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Chen, M.; Zhang, T.; Hu, C.; Zhang, J. Drought and Temperature Stress Induced Flowering. Encyclopedia. Available online: https://encyclopedia.pub/entry/53108 (accessed on 01 June 2024).
Chen M, Zhang T, Hu C, Zhang J. Drought and Temperature Stress Induced Flowering. Encyclopedia. Available at: https://encyclopedia.pub/entry/53108. Accessed June 01, 2024.
Chen, Min, Tian-Liang Zhang, Chun-Gen Hu, Jin-Zhi Zhang. "Drought and Temperature Stress Induced Flowering" Encyclopedia, https://encyclopedia.pub/entry/53108 (accessed June 01, 2024).
Chen, M., Zhang, T., Hu, C., & Zhang, J. (2023, December 25). Drought and Temperature Stress Induced Flowering. In Encyclopedia. https://encyclopedia.pub/entry/53108
Chen, Min, et al. "Drought and Temperature Stress Induced Flowering." Encyclopedia. Web. 25 December, 2023.
Drought and Temperature Stress Induced Flowering
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This entry is adapted from the peer-reviewed paper 10.3390/agronomy13123034

Plants experience a variety of adverse environments during their vegetative growth and reproductive development, and to ensure that they complete their life cycle successfully, they have evolved specific defense mechanisms to cope with unfavorable environments. Flowering is a vital developmental stage and an important determinant of productivity in the lifetime of plants, which can be vulnerable to multiple abiotic stresses. Exposure to stress during this period can have dramatic effects on flower physiological and morphological development, which may ultimately lead to a substantial loss of yield in seed-producing plants. However, there has been increasing research evidence that diverse abiotic stresses, ranging from drought, low temperature, and heat stress can promote or delay plant flowering.

abiotic stress drought plants flowering time molecular regulatory mechanisms

1. Introduction

Plants are sessile and cannot move to escape from adverse environmental conditions. Hence, the developmental process of many plants is highly changeable in response to the environmental stresses they encounter. Abiotic stresses, including drought, salinity, devastating temperature (extreme high or low), and nutrient (mainly nitrogen, phosphorus, and potassium) starvation [1], can have a dramatic impact on plant growth and productivity, such as cellular water scarcity, cell membrane damage, enzyme inactivation, and other defects, ultimately leading to severe yield reductions and huge economic losses [2][3][4][5]. Therefore, abiotic stress has been an important issue in plant vegetative [6][7] and reproductive [8][9] development, for which the study of abiotic stress effects during reproductive development is of great significance for the maintenance of food production as well as for the world economy.
Flowering is an important agricultural trait in the successful transition of plants from vegetative to reproductive growth, as the optimal flowering time is critical for maximizing reproductive success and ensuring seed production, which is a key step in the evolutionary success of plants. Due to the continuously fluctuated environmental conditions, plants have evolved specific defense mechanisms to ensure maximum reproductive success [10]. For example, when individuals cannot survive under severe stress conditions, they produce seeds by adjusting the timing of flowering. In recent years, the effects of abiotic stresses on flowering induction have been documented in numerous plant species [11][12][13][14][15][16][17][18][19]. The ability of abiotic stresses to regulate flowering, with drought and temperature being important stress factors, suggests that plants can combine abiotic stresses effects with flowering signaling pathways. Thus, stress-induced flowering has been recognized as a new means of flowering response due to its important biological benefits throughout the plant life cycle [20].
Global warming and the continued increase in the world’s population have led to a shortage of freshwater resources and a further decline in groundwater levels, posing a major challenge to agriculture worldwide [21]. Drought, which is defined as being in a state of water shortage for several consecutive weeks [22], is the most common abiotic stress around the world and severely affects flowering time, flower morphological developmental processes, and the seed productivity of several plant species. It is particularly noteworthy that drought stress can also cause flower abortion and eventually plant sterility by altering the expression levels of various genes critical to flowering regulation pathways, which regulate both flowering time and response to drought stress [23]. In the following, how plants perceive and respond to drought stress is discussed, the differential physiological phenotypes of various plant species under drought stress conditions are further summarized, and, finally, the potential molecular mechanisms underlying drought-stress-induced flowering are focused on.

2. Perception and Coping Strategies of Drought Stress

Plants perceive drought stress signals mainly through the leaves and the root system. Stomatal movement can be observed in leaves, and drought stress can lead to the accumulation of reactive oxygen species (ROS) (7, Table 1) and of abscisic acid (ABA) (8, Table 1) in leaves, which, in turn, regulates the movement of guard cells and ultimately determines the opening and closing state of stomata [24]. However, it is difficult to determine how plants respond to drought stress in the root system [25][26]. A deficiency of water can constrain the growth and development process of plants, and can even have a significant impact on plant survival [1][27]. As a result, plants have evolved a variety of strategies to cope with damage caused by drought stress. The process by which plants sense water deficit signals and further initiate coping strategies in response to drought stress is known as drought resistance. The adaptability of plants to drought stress mainly consists of three different coping strategies, namely, drought escape, drought avoidance, and drought tolerance [28]. Drought escape, a common strategy exploited in response to drought stress, refers to plants that accelerate flowering and shorten their entire life cycle before severe drought stress hinders their survival [29][30]. However, in order to achieve early flowering, a drought escape strategy will terminate vegetative growth in advance, which can severely influence the growth and development of vegetative organs, and eventually lead to a dramatic decrease in seed yield. Drought avoidance (also known as drought dehydration) is another strategy for plants to cope with external drought conditions by increasing the internal water content (by reducing water loss or maximizing water uptake) [31]. The drought tolerance strategy is the ability of plants to tolerate low internal water content and to adapt to the drought stress while initiating reproduction [32].
Table 1. Specialized terms and their abbreviations appearing in this research.
Number Abbreviations Full-Name Number Abbreviations Full-Name
1 CO CONSTANS 24 HDA6 HISTONE DEACETYLASE 6
2 FT FLOWERING LOCUS T 25 FES1 FRI ESSENTIAL 1
3 LFY LEAFY 26 FRL1 FRI-LIKE 1
4 AP1 APETALA1 27 FLX FLC EXPRESSOR
5 GI GIGANTEA 28 SUF4 SUPPRESSOR OF FRI 4
6 SOC1 SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 29 VRN1 VERNALIZATION1
7 ROS reactive oxygen species 30 FUL FRUITFULL
8 ABA abscisic acid 31 VAL CAULIFLOWER
9 SD short-day conditions 32 PIF4 PHYTOCHROME-INTERACTING TRANSCRIPTION 4
10 LD long-day conditions 33 MAF2 MADSAFFECTING FLOWERING 2
11 TSF TWIN SISTER OF FT 34 FCA FLOWERING CONTROL LOCUS A
12 SVP SHORT VEGETATIVE PHASE 35 FVE FLOWERING LOCUS VE
13 FLC FLOWERING LOCUS C 36 FLM FLOWERING LOCUS M
14 Hd3a HEADING DATE 3a 37 HOS1 HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENE 1
15 RFT1 RICE FLOWERING LOCUS T1 38 HSR heat stress response
16 Ehd1 EARLY HEADING DATE 1 39 HSPs heat shock proteins
17 RCN1 RICE CENTRORADIALIS 1 40 HSFs heat stress transcription factors
18 FD FLOWERING LOCUS D 41 BOB1 BOBBER1
19 FAC florigen activation complex 42 FTL3 FLOWERING LOCUS T-like 3
20 FRI FLOWERING CONTROL LOCUS A 43 PRR PSEUDO RESPONSE REGULATOR
21 OST1 OPEN STOMATA 1 44 LUX LUX ARRHYTHMO
22 VOZ1 VASCULAR PLANT ONE-ZINC FINGER 1 45 Eps-D1 Earliness per se locus
23 RFS Regulator of Flowering and Stress 46 EG1 EXTRA GLUME 1
Under drought stress conditions, plants can respond by early or late flowering, depending on the onset, duration, and severity of drought [20][33]. A bibliometrics analysis showed that plant response to drought has become an important research topic [34]. When plants are adequately supplied with water, the stomata remain open to a large extent to enable the plants to fully photosynthesize, while under mild drought stress, plants will appropriately regulate stomatal closure to minimize water loss by reducing transpiration, but this will result in a decrease in the rate of photosynthesis. When subjected to severe drought stress, the stomata are generally in a minimally open state to ensure that some photosynthesis can take place, thus guaranteeing the normal survival needs of plants [35]. This is one of the main approaches for plants to avoid damage caused by drought stress in the short term [36]. Influenced by geography, many terrestrial plants are frequently affected by drought stress and have developed various drought-tolerant mechanisms to adapt to or to resist the drought environment through a long-term evolutionary process [37][38]. The adaptation of plants to the drought environment is mainly reflected both morphologically and biochemically [39][40][41]. Morphologically, adaptation is manifest in the presence of a very thick cuticle on the leaf surface, with the fenestrated cells being tightly arranged, while some leaves have a tomentum on the surface, which can effectively control water loss, and can also absorb dew at night to replenish the plant’s own water [42]. Generally, there is a very well-developed root structure with greater water and nutrient absorption capacity and a poorly developed aboveground branching structure with weaker transpiration and better water retention capacity [43]. The more drought-resistant the plant, the greater the root–crown ratio. These morphological adaptations are closely related to the cell division, elongation, and differentiation of the root apex. Plant vascular tissue systems, such as the xylem and phloem, are involved in the transport of substances, while their developmental status also affects plant drought resistance [44]. In Arabidopsis, drought-escape-induced early flowering is associated with the phloem tissue transport of the florigen FT protein from the leaves to the shoot apical meristems [45]. Biochemically, it is manifested in the high expression of some drought resistance genes that positively increase the content of amino acids and sugars in plants (such as proline and trehalose), the enhanced activity of antioxidant-related enzymes, and inhibition of the activity of enzymes involved in degradation pathways to ensure that normal metabolic homeostasis is maintained under drought stress condition [46]. ROS, including superoxide radicals (O2−), hydrogen peroxide (H2O2), and hydroxyl radicals (OH−), regulate plant growth and development at lower concentrations [47][48]. Excessive accumulation of ROS under drought stress leads to membrane lipid peroxidation [49][50]. Previous studies have shown that excessive ROS in plants will be scavenged by antioxidant mechanisms, including the enzymatic antioxidants, SOD (superoxide dismutase), CAT (catalase), POD (peroxidase), and the non-enzymatic antioxidants, ascorbic acid, proline, flavonoids, and polyphenols, which ultimately improve the plant’s drought resistance [51][52][53][54]. Ascorbic acid has also been reported to play a role in controlling the flowering time in plants [55]. Understanding the perception of drought stress and the coping strategies (early or late flowering) used by plants in response to drought provides a physiological basis for subsequent studies on the molecular mechanisms of drought-stress-induced flowering.

3. Flowering Time of Various Plant Species in Response to Drought Stress

Most plants have evolved and adapted to the frequent fluctuations in the natural environment, especially the severe damage caused by droughts due to water deficit. Drought stress can lead to alterations in the flowering time of various plants, effects on flower development (including reduced flower number, restricted filament elongation, and delayed anther development), immature seed development, and reduced yields [23][56][57]. Therefore, the flowering time is an important agricultural characteristic for the development of adaptation to drought stress in a wide range of plants (Table 2). The discrepancy between early and late flowering resulting from the effects of drought stress depends on the plant species [20][58]. For example, forage and biofuel crops generally have delayed flowering as a desirable target for them due to the importance of the plant vegetative biomass. Cereal crops, by contrast, usually exhibit early flowering as an ideal trait to shorten the harvest time, and, thus, increase the number of plantings during the growing season, while growing as fast as possible to minimize damage from drought stress caused by environmental fluctuations [56][59]. Drought stress caused by water deficit delays the flowering time of Arabidopsis under short-day (SD) (9, Table 1) conditions but accelerates flowering time under long-day (LD) (10, Table 1) conditions [11][29]. Drought stress causes premature bolting of Chinese cabbage in the growing season, which leads to insufficient vegetative growth and influences yield and quality [60]. By studying the effect of drought stress on flowering time in Brassica rapa offspring, it was found that materials with seeds collected after drought flowered earlier than those collected before drought, suggesting that Brassica rapa responds to drought stress and evolves towards earlier flowering [61]. Studies of drought-induced flowering in the chickpea suggest that drought stress generally accelerates the flowering time of temperate grain legumes [62][63]. The role of drought in influencing the flowering time varies among plant species and with environmental conditions, so that drought regulation of flowering is the result of multiple factors.
Recently, there have been studies on drought-induced flowering in several other plant species [12][64][65][66][67]. In contrast to early flowering induced by drought stress, the flowering time of rice is delayed under water deficit conditions to avoid reproductive growth in unfavorable environmental conditions, but water shortage still results in the retardation of plant growth and spikelet development, which leads to reduced crop yield and ultimately economic losses [68][69][70]. Water deficiency can also delay the first flowering of Medicago polymorpha. The effect of drought stress on early and late flowering in plants is closely related to the intensity and duration of the water deficit, in addition to varying by plant species. The artificial control of the duration and intensity of drought treatment in agricultural production plays an important role in accelerating plant development, especially regarding flowering. It was found that the response of rice to drought stress was dependent on the intensity of drought, and mild water deficit in the early development stage triggered a drought escape response with accelerated flowering and reduced tillering [71][72]. In a study of wheat response to drought stress, it was also found that the flowering time showed a nonlinear relationship with the plant water content status, with mild water deficit shortening the flowering time, while severe drought stress delayed flowering [73].
Drought-induced flowering is a phenomenon more common in annual plants. The drought stress regulation of plant flowering has been less well studied in woody plants and remains poorly understood, mainly due to the long duration of vegetative growth in perennials and the excessive long period of research. Drought stress is one of the major environmental factors inducing flowering in adult citrus in subtropical regions. Different citrus species are induced to flower by different environmental conditions, with lemon, four-season orange, and kumquat being mainly affected by drought stress, while sweet orange, trifoliate orange, mandarin orange, grapefruit, and tangerine are mainly affected by seasonal low temperature [22][74]. Notably, drought-induced flowering in citrus was also accompanied by the upregulation of the CiFT expression level [74][75]. Earlier studies have also shown that Citrus latifolia flowering is also induced by drought stress, and that all citrus plant species share this same flowering mechanism [76][77]. Additionally, the perennial woody plant Sapium sebiferum takes 3–5 years to flower normally, but one-year-old seedlings under drought stress flower early, which provides a feasible way to shorten the vegetative growth years of woody plants in genetic research and breeding efforts [78]. These indicate that the effect of drought stress on the flowering time is not specific to a particular plant species but is conserved in annuals as well as perennials. There are few studies on the regulation of flowering time by drought stress in perennials due to the long study time and the lack of phenotypes, but the available evidence supports the feasibility of researching this topic in perennials. Moreover, studies on drought-induced flowering in perennial plants can be carried out on the basis of sufficient theoretical evidence in annual plants.

4. Molecular Regulatory Mechanisms of Flowering Involved in Drought Stress

Drought-stress-induced flowering, as well as the traditional flower formation pathway, accomplish the same flowering purpose, but the traditional pathway is the primary option for flowering under normal environmental conditions, whereas drought-induced flowering is an emergency response under stressful conditions [20][79]. Compared with the in-depth studies of the flower formation regulatory pathways in plants, the molecular regulatory mechanisms of flowering involved in drought stress are still obscure. Drought stress triggers the differential expression of a variety of genes, including flowering time regulation genes and transcription factors associated with the stress response. Among them, the key genes of flowering regulation in response to drought stress tolerance are FT, CO, LFY, GI, SOC1, and TWIN SISTER OF FT (TSF) (11, Table 1) [11][23][29][80] (Figure 1).
Figure 1. Simplified regulatory pathways linking drought stress and flowering in Arabidopsis thaliana. Drought escape: ABF3/ABF4 further activates the expression of LFY, AP1, and SOC1 by targeting NF-YC [81]. GI accelerates flowering under drought conditions by positively regulating the expression of CO and miR172 [80], which, in turn, activate the expression of FT, or directly activate the transcription of TSF, which ultimately upregulates the expression levels of LFY, AP1, and SOC1 [11][29][82]. Drought tolerance: miR169 targets NF-YA2 to reduce its transcriptional abundance [83], which attenuates the repressive effect on downstream genes FLC and SVP [84], while FRI positively regulates the expression of FLC and SVP, resulting in the repression of FT transcription and delayed flowering under drought conditions [85]. Solid lines indicate identified associations, arrows indicate positive regulation, and horizontal bars indicate negative regulation.
The molecular mechanisms by which drought stress regulates flowering time in Arabidopsis have been partially elucidated. Emerging evidence suggests that GI, a photoperiodic pathway gene that promotes flowering, is a pivotal regulator of the abiotic stress response and can influence plant tolerance to abiotic stresses, especially drought [11][86]. Under long-day environmental conditions, water deprivation achieves drought-induced early flowering in Arabidopsis through ABA-dependent control of GI signaling that activates expression of the florigen genes FT and TSF. Under short-day conditions, the drought and plant stress hormone ABA is considered to inhibit the transcription of FT and TSF via activating repressors of floral formation, which, in turn, leads to late flowering in Arabidopsis [11][20][29][82][87]. It has been confirmed that the GI-miR172 pathway is involved in drought-induced early flowering by downregulating WRKY44 (directly repressed by miR172) [80] (Figure 1). Several other flowering inhibition genes are also induced by drought stress. For example, water deficit induces the flowering repressor gene SHORT VEGETATIVE PHASE (SVP) (12, Table 1), which represses the transcription of genes related to ABA catabolism, and increases ABA accumulation, which improves drought tolerance in Arabidopsis, but flowering is delayed [84]. Similarly, FLOWERING LOCUS C (FLC) (13, Table 1), a flowering suppressor gene, also plays a role in the drought stress pathway, and the loss of FLC function leads to early flowering and decreased drought tolerance in Arabidopsis [88]. In rice (Oryza sativa), activation of the florigen genes HEADING DATE 3a (Hd3a) (14, Table 1), flowering integration factor OsMADS50 (an orthologue gene of SOC1 in Arabidopsis), and RICE FLOWERING LOCUS T1 (RFT1) (15, Table 1) (AtFT-like gene) coordinates the modulation of the drought escape response [71]. Meanwhile, the CCT domain protein Ghd7 plays an important role in delaying the rice heading date and regulating drought stress tolerance under long-day conditions [89][90]. The transcription levels of Hd3a, RFT1,and EARLY HEADING DATE 1 (Ehd1, upstream of the florigen genes) (16, Table 1) are drastically decreased under drought environmental conditions, which eventually leads to delayed floral transition [69]. RICE CENTRORADIALIS 1 (RCN1, an orthologue of TFL in Arabidopsis) (17, Table 1) is reported in rice as a flowering time regulation gene in the pathway of drought-regulated floral transition that interacts with the 14-3-3 protein and OsFD1 to repress Hd3a protein function but not its transcriptional level, causing delayed flowering in rice under drought stress [68][91] (Table 2). These results suggest that when plants are subjected to drought stress, a large number of genes are induced to be expressed, including genes critical to the flowering pathway, and that differences in the expression of these genes between species ultimately lead to different flowering outcomes.
Table 2. Some examples of stress-induced flowering associated with flowering pathway genes. 
Abiotic Stress Factors Species Flowering Response Related Flowering Pathway Genes References
Drought (LD) Arabidopsis early flowering FT, GI, SOC1, TSF [11]
Drought (SD) Arabidopsis delayed flowering FT, TSF [29]
Drought Rice early flowering Hd3a (AtFT), OsMADS50 (AtSOC1), RFT1, Ehd1, OsTIR1, OsABF2, OsmiR393 [69][71][92]
delayed flowering RCN1 (AtFT) [68]
Maize early flowering ZmNF-YA3 [93]
Barley early flowering miR172, AP2-like [94]
Citrus induction CiNF-YA1 [77]
CiFD [13]
Brachypodium delayed flowering BdRFS [17]
Solanum lycopersicum early flowering SlOST1, SlVOZ1 [18]
Arabidopsis delayed flowering OXS3, AP1 [32]
OXS2, SOC1 [66]
early flowering ABF3/4, NF-YC, SOC1 [81]
miR169d, AtNF-YA2 [83]
Sapium sebiferum induction GA1, AP2, CYR2 [78]
Low
temperature		 Arabidopsis delayed flowering FCA, FVE, SVP, FLM [95][96]
MAF2 [97][98]
HOS1, CO, FLC [99][100][101]
HOS15, GI [102]
early flowering miR169d, AtNF-YA2 [83]
Phaibitis induction PnFT1, PnFT2 [64][103]
Chrysanthemum induction MAF2 (AtFLC) [98]
Poplar induction FT1 [104]
Citrus induction CiNF-YA1, CiFT [77]
CiFD [13]
CiFT, CsFT [22][105]
Medicago sativa delayed flowering MsFRI-L [106]
Barley/Wheat induction VRN1, VIN2, VRN3 [107][108][109]
Cymbidium goeringii induction CgSVP [110]
Heat stress Arabidopsis early flowering FT [111]
PIF4, PIF5 [112][113]
Soybean induction GmFT2a, GmFT5a [114]
Barley delayed flowering FLC gene family [115]
Rice early flowering EG1, OsGI [116]
Maize early flowering ZmNF-YA3, ZmFTL12 [93]
Chrysanthemum delayed flowering FTL3 (AtFT) [117]
Brassica rapa delayed flowering H2A.Z, FT [118]
A nuclear factor-Y (NF-Y) transcription factor, ZmNF-YA3, has the dual function of promoting maize flowering while increasing plant drought tolerance, but there is a lack of evidence on the specific mechanism of ZmNF-YA3 in drought-affected maize flower formation [93]. Also, Arabidopsis ABF3 and ABF4 act with NF-YCs to mediate drought-accelerated flowering by regulating SOC1 [81] (Figure 1). In citrus, CiNF-YA1 was also found to promote drought-induced flowering by forming a complex with CiNF-YB2 and CiNF-YC2 to activate CiFT expression, and overexpression of CiNF-YA1 in citrus increased plants drought-sensitivity [77]. It is evident that NF-YAs are likely to be functionally conserved in regulating flowering in annual and perennial plants, with functional diversity resulting from physiological differences in response to stress. These studies support a critical role for NF-YAs in promoting not only the flowering time but also drought response (tolerance/sensitivity). However, future studies are needed to clarify whether NF-YAs are directly involved in regulating drought-affected flowering. The bZIP transcription factor FLOWERING LOCUS D (FD) (18, Table 1), together with FT and the 14-3-3 proteins, is the florigen activation complex (FAC) (19, Table 1) that regulates plant flowering [119]. CiFD was found to form two distinct proteins through alternative splicing, CiFDα and CiFDβ, that both initiate flowering in citrus. Among them, CiFDα was induced by low temperature while CiFDβ was induced by drought stress. The regulatory mechanism of CiFDβ promoting drought-induced flowering is independent of FAC and interacts directly with AP1 [13] (Table 2). FRIGIDA (FRI) (20, Table 1) is an essential regulator of flowering in various plant species, including Populus balsamifera [120], Medicago sativa [106], Brassica napus [121], and Vitis vinifera [122]. Importantly, FRI modulates drought tolerance through the FLC–OST1 regulatory module [88] (Figure 1). CiFRI, a homologue of FRI in citrus, was drought-induced, and overexpression of CiFRI enhanced drought tolerance in Arabidopsis and citrus, whereas silenced plants showed drought sensitivity, and the ectopic expression in Arabidopsis exhibited late flowering. The citrus dehydrogenase gene CiDHN may maintain the stability of the CiFRI protein during drought-induced degradation [14]. Therefore, the drought-induced flowering regulation genes are conserved between annual and perennial plants. Together, these studies strongly support the pivotal roles of flowering-time-regulated genes in drought stress response and tolerance. The main challenge in woody plants is that the regulatory role of genes in drought-induced flowering can be demonstrated, but there is no phenotypic evidence of flowering, which is related to its own longer developmental process.
In addition, drought-induced transcription factors are closely related to the existing flowering regulatory pathways, and these TFs affect the flowering process of plants by regulating the transcription level of flowering-regulated genes [12][17][123]. The tomato OPEN STOMATA 1 (SlOST1) (21, Table 1) loss-of-function mutant causes reduced drought tolerance in plants, and the slost1 mutant exhibits a late-flowering phenotype under both normal and drought environmental conditions. SlOST1 combines with the flowering integrated gene VASCULAR PLANT ONE-ZINC FINGER 1 (SlVOZ1) (22, Table 1) to form a regulatory module, and then interacts with the promoter of SINGLE FLOWER TRUSS to regulate tomato flowering under drought stress [18]. A conserved and specific gene family in plants, the Regulator of Flowering and Stress (RFS) family (23, Table 1), produces dramatic alterations in transcriptional levels in response to drought environmental stimuli. Overexpression of BdRFS in Brachypodium distachyon not only substantially delayed flowering but also promoted drought tolerance. The rfs mutants in Arabidopsis and Brachypodium distachyon displayed an early flowering phenotype and were susceptible to water deprivation [17].
Studies have reported that epigenetic mechanisms, including histone acetylation as well as methylation, are involved in the plant stress response and flowering time regulation. Histone deacetylase HISTONE DEACETYLASE 6 (HDA6)-deficient mutant plants (24, Table 1) exhibited a phenotype of reduced drought stress tolerance and delayed flowering with the repression of FLC expression [124][125][126]. The histone H4 gene BrHIS4.A04, which interacts with BrVIN3.1, is overexpressed in Chinese cabbage and reduces plant susceptibility to drought stress and accelerates flowering under normal growth conditions, whereas under water deficit environmental conditions, the histone H4 gene represses the expression of photoperiodic flowering genes to prevent premature bolting [60]. The regulation of flowering time under drought stress is also related to microRNAs (miRNAs). miRNAs are considered to be important suppressors of gene expression at the transcriptional and post-transcriptional levels. The involvement of miRNAs in regulating drought-stress-induced plant flowering responses has been found in many species, such as the annual plants Arabidopsis [127], rice [128], wheat [129], and maize [130], as well as in perennial plant species [131]. miR172 acts in the process of drought tolerance and flowering time regulation. miR172b-3p and miR172b-5p, derived from a common precursor, promoted flowering and enhanced drought tolerance in barley (Table 2). miR172b-3p expression was upregulated under drought stress treatment, which suppressed the four AP2-like transcription factors in barley to accelerate flowering. The expression of miR172b-5p was inhibited under drought conditions; thus, trehalose-6-phosphate synthase (TPS), a key enzyme for trehalose biosynthesis targeted by miR172b-5p, was significantly accumulated to enhance drought tolerance in barley [94]. miR156, which is in the same age pathway regulating plant flowering as miR172, is also induced by drought stress and delays flowering of Arabidopsis and tobacco [127][132]. miR169 family members play an important role in stress-induced flowering by inhibiting NF-YA2, which, in turn, decreases FLC expression, allowing the promotion of flowering [83] (Figure 1). In OsmiR393-overexpressing rice plants, miR393 responds to drought stress by targeting and, thus, repressing the expression of the auxin receptor genes OsTIR1 and OsAFB2 for early flowering [92]. In addition, differential expression of key proteins and post-translational modifications, such as SUMOylation, act in regulating plants’ flowering processes under drought stress conditions [133]. Taken together, when plants are subjected to drought, a variety of molecular regulatory mechanisms can be activated, suppressed, and integrated to maintain survival through the adjustment of flowering time.

References

  1. Zhu, J.-K. Abiotic stress signaling and Responses in plants. Cell 2016, 167, 313–324.
  2. Hu, H.H.; Xiong, L.Z. Genetic engineering and breeding of drought-resistant crops. Annu. Rev. Plant Biol. 2014, 65, 715–741.
  3. Webber, H.; Ewert, F.; Olesen, J.E.; Müller, C.; Fronzek, S.; Ruane, A.C.; Bourgault, M.; Martre, P.; Ababaei, B.; Bindi, M.; et al. Diverging importance of drought stress for maize and winter wheat in Europe. Nat. Commun. 2018, 9, 4249.
  4. Kopecká, R.; Kameniarová, M.; Cerny, M.; Brzobohaty, B.; Novák, J. Abiotic stress in crop production. Int. J. Mol. Sci. 2023, 24, 6603.
  5. Nadarajah, K.K. ROS homeostasis in abiotic stress tolerance in plants. Int. J. Mol. Sci. 2020, 21, 5208.
  6. Bechtold, U.; Field, B. Molecular mechanisms controlling plant growth during abiotic stress. J. Exp. Bot. 2018, 69, 2753–2758.
  7. Kollist, H.; Zandalinas, S.I.; Sengupta, S.; Nuhkat, M.; Kangasjärvi, J.; Mittler, R. Rapid responses to abiotic stress: Priming the landscape for the signal transduction network. Trends Plant Sci. 2019, 24, 25–37.
  8. De Storme, N.; Geelen, D. The impact of environmental stress on male reproductive development in plants: Biological processes and molecular mechanisms. Plant Cell Environ. 2013, 37, 1–18.
  9. Hasanuzzaman, M.; Nahar, K.; Alam, M.; Roychowdhury, R.; Fujita, M. Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int. J. Mol. Sci. 2013, 14, 9643–9684.
  10. Chirivì, D.; Betti, C. Molecular links between flowering and abiotic stress response: A focus on Poaceae. Plants 2023, 12, 331.
  11. Riboni, M.; Galbiati, M.; Tonelli, C.; Conti, L. GIGANTEA enables drought escape response via abscisic acid-dependent activation of the florigens and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1. Plant Physiol. 2013, 162, 1706–1719.
  12. Kazan, K.; Lyons, R. The link between flowering time and stress tolerance. J. Exp. Bot. 2016, 67, 47–60.
  13. Ye, L.X.; Wu, Y.M.; Zhang, J.X.; Zhang, J.X.; Zhou, H.; Zeng, R.F.; Zheng, W.X.; Qiu, M.Q.; Zhou, J.J.; Xie, Z.Z.; et al. A bZIP transcription factor (CiFD) regulates drought- and low-temperature-induced flowering by alternative splicing in citrus. J. Integr. Plant Biol. 2022, 65, 674–691.
  14. Xu, Y.Y.; Zeng, R.F.; Zhou, H.; Qiu, M.Q.; Gan, Z.M.; Yang, Y.L.; Hu, S.F.; Zhou, J.J.; Hu, C.G.; Zhang, J.Z. Citrus FRIGIDA cooperates with its interaction partner dehydrin to regulate drought tolerance. Plant J. 2022, 111, 164–182.
  15. Osnato, M. The floral transition and adaptation to a changing environment: From model species to cereal crops. Plant Cell 2022, 34, E2.
  16. Forestan, C.; Farinati, S.; Zambelli, F.; Pavesi, G.; Rossi, V.; Varotto, S. Epigenetic signatures of stress adaptation and flowering regulation in response to extended drought and recovery in Zea mays. Plant Cell Environ. 2020, 43, 55–75.
  17. Ying, S.; Scheible, W.R.; Lundquist, P.K. A stress-inducible protein regulates drought tolerance and flowering time in Brachypodium and Arabidopsis. Plant Physiol. 2023, 191, 643–659.
  18. Chong, L.; Xu, R.; Huang, P.C.; Guo, P.C.; Zhu, M.K.; Du, H.; Sun, X.L.; Ku, L.X.; Zhu, J.K.; Zhu, Y.F. The tomato OST1-VOZ1 module regulates drought-mediated flowering. Plant Cell 2022, 34, 2001–2018.
  19. Fletcher, R.S.; Mullen, J.L.; Heiliger, A.; McKay, J.K. QTL analysis of root morphology, flowering time, and yield reveals trade-offs in response to drought in Brassica napus. J. Exp. Bot. 2015, 66, 245–256.
  20. Takeno, K. Stress-induced flowering: The third category of flowering response. J. Exp. Bot. 2016, 67, 4925–4934.
  21. Abdelrahman, M.; Jogaiah, S.; Burritt, D.J.; Tran, L.-S.P. Legume genetic resources and transcriptome dynamics under abiotic stress conditions. Plant Cell Environ. 2018, 41, 1972–1983.
  22. Nishikawa, F. Regulation of floral induction in citrus. J. Jpn. Soc. Hortic. Sci. 2013, 82, 283–292.
  23. Su, Z.; Ma, X.; Guo, H.H.; Sukiran, N.L.; Guo, B.; Assmann, S.M.; Ma, H. Flower development under drought stress: Morphological and transcriptomic analyses reveal acute responses and long-term acclimation in Arabidopsis. Plant Cell 2013, 25, 3785–3807.
  24. Qi, J.; Song, C.-P.; Wang, B.; Zhou, J.; Kangasjärvi, J.; Zhu, J.-K.; Gong, Z. Reactive oxygen species signaling and stomatal movement in plant responses to drought stress and pathogen attack. J. Integr. Plant Biol. 2018, 60, 805–826.
  25. Ogura, T.; Goeschl, C.; Filiault, D.; Mirea, M.; Slovak, R.; Wolhrab, B.; Satbhai, S.B.; Busch, W. Root system depth in Arabidopsis is shaped by EXOCYST70A3 via the dynamic modulation of auxin transport. Cell 2019, 178, 400–412.
  26. Pennisi, E. Plant genetics: Getting to the root of drought responses. Science 2008, 320, 173.
  27. Duan, H.L.; de Dios, V.R.; Wang, D.F.; Zhao, N.; Huang, G.M.; Liu, W.F.; Wu, J.P.; Zhou, S.X.; Choat, B.; Tissue, D.T. Testing the limits of plant drought stress and subsequent recovery in four provenances of a widely distributed subtropical tree species. Plant Cell Environ. 2022, 45, 1187–1203.
  28. Basu, S.; Ramegowda, V.; Kumar, A.; Pereira, A. Plant adaptation to drought stress. F1000Research 2016, 5, 1554.
  29. Riboni, M.; Test, A.R.; Galbiati, M.; Tonelli, C.; Conti, L. ABA-dependent control of GIGANTEA signalling enables drought escape via up-regulation of FLOWERING LOCUS T in Arabidopsis thaliana. J. Exp. Bot. 2016, 67, 6309–6322.
  30. Verslues, P.E.; Bailey-Serres, J.; Brodersen, C.; Buckley, T.N.; Conti, L.; Christmann, A.; Dinneny, J.R.; Grill, E.; Hayes, S.; Heckman, R.W.; et al. Burning questions for a warming and changing world: 15 unknowns in plant abiotic stress. Plant Cell 2023, 35, 67–108.
  31. Kooyers, N.J. The evolution of drought escape and avoidance in natural herbaceous populations. Plant Sci. 2015, 234, 155–162.
  32. Liang, M.T.; Xiao, S.M.; Cai, J.J.; Ow, D.W. OXIDATIVE STRESS 3 regulates drought-induced flowering through APETALA 1. Biochem. Biophys. Res. Commun. 2019, 519, 585–590.
  33. Pajoro, A.; Biewers, S.; Dougali, E.; Leal Valentim, F.; Mendes, M.A.; Porri, A.; Coupland, G.; Van de Peer, Y.; van Dijk, A.D.J.; Colombo, L.; et al. The evolution of gene regulatory networks controlling Arabidopsis plant reproduction: A two-decade history. J. Exp. Bot. 2014, 65, 4731–4745.
  34. Cui, Y.; Ouyang, S.; Zhao, Y.; Tie, L.; Shao, C.; Duan, H. Plant responses to high temperature and drought: A bibliometrics analysis. Front. Plant Sci. 2022, 13.
  35. Yang, Y.J.; Bi, M.H.; Nie, Z.F.; Jiang, H.; Liu, X.D.; Fang, X.W.; Brodribb, T.J. Evolution of stomatal closure to optimize water-use efficiency in response to dehydration in ferns and seed plants. N. Phytol. 2021, 230, 2001–2010.
  36. Marchin, R.M.; Backes, D.; Ossola, A.; Leishman, M.R.; Tjoelker, M.G.; Ellsworth, D.S. Extreme heat increases stomatal conductance and drought-induced mortality risk in vulnerable plant species. Glob. Chang. Biol. 2022, 28, 1133–1146.
  37. Groen, S.C.; Joly-Lopez, Z.; Platts, A.E.; Natividad, M.; Fresquez, Z.; Mauck, W.M.; Quintana, M.R.; Cabral, C.L.U.; Torres, R.O.; Satija, R.; et al. Evolutionary systems biology reveals patterns of rice adaptation to drought-prone agro-ecosystems. Plant Cell 2022, 34, 759–783.
  38. Juenger, T.E.; Verslues, P.E. Time for a drought experiment: Do you know your plants’ water status? Plant Cell 2023, 35, 10–23.
  39. Ahanger, M.A.; Bhat, J.A.; Siddiqui, M.H.; Rinklebe, J.; Ahmad, P. Integration of silicon and secondary metabolites in plants: A significant association in stress tolerance. J. Exp. Bot. 2020, 71, 6758–6774.
  40. Shao, C.C.; Duan, H.L.; Ding, G.J.; Luo, X.Y.; Fu, Y.H.; Lou, Q. Physiological and biochemical dynamics of Pinus massoniana Lamb. seedlings under extreme drought stress and during recovery. Forests 2022, 13, 65.
  41. Li, Y.; Xu, Y.; Chen, Y.; Ling, L.; Jiang, Y.; Duan, H.; Liu, J. Effects of drought regimes on growth and physiological traits of a typical shrub species in subtropical China. Glob. Ecol. Conserv. 2020, 24, e01269.
  42. Hu, Y.; Yang, L.; Gao, C.; Liao, D.; Long, L.; Qiu, J.; Wei, H.; Deng, Q.; Zhou, Y. A comparative study on the leaf anatomical structure of Camellia oleifera in a low-hot valley area in Guizhou Province, China. PLoS ONE 2022, 17, e0262509.
  43. Gao, J.; Zhao, Y.; Zhao, Z.K.; Liu, W.; Jiang, C.H.; Li, J.J.; Zhang, Z.Y.; Zhang, H.L.; Zhang, Y.G.; Wang, X.N.; et al. RRS1 shapes robust root system to enhance drought resistance in rice. N. Phytol. 2023, 238, 1146–1162.
  44. Scharwies, J.D.; Dinneny, J.R. Water transport, perception, and response in plants. J. Plant Res. 2019, 132, 311–324.
  45. Andrés, F.; Coupland, G. The genetic basis of flowering responses to seasonal cues. Nat. Rev. Genet. 2012, 13, 627–639.
  46. Su, P.; Sui, C.; Niu, Y.; Li, J.; Wang, S.; Sun, F.; Yan, J.; Guo, S. Comparative transcriptomic analysis and functional characterization reveals that the class III peroxidase gene TaPRX-2A regulates drought stress tolerance in transgenic wheat. Front. Plant Sci. 2023, 14, 1119162.
  47. Castro, B.; Citterico, M.; Kimura, S.; Stevens, D.M.; Wrzaczek, M.; Coaker, G. Stress-induced reactive oxygen species compartmentalization, perception and signalling. Nat. Plants 2021, 7, 403–412.
  48. Phua, S.Y.; De Smet, B.; Remacle, C.; Chan, K.X.; Van Breusegem, F. Reactive oxygen species and organellar signaling. J. Exp. Bot. 2021, 72, 5807–5824.
  49. Duan, Y.; Han, J.; Guo, B.; Zhao, W.; Zhou, S.; Zhou, C.; Zhang, L.; Li, X.; Han, D. MbICE1 confers drought and cold tolerance through up-regulating antioxidant capacity and stress-resistant genes in Arabidopsis thaliana. Int. J. Mol. Sci. 2022, 23, 16072.
  50. Yang, Y.Q.; Guo, Y. Unraveling salt stress signaling in plants. J. Integr. Plant Biol. 2018, 60, 796–804.
  51. Jia, X.; Jia, X.; Li, T.; Wang, Y.; Sun, X.; Huo, L.; Wang, P.; Che, R.; Gong, X.; Ma, F. MdATG5a induces drought tolerance by improving the antioxidant defenses and promoting starch degradation in apple. Plant Sci. 2021, 312, 111052.
  52. Wei, T.L.; Wang, Y.; Xie, Z.Z.; Guo, D.Y.; Chen, C.W.; Fan, Q.J.; Deng, X.D.; Liu, J.H. Enhanced ROS scavenging and sugar accumulation contribute to drought tolerance of naturally occurring autotetraploids in Poncirus trifoliata. Plant Biotechnol. J. 2019, 17, 1394–1407.
  53. Zhao, S.; Gao, H.B.; Jia, X.M.; Wang, H.B.; Ke, M.; Ma, F.W. The HD-Zip I transcription factor MdHB-7 regulates drought tolerance in transgenic apple (Malus domestica). Environ. Exp. Bot. 2020, 180, 104246.
  54. Srivastava, R.; Kobayashi, Y.; Koyama, H.; Sahoo, L. Cowpea NAC1/NAC2 transcription factors improve growth and tolerance to drought and heat in transgenic cowpea through combined activation of photosynthetic and antioxidant mechanisms. J. Integr. Plant Biol. 2022, 65, 25–44.
  55. Barth, C. The role of ascorbic acid in the control of flowering time and the onset of senescence. J. Exp. Bot. 2006, 57, 1657–1665.
  56. Shavrukov, Y.; Kurishbayev, A.; Jatayev, S.; Shvidchenko, V.; Zotova, L.; Koekemoer, F.; de Groot, S.; Soole, K.; Langridge, P. Early flowering as a drought escape mechanism in plants: How can it aid wheat production? Front. Plant Sci. 2017, 8, 1950.
  57. Feng, X.; Zhou, L.; Sheng, A.; Lin, L.; Liu, H. Comparative transcriptome analysis on drought stress-induced floral formation of Curcuma kwangsiensis. Plant Signal. Behav. 2022, 17, 2114642.
  58. Verslues, P.E.; Juenger, T.E. Drought, metabolites, and Arabidopsis natural variation: A promising combination for understanding adaptation to water-limited environments. Curr. Opin. Plant Biol. 2011, 14, 240–245.
  59. Bheemanahalli, R.; Sathishraj, R.; Manoharan, M.; Sumanth, H.N.; Muthurajan, R.; Ishimaru, T.; Krishna, J.S.V. Is early morning flowering an effective trait to minimize heat stress damage during flowering in rice? Field Crops Res. 2017, 203, 238–242.
  60. Xin, X.Y.; Su, T.B.; Li, P.R.; Wang, W.H.; Zhao, X.Y.; Yu, Y.J.; Zhang, D.S.; Yu, S.C.; Zhang, F.L. A histone H4 gene prevents drought-induced bolting in Chinese cabbage by attenuating the expression of flowering genes. J. Exp. Bot. 2021, 72, 623–635.
  61. Franks, S.J. Plasticity and evolution in drought avoidance and escape in the annual plant Brassica rapa. N. Phytol. 2011, 190, 249–257.
  62. Anbazhagan, K.; Bhatnagar-Mathur, P.; Sharma, K.K.; Baddam, R.; Kishor, P.B.K.; Vadez, V. Changes in timing of water uptake and phenology favours yield gain in terminal water stressed chickpea AtDREB1A transgenics. Funct. Plant Biol. 2015, 42, 84–94.
  63. Chauhan, Y.; Allard, S.; Williams, R.; Williams, B.; Mundree, S.; Chenu, K.; Rachaputi, N.C. Characterisation of chickpea cropping systems in Australia for major abiotic production constraints. Field Crops Res. 2017, 204, 120–134.
  64. Wada, K.C.; Yamada, M.; Shiraya, T.; Takeno, K. Salicylic acid and the flowering gene FLOWERING LOCUS T homolog are involved in poor-nutrition stress-induced flowering of Pharbitis nil. J. Plant Physiol. 2010, 167, 447–452.
  65. Yaish, M.W.; Colasanti, J.; Rothstein, S.J. The role of epigenetic processes in controlling flowering time in plants exposed to stress. J. Exp. Bot. 2011, 62, 3727–3735.
  66. Blanvillain, R.; Wei, S.; Wei, P.; Kim, J.H.; Ow, D.W. Stress tolerance to stress escape in plants: Role of the OXS2 zinc-finger transcription factor family. EMBO J. 2011, 30, 3812–3822.
  67. Riboni, M.; Robustelli Test, A.; Galbiati, M.; Tonelli, C.; Conti, L. Environmental stress and flowering time: The photoperiodic connection. Plant Signal. Behav. 2014, 9, e29036.
  68. Wang, Y.; Lu, Y.Y.; Guo, Z.Y.; Ding, Y.F.; Ding, C.Q. RICE CENTRORADIALIS 1, a TFL1-like gene, responses to drought stress and regulates rice flowering transition. Rice 2020, 13, 70.
  69. Galbiati, F.; Chiozzotto, R.; Locatelli, F.; Spada, A.; Genga, A.; Fornara, F. Hd3a, RFT1 and Ehd1 integrate photoperiodic and drought stress signals to delay the floral transition in rice. Plant Cell Environ. 2016, 39, 1982–1993.
  70. Bocco, R.; Lorieux, M.; Seck, P.A.; Futakuchi, K.; Manneh, B.; Baimey, H.; Ndjiondjop, M.N. Agro-morphological characterization of a population of introgression lines derived from crosses between IR 64 (Oryza sativa indica) and TOG 5681 (Oryza glaberrima) for drought tolerance. Plant Sci. 2012, 183, 65–76.
  71. Du, H.; Huang, F.; Wu, N.; Li, X.H.; Hu, H.H.; Xiong, L.H. Integrative regulation of drought escape through ABA-dependent and -independent pathways in rice. Mol. Plant 2018, 11, 584–597.
  72. Ghneim-Herrera, T.; Selvaraj, M.G.; Meynard, D.; Fabre, D.; Peña, A.; Ben Romdhane, W.; Ben Saad, R.; Ogawa, S.; Rebolledo, M.C.; Ishitani, M.; et al. Expression of the Aeluropus littoralis AlSAP gene enhances rice yield under field drought at the reproductive stage. Front. Plant Sci. 2017, 8, 994.
  73. Schmidt, J.; Tricker, P.J.; Eckermann, P.; Kalambettu, P.; Garcia, M.; Fleury, D. Novel alleles for combined drought and heat stress tolerance in wheat. Front. Plant Sci. 2020, 10, 1800.
  74. Li, J.-X.; Hou, X.-J.; Zhu, J.; Zhou, J.-J.; Huang, H.-B.; Yue, J.-Q.; Gao, J.-Y.; Du, Y.-X.; Hu, C.-X.; Hu, C.-G.; et al. Identification of genes associated with lemon floral transition and flower development during floral inductive water deficits: A hypothetical model. Front. Plant Sci. 2017, 8, 1013.
  75. Agustí, M.; Reig, C.; Martínez-Fuentes, A.; Mesejo, C. Advances in citrus flowering: A review. Front. Plant Sci. 2022, 13, 868831.
  76. Southwick, S.; Davenport, T. Characterization of water stress and low temperature effects on flower induction in citrus. Plant Physiol. 1986, 81, 26–29.
  77. Zhou, H.; Zeng, R.F.; Liu, T.J.; Ai, X.Y.; Ren, M.K.; Zhou, J.J.; Hu, C.G.; Zhang, J.Z. Drought and low temperature-induced NF-YA1 activates FT expression to promote citrus flowering. Plant Cell Environ. 2022, 45, 3505–3522.
  78. Yang, M.; Wu, Y.; Jin, S.; Hou, J.; Mao, Y.; Liu, W.; Shen, Y.; Wu, L. Flower bud transcriptome analysis of Sapium sebiferum (Linn.) Roxb. and primary investigation of drought induced flowering: Pathway construction and G-Quadruplex prediction based on transcriptome. PLoS ONE 2015, 10, e0118479.
  79. Ma, X.W.; Su, Z.; Ma, H. Molecular genetic analyses of abiotic stress responses during plant reproductive development. J. Exp. Bot. 2020, 71, 2870–2885.
  80. Han, Y.; Zhang, X.; Wang, Y.; Ming, F. The suppression of WRKY44 by GIGANTEA-miR172 pathway is involved in drought response of Arabidopsis thaliana. PLoS ONE 2013, 8, e73541.
  81. Hwang, K.; Susila, H.; Nasim, Z.; Jung, J.Y.; Ahn, J.H. Arabidopsis ABF3 and ABF4 transcription factors act with the NF-YC complex to regulate SOC1 expression and mediate drought-accelerated flowering. Mol. Plant 2019, 12, 489–505.
  82. Kim, W.-Y.; Ali, Z.; Park, H.J.; Park, S.J.; Cha, J.-Y.; Perez-Hormaeche, J.; Quintero, F.J.; Shin, G.; Kim, M.R.; Qiang, Z.; et al. Release of SOS2 kinase from sequestration with GIGANTEA determines salt tolerance in Arabidopsis. Nat. Commun. 2013, 4, 1352.
  83. Xu, M.Y.; Zhang, L.; Li, W.W.; Hu, X.L.; Wang, M.B.; Fan, Y.L.; Zhang, C.Y.; Wang, L. Stress-induced early flowering is mediated by miR169 in Arabidopsis thaliana. J. Exp. Bot. 2014, 65, 89–101.
  84. Wang, Z.; Wang, F.X.; Hong, Y.C.; Yao, J.J.; Ren, Z.Z.; Shi, H.Z.; Zhu, J.K. The flowering repressor SVP confers drought resistance in Arabidopsis by regulating abscisic acid catabolism. Mol. Plant 2018, 11, 1184–1197.
  85. Choi, K.; Kim, J.; Hwang, H.J.; Kim, S.; Park, C.; Kim, S.Y.; Lee, I. The FRIGIDA complex activates transcription of FLC, a strong flowering repressor in Arabidopsis, by recruiting chromatin modification factors. Plant Cell 2011, 23, 289–303.
  86. Sawa, M.; Kay, S.A. GIGANTEA directly activates Flowering Locus T in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 2011, 108, 11698–11703.
  87. Fornara, F.; Montaigu, A.; Sánchez-Villarreal, A.; Takahashi, Y.; Ver Loren van Themaat, E.; Huettel, B.; Davis, S.J.; Coupland, G. The GI–CDF module of Arabidopsis affects freezing tolerance and growth as well as flowering. Plant J. 2015, 81, 695–706.
  88. Chen, L.; Hu, P.C.; Lu, Q.Q.; Zhang, F.; Su, Y.H.; Ding, Y. Vernalization attenuates dehydration tolerance in winter-annual Arabidopsis. Plant Physiol. 2022, 190, 732–744.
  89. Weng, X.; Wang, L.; Wang, J.; Hu, Y.; Du, H.; Xu, C.; Xing, Y.; Li, X.; Xiao, J.; Zhang, Q. Grain number, plant height, and heading date7 is a central regulator of growth, development, and stress response. Plant Physiol. 2014, 164, 735–747.
  90. Xue, W.; Xing, Y.; Weng, X.; Zhao, Y.; Tang, W.; Wang, L.; Zhou, H.; Yu, S.; Xu, C.; Li, X.; et al. Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat. Genet. 2008, 40, 761–767.
  91. Kaneko-Suzuki, M.; Kurihara-Ishikawa, R.; Okushita-Terakawa, C.; Kojima, C.; Nagano-Fujiwara, M.; Ohki, I.; Tsuji, H.; Shimamoto, K.; Taoka, K.I. TFL1-Like proteins in rice antagonize rice FT-Like protein in inflorescence development by competition for complex formation with 14-3-3 and FD. Plant Cell Physiol. 2018, 59, 458–468.
  92. Xia, K.F.; Wang, R.; Ou, X.J.; Fang, Z.M.; Tian, C.G.; Duan, J.; Wang, Y.Q.; Zhang, M.Y. OsTIR1 and OsAFB2 downregulation via OsmiR393 overexpression leads to more tillers, early flowering and less tolerance to salt and drought in rice. PLoS ONE 2012, 7, 364–373.
  93. Su, H.H.; Cao, Y.Y.; Ku, L.X.; Yao, W.; Cao, Y.Y.; Ren, Z.Z.; Dou, D.D.; Wang, H.T.; Ren, Z.B.; Liu, H.F.; et al. Dual functions of ZmNF-YA3 in photoperiod-dependent flowering and abiotic stress responses in maize. J. Exp. Bot. 2018, 69, 5177–5189.
  94. Swida-Barteczka, A.; Pacak, A.; Kruszka, K.; Nuc, P.; Karlowski, W.M.; Jarmolowski, A.; Szweykowska-Kulinska, Z. MicroRNA172b-5p/trehalose-6-phosphate synthase module stimulates trehalose synthesis and microRNA172b-3p/AP2-like module accelerates flowering in barley upon drought stress. Front. Plant Sci. 2023, 14, 1124785.
  95. Blázquez, M.A.; Ahn, J.H.; Weigel, D. A thermosensory pathway controlling flowering time in Arabidopsis thaliana. Nat. Genet. 2003, 33, 168–171.
  96. Jin, S.; Kim, S.Y.; Susila, H.; Nasim, Z.; Youn, G.; Ahn, J.H. FLOWERING LOCUS M isoforms differentially affect the subcellular localization and stability of SHORT VEGETATIVE PHASE to regulate temperature-responsive flowering in Arabidopsis. Mol. Plant 2022, 15, 1696–1709.
  97. Bendahmane, M.; Airoldi, C.A.; McKay, M.; Davies, B. MAF2 is regulated by temperature-dependent splicing and represses flowering at low temperatures in parallel with FLM. PLoS ONE 2015, 10, e0126516.
  98. Lyu, J.; Aiwaili, P.; Gu, Z.Y.; Xu, Y.J.; Zhang, Y.H.; Wang, Z.L.; Huang, H.F.; Zeng, R.H.; Ma, C.; Gao, J.P.; et al. Chrysanthemum MAF2 regulates flowering by repressing gibberellin biosynthesis in response to low temperature. Plant J. 2022, 112, 1159–1175.
  99. Jung, J.-H.; Seo, P.J.; Park, C.-M. The E3 ubiquitin ligase HOS1 regulates Arabidopsis flowering by mediating CONSTANS degradation under cold stress. J. Biol. Chem. 2012, 287, 43277–43287.
  100. Jung, J.-H.; Park, J.-H.; Lee, S.; To, T.K.; Kim, J.-M.; Seki, M.; Park, C.-M. The cold signaling attenuator HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENE1 activates FLOWERING LOCUS C transcription via chromatin remodeling under short-term cold stress in Arabidopsis. Plant Cell 2013, 25, 4378–4390.
  101. Jung, J.-H.; Park, C.-M. HOS1-mediated activation of FLC via chromatin remodeling under cold stress. Plant Signal. Behav. 2014, 8, e27342.
  102. Ahn, G.; Park, H.J.; Jeong, S.Y.; Shin, G.-I.; Ji, M.G.; Cha, J.-Y.; Kim, J.; Kim, M.G.; Yun, D.-J.; Kim, W.-Y. HOS15 represses flowering by promoting GIGANTEA degradation in response to low temperature in Arabidopsis. Plant Commun. 2023, 4, 100570.
  103. Yamada, M.; Takeno, K. Stress and salicylic acid induce the expression of PnFT2 in the regulation of the stress-induced flowering of Pharbitis nil. J. Plant Physiol. 2014, 171, 205–212.
  104. Hsu, C.-Y.; Adams, J.P.; Kim, H.; No, K.; Ma, C.; Strauss, S.H.; Drnevich, J.; Vandervelde, L.; Ellis, J.D.; Rice, B.M.; et al. FLOWERING LOCUS T duplication coordinates reproductive and vegetative growth in perennial poplar. Proc. Natl. Acad. Sci. USA 2011, 108, 10756–10761.
  105. Chica, E.J.; Albrigo, L.G. Changes in CsFT transcript abundance at the onset of low-temperature floral induction in sweet orange. J. Am. Soc. Hortic. Sci. 2013, 138, 184–189.
  106. Chao, Y.; Yang, Q.; Kang, J.; Zhang, T.; Sun, Y. Expression of the alfalfa FRIGIDA-like Gene, MsFRI-L delays flowering time in transgenic Arabidopsis thaliana. Mol. Biol. Rep. 2012, 40, 2083–2090.
  107. Yan, L.; Fu, D.; Li, C.; Blechl, A.; Tranquilli, G.; Bonafede, M.; Sanchez, A.; Valarik, M.; Yasuda, S.; Dubcovsky, J. The wheat and barley vernalization gene VRN3 is an orthologue of FT. Proc. Natl. Acad. Sci. USA 2006, 103, 19581–19586.
  108. Oliver, S.N.; Finnegan, E.J.; Dennis, E.S.; Peacock, W.J.; Trevaskis, B. Vernalization-induced flowering in cereals is associated with changes in histone methylation at the VERNALIZATION1 gene. Proc. Natl. Acad. Sci. USA 2009, 106, 8386–8391.
  109. Trevaskis, B.; Chen, A.; Dubcovsky, J. Wheat TILLING mutants show that the vernalization gene VRN1 down-regulates the flowering repressor VRN2 in leaves but is not essential for flowering. PLoS Genet. 2012, 8, e1003134.
  110. Yang, F.X.; Zhu, G.F.; Wei, Y.L.; Gao, J.; Liang, G.; Peng, L.Y.; Lu, C.Q.; Jin, J.P. Low-temperature-induced changes in the transcriptome reveal a major role of CgSVP genes in regulating flowering of Cymbidium goeringii. BMC Genom. 2019, 20, 53.
  111. Vu, L.D.; Xu, X.Y.; Gevaert, K.; De Smet, I. Developmental plasticity at high temperature. Plant Physiol. 2019, 181, 399–411.
  112. Kumar, S.V.; Lucyshyn, D.; Jaeger, K.E.; Alos, E.; Alvey, E.; Harberd, N.P.; Wigge, P.A. Transcription factor PIF4 controls the thermosensory activation of flowering. Nature 2012, 484, 242–245.
  113. Thines, B.C.; Youn, Y.W.; Duarte, M.I.; Harmon, F.G. The time of day effects of warm temperature on flowering time involve PIF4 and PIF5. J. Exp. Bot. 2014, 65, 1141–1151.
  114. No, D.H.; Baek, D.; Lee, S.H.; Cheong, M.S.; Chun, H.J.; Park, M.S.; Cho, H.M.; Jin, B.J.; Lim, L.H.; Lee, Y.B.; et al. High-temperature conditions promote soybean flowering through the transcriptional reprograming of flowering genes in the photoperiod pathway. Int. J. Mol. Sci. 2021, 22, 1314.
  115. Hemming, M.N.; Walford, S.A.; Fieg, S.; Dennis, E.S.; Trevaskis, B. Identification of high-temperature-responsive genes in cereals. Plant Physiol. 2012, 158, 1439–1450.
  116. Zhang, B.Y.; Wu, S.H.; Zhang, Y.E.; Xu, T.; Guo, F.F.; Tang, H.S.; Li, X.; Wang, P.F.; Qian, W.F.; Xue, Y.B. A high temperature-dependent mitochondrial lipase EXTRA GLUME1 promotes floral phenotypic robustness against temperature fluctuation in rice (Oryza sativa L.). PLoS Genet. 2016, 12, e1006152.
  117. Nakano, Y.; Higuchi, Y.; Sumitomo, K.; Hisamatsu, T. Flowering retardation by high temperature in chrysanthemums: Involvement of FLOWERING LOCUS T-like 3 gene repression. J. Exp. Bot. 2013, 64, 909–920.
  118. del Olmo, I.; Poza-Viejo, L.; Pineiro, M.; Jarillo, J.A.; Crevillen, P. High ambient temperature leads to reduced FT expression and delayed flowering in Brassica rapa via a mechanism associated with H2A.Z dynamics. Plant J. 2019, 100, 343–356.
  119. Taoka, K.; Ohki, I.; Tsuji, H.; Kojima, C.; Shimamoto, K. Structure and function of florigen and the receptor complex. Trends Plant Sci. 2013, 18, 287–294.
  120. Keller, S.R.; Levsen, N.; Ingvarsson, P.K.; Olson, M.S.; Tiffin, P. Local selection across a latitudinal gradient shapes nucleotide diversity in Balsam Poplar, Populus balsamifera L. Genetics 2011, 188, 941–952.
  121. Irwin, J.A.; Lister, C.; Soumpourou, E.; Zhang, Y.; Howell, E.C.; Teakle, G.; Dean, C. Functional alleles of the flowering time regulator FRIGIDA in the Brassica oleracea genome. BMC Plant Biol. 2012, 12, 21.
  122. Hyun, K.-g.; Oh, J.E.; Park, J.; Noh, Y.-S.; Song, J.-J. Structural analysis of FRIGIDA flowering-time regulator. Mol. Plant 2016, 9, 618–620.
  123. Renau-Morata, B.; Carrillo, L.; Dominguez-Figueroa, J.; Vicente-Carbajosa, J.; Molina, R.V.; Nebauer, S.G.; Medina, J. CDF transcription factors: Plant regulators to deal with extreme environmental conditions. J. Exp. Bot. 2020, 71, 3803–3815.
  124. Wu, K.; Zhang, L.; Zhou, C.; Yu, C.W.; Chaikam, V. HDA6 is required for jasmonate response, senescence and flowering in Arabidopsis. J. Exp. Bot. 2008, 59, 225–234.
  125. Kim, J.M.; To, T.K.; Matsui, A.; Tanoi, K.; Kobayashi, N.I.; Matsuda, F.; Habu, Y.; Ogawa, D.; Sakamoto, T.; Matsunaga, S.; et al. Acetate-mediated novel survival strategy against drought in plants. Nat. Plants 2017, 3, 17097.
  126. Yu, C.W.; Liu, X.C.; Luo, M.; Chen, C.Y.; Lin, X.D.; Tian, G.; Lu, Q.; Cui, Y.H.; Wu, K.Q. HISTONE DEACETYLASE6 interacts with FLOWERING LOCUS D and regulates flowering in Arabidopsis. Plant Physiol. 2011, 156, 173–184.
  127. Cui, L.G.; Shan, J.X.; Shi, M.; Gao, J.P.; Lin, H.X. The miR156-SPL9-DFR pathway coordinates the relationship between development and abiotic stress tolerance in plants. Plant J. 2014, 80, 1108–1117.
  128. Zheng, L.-L.; Qu, L.-H. Application of microRNA gene resources in the improvement of agronomic traits in rice. Plant Biotechnol. J. 2015, 13, 329–336.
  129. Giusti, L.; Mica, E.; Bertolini, E.; De Leonardis, A.M.; Faccioli, P.; Cattivelli, L.; Crosatti, C. microRNAs differentially modulated in response to heat and drought stress in durum wheat cultivars with contrasting water use efficiency. Funct. Integr. Genom. 2017, 17, 293–309.
  130. Pegler, J.; Grof, C.; Eamens, A. Profiling of the differential abundance of drought and salt stress-responsive microRNAs across grass crop and genetic model plant species. Agronomy 2018, 8, 118.
  131. Fang, L.; Wang, Y. MicroRNAs in woody plants. Front. Plant Sci. 2021, 12, 686831.
  132. Zhang, T.Q.; Wang, J.W.; Zhou, C.M. The role of miR156 in developmental transitions in Nicotiana tabacum. Sci. China Life Sci. 2015, 58, 253–260.
  133. Benlloch, R.; Lois, L.M. Sumoylation in plants: Mechanistic insights and its role in drought stress. J. Exp. Bot. 2018, 69, 4539–4554.
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Subjects: Agronomy
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
Min Chen
,
Tian-Liang Zhang
,
Chun-Gen Hu
,
Jin-Zhi Zhang
View Times: 272
Revisions: 2 times (View History)
Update Date: 25 Dec 2023
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