, G., \& Bartels, D. (2015). Lipid signalling in plant
responses to abiotic stress. \emph{Plant Cell Environ} .
https://doi.org/10.1111/pce.12666

Howarth, C. J., \& Ougham, H. J. (1993). Gene expression under
temperature stress*. \emph{New Phytologist} , \emph{125} (1), 1--26.
https://doi.org/10.1111/j.1469-8137.1993.tb03862.x

Huang, H., Alvarez, S., Bindbeutel, R., Shen, Z., Naldrett, M. J.,
Evans, B. S., Briggs, S. P., Hicks, L. M., Kay, S. A., \& Nusinow, D. A.
(2016). Identification of Evening Complex Associated Proteins
in\emph{Arabidopsis} by Affinity Purification and Mass
Spectrometry.\emph{Molecular \& Cellular Proteomics} , \emph{15} (1),
201--217. https://doi.org/10.1074/mcp.M115.054064

Jahns, P., Latowski, D., \& Strzalka, K. (2009). Mechanism and
regulation of the violaxanthin cycle: The role of antenna proteins and
membrane lipids. \emph{Biochimica et Biophysica Acta (BBA) -
Bioenergetics} , \emph{1787} (1), 3--14.
https://doi.org/10.1016/j.bbabio.2008.09.013

Jaillais, Y., \& Ott, T. (2020). The Nanoscale Organization of the
Plasma Membrane and Its Importance in Signaling: A Proteolipid
Perspective. \emph{Plant Physiology} , \emph{182} (4), 1682--1696.
https://doi.org/10.1104/pp.19.01349

Janda, M., Lamparová, L., Zubíková, A., Burketová, L., Martinec, J., \&
Kr\selectlanguage{polish}č\selectlanguage{english}kov\selectlanguage{ngerman}á, Z. (2019). Temporary heat stress suppresses PAMP\selectlanguage{english}-triggered
immunity and resistance to bacteria in \emph{Arabidopsis thaliana}
.\emph{Molecular Plant Pathology} , \emph{20} (7), 1005--1012.
https://doi.org/10.1111/mpp.12799

Jung, J.-H., Barbosa, A. D., Hutin, S., Kumita, J. R., Gao, M., Derwort,
D., Silva, C. S., Lai, X., Pierre, E., Geng, F., Kim, S.-B., Baek, S.,
Zubieta, C., Jaeger, K. E., \& Wigge, P. A. (2020). A prion-like domain
in ELF3 functions as a thermosensor in Arabidopsis. \emph{Nature} .
https://doi.org/10.1038/s41586-020-2644-7

Jung, J.-H., Domijan, M., Klose, C., Biswas, S., Ezer, D., Gao, M.,
Khattak, A. K., Box, M. S., Charoensawan, V., Cortijo, S., Kumar, M.,
Grant, A., Locke, J. C. W., Schafer, E., Jaeger, K. E., \& Wigge, P. A.
(2016). Phytochromes function as thermosensors in \emph{Arabidopsis}
.\emph{Science} , \emph{354} (6314), 886--889.
https://doi.org/10.1126/science.aaf6005

Kang, Y., Khan, S., \& Ma, X. (2009). Climate change impacts on crop
yield, crop water productivity and food security -- A
review.\emph{Progress in Natural Science} , \emph{19} (12), 1665--1674.
https://doi.org/10.1016/j.pnsc.2009.08.001

Kim, C. (2020). High Ambient Temperature Accelerates Leaf Senescence via
PHYTOCHROME-INTERACTING FACTOR 4 and 5 in Arabidopsis. \emph{Molecules
and Cells} , \emph{43} (7). https://doi.org/10.14348/MOLCELLS.2020.0117

Kim, S.-C., Guo, L., \& Wang, X. (2020). Nuclear moonlighting of
cytosolic glyceraldehyde-3-phosphate dehydrogenase regulates Arabidopsis
response to heat stress. \emph{Nature Communications} , \emph{11} (1).
https://doi.org/10.1038/s41467-020-17311-4

Koini, M. A., Alvey, L., Allen, T., Tilley, C. A., Harberd, N. P.,
Whitelam, G. C., \& Franklin, K. A. (2009). High Temperature-Mediated
Adaptations in Plant Architecture Require the bHLH Transcription Factor
PIF4. \emph{Current Biology} , \emph{19} (5), 408--413.
https://doi.org/10.1016/j.cub.2009.01.046

Kostaki, K.-I., Coupel-Ledru, A., Bonnell, V. C., Gustavsson, M., Sun,
P., McLaughlin, F. J., Fraser, D. P., McLachlan, D. H., Hetherington, A.
M., Dodd, A. N., \& Franklin, K. A. (2020). Guard Cells Integrate Light
and Temperature Signals to Control Stomatal Aperture. \emph{Plant
Physiology} , \emph{182} (3), 1404--1419.
https://doi.org/10.1104/pp.19.01528

Krumova, S. B., Dijkema, C., de Waard, P., Van As, H., Garab, G., \& van
Amerongen, H. (2008). Phase behavior of phosphatidylglycerol in spinach
thylakoid membranes as revealed by 31P-NMR. \emph{Biochimica et
Biophysica Acta (BBA) - Biomembranes} , \emph{1778} (4), 997--1003.
https://doi.org/10.1016/j.bbamem.2008.01.004

Kumar, S. V., \& Wigge, P. A. (2010). H2A.Z-Containing Nucleosomes
Mediate the Thermosensory Response in Arabidopsis. \emph{Cell}
,\emph{140} (1), 136--147. https://doi.org/10.1016/j.cell.2009.11.006

Latowski, D., Kruk, J., Burda, K., Skrzynecka-Jaskier, M.,
Kostecka-Guga\selectlanguage{polish}ł\selectlanguage{english}a, A., \& Strza\selectlanguage{polish}ł\selectlanguage{english}ka, K. (2002). Kinetics of violaxanthin
de-epoxidation by violaxanthin de-epoxidase, a xanthophyll cycle enzyme,
is regulated by membrane fluidity in model lipid bilayers: Violaxanthin
de-epoxidation in liposomes. \emph{European Journal of Biochemistry}
,\emph{269} (18), 4656--4665.
https://doi.org/10.1046/j.1432-1033.2002.03166.x

Lee, S., Lee, H.-J., Huh, S. U., Paek, K.-H., Ha, J.-H., \& Park, C.-M.
(2014). The Arabidopsis NAC transcription factor NTL4 participates in a
positive feedback loop that induces programmed cell death under heat
stress conditions. \emph{Plant Science} , \emph{227} , 76--83.
https://doi.org/10.1016/j.plantsci.2014.07.003

Legris, M., Klose, C., Burgie, E. S., Rojas, C. C. R., Neme, M.,
Hiltbrunner, A., Wigge, P. A., Sch\selectlanguage{ngerman}äfer, E., Vierstra, R. D., \& Casal,
J. J. (2016). Phytochrome B integrates light and temperature signals
in\emph{Arabidopsis} . \emph{Science} , \emph{354} (6314), 897--900.
https://doi.org/10.1126/science.aaf5656

Lenzoni, G., \& Knight, M. R. (2019). Increases in Absolute Temperature
Stimulate Free Calcium Concentration Elevations in the
Chloroplast.\emph{Plant and Cell Physiology} , \emph{60} (3), 538--548.
https://doi.org/10.1093/pcp/pcy227

Liang, M., Li, H., Zhou, F., Li, H., Liu, J., Hao, Y., Wang, Y., Zhao,
H., \& Han, S. (2015). Subcellular Distribution of NTL Transcription
Factors in \emph{Arabidopsis thaliana} : Subcellular Distribution of
AtNTLs. \emph{Traffic} , \emph{16} (10), 1062--1074.
https://doi.org/10.1111/tra.12311

Liao, C., Zheng, Y., \& Guo, Y. (2017). MYB30 transcription factor
regulates oxidative and heat stress responses through ANNEXIN-mediated
cytosolic calcium signaling in \emph{Arabidopsis} . \emph{New
Phytologist} , \emph{216} (1), 163--177.
https://doi.org/10.1111/nph.14679

Liu, H., \& Charng, Y. (2013). Common and Distinct Functions of
Arabidopsis Class A1 and A2 Heat Shock Factors in Diverse Abiotic Stress
Responses and Development. \emph{Plant Physiology} , \emph{163} (1),
276--290. https://doi.org/10.1104/pp.113.221168

Liu, H.-T., Li, B., Shang, Z.-L., Li, X.-Z., Mu, R.-L., Sun, D.-Y., \&
Zhou, R.-G. (2003). Calmodulin Is Involved in Heat Shock Signal
Transduction in Wheat. \emph{Plant Physiology} , \emph{132} (3),
1186--1195. https://doi.org/10.1104/pp.102.018564

Liu, H.-T., Li, G.-L., Chang, H., Sun, D.-Y., Zhou, R.-G., \& Li, B.
(2007). Calmodulin-binding protein phosphatase PP7 is involved in
thermotolerance in Arabidopsis. \emph{Plant, Cell \& Environment}
,\emph{30} (2), 156--164.
https://doi.org/10.1111/j.1365-3040.2006.01613.x

Liu, X., Lyu, Y., Yang, W., Yang, Z., Lu, S., \& Liu, J. (2020). A
membrane\selectlanguage{english}-associated NAC transcription factor OsNTL3 is involved in
thermotolerance in rice. \emph{Plant Biotechnology Journal} ,\emph{18}
(5), 1317--1329. https://doi.org/10.1111/pbi.13297

Lobell, D. B., \& Field, C. B. (2007). Global scale climate--crop yield
relationships and the impacts of recent warming. \emph{Environmental
Research Letters} , \emph{2} (1), 014002.
https://doi.org/10.1088/1748-9326/2/1/014002

Los, D. A., \& Murata, N. (2004). Membrane fluidity and its roles in the
perception of environmental signals. \emph{Biochimica et Biophysica Acta
(BBA) - Biomembranes} , \emph{1666} (1--2), 142--157.
https://doi.org/10.1016/j.bbamem.2004.08.002

Matsuda, O., Sakamoto, H., Hashimoto, T., \& Iba, K. (2005). A
Temperature-sensitive Mechanism That Regulates Post-translational
Stability of a Plastidial \selectlanguage{greek}ω-\selectlanguage{english}3 Fatty Acid Desaturase (FAD8)
in\emph{Arabidopsis} Leaf Tissues. \emph{Journal of Biological
Chemistry} ,\emph{280} (5), 3597--3604.
https://doi.org/10.1074/jbc.M407226200

McLoughlin, F., Arisz, S. A., Dekker, H. L., Kramer, G., de Koster, C.
G., Haring, M. A., Munnik, T., \& Testerink, C. (2013). Identification
of novel candidate phosphatidic acid-binding proteins involved in the
salt-stress response of Arabidopsis thaliana roots. \emph{Biochem J}
,\emph{450} (3), 573--581. https://doi.org/10.1042/BJ20121639

Miller, G., Schlauch, K., Tam, R., Cortes, D., Torres, M. A., Shulaev,
V., Dangl, J. L., \& Mittler, R. (2009). The Plant NADPH Oxidase RBOHD
Mediates Rapid Systemic Signaling in Response to Diverse
Stimuli.\emph{Science Signaling} , \emph{2} (84), ra45--ra45.
https://doi.org/10.1126/scisignal.2000448

Mishkind, M., Vermeer, J. E. M., Darwish, E., \& Munnik, T. (2009). Heat
stress activates phospholipase D and triggers PIP
\textsubscript{2}accumulation at the plasma membrane and nucleus.
\emph{The Plant Journal} , \emph{60} (1), 10--21.
https://doi.org/10.1111/j.1365-313X.2009.03933.x

Mori, K., Renhu, N., Naito, M., Nakamura, A., Shiba, H., Yamamoto, T.,
Suzaki, T., Iida, H., \& Miura, K. (2018). Ca2+-permeable
mechanosensitive channels MCA1 and MCA2 mediate cold-induced cytosolic
Ca2+ increase and cold tolerance in Arabidopsis. \emph{Scientific
Reports} , \emph{8} (1). https://doi.org/10.1038/s41598-017-17483-y

Munnik, T. (2014). PI-PLC: Phosphoinositide-Phospholipase C in Plant
Signaling. In Xuemin Wang (Ed.), \emph{Phospholipases in Plant
Signaling} (Vol. 20, pp. 27--54). Springer Berlin Heidelberg.
https://doi.org/10.1007/978-3-642-42011-5\_2

Murakami, Y. (2000). Trienoic Fatty Acids and Plant Tolerance of High
Temperature. \emph{Science} , \emph{287} (5452), 476--479.
https://doi.org/10.1126/science.287.5452.476

Nawkar, G. M., Kang, C. H., Maibam, P., Park, J. H., Jung, Y. J., Chae,
H. B., Chi, Y. H., Jung, I. J., Kim, W. Y., Yun, D.-J., \& Lee, S. Y.
(2017). HY5, a positive regulator of light signaling, negatively
controls the unfolded protein response in \emph{Arabidopsis}
.\emph{Proceedings of the National Academy of Sciences} , \emph{114}
(8), 2084--2089. https://doi.org/10.1073/pnas.1609844114

Nickels, J. D., Smith, M. D., Alsop, R. J., Himbert, S., Yahya, A.,
Cordner, D., Zolnierczuk, P., Stanley, C. B., Katsaras, J., Cheng, X.,
\& Rheinst\selectlanguage{ngerman}ädter, M. C. (2019). Lipid Rafts: Buffers of Cell Membrane
Physical Properties. \emph{The Journal of Physical Chemistry B}
,\emph{123} (9), 2050--2056. https://doi.org/10.1021/acs.jpcb.8b12126

Nieto, C., López-Salmerón, V., Davière, J.-M., \& Prat, S. (2015).
ELF3-PIF4 Interaction Regulates Plant Growth Independently of the
Evening Complex. \emph{Current Biology} , \emph{25} (2), 187--193.
https://doi.org/10.1016/j.cub.2014.10.070

Niu, Y., \& Xiang, Y. (2018). An Overview of Biomembrane Functions in
Plant Responses to High-Temperature Stress. \emph{Frontiers in Plant
Science} , \emph{9} . https://doi.org/10.3389/fpls.2018.00915

Nusinow, D. A., Helfer, A., Hamilton, E. E., King, J. J., Imaizumi, T.,
Schultz, T. F., Farré, E. M., \& Kay, S. A. (2011). The ELF4--ELF3--LUX
complex links the circadian clock to diurnal control of hypocotyl
growth. \emph{Nature} , \emph{475} (7356), 398--402.
https://doi.org/10.1038/nature10182

O'Quin, J. B., Bourassa, L., Zhang, D., Shockey, J. M., Gidda, S. K.,
Fosnot, S., Chapman, K. D., Mullen, R. T., \& Dyer, J. M. (2010).
Temperature-sensitive Post-translational Regulation of Plant Omega-3
Fatty-acid Desaturases Is Mediated by the Endoplasmic
Reticulum-associated Degradation Pathway. \emph{Journal of Biological
Chemistry} , \emph{285} (28), 21781--21796.
https://doi.org/10.1074/jbc.M110.135236

Park, Y.-J., Lee, H.-J., Ha, J.-H., Kim, J. Y., \& Park, C.-M. (2017).
COP1 conveys warm temperature information to hypocotyl
thermomorphogenesis. \emph{New Phytologist} , \emph{215} (1), 269--280.
https://doi.org/10.1111/nph.14581

Park, Y.-J., \& Park, C.-M. (2019). Physicochemical modeling of the
phytochrome-mediated photothermal sensing. \emph{Scientific Reports}
,\emph{9} (1). https://doi.org/10.1038/s41598-019-47019-5

Pokotylo, I., Pejchar, P., Potocký, M., Kocourková, D., Kr\selectlanguage{polish}č\selectlanguage{english}kov\selectlanguage{ngerman}á, Z.,
Ruelland, E., Kravets, V., \& Martinec, J. (2013). The plant
non-specific phospholipase C gene family. Novel competitors in lipid
signalling. \emph{Progress in Lipid Research} , \emph{52} (1), 62--79.
https://doi.org/10.1016/j.plipres.2012.09.001

Prager-Khoutorsky, M., Khoutorsky, A., \& Bourque, C. W. (2014). Unique
Interweaved Microtubule Scaffold Mediates Osmosensory Transduction via
Physical Interaction with TRPV1. \emph{Neuron} , \emph{83} (4),
866--878. https://doi.org/10.1016/j.neuron.2014.07.023

Pudasaini, A., Shim, J. S., Song, Y. H., Shi, H., Kiba, T., Somers, D.
E., Imaizumi, T., \& Zoltowski, B. D. (2017). Kinetics of the LOV domain
of ZEITLUPE determine its circadian function in Arabidopsis.\emph{ELife}
, \emph{6} . https://doi.org/10.7554/eLife.21646

Quint, M., Delker, C., Franklin, K. A., Wigge, P. A., Halliday, K. J.,
\& van Zanten, M. (2016). Molecular and genetic control of plant
thermomorphogenesis. \emph{Nature Plants} , \emph{2} (1).
https://doi.org/10.1038/nplants.2015.190

Reddy, A. S. N., Day, I. S., Göhring, J., \& Barta, A. (2012).
Localization and Dynamics of Nuclear Speckles in Plants. \emph{Plant
Physiology} , \emph{158} (1), 67--77.
https://doi.org/10.1104/pp.111.186700

Riback, J. A., Katanski, C. D., Kear-Scott, J. L., Pilipenko, E. V.,
Rojek, A. E., Sosnick, T. R., \& Drummond, D. A. (2017).
Stress-Triggered Phase Separation Is an Adaptive, Evolutionarily Tuned
Response. \emph{Cell} , \emph{168} (6), 1028-1040.e19.
https://doi.org/10.1016/j.cell.2017.02.027

Richards, S. L., Laohavisit, A., Mortimer, J. C., Shabala, L.,
Swarbreck, S. M., Shabala, S., \& Davies, J. M. (2014). Annexin 1
regulates the H \textsubscript{2} O \textsubscript{2} -induced calcium
signature in \emph{Arabidopsis thaliana} roots. \emph{The Plant Journal}
, \emph{77} (1), 136--145. https://doi.org/10.1111/tpj.12372

Rivasseau, C., Seemann, M., Boisson, A.-M., Streb, P., Gout, E., Douce,
R., Rohmer, M., \& Bligny, R. (2009). Accumulation of 2-
\emph{C}-methyl-d-erythritol 2,4-cyclodiphosphate in illuminated plant
leaves at supraoptimal temperatures reveals a bottleneck of the
prokaryotic methylerythritol 4-phosphate pathway of isoprenoid
biosynthesis.\emph{Plant, Cell \& Environment} , \emph{32} (1), 82--92.
https://doi.org/10.1111/j.1365-3040.2008.01903.x

Ruiz-Lopez, N., Pérez-Sancho, J., del Valle, A. E., Haslam, R. P.,
Vanneste, S., Catalá, R., Perea-Resa, C., Van Damme, D.,
García-Hernández, S., Albert, A., Vallarino, J., Lin, J., Friml, J.,
Macho, A. P., Salinas, J., Rosado, A., Napier, J. A., Amorim-Silva, V.,
\& Botella, M. A. (2020). \emph{Synaptotagmins Maintain Diacylglycerol
Homeostasis at Endoplasmic Reticulum-Plasma Membrane Contact Sites
during Abiotic Stress} {[}Preprint{]}. Molecular Biology.
https://doi.org/10.1101/2020.07.28.222919

Rütgers, M., Muranaka, L. S., Mühlhaus, T., Sommer, F., Thoms, S.,
Schurig, J., Willmund, F., Schulz-Raffelt, M., \& Schroda, M. (2017).
Substrates of the chloroplast small heat shock proteins 22E/F point to
thermolability as a regulative switch for heat acclimation in
Chlamydomonas reinhardtii. \emph{Plant Molecular Biology} , \emph{95}
(6), 579--591. https://doi.org/10.1007/s11103-017-0672-y

Rütgers, M., Muranaka, L. S., Schulz-Raffelt, M., Thoms, S., Schurig,
J., Willmund, F., \& Schroda, M. (2017). Not changes in membrane
fluidity but proteotoxic stress triggers heat shock protein expression
in \emph{Chlamydomonas reinhardtii} . \emph{Plant, Cell \& Environment}
,\emph{40} (12), 2987--3001. https://doi.org/10.1111/pce.13060

Saenz, J. P., Sezgin, E., Schwille, P., \& Simons, K. (2012). Functional
convergence of hopanoids and sterols in membrane
ordering.\emph{Proceedings of the National Academy of Sciences} ,
\emph{109} (35), 14236--14240. https://doi.org/10.1073/pnas.1212141109

Saidi, Y., Finka, A., \& Goloubinoff, P. (2011). Heat perception and
signalling in plants: A tortuous path to thermotolerance:
Minireview.\emph{New Phytologist} , \emph{190} (3), 556--565.
https://doi.org/10.1111/j.1469-8137.2010.03571.x

Saidi, Y., Finka, A., Muriset, M., Bromberg, Z., Weiss, Y. G., Maathuis,
F. J. M., \& Goloubinoff, P. (2009). The Heat Shock Response in Moss
Plants Is Regulated by Specific Calcium-Permeable Channels in the Plasma
Membrane. \emph{The Plant Cell} , \emph{21} (9), 2829--2843.
https://doi.org/10.1105/tpc.108.065318

Sangwan, V., Orvar, B. L., Beyerly, J., Hirt, H., \& Dhindsa, R. S.
(2002). Opposite changes in membrane fluidity mimic cold and heat stress
activation of distinct plant MAP kinase pathways. \emph{The Plant
Journal} , \emph{31} (5), 629--638.
https://doi.org/10.1046/j.1365-313X.2002.01384.x

Schaller, S., Latowski, D., Jemio\selectlanguage{polish}ł\selectlanguage{english}a-Rzemi\selectlanguage{polish}ń\selectlanguage{english}ska, M., Wilhelm, C.,
Strza\selectlanguage{polish}ł\selectlanguage{english}ka, K., \& Goss, R. (2010). The main thylakoid membrane lipid
monogalactosyldiacylglycerol (MGDG) promotes the de-epoxidation of
violaxanthin associated with the light-harvesting complex of photosystem
II (LHCII). \emph{Biochimica et Biophysica Acta (BBA) - Bioenergetics}
,\emph{1797} (3), 414--424. https://doi.org/10.1016/j.bbabio.2009.12.011

Shiva, S., Samarakoon, T., Lowe, K. A., Roach, C., Vu, H. S., Colter,
M., Porras, H., Hwang, C., Roth, M. R., Tamura, P., Li, M., Schrick, K.,
Shah, J., Wang, X., Wang, H., \& Welti, R. (2020). Leaf Lipid
Alterations in Response to Heat Stress of Arabidopsis
thaliana.\emph{Plants} , \emph{9} (7), 845.
https://doi.org/10.3390/plants9070845

Silva, C. S., Nayak, A., Lai, X., Hutin, S., Hugouvieux, V., Jung,
J.-H., L\selectlanguage{ngerman}ópez-Vidriero, I., Franco-Zorrilla, J. M., Panigrahi, K. C. S.,
Nanao, M. H., Wigge, P. A., \& Zubieta, C. (2020). Molecular mechanisms
of Evening Complex activity in \emph{Arabidopsis} . \emph{Proceedings of
the National Academy of Sciences} , \emph{117} (12), 6901--6909.
https://doi.org/10.1073/pnas.1920972117

Song, P., Jia, Q., Chen, L., Jin, X., Su, Y., Zhang, W., \& Zhang, Q.
(2020). \selectlanguage{greek}\emph{Involvement of Phospholipase D δ in Regulation of
ROS-mediated Microtubule Organization and Stomatal Movement upon Heat
Shock}\selectlanguage{english} . 35.

Sun, A.-Z., \& Guo, F.-Q. (2016). Chloroplast Retrograde Regulation of
Heat Stress Responses in Plants. \emph{Frontiers in Plant Science}
,\emph{7} . https://doi.org/10.3389/fpls.2016.00398

Suri, S. S., \& Dhindsa, R. S. (2007). A heat-activated MAP kinase
(HAMK) as a mediator of heat shock response in tobacco cells: HAMK in
heat-shock response. \emph{Plant, Cell \& Environment} , \emph{31} (2),
218--226. https://doi.org/10.1111/j.1365-3040.2007.01754.x

Suzuki, N., Koussevitzky, S., Mittler, R., \& Miller, G. (2012). ROS and
redox signalling in the response of plants to abiotic stress: ROS and
redox signalling in plants. \emph{Plant, Cell \& Environment} ,\emph{35}
(2), 259--270. https://doi.org/10.1111/j.1365-3040.2011.02336.x

Tang, G.-Q., Novitzky, W. P., Carol Griffin, H., Huber, S. C., \& Dewey,
R. E. (2005). Oleate desaturase enzymes of soybean: Evidence of
regulation through differential stability and phosphorylation: Stability
and phosphorylation of FAD2 enzymes. \emph{The Plant Journal} ,\emph{44}
(3), 433--446. https://doi.org/10.1111/j.1365-313X.2005.02535.x

Theis, J., Gupta, T. K., Klingler, J., Wan, W., Albert, S., Keller, S.,
Engel, B. D., \& Schroda, M. (2019). VIPP1 rods engulf membranes
containing phosphatidylinositol phosphates. \emph{Scientific Reports}
,\emph{9} (1). https://doi.org/10.1038/s41598-019-44259-3

Thomas, L., Marondedze, C., Ederli, L., Pasqualini, S., \& Gehring, C.
(2013). Proteomic signatures implicate cAMP in light and temperature
responses in Arabidopsis thaliana. \emph{Journal of Proteomics}
,\emph{83} , 47--59. https://doi.org/10.1016/j.jprot.2013.02.032

T\selectlanguage{ngerman}örök, Z., Crul, T., Maresca, B., Schütz, G. J., Viana, F., Dindia, L.,
Piotto, S., Brameshuber, M., Balogh, G., Péter, M., Porta, A., Trapani,
A., Gombos, I., Glatz, A., Gungor, B., Peksel, B., Vigh, L., Csoboz, B.,
Horváth, I., \ldots{} Vigh, L. (2014). Plasma membranes as heat stress
sensors: From lipid-controlled molecular switches to therapeutic
applications. \emph{Biochimica et Biophysica Acta (BBA) - Biomembranes}
,\emph{1838} (6), 1594--1618.
https://doi.org/10.1016/j.bbamem.2013.12.015

van der Woude, L. C., Perrella, G., Snoek, B. L., van Hoogdalem, M.,
Novák, O., van Verk, M. C., van Kooten, H. N., Zorn, L. E., Tonckens,
R., Dongus, J. A., Praat, M., Stouten, E. A., Proveniers, M. C. G.,
Vellutini, E., Patitaki, E., Shapulatov, U., Kohlen, W.,
Balasubramanian, S., Ljung, K., \ldots{} van Zanten, M. (2019). HISTONE
DEACETYLASE 9 stimulates auxin-dependent thermomorphogenesis
in\emph{Arabidopsis thaliana} by mediating H2A.Z
depletion.\emph{Proceedings of the National Academy of Sciences} ,
\emph{116} (50), 25343--25354. https://doi.org/10.1073/pnas.1911694116

Voitsekhovskaja, O. V. (2019). Phytochromes and Other (Photo)Receptors
of Information in Plants. \emph{Russian Journal of Plant Physiology}
,\emph{66} (3), 351--364. https://doi.org/10.1134/S1021443719030154

Volkov, R. A., Panchuk, I. I., Mullineaux, P. M., \& Schöffl, F. (2006).
Heat stress-induced H2O2 is required for effective expression of heat
shock genes in Arabidopsis. \emph{Plant Molecular Biology} ,\emph{61}
(4--5), 733--746. https://doi.org/10.1007/s11103-006-0045-4

Vu, L. D., Gevaert, K., \& De Smet, I. (2019). Feeling the Heat:
Searching for Plant Thermosensors. \emph{Trends in Plant Science}
,\emph{24} (3), 210--219. https://doi.org/10.1016/j.tplants.2018.11.004

Walley, J., Xiao, Y., Wang, J.-Z., Baidoo, E. E., Keasling, J. D., Shen,
Z., Briggs, S. P., \& Dehesh, K. (2015). Plastid-produced
interorgannellar stress signal MEcPP potentiates induction of the
unfolded protein response in endoplasmic reticulum. \emph{Proceedings of
the National Academy of Sciences} , \emph{112} (19), 6212--6217.
https://doi.org/10.1073/pnas.1504828112

Wang, R., Zhang, Y., Kieffer, M., Yu, H., Kepinski, S., \& Estelle, M.
(2016). HSP90 regulates temperature-dependent seedling growth in
Arabidopsis by stabilizing the auxin co-receptor F-box protein
TIR1.\emph{Nature Communications} , \emph{7} (1).
https://doi.org/10.1038/ncomms10269

Wang, Xu, Ma, X., Wang, H., Li, B., Clark, G., Guo, Y., Roux, S., Sun,
D., \& Tang, W. (2015). Proteomic Study of Microsomal Proteins Reveals a
Key Role for \emph{Arabidopsis} Annexin 1 in Mediating Heat
Stress-Induced Increase in Intracellular Calcium Levels. \emph{Molecular
\& Cellular Proteomics} , \emph{14} (3), 686--694.
https://doi.org/10.1074/mcp.M114.042697

Wolf, S., Marani, A., \& Rudich, J. (1991). Effect of Temperature on
Carbohydrate Metabolism in Potato Plants. \emph{Journal of Experimental
Botany} , \emph{42} (5), 619--625. https://doi.org/10.1093/jxb/42.5.619

Wu, H.-C., Bulgakov, V. P., \& Jinn, T.-L. (2018). Pectin
Methylesterases: Cell Wall Remodeling Proteins Are Required for Plant
Response to Heat Stress. \emph{Frontiers in Plant Science} , \emph{9} .
https://doi.org/10.3389/fpls.2018.01612

Xiao, Y., Savchenko, T., Baidoo, E. E. K., Chehab, W. E., Hayden, D. M.,
Tolstikov, V., Corwin, J. A., Kliebenstein, D. J., Keasling, J. D., \&
Dehesh, K. (2012). Retrograde Signaling by the Plastidial Metabolite
MEcPP Regulates Expression of Nuclear Stress-Response Genes.\emph{Cell}
, \emph{149} (7), 1525--1535. https://doi.org/10.1016/j.cell.2012.04.038

Xu, Q., Paulsen, A. Q., Guikema, J. A., \& Paulsen, G. M. (1995).
Functional and ultrastructural injury to photosynthesis in wheat by high
temperature during maturation. \emph{Environmental and Experimental
Botany} , \emph{35} (1), 43--54.
https://doi.org/10.1016/0098-8472(94)00030-9

Yadav, D., Boyidi, P., Ahmed, I., \& Kirti, P. B. (2018). Plant annexins
and their involvement in stress responses. \emph{Environmental and
Experimental Botany} , \emph{155} , 293--306.
https://doi.org/10.1016/j.envexpbot.2018.07.002

Yan, Q., Huang, Q., Chen, J., Li, J., Liu, Z., Yang, Y., Li, X., \&
Wang, J. (2017). SYTA has positive effects on the heat resistance of
Arabidopsis. \emph{Plant Growth Regulation} , \emph{81} (3), 467--476.
https://doi.org/10.1007/s10725-016-0224-5

Yang, Z.-T., Lu, S.-J., Wang, M.-J., Bi, D.-L., Sun, L., Zhou, S.-F.,
Song, Z.-T., \& Liu, J.-X. (2014). A plasma membrane-tethered
transcription factor, NAC062/ANAC062/NTL6, mediates the unfolded protein
response in Arabidopsis. \emph{The Plant Journal} , \emph{79} (6),
1033--1043. https://doi.org/10.1111/tpj.12604

Zhang, L., Kondo, H., Kamikubo, H., Kataoka, M., \& Sakamoto, W. (2016).
VIPP1 Has a Disordered C-Terminal Tail Necessary for Protecting
Photosynthetic Membranes against Stress. \emph{Plant Physiology}
,\emph{171} (3), 1983--1995. https://doi.org/10.1104/pp.16.00532

Zhang, S.-S., Yang, H., Ding, L., Song, Z.-T., Ma, H., Chang, F., \&
Liu, J.-X. (2017). Tissue-Specific Transcriptomics Reveals an Important
Role of the Unfolded Protein Response in Maintaining Fertility upon Heat
Stress in Arabidopsis. \emph{The Plant Cell} , \emph{29} (5),
1007--1023. https://doi.org/10.1105/tpc.16.00916

Zheng, S.-Z., Liu, Y.-L., Li, B., Shang, Z.- lin, Zhou, R.-G., \& Sun,
D.-Y. (2012). Phosphoinositide-specific phospholipase C9 is involved in
the thermotolerance of Arabidopsis: AtPLC9 plays a role in
thermotolerance. \emph{The Plant Journal} , \emph{69} (4), 689--700.
https://doi.org/10.1111/j.1365-313X.2011.04823.x\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/Figure1-Review-Hayes2020/Figure1-Review-Hayes2020}

\end{center}
\end{figure}\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/Figure2-Review-Hayes2020/Figure2-Review-Hayes2020}

\end{center}
\end{figure}\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/Figure3-Review-Hayes2020/Figure3-Review-Hayes2020}

\end{center}
\end{figure}\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/Figure4-Review-Hayes2020/Figure4-Review-Hayes2020}

\end{center}
\end{figure}

\selectlanguage{english}
\FloatBarrier
\end{document}

