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\begin{document}

\title{Regulation mechanisms of bZIP transcription factors in plant grown on
drought, salt and cold soils}



\author[1]{yan Yu}%
\author[1]{Yuchen Qian}%
\author[1]{Mengyue Jiang}%
\author[1]{Jia Xu}%
\author[1]{Jingting Yang}%
\author[1]{Tongyao Zhang}%
\author[1]{Liangpeng Gou}%
\author[1]{Erxu Pi}%
\affil[1]{Hangzhou Normal University}%


\vspace{-1em}



  
  \date{May 17, 2024}


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\selectlanguage{english}
\begin{abstract}
The bZIP family is one of the most widely distributed and conserved
transcription factor categories in eukaryotes. They are widely involved
in processes of plant abiotic stress responses, such as improving the
ability of plants to adapt to drought, salinity and cold. To
comprehensively understand how plant bZIPs regulating these tolerances,
this article will have an overview of their distributions on different
species, characteristics of protein architecture, regulation mechanisms
for target genes' transcriptional expression, and relevant research
progresses in recent years. Specially, we will discuss the possible
roles of flavonoids, whose synthesis could be regulated by bZIPs, in
abovementioned plant tolerant responses.%
\end{abstract}%



\sloppy


\textbf{INTRODUCTION}

In the process of growth and development, plants are exposed to various
abiotic stress such as salinity, drought, low temperature, which limit
crop yield and quality. During evolution, plants acquire series of
resistances to these environmental stresses and survive through
physiological, biochemical and molecular responses. These responses are
usually originated by regulating the expression of relevant genes. bZIP
(basic leucine zipper) transcription factors, as one of the largest
transcription factor regulatory families, play very important roles in
the response to these abiotic stresses. bZIP TFs could be activated by
drought, high salt and chilling damage. By binding specifically
to\emph{cis} -elements in the promoter region of stress related genes,
they can regulate the transcriptional expressions of target genes,
thereby regulating stress resistance of plants. This article
comprehensively reviews the structural characteristics of bZIPs and
their regulation mechanisms on target genes.

\textbf{DISTRIBUTION AND CLASSIFICATION OF BZIP TRANSCRIPTION FACTORS}

Currently, there are at least 64 families of transcription factors have
been found in plants (P\selectlanguage{ngerman}érez-Rodriguez et al., 2010). According to their
differences in DNA-binding domains, transcription factors can be defined
as different families, such as bZIP, NAC, MYB, EREBP/AP2, Zinc-finger,
etc. Among which, bZIPs (basic region/leucine zipper motifs) are widely
found in humans, animals and plants, insects and microorganisms. To
date, a large number of bZIP transcription factors have been identified
in almost all eukaryotes. There are 77, 89, 247, 92, 89, 69, 125, 64,
55, 114 bZIP transcription factors been found in \emph{Arabidopsis
thaliana} ,\emph{Oryza sativa} , \emph{Glycine max} , \emph{Sorghum
bicolor} ,\emph{Hordeum vulgare L} , \emph{Solanum lycopersicum} ,
\emph{Zea mays} ,\emph{Cucumis sativus} , \emph{Vitis vinifera} and
\emph{Malus domestica} , respectively (Baloglu et al., 2014; Corrêa et
al., 2008; Li et al., 2015, 2016; Liu et al., 2014b; Nijhawan et al.,
2008; Pourabed et al., 2015; Wang et al. 2011; Wei et al., 2012; Zhang
et al. 2018). Only 25, 21 and 21 bZIP transcription factors were found
in yeast, nematode, and fruit fly (Riechmann et al., 2000). Compared to
other eukaryotes, plants have more bZIP homologous proteins and more
conserved amino acid sequences in these homologies (Ali et al., 2016).
Studies have shown that the structures of bZIP protein are closely
related to its biological function. Jakoby et al. (2002) used MEME
(multiple em for motif elicitation) to analyze a large number of bZIP
transcription factors in \emph{Arabidopsis thaliana} . Based on the
characteristics of both the bZIP and other conserved motifs, the 75
bZIPs in \emph{Arabidopsis thaliana}were classified into 10 subfamilies
of A, B, C, D, E, F, G, H, I and S. With similar method, the bZIP
transcription factor family genes in other plants have also been
categorized. The 131 bZIP transcription factors isolated from the
soybean genome were also divided into abovementioned 10 subfamilies A-S
(Liao et al., 2008). Though the 89 members of the bZIP transcription
factor family in rice were also divided into 10 subfamilies, the
subfamily S was replaced with J (Nijhawan et al., 2008). It seems that
most of these subfamilies of bZIPs are conserved among different plants.
Corrêa et al. (2008) identified the possible non-redundant complete sets
of bZIPs in rice, comprising 92 proteins, and in black cottonwood,
comprising 89 proteins. Based on both bZIP domain and other conserved
motifs similarities, these collections of bZIPs together with the 77
bZIPs from Arabidopsis were categorized into 13 subfamilies, including
A, B, C, D, E, F, G, H, I, J, K, L, and S, three subgroups J, K and L
were added.

With the advancement of bioinformatics, more and more conversed motifs,
except bZIP, were identified for categorizing bZIP subfamilies. Hence,
the classification of bZIP transcription factors has become more and
more sophisticated and scientific. Recent years, there are increasing
reports on regulation mechanism of various bZIPs on different stress
responses (Hwang et al., 2014; Ji et al., 2013; van Leene et al., 2016;
Liu et al., 2012; Tsugama et al., 2016; Wang et al., 2019; Zhang et al.,
2017a, b). Specific roles of bZIPs in different subgroups might also be
categorized into corresponding biological pathways, considering plenty
of functional annotated bZIPs been classified into the known subfamilies
with those sophisticated and scientific bioinformatics.

\textbf{ARCHITECTURE CHARACTERISTICS OF BZIP TRANSCRIPTION FACTORS}

Transcription factor (TF), also known as \emph{trans} -acting factor, is
a category of proteins that can specifically bind to \emph{cis} -acting
elements in the promoter region of eukaryotic genes, thereby activating
or silencing the expression of related genes in a specific time and
space. The structure of plant transcription factors generally includes
at least four functional domains, including the DNA binding domain, the
transcriptional regulatory domain, the nuclear localization signal and
the oligomerization site (Du et al., 2012). They work together to
regulate various biological processes.

Although the classification of bZIP varies depending on the researcher's
choice, there is currently a consensus on this type of transcription
factor that the protein sequence contains a conserved bZIP domain with
60-80 amino acids length. This domain is consisted of at least two
specific structures. Firstly, the N-terminus is a basic region composed
of about 20 basic amino acids, containing a nuclear localization signal
(NLS) and a N-x7-R/K structural unit that specifically binds to a DNA
sequence. This region is involved in nuclear localization and DNA
binding (Lee et al., 2006b). Secondly, the C-terminus, which is a
leucine zipper region, a heptad repeat of leucine or other bulky
hydrophobic amino acids (Ile, Val, Phe, or Met) positioned exactly nine
amino acids towards the C-terminus, creating an amphipathic helix. This
region is involved in the dimerization of the bZIP protein before it
binds to DNA (Hurst, 1994; Jakoby et al., 2002; Landschulz et al.,
1988). In addition to the bZIP conserved domain, the bZIPs also contain
other domains with transcriptional activation functions, such as the
R/KxxS/T and S/TxxD domains, which are phosphorylation sites of
Ca\textsuperscript{2+} independent protein kinase and casein kinase II
(Furihata et al., 2006). Besides, there are also some regions rich in
acidic amino acids such as Pro and Gln, which can activate the
transcriptional expression of downstream target genes (Liao et al.,
2008).

\textbf{MECHANISMS OF BZIP ON TRANSCRIPTIONAL REGULATION OF TARGET
GENES}

Through dimerization, phosphorylation, or interaction with other nuclear
proteins, the specificity and affinity of bZIP binding to DNA will
change, which will affect the activation of other genes, as well as its
own stability and subcellular localization (Schütze et al., 2008). By
forming homo- or heterodimers, binding specific gene promoters in its
basic region and interacting with \emph{cis} -acting elements of the
promoter region, the bZIP transcription factor inhibits or activates the
expression of multiple downstream related target genes, thereby
participating in transcriptional regulation process.

The binding specificity of bZIP factors in plants is mainly determined
by 3 bases flanking the 4 core nucleotides. Generally, bZIP factors
preferentially select ACGT core palindromes or pseudo-palindromic
\emph{cis} -acting elements to bind, such as G-box (CACGTG), C-box
(GACGTC), A-box (TACGTA), ABRE (ACGTGGC) (Izawa et al., 1993; Kim et al.
2004). Most of them are located in the ABA hormone-induced promoter
region. When the bZIP protein interacts with these \emph{cis} -acting
elements, the N-terminus of its basic domain is inserted into the large
groove of the DNA double-strand, and the C-terminus of the leucine
zipper is dimerized to form a superimposed curl helix (Landschulz et
al., 1988; Ellenberger et al., 1992).

G-box is one of the most common targets of bZIP transcription factors.
de Vetten and Ferl (1995) firstly found that corn GBF1 is a basic region
leucine zipper protein and could activate \emph{Adhl} expression by
binding to its G-box. After that, series of stress related genes were
found to be bound at their G-box and regulated by various bZIPs.
Kaminaka et al. (2006) found that\emph{Arabidopsis thaliana}
\emph{AtbZIP10} can combine G-box to negatively regulate plant
resistance to pathogenic bacteria and other stresses. Zou et al. (2008)
demonstrated that the rice OsbZIP10/OsABI5 could bind the G-box element
to \emph{trans} -activate the expression of stress resistance genes,
thereby inhibiting seed germination and seedling growth. Liu et al.
(2012) also studied rice and found that under low temperature
stress,\emph{OsbZIP52} /\emph{RISBZ5} can recognize the G-box on the
downstream target gene to enhance the low temperature sensitivity of
rice. The \emph{Arabidopsis thaliana}AtbZIP56/HY5 binds directly to the
promoters of light responsible element containing the G-box and thus
regulates their transcriptional activity (Yoon et al., 2006). Induced by
salt, the \emph{Tamarix hispida} bZIP1 bound to G-box of the stress
response gene and regulated the expression of downstream genes (Ji et
al., 2013). Using chromatin immunoprecipitation, Lee et al. (2006a)
demonstrated that CabZIP1 binds to the G-box elements in native promoter
of the hot pepper pathogenesis-related protein 1 (\emph{CaPR-1} ) gene
in vivo. Shaikhali et al. (2012) identified the AtbZIP16 as a component
binding to the G-box-containing promoter fragment of light-harvesting
chlorophyll a/b-binding protein2.4 (LHCB2.4) from nuclear extracts of
high light-treated Arabidopsis plants.

The ABRE element is also the most favorite target of bZIP transcription
factors. Sun et al. (2011) found that AtbZIP1 binds to ABRE active
elements and regulates the plant's response to low temperature stress
through ABA-dependent signaling pathways. Yoshida et al. (2015)
demonstrated that the \emph{Arabidopsis thaliana} bZIP transcription
factors ABF1, ABF2, ABF3, and ABF4 combined with ABRE and regulated the
expression of downstream genes related to salt and drought tolerance. In
maize, \emph{ZmbZIP17} functions as an ER stress transducer, interacting
with ABREs (Yang et al. 2013). Rice OsbZIP46/OsABF2 (Chang et al., 2017;
Hossain et al., 2010; Tang et al. 2012a), \emph{OsbZIP52/RISBZ5} (Liu et
al., 2012),\emph{OsbZIP10/OsABI5} (Zou et al., 2007; Zou et al., 2008),
OsbZIP05/OSBZ8 (Mukherjee et al., 2006; Nakagawa et al., 1996) all
regulate the expression of plant ABA-responsive genes by binding to the
ABRE element of the target gene. Zhang et al. (2017b) proved that wheat
TabZIP14-B showed transcriptional activation ability through the
transactivation assay and was capable of binding the abscisic acid (ABA)
responsive element (ABRE) in yeast. Wang et al. (2019) isolated and
functionally characterized the sweet potato \emph{IbABF4} gene, which
encodes a bZIP transcription factor. The IbABF4 protein localized to the
nucleus, exhibited transcriptional activation activity, and showed
binding to the cis-acting ABA-responsive element (ABRE) in vitro.

In addition, bZIP transcription factors could target on genes by C-Box
and A-box. Except for G-box, the C-box of pathogenic responsive genes
could also bound and negatively regulated by \emph{AtbZIP10}
in\emph{Arabidopsis thaliana} (Kaminaka et al., 2006). Induced by ABA
and drought, the \emph{Tamarix hispida} bZIP1 bound to C-box and
A-box\emph{cis} -elements of the stress response gene (Ji et al., 2013).

In summary, bZIP transcription factors regulate the transcriptional
expression by interacting with specific \emph{cis} -regulatory sequences
in the promoter region of response genes to regulate plant stress
tolerance (Sornaraj et al., 2016). To understand the actual relationship
between bZIP subfamilies and their binding \emph{cis} -regulator motifs
(Table I and Figure I), all the functional annotated bZIPs were
categorized into 13 known subgroups based on the method described by
Corrêa et al. (2008). It seems that the G-Box and ABRE attracts most
scientists' interests and are two most understood \emph{cis} -elements
of bZIP transcription factors (Table I). The bZIPs bind to G-Box are
categorized into subfamilies A, C, G, H, K and S; while those recognize
ABRE belong to the subgroups A, B, C, G and S (Table I). Besides, there
are also several reports on mechanisms about how bZIP transcription
factors regulate other two \emph{cis} -elements, C-box and A-box (Table
I). Interestingly, the bZIPs bind to C-box are usually belong to
subfamilies C and S; the functional annotated bZIP bind to A-box is
classified into subfamily S. Though the number of functional annotated
bZIP is limit, their binding activities of different subfamilies to
specific\emph{cis} -elements could also provide directional suggestions
for further research on de novo bZIPs and potential targets. However,
more evidences are still needed to fulfil the relevance between bZIP
subfamilies and corresponding \emph{cis} -elements.

\textbf{REGULATION MECHANISM OF PLANT BZIPS TO VARIOUS STRESSES}

Previous studies have found that bZIPs play important roles in response
to a variety of plant stresses, such as salinity, drought and cold
damage (Table II). Their regulation mechanism varies depending on
species of plant and types of stress.

\textbf{bZIP TFs involved in salt stress response}

Under salt stress, plant cell should successively face challenges of
osmotic stress, ion toxicity and oxidative stress (Rozema et al., 2008;
Munns et al., 2005). In these responses, bZIP transcription factors play
key roles in various physiological processes in \emph{Arabidopsis
thaliana} , tomato, tobacco, rice, and soybeans, etc.

In \emph{Arabidopsis thaliana} , AtbZIP17 was proven as a positive
regulator in the processes salt stress responses, it activates both the
expression of salt stress response gene \emph{ATHB-7} and
\emph{SES1}(Liu et al., 2007, 2008); while the AtbZIP24 was revealed as
a negative regulator in plant tolerance to salinity by RNAi interference
technology (Yang et al., 2009). Tang et al. (2012b) found that
heterologously expressing \emph{Arabidopsis thaliana} \emph{AtbZIP60}
could increase salt resistance and superoxide dismutase (SOD) activity
of tobacco, rice, and \emph{Pinus elliottii} . In \emph{Glycine max} ,
overexpression of the \emph{GmbZIP1} enhances salt tolerance in
transgenic plants (Gao et al., 2011). Besides, heterologously expressing
\emph{GmbZIP44} ,\emph{GmbZIP62} , and \emph{GmbZIP78} could
significantly increase salt resistance of transgenic \emph{Arabidopsis
thaliana} plants (Wang et al., 2015). In maize, the \emph{ABP9} was
found as a salinity responsible bZIP gene by Zhang et al. (2011a). Then,
Wang et al. (2017a) heterologously expressed it to improve the salt
tolerance of transgenic cotton. In \emph{Oryza sativa} , the
\emph{OsbZIP05/OSBZ8} firstly found with a higher transcriptional level
in salt tolerant cultivar than in salt sensitive cultivar, indicate that
\emph{OsbZIP05/OSBZ8} might play as a positive role in this stress
responses (Mukherjee et al., 2006). After that, OsbZIP12/OsABF1,
OsbZIP23, OsbZIP46/OsABF2, OsBZIP71 and OsbZIP72 were successively
proven to act as positive regulators in the process of salt tolerance
(Amir Hossain et al., 2010; Chang et al., 2017; Hossain et al., 2010;
Liu et al., 2014a; Lu et al., 2009; Tang et al. 2012a; Xiang et al.,
2008; Zhang et al., 2017a). OsbZIP71 can form both homodimers and
heterodimers with Group C members of the bZIP gene family, and
overexpression of \emph{OsbZIP71} can significantly enhance the salt
tolerance of transgenic rice (Liu et al., 2014a). On the contrary, the
plants overexpressing \emph{OsbZIP10/OsABI5} showed more obvious
chlorosis than wild type under high salt concentration, indicating that
\emph{OsbZIP10/OsABI5} participates in the salt stress tolerance
response of rice as a negative regulator, and gene silencing can reduce
the sensitivity of transgenic rice to salt (Zou et al., 2008).

Recent years, bZIPs in other plants have also been revealed to
participate salinity responsive processes. Cheng et al. (2013) isolated
a salt responsive transcriptional factor LrbZIP in lotus root and found
that transgenic lotus with \emph{LrbZIP} overexpression could grow with
normal root biomass, chlorophyll content, and electrolyte exudation rate
under NaCl treatment. Zhao et al. (2016) revealed that \emph{Brassica
napus} bZIP transcription factor BnaABF2 enhanced salt tolerance of
plants through the ABA pathway.

To sum up, many bZIP genes have been excavated in different plants and
confirmed that they can significantly enhance the salt tolerance of
plants, making the bZIP gene family a gene treasure house for improving
the salt tolerance of crops. Therefore, the use of bZIP transcription
factors to improve the salt tolerance of crops and breed new
salt-tolerant varieties is of great significance for improving
agricultural productivity and improving saline soils.

\textbf{bZIP TFs involved in drought stress response}

Drought is an adverse environmental factor that threatens plant growth
and development. Many plant bZIP family members are involved in response
to drought stress. Series of studies have shown that many rice bZIP
transcription factors are involved in drought resistance. Liu et al.
(2014b) found that rice\emph{OsbZIP71} directly binds to the promoters
of \emph{OsNHX1} and\emph{COR413-TM1} and activates their transcription
so as to enhance drought resistance of transgenic rice. Except rice,
some drought-related bZIP transcription factor genes cloned in other
plants also significantly enhanced the drought resistance of transgenic
crops. Overexpression of maize \emph{ABP9} confers excellent drought
tolerance to transgenic \emph{Arabidopsis thaliana} plant (Wang et al.,
2017a). During seed germination and plant development, transgenic ramie
plants overexpressing ramie \emph{BnbZIP2} were more tolerant to salt
stress than wild-type and more sensitive to drought stress (Huang et
al., 2016). In addition, overexpression of transcription factors such
as\emph{Arabidopsis thaliana} ABF3 (Wang et al., 2016b) and wheat
TabZIP60 (Zhang et al., 2015b) in plants can significantly improve the
drought resistance of transgenic plants. On the contrary, Lim et al.
(2018) found that the pepper bZIP transcription factor CaDILZ1 plays a
negative regulatory role in response to drought stress.

\textbf{bZIP TFs involved in cold stress response}

Low temperature stimulation will disturb the normal physiological and
metabolic activities and further affect the plant growth and
development. The plant mainly responds to low temperature stress through
the ICE-CBF-COR pathway. When the plant is exposed to low temperature,
it induces CBFs (C-repeat-binding Factors) expression by ICE (inducer of
CBF expression), which recognizes CRT/DRE (C-repeat/dehydration
responsive element) located on the target gene promoter and combines
with \emph{COR} (cold regulated genes) genes to regulate transcriptional
expression, thereby enhancing plant cold stress resistance (Shi et al.,
2018). bZIP transcription factors also play an indispensable role in
regulating plant cold stress responses.

According to incomplete statistics, the first rice bZIP-like
transcription factor identified and reported was OsbZIP38/LIP19 of the H
subfamily. Induced by low temperature, as a Fos-like molecular switch,
it is involved in the plant's response to cold signal pathways (Aguan et
al., 1991; Aguan et al., 1993; Shimizu et al., 2005). OsbZIP38/LIP19 and
subfamily member OsbZIP87/OsOBF1 are able to bind DNA and form
homodimers, and they are more likely to interact with OsbZIP38/LIP19 and
form heterodimers to participate in the plant's response to cold
signaling (Shimizu et al., 2005). In addition, OsbZIP52/RISBZ5,
OsbZIP68/ROS-bZIP1 and OsbZIP73/OsTFX1 in the rice bZIP transcription
factor family were also involved in cold resistance. OsbZIP52/RISBZ5 is
a member of the G subfamily. It is not induced by drought, salt, PEG,
and ABA, but by low temperature. It can form homodimers and specifically
bind G-box. However, the test of the cold tolerance of rice showed that
the survival rate of over-expressed \emph{OsbZIP52/RISBZ5} rice plants
was significantly lower than that of wild type. It can be seen that the
expression of \emph{OsbZIP52/RISBZ5} is inversely related to low
temperature tolerance (Liu et al., 2012). Cheng et al. (2007) found that
OsbZIP68/ROS-bZIP1 could be induced and responded quickly within 24
hours when rice was treated at 10 °C. Liu et al. (2018) identified a
total of 8 bZIP genes in rice, \emph{OsbZIP08} , \emph{OsbZIP35}
,\emph{OsbZIP38} , \emph{OsbZIP46} , \emph{OsbZIP63} , \emph{OsbZIP72}
,\emph{OsbZIP73} and \emph{OsbZIP76} , which are associated with low
temperature resistance at seedling stage. In addition, Liu et al. (2018,
2019a) also found and revealed the molecular mechanism
of\emph{OsbZIP73/OsTFX1} adapting to the cold climate in northern China
by comparing the whole genome sequences of Japonica and Indica rice.

Except for rice, carrot, soybean, wheat, tomato and other crops have
been successively excavated bZIP transcription factors in response to
low temperature stress. For example, Ito et al. (1999) found that the
expression of bZIP-like protein Lip (Low temperature-Induced protein) in
the roots of radish was up-regulated under low temperature treatment,
thereby enhancing the cold resistance of radish. Soybeans GmbZIP44,
GmbZIP62 and GmbZIP78 can regulate and promote the synthesis of proline
(plant cold tolerance osmotic regulator) to enhance the tolerance of
plants to cold stress. At the same time, GmbZIP44, GmbZIP62, and
GmbZIP78 can enhance their ability to respond to cold damage and high
salt stress by activating the expression of their downstream genes
\emph{ERF5} , \emph{KIN1} ,\emph{CORl5A} , and \emph{COR78} (Liao et
al., 2008). Hwang et al. (2014) treated \emph{Brassica rapa} with low
temperature stress and found that the expression of 27 BrbZIPs were
significantly up-regulated, among which \emph{Bra000256} ,
\emph{Bra003320} , \emph{Bra004689} ,\emph{Bra011648} , \emph{Bra020735}
and \emph{Bra023540} may be the key genes involved in the response to
low temperature stress. Compared with wild-type \emph{Arabidopsis
thaliana} , heterologous expression of\emph{TabZIP6} in wheat under cold
treatment significantly reduced the expression of \emph{CBFs} , key
\emph{CORs} and other genes in transgenic plants, making the transgenic
plants sensitive to low temperature (Cai et al., 2018). However, the
over-expressed wheat \emph{TabZIP14-B} ,\emph{TaAREB3} and
\emph{TabZIP60} in \emph{Arabidopsis thaliana} can significantly enhance
the ability of plants to resist cold stress, and the expression of
corresponding stress-responsive genes in transgenic plants was
significantly up-regulated. In addition, transgenic plants are more
sensitive to ABA than wild type, indicating that T\emph{abZIP14-B} ,
\emph{TaAREB3} , and \emph{TabZIP60} all enhance the cold resistance of
plants through the ABA pathway (Wang et al., 2016a; Zhang et al., 2015b;
Zhang et al., 2017b). Xu et al. (2014) found that over-expression of
wheat bZIP transcription factor TaABL 1 (ABI-like) elevated cold
tolerance in wheat. Apple bZIP transcription factor MdHY5 can respond to
low temperature stress at both the transcriptional and protein levels.
Overexpression of \emph{MdHY5} can significantly enhance cold stress
resistance in apple callus and transgenic \emph{Arabidopsis thaliana} .
EMSA results indicate that MdHY5 can bind to G-Box on the\emph{MdCBF1}
promoter, thereby increasing its transcription level and regulating the
expression of \emph{COR} genes independent of CBF (An et al., 2017b).
Wang et al. (2017b) found that transgenic \emph{Arabidopsis thaliana}
plants showed reduced survival, increased electrical conductivity,
increased malondialdehyde content, and reduced soluble sugar content
when overexpressed \emph{Camellia sinensis} \emph{CsbZIP6}in it.
Transcriptome analysis found that the expression of low-temperature and
drought-responsive genes in over-expressed plants was significantly
lower than that of wild type, indicating that\emph{CsbZIP6} plays a
negative regulatory role in low-temperature stress response.

\textbf{bZIP TFs involved in osmotic stress response}

Salinity and drought usually induce secondary stress, osmotic stress.
Hence, it's not difficult to understand that plant bZIPs also act as
significant roles in response to osmotic stress.

The rice OsbZIP71 transcription factor recognizes and combines with the
promoter of the osmo-regulatory gene \emph{OsNHX1} , transports excess
Na\textsuperscript{+} and K\textsuperscript{+} in the cytoplasm to the
vacuole, reducing salt concentration in the cytoplasm to improve rice
salt tolerance (Liu et al., 2014a). In \emph{Arabidopsis thaliana} , the
AtbZIP63 can regulate protein-protein interactions to regulate the
activity of proline dehydrogenase I, thereby enhancing the ability of
the plant to tolerate hypotonic stress (Veerabagu et al., 2014); the
VIP1 (AtbZIP51) rapidly accumulates in the nucleus in response to
hypotonic stress (Hwang et al., 2014; Tsugama et al., 2016). Actually,
VIP1/AtbZIP51 and bZIP29 can form a heterodimer to enhance their binding
to the hypotonic response element (AGCTGK) in the promoters of osmotic
response genes \emph{CYP707A1} and \emph{CYP707A3} (Van Leene et al.,
2016).

\textbf{bZIP TFs involved in regulating ABA signaling pathway}

As a `emergency hormone' in plants, ABA is an important signaling
molecule in plants. When plants encounter abiotic stress such as salt,
drought, or low temperature, they will activate both ABA-dependent and
ABA-independent signaling pathways (Bray et al., 1997; Shinozaki et al.,
1996; Thomashow et al., 1998; Verslues et al., 2005). Genes involved in
the ABA-dependent pathway not only induce ABA biosynthesis, but also
regulate the expression of genes containing ABRE elements (Shinozaki et
al., 2007; Zhu et al., 2002). The bZIP transcription factor family can
bind to ABRE elements and is called ABA response element binding factors
(AREBs) or ABRE binding factors (ABF) (Choi et al., 2000; Uno et al.,
2000). So far, bZIP transcription factors are proven to participate in
ABA-dependent stress signaling in various plants, including
\emph{Arabidopsis thaliana} , rice, soybean, wheat. (Casaretto et al.,
2003; Fujita et al., 2005; Kobayashi et al., 2008; Lu et al., 2009).

The A subfamily bZIP transcription factor in \emph{Arabidopsis thaliana}
is a major regulator of ABA-dependent responses (Satoh et al., 2004).
AtbZIP1 regulates ABA signal transduction by binding to the ABREs and
alters the expressions of the ABA responsive genes to tolerate the cold
stress (Sun et al., 2011). In rice, OsbZIP23 and OsbZIP46 can directly
target the expression of multiple stress genes through the ABA pathway,
thereby significantly improving drought- and salt-resistance of rice
(Dey et al., 2016; Tang et al., 2012a; Xiang et al., 2008; Zong et al.,
2016). In the transgenic plants over-expressing \emph{OsbZIP42} , it
showed a rapid rise of transcriptional expression of ABA responsive
\emph{LEA3} and\emph{Rab16} and increased tolerance to drought stress
(Joo et al., 2019). In soybeans, GmbZIP44, GmbZIP62, and GmbZIP78 can
positively regulate the expression of \emph{ABI1} and \emph{ABI2} genes
and further induce the expression of downstream genes such as
\emph{ERF5} ,\emph{KIN1} , \emph{COR15A} , and \emph{COR78} in response
to ABA treatment (Liao et al., 2008).

Recent years, bZIPs are also found with increasing contributions in
regulating ABA responses in other plants. Overexpression of the
ABA-depended grapevine \emph{VvABF2} gene could enhance osmotic stress
tolerance in \emph{Arabidopsis thaliana}and thereby reduce the cell
membrane damage (Liu et al., 2019b). Wang et al. (2019) found that sweet
potato \emph{IbABF4} gene, encodes a bZIP transcription factor,
overexpression in \emph{Arabidopsis thaliana} and sweet potato could
enhance their tolerance to multiple abiotic stresses through the ABA
signaling pathway.

In short, bZIP family members play an important role in the abscisic
acid signaling pathway under various stresses. A large number of studies
have shown that bZIP transcription factors affect ABA biosynthesis
through the ABA-mediated signal transduction pathways and thus improve
plant stress resistances.

To reveal the relevance between bZIP subfamilies and stress types, the
functional annotated bZIPs were also classified into 13 verified clades
followed the approach used by Corrêa et al. (2008) (Table II and Figure
I). There is yet not any functional report on bZIPs in subfamilies H, J
and L on abiotic stresses. Among the rest 10 subfamilies, there are 8,
7, 6 and 3 of which involved in salinity, drought, cold and osmotic
stress, respectively. The bZIPs for regulating salinity tolerance are
most frequently found in subgroups A, D, G and S; while for modulating
resistances to both drought and osmotic stress are most members in
subgroup A; and for controlling cold responses are most those from
subgroups A, C and S (Table II).

\textbf{REGULATION OF BZIPS ON METABOLISM OF FLAVONOIDS}

Recently, a plenty of flavonoids show significant contributions to plant
tolerances to abiotic stresses (Agati et al., 2012; Pi et al., 2016,
2018, 2019; Yamasaki et al., 1997; Yan, et al., 2014). Interestingly,
many bZIP transcription factors usually play a key regulatory roles in
the process of flavonoid biosynthesis. They regulate the expression of
key enzyme genes in the synthetic pathway, thereby regulating the
metabolism and synthesis of flavonoids.

Matousek et al. (2010) found that both hop HlbZIP1 and HlbZIP2 could
activate the expression of chalcone synthase \emph{chs\_H1} and the
\emph{O-methyl transferase 1} genes to regulate the accumulation of
flavonoid glycosides and anthocyanins. Akagi et al. (2012) found that
ectopic \emph{DkbZIP5} overexpression in persimmon calluses could
induced the up-regulation of \emph{DkMyb4} and then affect the seasonal
biosynthesis of proanthocyanidins in persimmon fruit. Malacarne et al.
(2016) showed that VvibZIPC22, a member of clade C of the grapevine bZIP
family, was able to activate the transcriptional expression of specific
genes of the flavonoid pathway including\emph{VviCHS3} , \emph{VviCHI} ,
\emph{VviFLS1} and \emph{VviANR} , alone or together with other factors
to participate in the biosynthesis of flavonols during flowering and UV
light-mediated induction. Dash et al. (2017) found that the poplar
PatbZIP1 transcription factor regulated the expression of two flavonol
synthase genes \emph{PtaFLS2} and\emph{PtaFLS4} in the flavonoid
synthesis pathway to promote the synthesis of related flavonoids and
thus promotes the lateral root formation. bZIP transcription factor HY5
plays a multifaceted role in plant growth and development. Apple
\emph{MdHY5} gene, induced by light and abscisic acid treatments,
promoted anthocyanin accumulation by regulating expression of the
\emph{MdMYB10} gene and downstream anthocyanin biosynthesis genes (An et
al., 2017a). Zhang et al. (2011b) found that the protein levels of two
bZIP transcription factors AtbZIP56/HY5 and AtbZIP64/HYH in
\emph{Arabidopsis thaliana} induced the accumulation of anthocyanins
under low temperature induction. In addition, ABA can induce the
expression of \emph{Artemisia annuaAabZIP1} to activate the expression
of downstream gene \emph{ADS}and \emph{CYP71AV1} , thereby regulating
the biosynthesis of artemisinin (Zhang et al., 2015a). Fan et al. (2019)
showed that the expression of\emph{RsbZIP011} and \emph{RsbZIP102} was
significantly up-regulated in radish tissue with higher anthocyanin
content under heat and salt stress.

So far, the bZIPs that involve in flavonoid synthesis varies from plant
species and their target genes (coding for different enzymes in
flavonoid metabolism). To uncover the relationship between bZIP
subfamilies and flavonoid synthesis, all the functional annotated bZIPs
were also categorized into the 13 known subgroups according to Corrêa et
al. (2008) (Table III and Figure I). It seems that only bZIPs in
subfamilies A, H and S could regulate flavonoid metabolism.

\textbf{EFFECTS OF FLAVONOID METABOLISM ON PLANT RESPONSE TO STRESS
TOLERANCE}

Flavonoids are a class of secondary metabolites of polyphenols with
C6-C3-C6 as the basic structure or phenyl-benzopyran structure.
Flavonoids also are a large class of secondary metabolites formed by
plants in the long-term ecological adaptation process to withstand the
stress of harsh ecological conditions, animals, and microorganisms. They
are widely distributed in the plant kingdom and are abundant in flowers,
fruits and leaves of many plants (Du et al., 2010). Based on the
different oxygen rings and conformations of the basic molecular
structure of flavonoids, flavonoids are generally divided into six
categories: flavone, flavonol, isoflavone, flavanone, flavanol and
anthocyanidin (Rice-Evans et al., 2010). The starting substrate for
plant flavonoid biosynthesis is derived from coumaroyl-CoA of the
phenylpropane metabolic pathway and malonyl-CoA from acetyl-coenzymes.
Under the action of chalcone synthase (CHS), they first form chalcone
(Aoki et al., 2000), and then the naringenin is formed by the catalytic
action of chalcone isomerase (CHI) (McKhann and Hirsch, 1994). Under the
catalysis of cytochrome P450 monooxygenase (CPM) and other enzymes,
naringen can be used as a major intermediate metabolite to synthesize
other flavonoids (Akashi et al., 1999; Falcone Ferreyra et al., 2012;
Lam et al., 2014; Liu et al., 2003; Uchida et al., 2015).

More than 10,000 plant flavonoids have been discovered (Aoki et al.,
2000; Jiang et al., 2010). They play very important roles in plant
resistance to various stress tolerances (Agati et al., 2012; Yamasaki et
al., 1997; Yan, et al., 2014). They could remove free radicals under
ultraviolet radiation (Li et al., 1993; Treutter et al., 2005), improve
seed storage capacity and prolong life (Debeaujon et al., 2000), change
petal color (Mola et al., 1998), interfere with the polar distribution
of auxin (Buer et al., 2004), affect the accumulation and composition of
fatty acids (Lian et al., 2017), etc.

Early studies on the mechanism of flavonoids involved in stress
resistance mainly focused on their regulations on response to
ultraviolet radiation (Mellway et al., 2009; Tattini et al., 2006).
Later, flavonoids were found with strong antioxidant activity (Agati et
al., 2007; Hernández et al., 2009; Pourcel et al., 2007; Treutter et
al., 2006). Since various stresses can cause excessive peroxide to
accumulate in plants, the significant role of flavonoids in plants'
stress resistance attracts increasing interests (Fasano et al., 2014;
Qiu et al., 2008; Rai et al, 2016; Watkins et al., 2014). Tattini et al.
(2004) reported that European privet flavonoids as antioxidants respond
to strong light and drought stress. Li et al. (2011) found a conserved
trans-acting element (G-box, CACGTG) in the promoter region of the
chalcone synthase family gene (\emph{AtCHS} ) in \emph{Arabidopsis
thaliana} , which regulates the accumulation of
H\textsubscript{2}O\textsubscript{2} by responding to cGMP signals (Abu
Zahra et al., 2014). Yan et al. (2014) found that the cytochrome P450
monooxygenase GmFNSII/GmCPM in soybean was beneficial to the
accumulation of flavonoid aglycones in plants and the reduction of
H\textsubscript{2}O\textsubscript{2} content. In previous studies, we
found that the content of flavonoids such as quercimeritrin in
salt-tolerant soybeans is relatively higher than that of salt-sensitive
soybeans, which is beneficial for soybeans to adapt to salt stress (Lu
et al., 2013). With the deepening of research, we further discovered
that enzymes related to the flavonoid metabolism pathway are important
salt stress response factors, and they can significantly regulate the
salt tolerance of plants such as \emph{Arabidopsis thaliana} and soybean
(Pi et al., 2016). We recently found that the salt-triggered
phosphorylation of GmMYB173, subsequent elevates the transcription
of\emph{GmCHS5} for enhancing the accumulation of dihydroxy B-ring
flavonoids (such as cyaniding-3-arabinoside chloride) (Pi et al., 2018);
while salt-inhibited phosphorylation of GmMYB183 subsequently decreases
the transcription of \emph{GmCYP81E11} for reducing monohydroxy B-ring
flavonoids (such as ononin) (Pi et al., 2019). Actually, both GmMYB173
phosphorylation and GmMYB183 dephosphorylation contribute to soybean
salt tolerance.

The abovementioned studies showed that flavonoids played a very
important role in the response of plants to stress. However, there is no
direct evidence been found to show us whether bZIP could regulate
flavonoid accumulation for plant adaption to these stresses.

\textbf{CONCLUDING REMARKS} Due to their significant roles in plant
tolerances to various stress, the bZIP transcription factors have been
comprehensively studied, including their categorization and regulatory
mechanisms of target genes. However, there is at least one interesting
issue worthy of further investigation: Whether bZIP transcription factor
regulates plant stress tolerance by modulating the synthesis of
flavonoids.

To date, plenty of literatures show that bZIPs regulate plant tolerances
to various abiotic stresses, such as low temperature, drought, and high
salt. Besides, there are many reports reveal that flavonoids participate
in various stress responses. Moreover, a lot of researches have now
confirmed that bZIP transcription factors play an important role in the
synthesis of flavonoids. Specially, bZIPs in subfamily H could bind to
G-box in promoter of cold responsive genes (Table I and II); members of
this subfamily also could modulate the synthesis of some flavonoids
(Table III). Since members in this group shares similar conversed
protein motifs (supplemental Figure S1 and S2), it is reasonable to
hypothesize that plant bZIPs in subfamily H could bind to G-box of
cold-responsive genes to further regulate the synthesis of flavonoids.
Similarly, it also makes sense that bZIPs in subfamily A could regulate
the synthesis of flavonoids by binding to G-box or ABRE of genes
involved in cold, salinity, drought and osmotic stresses; subfamily S
could regulate the synthesis of flavonoids by bind to G-box or C-box or
A-box or ABRE of genes involved in cold, salinity and drought stresses
(Table I, II and III). However, these hypotheses are still needed to be
further verified.

\textbf{ACKNOWLEDGEMENTS}

This work was supported by the grants 31970286 and 31301053 from the
National Science Foundation of China, LY17C020004 from the Natural
Science Foundation of Zhejiang Province.

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\verb`Table II-7.xls`  available at \url{https://authorea.com/users/307265/articles/438219-regulation-mechanisms-of-bzip-transcription-factors-in-plant-grown-on-drought-salt-and-cold-soils}

\textbf{Hosted file}

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