Plant Physiology and Biochemistry 210 (2024) 108630 Available online 16 April 2024 0981-9428/© 2024 Elsevier Masson SAS. All rights reserved. WRKY transcription factors modulate flowering time and response to environmental changes Hui Song a,b,*, Zhenquan Duan a,b, Jiancheng Zhang c a Key Laboratory of National Forestry and Grassland Administration on Grassland Resources and Ecology in the Yellow River Delta, College of Grassland Science, Qingdao Agricultural University, Qingdao 266109, China b Qingdao Key Laboratory of Specialty Plant Germplasm Innovation and Utilization in Saline Soils of Coastal Beach, College of Grassland Science, Qingdao Agricultural University, Qingdao 266109, China c Key Laboratory of Biology and Genetic Improvement of Peanut, Ministry of Agriculture and Rural Affairs, PR China, Shandong Peanut Research Institute, Qingdao 266000, China A R T I C L E I N F O Keywords: Environmental change Flowering time Phytohormone WRKY A B S T R A C T WRKY transcription factors (TFs), originating in green algae, regulate flowering time and responses to envi ronmental changes in plants. However, the molecular mechanisms underlying the role of WRKY TFs in the correlation between flowering time and environmental changes remain unclear. Therefore, this review sum marizes the association of WRKY TFs with flowering pathways to accelerate or delay flowering. WRKY TFs are implicated in phytohormone pathways, such as ethylene, auxin, and abscisic acid pathways, to modulate flowering time. WRKY TFs can modulate salt tolerance by regulating flowering time. WRKY TFs exhibit func tional divergence in modulating environmental changes and flowering time. In summary, WRKY TFs are involved in complex pathways and modulate response to environmental changes, thus regulating flowering time. 1. Introduction Flowering, a crucial process in plant growth and development, marks the transition from vegetative to reproductive development. Internal and external factors affect plant flowering (Fig. 1). There are five well- known pathways involved in flowering: photoperiod, autonomous, vernalization, gibberellin, and aging pathways (Amasino, 2010; Mi chaels, 2009; Strikanth and Schmid, 2011). The photoperiod and vernalization pathways are regulated by environmental factors, whereas autonomous, gibberellin, and aging pathways are inherent to the plant (Amasino, 2010). Previous findings show that these pathways undergo gene expression changes that modulate the flowering time (Fig. 1). In the photoperiod pathway, the leaf tissue receives light to regulate GIGANTEA (GI), increasing the expression of CONSTANS (CO), ulti mately leading to the activation of FLOWERING LOCUS T (FT)/TWIN SISTER OF FT (TSF) (Amasino, 2010; Strikanth and Schmid, 2011). Subsequently, the phloem tissue transfers FT/TSF proteins from the leaf into the apex. At the apex, an interaction between FT and FLOWERING LOCUS D (FD) forms a complex protein that promotes the expression of SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1) and APETALA 1 (AP1) (Freytes et al., 2021). Further, SCO1 induces the expression of FRUITFULL (FUL) and LEAFY (LFY), resulting in early flowering (Amasino, 2010; Strikanth and Schmid, 2011). FLOWERING LOCUS C (FLC), a key gene in the vernalization and autonomous path ways, positively regulates flowering time by downregulating the expression of TF/TSF and SOC1 (Amasino, 2010; Michaels, 2009; Stri kanth and Schmid, 2011). Repressing the expression of FLC in the autonomous and vernalization pathways leads to early flowering (Amasino, 2010; Strikanth and Schmid, 2011). Similarly, in the gibberellin pathway, gibberellic acid (GA) represses DELLA to upregu late the expression of SOC1 and LFY, resulting in early flowering (Amasino, 2010; Strikanth and Schmid, 2011). In the aging pathway, miR156 binds and downregulates the expression of SQUAMOSAMSA PROMOTER BINDING PROTEIN-LIKE (SPL), modulating the expression of downstream genes to promote flowering (Amasino, 2010). The WRKY transcription factor (TF), originating in green algae, plays a significant role in plant growth and development and response to abiotic and biotic stress by binding to cis-acting elements in the pro moter regions of downstream genes and forming protein complexes with other proteins in plants (Chen et al., 2017; Javed and Gao, 2023; Song * Corresponding author. Key Laboratory of National Forestry and Grassland Administration on Grassland Resources and Ecology in the Yellow River Delta, College of Grassland Science, Qingdao Agricultural University, Qingdao 266109, China. E-mail address: biosonghui@outlook.com (H. Song). Contents lists available at ScienceDirect Plant Physiology and Biochemistry journal homepage: www.elsevier.com/locate/plaphy https://doi.org/10.1016/j.plaphy.2024.108630 Received 24 February 2024; Received in revised form 30 March 2024; Accepted 13 April 2024 mailto:biosonghui@outlook.com www.sciencedirect.com/science/journal/09819428 https://www.elsevier.com/locate/plaphy https://doi.org/10.1016/j.plaphy.2024.108630 https://doi.org/10.1016/j.plaphy.2024.108630 https://doi.org/10.1016/j.plaphy.2024.108630 http://crossmark.crossref.org/dialog/?doi=10.1016/j.plaphy.2024.108630&domain=pdf Plant Physiology and Biochemistry 210 (2024) 108630 2 et al., 2023; Wang et al., 2023). The WRKY TFs derive their name from a conserved domain, WRKYGQK, found in their peptide sequences (Eulgem et al., 2000; Rinerson et al., 2015). WRKY TFs are broadly classified into three groups (I-III) based on the number of the WRKY domains and zinc finger structures they possess (Eulgem et al., 2000; Rushton et al., 2010). Group I is characterized by two WRKY domains and two C-X4-5-C-X22-23-H-X-H (C2H2) zinc finger structures, group II comprises one WRKY domain and C2H2 motif, and group III has one WRKY domain and a C-X7-C-X23-H-X-C (C2HxC) motif (Eulgem et al., 2000; Rushton et al., 2010). Group II is further classified into five sub groups (IIa-IIe) based on their evolutionary relationships (Zhang and Wang, 2005). Previous studies demonstrate that WRKY TFs play a role in responding to environmental cues and modulating flowering time in plants. However, the molecular mechanisms underlying the association between environmental changes and flowering time regulation by WRKY TFs have not been comprehensively reviewed. Therefore, the aim of this review was to summarize the correlation between environmental changes and flowering time, and the mechanisms underlying the role of WRKY TFs in mediating this relationship. 2. Effect of environmental changes on flowering time Environmental factors significantly affect plant growth and devel opment (Fig. 1). These factors include salt, drought, extreme tempera ture, nutrients, biotic stress, and phytohormones. Salt stress delays flowering time by altering the expression of genes implicated in photoperiod and gibberellin pathways (Achard et al., 2006; Li et al., 2007). For instance, salt stress downregulates the expression of CO and LFY leading to prolonged flowering time (Li et al., 2007). Drought stress modulates the photoperiod pathway to exert con trasting effects on flowering depending on day length (Yoshida et al., 2021). Under long-day conditions, drought stress upregulates GI expression to activate CO and FT, resulting in early flowering (Yoshida et al., 2021). Additionally, drought stress induces the accumulation of abscisic acid (ABA) content, which further upregulates the expression of GI and downstream genes, leading to early flowering under long-day conditions. Conversely, ABA accumulation downregulates FT expres sion to delay flowering under short-day conditions (Yoshida et al., 2021). Drought stress promotes ABA accumulation, which modulates flowering pathways and regulates the flowering time (Yoshida et al., 2021). Low temperature delays flowering, whereas high temperature pro motes flowering (Li et al., 2014b; Stratonovitch and Semenov 2015). Under low-temperature conditions, the SHORT VEGETATIVE GROWTH-FLOWERING LOCUS M-β (SVP-FLM-β) protein complex in teracts with FT and represses its expression, whereas SVP-FLM-ρ upre gulates FT expression under high temperatures (Lee et al., 2013; Lutz et al., 2015; Posé et al., 2013). MicroRNAs play a crucial role in temperature-mediated flowering. For instance, miR156 downregulates SPL3 expression, leading to prolonged flowering time under low tem peratures. Conversely, high temperatures upregulate miR172 expression to promote flowering (Aukerman and Sakai, 2003; Cho et al., 2012; Kim et al., 2012). Low temperatures also downregulate FLC expression to activate genes associated with the flowering pathway, resulting in early flowering (Levy et al., 2002). Nutrient availability also influences flowering time. For instance, low nitrate levels promote flowering by upregulating CO expression in Arabidopsis thaliana (He et al., 2004). Exogenous nitric oxide (NO) de lays flowering time by downregulating GI expression and upregulating FLC expression in A. thaliana (Cho et al., 2017). Additionally, high sugar content delays flowering by inhibiting LFY expression, whereas low sugar (or lipid) content promotes flowering by increasing FT expression (Ohto et al., 2001). Trehalose-6-phosphate (TSP), a glycosynthesis activator (van Dijken et al., 2004), modulates flowering through the photoperiod and aging pathways (Wahl et al., 2013). In the photoperiod pathway, TSP upregulates FT expression to promote flowering, whereas in the aging pathway, it regulates the expression of SPLs to regulate flowering (Wahl et al., 2013). Biotic stress triggers the immune system, consequently impacting plant developmental processes such as flowering. For example, infection by Pseudomonas syringae and Xanthomonas campestris promotes early Fig. 1. Flowering pathways. H. Song et al. Plant Physiology and Biochemistry 210 (2024) 108630 3 flowering in A. thaliana (Korves and Bergelson, 2003). P. syringae infection downregulates FLC expression to accelerate flowering (He et al., 2003; Singh et al., 2013). Several phytohormone pathways that regulate flowering and re sponses to abiotic stresses are associated with changes in jasmonic acid (JA) and salicylic acid (SA) contents. JA activates CORONATINE INSENSITIVE 1 (COI1), whereas SA inhibits FLC expression, altering the flowering time (Cho et al., 2017; Ionescu et al., 2017; Kazan and Lyons, 2016). Similarly, brassinolide (BR) downregulates FLC expression to promote flowering (Cho et al., 2017; Ionescu et al., 2017; Kazan and Lyons, 2016). Exogenous GA inhibits DELLA gene expression to promote flowering (Cho et al., 2017; Ionescu et al., 2017; Kazan and Lyons, 2016). On the contrary, exogenous ethylene (ET) induces the expression of the DELLA gene, causing delayed flowering (Cho et al., 2017; Ionescu et al., 2017; Kazan and Lyons, 2016). Cytokinin (CK) hormone modu lates flowering by regulating the expression of FT and SOC1 (Cho et al., 2017; Ionescu et al., 2017; Kazan and Lyons, 2016). Auxin (IAA) acti vates AUXIN RESPONSE FACTOR 2 (ARF2) to downregulate the expression of GATA, NITRATE-INDUCIBLE, CARBON-METABOLISM INVOLVED/CYTOKININ-RESPONSIVE GATA FACTOR 1 (GNC/GNL), leading to early flowering (Cho et al., 2017; Ionescu et al., 2017; Kazan and Lyons, 2016). 3. WRKY TFs regulate flowering time through multiple pathways 3.1. WRKY TFs regulate flowering time through flowering pathways Studies have identified WRKY TFs that regulate flowering time. Approximately 27 WRKY TFs identified in 16 species are implicated in modulating flowering pathways to regulate flowering time (Figs. 2 and 3). CsWRKY7 downregulates the expression of FT, AP1, and LFY involved in the photoperiod pathway to extend flowering time in Camellia sinensis (Chen et al., 2019). MlWRKY12 upregulates the expression of CO, FT, LFY, AP1, CAULIFLOWER (CAL), and FUL genes to promote flowering in Miscanthus lutarioriparius (Yu et al., 2013). In Fragaria vesca, FvWRKY71 increases the expression of LFY, AGAMOUS LIKR 42 (AGL42), FUL, FLOWERING PROMOTING FACTOR 1 (FPF1), and SEPALLATA 1 (SEP1), accelerating the flowering time (Lei et al., 2020). Furthermore, in Oryza sativa, OsWRKY11 upregulates the expression of EARLY HEADING DATE (Ehd2), RICE INDETERMINATE 1 (RID1), and INDETERMINATE 1 (ID1) to negatively regulate flowering time under long- and short-day conditions (Cai et al., 2014). In Brassica juncea, BjuWRKY75 promotes flowering by activating FT expression (Feng et al., 2022). In the vernalization pathway, AtWRKY34 induces degradation of FRIGIDA (FRI) by activating CULLIN3A (CUL3A), leading to down regulation of FLC expression and consequently promotes early flowering (Hu et al., 2014). In addition, AtWRKY63 promotes the downregulation of FLC expression by activating CoolAIR and ColdAIR under vernaliza tion conditions, resulting in early flowering (Hung et al., 2022). On the contrary, AtWRKY64 upregulates FLC expression under non-vernalization conditions, delaying the flowering time (Hung et al., 2022). In the gibberellin pathway, AtWRKY75 binds to the W-box of FT to promote its expression, resulting in early flowering (Zhang et al., 2018). However, this effect can be impaired when RGA-LIKE 1 (RGL1, a member of the DELLA family) inhibits AtWRKY75 through their inter action (Zhang et al., 2018). Conversely, GIBBERELLIN INSENSITIVE (GAI, a member of DELLA family) also interacts with AtWRKY75, forming a protein complex that activates AtWRKY75 expression (Zhang et al., 2018). Similarly, in Malus domestica, MdWRKY24 interacts with RGL to delay flowering by modulating the GA pathway (Zhang et al., 2022). In Gossypium hirsutum, GhWRKY1 upregulates the expression of JAZ1, a gene involved in the GA pathway, to promote early flowering (Li et al., 2014a). AtWRKY12 and AtWRKY13 are involved in gibberellin and aging pathways and interact with DELLA to form complex proteins (Li et al., 2016). Under short-day conditions, GA responses are repressed by DELLA proteins to activate AtWRKY12, leading to upregulation of FUL expression and early flowering (Li et al., 2016). Conversely, DELLA in hibits AtWRKY13 to downregulate FUL expression, delaying flowering (Li et al., 2016). Furthermore, the SPLs gene family is involved in the aging pathway. For instance, SPL10 interacts with AtWRKY12 and AtWRKY13 to form a complex protein (Ma et al., 2020), thus activating AtWRKY12 and repressing AtWRKY13 (Ma et al., 2020). The interaction between AtWRKY12 and SPL10 protein promotes miR172b expression, whereas the interaction between AtWRKY13 and SPL10 protein down regulates miR172b expression to regulate flowering time in plants (Ma et al., 2020). ArWRKY5 and ArWRKY20 from Anoectochilus roxburghii are orthologs with AtWRKY12 and AtWRKY13, respectively (Xing et al., 2023). ArWRKY5 negatively regulates flowering time, whereas ArWRKY20 promotes early flowering (Xing et al., 2023). However, the molecular mechanism underlying the regulation of flowering time by ArWRKY5 and ArWRKY20 remains unclear. CaWRKY50 protein identified in Cicer arietinum and CpWRKY71 protein in Chimonanthus praecox are potentially involved in the aging pathway. These two WRKY TFs promote flowering and senescence (Huang et al., 2019; Kumar et al., 2016), indicating their involvement in regulating the expression of aging-related genes to modulate flowering time. GsWRKY20 and CpWRKY75 are involved in multiple pathways to regulate flowering time in Glycine soja and C. praecox, respectively (Huang et al., 2021; Luo et al., 2013). These two WRKY TFs indirectly regulate expression of genes associated with flowering and floral meri stem identity, thereby modulating flowering time (Fig. 3). These findings indicate that (1) WRKY TFs can accelerate or delay the flowering, and (2) the molecular mechanisms underlying regulation of flowering by WRKY TFs are complex. Consequently, WRKY TFs are potentially implicated in multiple pathways that regulate flowering time. Based on these observations, we hypothesize that WRKY TFs regulate the expression of genes containing WRKY TF binding sites involved in flowering pathways. However, establishing the relationships between WRKY TFs and their target genes is challenging due to their abundance in the genome. Fig. 2. WRKY transcription factors involved in the regulation of flowering time in plants. H. Song et al. Plant Physiology and Biochemistry 210 (2024) 108630 4 3.2. WRKY TFs regulate flowering time and modulate salt stress Environmental changes affect flowering time, whereas WRKY TFs only regulate the association between flowering time and salt stress. For instance, RtWRKY23 improves salt tolerance in Reaumuria trigyna and delays flowering time under salt stress conditions (Du et al., 2019). Plants overexpressing RtWRKY23 exhibit smaller pods but generate similar seed yields compared with the control groups under salt stress (Du et al., 2019). However, the precise regulatory mechanism under lying the role of RtWRKY23 in modulating salt stress, flowering time, and seed development remains unclear. Moreover, AtWRKY71 acceler ates flowering as a strategy to mitigate damage following salt stress but does not promote salt tolerance (Yu et al., 2018). Research should be conducted to elucidate the role of WRKY TFs in regulating flowering time and other stresses in addition to salt stress. 3.3. WRKY TFs regulate phytohormone pathways to modulate flowering time WRKY TFs are involved in senescence to modulate flowering time through phytohormone pathways (Fig. 3). For instance, AtWRKY71 negatively regulates flowering time by promoting leaf senescence through the ET pathway (Yu et al., 2016, 2021). Moreover, WRKY TFs are involved in the IAA and ABA pathways to modulate flowering time. For instance, OsWRKY72 activates AUXIN-INFLUX 1 (AUX1), AUXIN RESISTANT 1 (AXR1), and BUD1 genes involved in the IAA pathway, and ABSCISIC ACID 2 (ABA2) and ABSCISIC ACID-INSENSITIVE 4 (ABI4) implicated in the ABA pathway to promote early flowering (Song et al., 2010). Studies conducted using model plants such as A. thaliana and O. sativa have revealed the regulatory role of WRKY TFs in regulating phytohormones, thus modulating flowering time. These regulatory roles of WRKY TFs should be explored in non-model crops to ensure their application in crop improvement efforts. Additionally, phytohormones, such as CK, SA, and BR, play key roles in regulating flowering time (Fig. 1). However, their interactions with WRKY TFs leading to modu lation of flowering time are unclear. 3.4. WRKY TFs involved in the regulation of flowering time exhibit functional divergence Some WRKY TFs, such as RtWRKY23 and AtWRKY71, regulate flowering time and modulate other physiological process. However, the specific correlations between flowering time and other physiological process are unclear. Therefore, we hypothesized that these WRKY TFs exhibit functional divergence. For instance, AtWRKY34 negatively modulates flowering time and positively regulates cold tolerance and pollen development (Lei et al., 2017; Zheng et al., 2018; Zou et al., 2010). Conversely, AtWRKY63 positively regulates flowering time, drought tolerance, and high-intensity light tolerance (Ren et al., 2010; Van Aken et al., 2013). Similarly, AtWRKY75, BnWRKY184, GhWRKY1, GmWRKY58, GmWRKY76, GsWRKY20, MdWRKY24, MlWRKY12, OsWRKY11, and OsWRKY72 regulate flowering time and other physi ological changes (Fig. 4). Several studies report that WRKY TFs balance flowering time and responses to environmental changes. For instance, AtWRKY12, which promotes flowering and AtWRKY13, which delays flowering, exhibit opposite functions in regulating flowering time (Li et al., 2016). AtWRKY12 negatively regulates cadmium tolerance by downregulating Fig. 3. The molecular mechanisms underlying the role of WRKY transcription factors in regulating flowering time. H. Song et al. Plant Physiology and Biochemistry 210 (2024) 108630 5 GLUTATHIONE 1 (GSH1) expression (Han et al., 2019). On the contrary, AtWRKY13 positively regulates cadmium tolerance by activating PLEIOTROPIC DRUG RESISTANCE 8 (PDR8) and D-CYSTEINE DESULFHYDRASE (DCD) proteins (Sheng et al., 2019; Zhang et al., 2020). Therefore, AtWRKY12 and AtWRKY13 may potentially interact to regulate both flowering time and cadmium tolerance. Furthermore, paralogous WRKY TFs exhibit distinct roles in regu lating flowering time and other physiological processes. For instance, AtWRKY8, AtWRKY28, and AtWRKY71 are paralogs that accelerate flowering time (Yu et al., 2016, 2018). Although AtWRKY8 and AtWRKY28 promote salt tolerance, AtWRKY71 does not affect salt tolerance (Babitha et al., 2013; Hu et al., 2013; Yu et al., 2018). AtWRKY71 is mainly implicated in plant growth and development (Guo et al., 2015; Yu et al., 2021), whereas AtWRKY8 and AtWRKY28 pri marily regulate resistance to biotic and abiotic stress (Babitha et al., 2013; Chen et al., 2010, 2013a, 2013b, 2018; Hu et al., 2013). In summary, these findings indicate that AtWRKY8, AtWRKY28, and AtWRKY71 have redundant functions in regulating flowering time. However, they develop various complex regulatory networks involving multiple biological pathways. AtWRKY71 upregulates expression of FT and LFY to modulate flowering time (Yu et al., 2016, 2018). AtWRKY8 and AtWRKY28 potentially utilize different molecular mechanisms for modulating flowering time compared to AtWRKY71. 4. Conclusions and future research avenues WRKY TFs regulate flowering time and responses to environmental changes. However, the correlation between the regulation of flowering time by WRKY TFs and their modulation of environmental changes re mains unclear. This review provides a summary of the role of WRKY TFs in regulating flowering time, emphasizing the involvement of WRKY TFs in flowering pathways. Experimental studies show that WRKY TFs regulate flowering time to modulate salt tolerance. WRKY TFs are also involved in GA, ET, IAA, and ABA pathways, ultimately modulating flowering time. However, most studies have predominantly focused on model plants, thus the role of WRKY TFs in non-model crop plants has not been explored. Additionally, phytohormones such as CK, SA, JA, and BR affect flowering time, but studies on the direct involvement of WRKY TFs modulate these phytohormonal pathways to regulate flowering time remain unclear. Early and late flowering times have distinct implications for plants. For example, delayed flowering can extend vegetative growth, enabling plants to accumulate high aboveground biomass. Conversely, the yield and quality of crops potentially decrease in early-flowering plants under normal growth conditions due to the short vegetative growth, leading to low biomass accumulation (Mathan et al., 2016; Shavrukov et al., 2017). Nevertheless, early-flowering plants have higher yields than plants with normal flowering times under drought stress (Mathan et al., 2016; Shavrukov et al., 2017). Therefore, breeders should carefully balance the relationship between flowering time and crop yield, a dynamic process regulated by WRKY TFs. CRediT authorship contribution statement Hui Song: Conceptualization, Formal analysis, Writing – original draft, Writing – review & editing. Zhenquan Duan: Data curation. Jiancheng Zhang: Supervision. Declaration of competing interest The authors declare no conflict of interest, including no competing financial interests or personal relationships that could have influenced the reported work in this paper. Fig. 4. 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