Abstract
As sessile organisms, plants must respond constantly to ever-changing environments to complete their life cycle; this includes the transition from vegetative growth to reproductive development. This process is mediated by photoperiodic response to sensing the length of night or day through circadian regulation of light-signaling molecules, such as phytochromes, to measure the length of night to initiate flowering. Flowering time is the most important trait to optimize crop performance in adaptive regions. In this review, we focus on interplays between circadian and light signaling pathways that allow plants to optimize timing for flowering and seed production in Arabidopsis, rice, soybean, and cotton. Many crops are polyploids and domesticated under natural selection and breeding. In response to adaptation and polyploidization, circadian and flowering pathway genes are epigenetically reprogrammed. Understanding the genetic and epigenetic bases for photoperiodic flowering will help improve crop yield and resilience in response to climate change.
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Introduction
Earth’s orbit and rotation around the sun lead to cyclical changes in environmental factors, such as daily and seasonal changes in light, temperature, water, and nutrients, directly affecting plant growth and development, especially the transition from vegetative growth to reproductive development1. The sessile plants have evolved multiple strategies to anticipate these changes, synchronizing their life activities accordingly for survival and reproduction. Photoperiodism is a physiological reaction of plants to sense external environmental cues and to anticipate seasonal growth2,3,4. For many annual plants, the flowering time depends on the length of daily exposure to light. Based on whether their day length requirement is greater than the critical day length for reproductive transition, they are classified into long-day, short-day, and day-neutral plants5.
The hourglass and the circadian rhythm models are two main hypotheses underlying mechanistic understanding of the photoperiodic response in plants6,7,8. The hourglass hypothesis assumes that the photoperiodic response of plants to short- and long-day conditions depends mainly on the length measurement of the dark period and the accumulation or activity change of specific chemical components7. This model can explain some photoperiodic events, but is contradictory to others when growing long-day plants under short-day conditions, a short amount of nighttime light can promote their flowering9. Thus, the hourglass model cannot fully explain all photoperiodic flowering phenomena. An alternative hypothesis can better explain them; the circadian rhythm hypothesis emphasizes the interplay of circadian rhythms and light signals in the organism10,11 and proposes key components in regulation of the light-controlled enzyme and substrate by the circadian clock. When the external light cycle synchronizes with the internal rhythm, the enzyme is activated by light and interacts with the substrate, inducing the expression of floral identity genes such as CONSTANS (CO) and FLOWERING LOCUS T (FT), leading to flowering transition2,3,4,8.
The circadian clock regulates various transcriptional and post-transcriptional events at specific times of day, dating back to redox homeostatic mechanisms after the Great Oxidation Event at ~2.5 billion years ago12. This mechanism, known as circadian gating, adjusts an organism’s sensitivity to environmental stimuli throughout the day. Circadian rhythm model of photoperiodic flowering is a good example. In Arabidopsis, precise daily control of CO expression by the circadian clock is essential for accurately measuring day length. During short winter days, CO peaks at night, leading to protein degradation. Conversely, in early summer’s long days, CO peaks during daylight, stabilizing its protein and activating FT transcription for earlier flowering13,14. In addition to light, daily timing signals are provided by changes in temperature, which allow the clock to be entrained to run within a physiologically critical temperature range for a relatively constant amount of time. In plants, temperature responses and light signals are linked, and this emphasizes how complexly light, temperature, and clock genes interact to enable plants to synchronize their physiological activities with daily and seasonal cycles15.
Notably, key flowering time controlling genes, such as Flowering Wageningen (FWA)16,17 and Flowering Locus C (FLC)18,19,20,21 in Arabidopsis and CONSTANS-Like2 (GhCOL2) Gossypium hirsutum (Upland cotton)22, are epigenes or epialleles, and their expression is regulated by DNA methylation, chromatin modification, and/or RNA-mediated mechanisms. Moreover, circadian clock gene expression is epigenetically regulated to promote growth vigor and defense in plant hybrids and allopolyploids23,24,25,26,27. In this review, we outline current progress in understanding the role of circadian regulation in the control of day-length-dependent flowering time in the model plant Arabidopsis thaliana and crops. Understanding circadian and epigenetic regulation of flowering time is crucial for improving crop yield and growth resilience, which may help develop gene-editing and epigenetic engineering technologies to optimize flowering times and yield potential and stability to meet the growing demand for food, feed, fuel, and biomaterials.
Transcriptional architecture of the circadian clock in Arabidopsis
In Arabidopsis, the circadian clock network responsible for generating rhythmic outputs has been dominated by repressive feedback loops (Fig. 1). The central loop of core oscillators consist of two dawn-phased transcription factors CIRCADIAN CLOCK-ASSOCIATED1 (CCA1) and LATE ELONGATED HYPOCOTYL (LHY), and their reciprocal regulator TIMING OF CAB EXPRESSION1 (TOC1), aka, PSEUDO-RESPONSE REGULATOR1 (PRR1), whose expression peaks in the evening; they constitute the central loop of the core oscillator28,29,30. Another factor CCA1 HIKING EXPEDITION (CHE), a TCP transcription factor, suppresses CCA1 suppression through interaction with TOC131. The TOC1 homologs PRR9, PRR7, PRR5, and PRR3 are sequentially expressed throughout the day and show partially redundant functions in repressing CCA1 and LHY transcription from dawn to dusk; they form an additional regulatory circuit with CCA1 and LHY1,32. In turn, CCA1 and LHY transcription represses expression of PRR5, PRR3, TOC1, GIGANTEA (GI), and the evening complex (EC) that comprises EARLY FLOWERING3 (ELF3), ELF4, and LUX ARRHYTHMO (LUX)33,34,35, but activates PRR9 and PRR7 expression in the morning36. In the evening, the EC functions as a transcriptional repressor to inhibit PRR9 and PRR7 expression, leading to the release of CCA1 and LHY from repression33,37. Moreover, GI, a plant-specific protein gene that is repressed by CCA1 and LHY complex in the morning and by TOC1 and EC in the evening, induces CCA1 and LHY expression through an unknown mechanism30,38,39. GI is localized in the cytosol where it physically interacts with a light photoreceptor ZEITLUPE (ZTL) with E3 ubiquitin ligase activity to mediate proteasomal degradation of PRR5 and TOC140,41.
The circadian clock in A. thaliana is regulated by a complex network of transcriptional feedback and feedforward loops that involve multiple clock genes. CCA1 and LHY are key transcriptional repressors that negatively regulate the expression of TOC1, PRRs, as well as their own transcription, and in turn, TOC1 and PRRs inhibit the expression of CCA1 and LHY, creating a central feedback loop that helps regulate the clock and its output pathways. The evening complex (EC) formed by ELF3, ELF4 LUX, and GI, respectively, also regulates CCA1 and LHY expression. RVEs are transcriptional activators that directly bind to the promoters of evening-phased genes repressed by CCA1 and LHY and promote their expression, thereby rest the internal oscillator. LNK1 and LNK2 serve as transcriptional coactivators via interaction with RVE to regulate target genes. LWD1 and LWD2 are both involved in perceiving light input to activate the central clock genes, including CCA1, TOC1, PRR9, and PRR5. White and gray shades indicate morning-phased (sun) and evening-phased (moon) events. Arrows and blunt ends show positive and negative regulation, respectively, while dashed boxes indicate proteins in a complex. For simplicity, protein and gene symbols are interchangeable in this and other figures.
In addition to the negative interactions, multiple transcriptional activators are found to complement the plant circadian regulation. LIGHT-REGULATED WD1 (LWD1) and LWD2 are part of a larger family of proteins known as WD-repeat proteins, which are involved in transmitting light signals to the circadian clock to promote expression of CCA1, TOC1, PRR5, and PRR9 in the morning42,43,44. The midday-phased components REVEILLEs (RVE4, RVE6, and RVE8) are considered to be homologs of CCA1 and LHY due to their shared structural and functional similarities45. Interestingly, RVEs antagonize the action of CCA1 and LHY and bind to the same evening element (EE) during the midday period. This competition results in the activation of clock genes such as PRR9, PRR5, TOC1, GI, ELF4, and LUX. In turn, PRR5, PRR7, and PRR9 repress RVE8 expression, indicating that RVEs play an important role in maintaining the balance and robustness of the circadian regulation45,46. Two other activating components NIGHT LIGHT INDUCIBLE AND CLOCK-REGULATED1 (LNK1) and LNK2 are transcriptional coactivators of RVE8 to regulate expression of PRR5 and TOC1, both of which repress LNK1 and LNK2 expression in return, forming another loop47.
Circadian-dependent CO accumulation regulates photoperiodic flowering in Arabidopsis
Arabidopsis is a facultative long-day plant with metabolic pathways adapted to different photoperiods for flowering, and the control of its flowering timing involves the circadian clock, light signaling pathways, and transcription factor networks (Fig. 2). Among these, CO is one of the key genes that control the photoperiodic flowering response. In long-day conditions, CO transcripts accumulate from the afternoon into the night, which leads to the stabilization of CO protein and the activation of FT, a downstream gene that promotes flowering48. In short-day conditions, CO transcription is restricted to the dark, and FT expression is not activated. CYCLING DOF FACTORs (CDFs) are a family of transcription factors and can directly bind to the promoter region of the CO gene and repress its transcription in the morning49,50, and this repression is necessary to ensure that flowering occurs at the appropriate time in response to seasonal changes8,51. Natural variations in CDF binding sites are correlated with differences in CO transcript abundance and flowering time52. Thus, precise control of daily CDFs expression and CO protein abundance is crucial for the proper regulation of flowering timing and adaption to changing environmental conditions.
CO and FT are key regulators in the photoperiodic flowering pathway. CO is tightly regulated by the circadian clock and external light signals, and it activates FT expression to initiate flowering. The interaction between FKBP12 and CO protein prevents CO degradation and modulates its nuclear localization. In the early morning, CDF transcription factors that are regulated by the circadian clock accumulate at high levels and directly repress CO expression, thereby delaying flowering. GI is another key player in regulating circadian outputs. Under long-day conditions, high levels of GI work together with the blue-light receptor FKF1 to facilitate the degradation of the flowering repressor CDFs, promoting the initiation of flowering. Conversely, the core clock component CCA1 promotes the expression of CDFs by directly binding to their promoters, which enhances the inhibitory effect of CDFs on CO expression, leading to delayed flowering. Additionally, PRRs can directly or indirectly regulate CDF expression, affecting flowering. The light-sensitive proteins CRYs, UVR8, PhyB, and PhyA are capable of sensing blue, UV-B, red, and far-red light, respectively, and modulating the activity of CO protein to regulate FT expression and flowering. The line graphs at the bottom panel indicate mRNA oscillation of CO, CO/FKBP12, and FT, respectively. Arrows, lines, and shades are the same as in Fig. 1.
In Arabidopsis, the transcription of CDFs is regulated by various clock components. Specifically, CDFs are induced by the morning clock genes CCA1/LHY and repressed by the evening clock genes PRR5, PRR7, and PRR932. This leads to a typical diurnal expression pattern of CDFs with a peak at dawn and this regulation is essential for plants to optimize their reproductive success by flowering at the appropriate time of year53,54,55,56. Loss-of-function mutations in CCA1 and LHY lead to early flowering 29, while constitutive expression of CCA1 leads to circadian arrhythmicity and late flowering 28. Additionally, the evening clock genes PRR9, PRR7, and PRR5 function antagonistically with CCA1/LHY and coordinately and positively regulate CO dependent photoperiodic flowering process53. CCA1/LHY also represses the transcription of CO by adjusting the rhythmic expression of the clock component GI and the F-box protein FKF1, and this leads to the appropriate timing of CO expression and photoperiodic flowering35.
The photoperiodic flowering pathway is regulated by the interaction of various proteins. GI together with the blue-light receptors ZTL, LKP2, and FKF1 regulates the degradation of the flowering repressor CDFs to control the clock-mediated photoperiodic flowering pathway 57. Under long-day conditions, the timing of GI and FKF1 expression is synchronized, peaking in the late afternoon, and the blue-light absorption enables FKF1 to form a sufficient protein complex with GI to target CDF proteins for degradation, which alleviates the transcriptional repression of the CO gene and promotes flowering50. In contrast, diurnal expression of FKF1 and GI proteins is out of phase during short days, leading to low levels of FKF1-GI complex and CO expression under light, and consequently, the flowering is delayed. A computational model predicts that FKF1 may control FT expression directly in addition to its role in CO transcriptional activation58. ZTL and LKP2 also play important roles in regulation of flowering time and the circadian clock by ubiquitin-mediated degradation of clock components. Introducing both ztl and lkp2 mutations into the fkf1 mutant further enhances the late-flowering phenotype of the fkf1 mutant and reduces the CO expression level, due to the increased abundance of CDF2 protein59. In contrast to FKF1, overexpression of ZTL or LKP2 leads to an unexpected late-flowering phenotype accompanied with low levels of CO expression, similar to the ztl fkf1 lkp2 triple mutant and the gi mutant60. One explanation for this late-flowering phenotype of these overexpressing lines is that a high level of the ZTL/LKP2 sequester FKF1 in the cytosol by forming the ZTL/LKP2-FKF1 complex. This reduces the amount of FKF1-GI-CDF1 complex in the nucleus, causing repression of CO expression61. Another possibility is that a high level of ZTL/LKP2 destabilizes core clock components TOC1 and PRR5, which interact with and stabilize CO protein to promote flowering in response to the day length40,41,55.
Light controls CO protein stability in Arabidopsis
Transcript levels of CO, CO/FKBP12, and FT, respectively, are diurnally oscillated (Fig. 2, bottom panel). At the post-transcriptional level, the stability of CO protein is compromised by the action of post-translational modification. The degradation of CO protein is mainly controlled by two RING-finger E3 ubiquitin ligases, HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENE1 (HOS1)62 and CONSTITUTIVE PHOTOMORPHOGENIC 1 (COP1)63, which act in a light-dependent manner. HOS1 directly targets to CO protein to promote its degradation in the early morning, and mutation in HOS1 causes extreme early flowering in both long- and short-day conditions62. However, COP1 promotes CO degradation during night, leading to suppression of the floral integrator FT and delayed flowering64, and SUPPRESSOR OF PHYA (SPA1) can enhance the E3 ubiquitin ligase activity of COP165. In contrast, the small immunophilin FK506 BINDING PROTEIN 12 KD (FKBP12) physically interacts with CO to prevent its degradation by COP1, and this interaction can also modulate its phosphorylation and nuclear localization, enabling it to trigger FT expression and flowering66.
Photoreceptors also play critical roles in regulating CO stability and act antagonistically to generate daily rhythms in CO abundance14. The blue-light photoreceptors cryptochrome1 (CRY1) and CRY2 physically interact with SPA1 to suppress the activity of COP1/SPA1 ubiquitin ligase and stabilize CO protein in a blue-light-dependent manner67. The red/far-red responsive phytochromes (PhyA–PhyE in Arabidopsis) also control flowering time68. Among the five phytochromes, PhyA and PhyB play the most predominant function in CO protein stability8,69. Under the far-red light, PhyA stabilizes CO protein and promotes flowering by inhibiting the COP1-SPA1 complex, while red light-activated PhyB interacts with HOS1 to promote CO protein degradation14,62. The light-dependent control of CO protein stability is a complex and tightly regulated process that controls photoperiodic flowering. The knowledge gained from Arabidopsis research has provided fundamental insights into the mechanisms controlling photoperiodic flowering in other plant species including agricultural crops.
Photoperiodic flowering mechanism in rice
The function of core circadian regulators is conserved among Arabidopsis and crops. For example, the function of CCA1, LHY, and TOC1 is conserved in rice70,71, maize72, and duckweed73. Overexpressing maize ZmCCA1b and rice OsPRR homologs, respectively, can complement mutant phenotypes in Arabidopsis71,72. In rice, OsCCA1 upregulates expression of strigolactone receptor and signaling and responsive genes to repress tiller-bud outgrowth70. Down-regulating and overexpressing OsCCA1 increases and reduces tiller numbers, respectively, while altering OsPRR1 expression leads to the opposite effects. Moreover, both exogenous and endogenous sugars negatively regulate expression of OsCCA1, which in turn mediates expression of strigolactone receptor and signaling pathway genes to control tillering, flowering, and panicle development.
Rice is a facultative short-day plant; flowering is accelerated under short-day conditions and repressed by long-day conditions (Fig. 3). The floral transition in rice is dependent on the transcription of two florigen genes Heading date3a (Hd3a) and Rice FT1 (RFT1)74,75,76, which are mainly controlled by two important transcription factors Heading date1 (Hd1)77, an ortholog of the Arabidopsis CO, and Early heading date1 (Ehd1)78 that is unique in rice. Similar to Arabidopsis FT, both Hd3a and RFT1 are expressed in the vascular tissue of leaves and move to the shoot apical meristem, where they enhance the expression of floral meristem identity genes, such as OsMADS14 and OsMADS15, and trigger flowering75,76. Hd3a and RFT1 are essential for promoting rice flowering under short-day conditions, while RFT1 functions as a floral activator under long-day conditions. At least two distinct pathways regulate rice floral transition, the conserved OsGI-Hd1-Hd3a pathway and a unique Grain number, Plant Height, and Heading date1 (Ghd7)-Ehd1-Hd3a/RFT1 pathway (Fig. 3), which are both regulated by the circadian clock and light perception8.
Rice has evolved two distinct photoperiodic flowering pathways to adapt varying short (SD) and long (LD) day lengths. The evolutionarily conserved Hd1-Hd3a pathway is activated under SD conditions and the uniquely evolved Ghd7-Ehd1-Hd3a/RFT1 pathway is activated under LD conditions, and they are regulated by both the circadian clock and light signaling. Hd1 plays a crucial role in regulating rice flowering time by interacting with the NF-YB transcription factor DTH8 in response to day length changes. Under SD conditions, Hd1 promotes the expression of Hd3a and Ehd1 to activate floral meristem identity genes. However, under LD conditions, Hd1 suppresses the expression of Hd3a and Ehd1 to prevent premature flowering, contributing to the photoperiodic adaptability of rice. Hd1 also interacts with the flowering repressor Ghd7 to inhibit Ehd1 expression, thereby delaying flowering under LD conditions. OsGI triggers the initiation of the Hd1-Hd3a pathway by activating Hd1 expression and can enhance Hd3a and Ehd1 expression by inhibiting Ghd7, leading to flowering. The clock gene OsPRR37 also regulates photoperiodic flowering by activating Hd3a expression under SD conditions and suppressing it under LD conditions, allowing rice plants to fine-tune flowering timing for optimal reproductive success under changing environmental conditions. Sugar suppresses expression of OsCCA1, which in turn controls strigolactone pathway genes to regulate tiller buds and flowering. MADS14/15 are floral identity genes. Arrows, lines, and shades are the same as in Fig. 1.
Unlike CO in Arabidopsis, the Hd1 gene in rice is regulated by the circadian component OsGI and displays bifunctional responses to day length: promoting flowering by activating the expression of Hd3a under short-day conditions, but repressing Hd3a expression to delay flowering under long-day conditions77,79. This photoperiod-dependent conversion of Hd1 function from activation to repression is modulated by phytochromes and circadian clock. Photoperiodic Sensitivity5 (SE5) encodes a putative heme oxygenase involved in the biosynthesis of the phytochrome chromophore. In the se5 mutant, Hd3a expression is strongly induced by Hd1 under long-day conditions, resulting in early flowering phenotype similar to phytochrome-deficient mutants, such as OsphyB and OsphyC 80,81. Furthermore, overexpression of Hd1 can repress Hd3a expression and delay flowering under short-day conditions, and this effect requires functional phytochromes82. Therefore, phytochrome signals are essential for the conversion of Hd1 from an activator to a repressor of Hd3a transcription.
The rice-specific regulator Ghd7 encoding a CCT (CO, CO-LIKE, and TIMING OF CAB1) domain transcriptional regulator was identified as a major target of phytochrome signals in flowering control and acts as a repressor of Ehd178,83,84. Ehd1 is an important B-type response regulator that activates expression of Hd3a and RFT1, which are responsible for the transition from vegetative to reproductive growth in rice78,84. Ghd7 acting as a repressor of flowering is acutely induced by red light in morning through the PhyA homodimer or the PhyBPhyC heterodimer, and the repressor activity of Ghd7 is modulated post-transcriptionally by PhyB. Specifically, when PhyB is activated by red light, it undergoes a conformational change that allows it to interact with Ghd7 protein, and this interaction leads to the ubiquitination and subsequent degradation of Ghd7 through the 26 S proteasome pathway, which relieves its repressor activity and promotes flowering85. Days to heading8 (DTH8) encodes a putative HAP3 subunit of NF-YB transcription factor that is capable of binding to Hd3a promoter to enhance H3K27 trimethylation and repress Hd3a expression86,87. Under long-day conditions, both Ghd7 and DTH8 can interact with Hd1 to form a strong repressor complex that inhibits Ehd1 expression, and this effect of the Hd1-Ghd7-DTH8 complex on Ehd1 expression can also partly explain the photoperiod-dependent conversion of Hd1 from activation to repression86,88,89.
In sorghum, SbPRR37 activates expression of several downstream genes that repress flowering in long days90. SbPRR37 expression is dependent on light and regulated by the circadian clock. In short days, SbPRR37 is not expressed during the evening phase, allowing sorghum to flower. Similarly, clock components such as OsPRR37/DTH7 and the EC components, also regulate rice flowering by enhancing photoperiod sensitivity. OsPRR37 is predicted to act downstream of the OsPhyB to switch the genetic effects of Hd1 on Hd3a expression and delay flowering in long-day conditions through the formation of a transcriptional repressor complex91,92,93.
The EC is a crucial flowering repressor33. OsELF3-1 and OsELF3-2, two rice ELF3 paralogs, physically interact with OsELF4a in the nucleus, whilst OsELF3-1 shows a stronger interaction with OsLUX compared to OsELF3-294. Recent studies have shown that functional OsELF3 proteins accumulate during the evening in short-day conditions, forming the EC to induce flowering by inhibiting the expression of floral repressors OsPRR37 and Ghd7 93. However, in long-day conditions, OsELF3 protein levels are low and insufficient to suppress floral repressors, resulting in delayed flowering95. Taken together, these data indicate that rice possesses several complex genetic pathways to affect flowering time and photoperiod sensitivity.
Photoperiodic flowering mechanism in soybean
Soybean is a sensitive short-day plant, and this sensitivity limits the regional adaptation and crop yield. A series of genes have been identified to play a role in fine-tuning soybean flowering and maturity time and improve the regional adaptation (Fig. 4). The genome of soybean, being a paleopolyploid96, has at least 12 FT homologs. Among these, GmFT2a and GmFT5a are considered to be major functional FT orthologues, as they are highly induced under short-day conditions97. These genes promote flowering in response to short-day conditions, which is important for soybean adaptation to short-day regions. On the contrary, GmFT1a and GmFT4a appear to be inhibitors of flowering, and they are highly induced under long-day conditions98,99. These genes prevent premature flowering in response to long-day conditions, which is important for soybean adaptation to long-day regions. The remaining 8 FT homologs are nonfunctional or expressed at low levels in soybean leaves under inductive short-day conditions100. Flowering QTLs are associated with circadian clock regulators, GI in soybean101, and CO in sorghum102. The soybean genome has 28 CONSTANS-like genes (GmCOLs), and some of these genes, including GmCOL1a and GmCOL1b, are induced under long-day conditions and can activate the expression of florigen genes GmFT2a and GmFT5a, promoting soybean flowering103. Other GmCOLs have different expression patterns and functions in regulating soybean photoperiodic flowering104.
Soybean has multiple FT-like genes, and GmFT2a and GmFT5a promote flower formation by enhancing the expression of flower meristem identity genes, including GmSOC1, GmAP1, and GmLFY. Conversely, GmFT1a and GmFT4a inhibit flower formation by repressing these genes. The central regulator E1 inhibits soybean flowering by downregulating expression of GmFT2a and GmFT5a and upregulating expression of GmFT1a and GmFT4a. Under LD conditions, E1 expression is strongly induced by the red/far-red light receptors GmPhyA2 and GmPhyA3, leading to delayed flowering. These photoreceptors can also transmit light signals to circadian clock factor homologs such as GmGIa, GmPRR3a/b, GmELF3, and GmLUX. These factors mediate expression of GmLHYs, leading to distinct expression rhythms under SD and LD conditions, affecting flowering time in soybean plants. GmCOLs and GmFT2a/5a may form CO-FT regulons and play an important role in photoperiodic flowering in soybean. These models are based on genetic and gene expression results and may be refined by biochemical studies. Arrows, lines, and shades are the same as in Fig. 1, while dashed arrows indicate predicted interactions.
The flowering repressor gene E1 encodes a legume-specific transcription factor that induces GmFT1a and GmFT4a expression but represses GmFT2a and GmFT5a expression. This gene is directly repressed by four soybean CCA1/LHY genes (GmLHY1a, GmLHY1b, GmLHY2a and GmLHY2b) at the transcriptional levels98,99,105. Indeed, the soybean quadruple knockout mutant lhy1a lhy1b lhy2a lhy2b generated by CRISPR-Cas9 displayed late flowering and high E1 transcript levels in long days105. Meanwhile, GmPRR3a and GmPRR3b, orthologs of Arabidopsis PRR3, induce E1 expression to delay photoperiodic flowering through downregulation of GmLHY genes105,106. This pathway provides an additional layer of regulation for soybean flowering. The E2 locus in soybean encodes a homolog (GmGIa) of the Arabidopsis GI, which acts upstream of CO and FT in the photoperiodic flowering pathway. Like the role of GI in Arabidopsis, GmGIa plays a crucial role in integrating light and circadian signals in response to photoperiodic changes, ultimately leading to the transition from vegetative growth to reproductive development101. GmGIb and GmGIc are two homologs of GmGIa and can interact with two Arabidopsis FKF1 orthologs (GmFKF1 and GmFKF2) and one Arabidopsis CDF1 ortholog (GmCDF1) proteins, but GmGIa cannot interact with these three proteins, suggesting that GmGIa may play a unique role in regulating soybean flowering107. GmELF3, an ortholog of clock component ELF3, physically interacts with GmLUX2 to directly repress E1 expression and promotes soybean flowering108.
In addition to these genes, two maturity loci, E3 and E4, encode the phytochrome A proteins GmPhyA3 and GmPhyA2, respectively. These proteins induce expression of E1 and which, in turn, suppresses expression of GmFT2a and GmFT5a, resulting in delayed flowering under both natural day length and artificially long-day conditions109,110. The PhyA-regulated E1-GmFT pathway is a key determinant for soybean adaption to different latitude environments. The blue-light photoreceptor protein cryptochromes also play an essential role in regulating circadian rhythm and flowering time. Soybean contains two cryptochrome genes, GmCRY1a and GmCRY2a. However, only GmCRY1a has been found to strongly promote floral initiation in soybean, and the circadian rhythm of GmCRY1a protein has different phase characteristics in different photoperiods, which suggests that GmCRY1a plays a more predominant role in regulating flowering time in response to changes in day length111. The role of GmCRY2a in soybean flowering remains unclear and to be further investigated to elucidate its function.
Epistasis and epigenetic regulation of photoperiodic flowering in Arabidopsis and crops
Epigenetic regulation of circadian and flowering-time pathway genes plays a broader role in determining photoperiodic flowering in plants. Epigenetics refers to heritable changes in gene expression that do not involve alterations to the DNA sequence. Epigenetic mechanisms, involving DNA methylation, chromatin modifications, long-noncoding RNAs, and small interferring RNAs, have been shown to regulate expression of key photoperiodic flowering pathway genes and flowering time.
One of the best-studied epigenetic flowering events is known as vernalization, which refers to the induction of flowering after prolonged exposure to cold temperatures in winter, mediated by changes in the chromatin status of FLC112. COLD INDUCED LONG ANTISENSE INTRAGENIC RNA (COOLAIR)113 and COLD ASSISTED INTRONIC NONCODING RNA (COLDAIR)114 originated from the first intron and 3’ end of FLC, respectively. They have been proposed to facilitate FLC silencing by removing H3K36me3 from chromatin during vernalization, particularly under low-temperature conditions113,114. However, recent research suggests that the COOLAIR is not required for vernalization. Support for this notion comes from the normal vernalization response observed in the CRT/DRE-binding factors (CBFs) cbfs mutants with reduced levels of COOLAIR induction; moreover, both cbfs and FLCΔCOOLAIR mutants show a normal vernalization response despite their inability to activate COOLAIR expression during cold115. This work also highlights the importance of CBFs in initiating COOLAIR expression during the early stage of vernalization. CBFs bind to CRT/DREs at the 3’-end of FLC and increase progressively during vernalization, promoting COOLAIR expression. As vernalization progresses, FLC chromatin shifts to an inactive state, prompting CBF proteins to detach from the CRT/DREs in the COOLAIR promoter, thereby diminishing COOLAIR levels.
In Arabidopsis, FWA is an epiallele and encodes a flowering suppressor capable of specifically inhibiting the function of FT by directly binding to the FT protein17,116 (Fig. 5a). In the wild type, two repeats in the promoter region of FWA is heavily methylated and its expression is repressed, while the FWA promoter is demethylated and FWA is expressed in the fwa mutant17. Removal of DNA methylation in the FWA promoter can lead to activation of FWA and late flowering, as observed in multiple late-flowering mutants that were found in the decrease in DNA methylation1 (ddm1) genetic background16. These epialleles likely result from the plant adaptation in response to changing environments.
a FWA and FLC proteins inhibit flowering pathway genes by binding to their promoters or proteins. In the wild-type, FWA locus was methylated to suppress its activity. In the fwa mutant or epiallele induced by DDM1, FWA is demethylated to activate its expression, which represses floral pathway genes such as FT and FLC to inhibit flowering. Vernalization can induce long-noncoding RNAs like COOLAIR or COLDAIR in the first intron of FLC locus and H3K27me3 through polycomb-group2 (PRC2) protein complex, which coincides with repression of FLC to promote flowering. b In Arabidopsis suecica allotetraploids that were formed from A. thaliana and A. arenosa, AtFRI is silenced, while AaFRI is expressed. AaFRI trans-actives AtFLC expression, consistent with a wide range of flowering phenotypes in resynthesized and natural A. suecica. c In allotetraploid Upland cotton (Gossypium hirsutum, A2A2D5D5), CONSTANS-LIKE2 (COL2) has two homoeologs GhCOL2A and GhCOL2D. GhCOL2A promoter is heavily methylated and silenced, while GhCOLD2 is a reversible epiallele, which is methylated and repressed in wild relatives of G. hirsutum but demethylated and expressed in cultivated cotton to promote GhFT expression and photoperiodic flowering. This may contribute to worldwide cultivation of Upland cotton. Photos are not in scale.
Epialleles or epigenes can also result from cross-fertilization such as imprinting117,118 and polyploidy 25,26. In Arabidopsis intraspecific hybrids119,120 and allotetraploids121, expression waveforms of circadian clock genes such as CCA1 and LHY are altered by epigenetic and chromatin modifications to increase photosynthesis, chlorophyll biosynthesis, and starch metabolism121. The more starch accumulates during the day, the more it can be degraded at night to promote growth vigor, in a widespread phenomenon known as hybrid vigor or heterosis24,27. Stress-responsive gene expression is gated by the circadian clock122. Altered circadian gene expression in the hybrids also regulates expression of abiotic and biotic stress-responsive genes as a trade-off to balance the energy used for growth and defense119, as well as mediates ethylene biosynthesis that in turn regulates growth vigor123. Mechanistically, CCA1 expression changes are related to parent-of-origin effect on DNA methylation120, suggesting an epigenetic cause. Further analysis showed that circadian clock genes mediate diurnal regulation of histone H3K4 methylation reader and eraser genes, which in turn regulate rhythmic histone modification dynamics for the clock and its output genes124. This reciprocal regulatory module between chromatin modifiers and circadian clock oscillators orchestrates diurnal gene expression that governs plant growth and development.
All flowering plants are polyploids or of polyploid origin125,126, which result in genetic and epigenetic changes25,26. Duplication of flowering pathway genes in polyploids may increase the range of flowering time variation or induce other changes including epigenetic modifications and epistasis or trans-acting effects25,127,128. Natural variation of flowering time in Arabidopsis suecica allotetraploids is largely controlled by two epistatically acting loci, namely FRIGIDA (FRI) and FLC129,130. FRI upregulates FLC expression that represses flowering131. In Arabidopsis allotetraploids that are formed by pollinating A. arenosa with A. thaliana132,133, there are two sets of FLC and FRI genes and they flower late128. Inhibition of early flowering is caused by upregulation of A. thaliana FLC (AtFLC) that is trans-activated by A. arenosa FRI (AaFRI) (Fig. 5b). Two duplicate FLCs (AaFLC1 and AaFLC2) originating from A. arenosa are expressed in some allotetraploids but silenced in other lines. The expression variation of FLCs in the allotetraploids is associated with deletions in the promoter regions and first introns of A. arenosa FLCs. The strong AtFLC and AaFLC loci are maintained in natural Arabidopsis allotetraploids, leading to extremely late flowering128. Furthermore, FLC expression correlates positively with histone H3K4me2 and H3K9ac marks and negatively with the H3K9me2 mark. This combination of epistasis between loci and chromatin regulation within a locus may provide a complexity of flowering time variation in polyploid plants in response to environmental cues and adaptive niches.
Cotton allotetraploids were formed ~1–1.5 million years ago (Mya)134 (Fig. 5c), followed by natural diversification and crop domestication135. Polyploidization between an A-genome African species (Gossypium arboreum-like) and a D-genome American species (G. raimondii-like) in the New World created a new allotetraploid or amphidiploid (AD-genome) cotton clade134, which has diversified into five polyploid lineages, Gossypium hirsutum (Gh) (AD)1, G. barbadense (Gb) (AD)2, G. tomentosum (AD)3, G. mustelinum (AD)4, and G. darwinii (AD)5. Gossypium ekmanianum and G. stephensii are recently characterized and closely related to G. hirsutum136. Gh and Gb were separately domesticated from perennial shrubs to become annualized Upland and Pima cottons135.
Interspecific hybridization induces genome shock, including nonadditive gene expression and epigenetic changes in polyploid plants and crops133,137. The epigenetic changes produce epigenes or epialleles, which are selected during evolution and domestication. In allotetraploid cotton, over 500 epigenes have been identified and maintained over 600,000 years of genomic diversification, some of which are predicted to originate during polyploidization over 1–1.5 million years ago22. Many of these epigenes are related to domestication traits including flowering time, stress response, seed development, and seed dormancy.
Cotton, being originated in tropical and subtropical areas, flowers in short-day conditions138. Loss of photoperiod sensitivity is a major “domestication syndrome” trait139 of Upland or American cotton (G. hirsutum L.) and Pima or Egyptian cotton (G. barbadense L.) that accounts for >95% and ~5% of annual cotton crop worldwide, respectively140. This process is associated with cotton CO-liked (COL) genes, which are Arabidopsis CO homolog141. Among 23 COLs identified in cotton142, eight G. hirsutum COLs (GhCOLs) are in the same subgroup. Among them, only GhCOL2 exhibited similar expression rhythms with GhFT, indicating that GhCOL2 is a major regulator of GhFT.
Allotetraploid cotton has two COL2 homoeologs, GhCOL2A and GhCOL2D (Fig. 5c). COL2D is heavily methylated and silenced in G. raimondii that is photoperiod sensitive, while COL2A is hypomethylated and highly expressed in cultivated G. arboreum, which is photoperiod insensitive138. In allotetraploid cotton, the COL2A homoeolog was hypermethylated and repressed in cultivated Upland and Pima cottons, while the COL2D homoeolog was highly expressed. This suggests that COL2A in the allotetraploid cottons is likely silenced after polyploid formation since it is expressed in the extant G. arboreum species. The high-level expression of COL2D is likely associated with positive selection and loss of DNA methylation of COL2D during domestication of Upland and Pima cottons142, which could lead to the loss of photoperiod sensitivity for global cotton cultivation. Indeed, methylation levels of COL2D are lower and their expression levels are higher in cultivated and photoperiod-insensitive G. hirsutum and G. barbadense than in their photoperiod-sensitive wild relatives. Removal of DNA methylation in the wild G. hirsutum (TX2095) seedlings using 5’-aza-2’-deoxycytidine (5-aza-dC), a chemical inhibitor for DNA methylation143, activates COL2D expression. Moreover, using virus induced gene silencing (VIGS)144, GhCOL2 is down-regulated, which is consistent with the repression of GhFT. Down-regulating COL2 and GhFT expression has delayed flowering time for 9 days, compared to the control plants and wild cottons that do not flower in the LD conditions138. This example has demonstrated important roles of epigenes and epialleles in photoperiodic flowering during natural selection and crop domestication. These epigenes and epialleles can be candidate targets for gene-editing and biological breeding to improve crop production and resilience.
Concluding remarks
Growth, development, and reproduction during appropriate times of the year is essential for plants to adapt to seasonal changes. The photoperiodic response to flowering is a key mechanism for plants to optimize utilization of natural resources, adapt crop varieties in regional environments, and significantly impact crop yield stability and potential. Insights gained from studying the interplay between light signaling, the circadian clock, and photoperiodism in the model plant Arabidopsis have facilitated the discovery of complex molecular circuitry networks underlying photoperiodic flowering pathways in both short- and long-day crops, many of which are polyploids and have genomic redundancy that is subject to epigenetic modifications. Indeed, some key regulators, including circadian clock genes, are epigenetically regulated, presumably resulting from natural selection, crop domestication, and/or modern breeding.
Genome sequencing and genome-wide association studies in crop plants have supported that allele variants of several key circadian genes have been selected by breeding and under agricultural culture of adapting crop flowering time to certain seasons. While most current studies are focused on light and circadian control of photoperiodic flowering, temperature changes can drastically affect plant flowering and have been grossly under-investigated. Further investigations are needed to maintain agricultural and ecological sustainability in response to changes in extreme weather and climate such as drought, heat, and flood.
There are good examples of the genes in the circadian clock and photoperiodic flowering pathways that are associated with agronomic traits in crops. Rice Hd177, an ortholog of the Arabidopsis CO, controls expression of two florigen genes Hd3a and RFT174,75,76 during the floral transition. ZmCCT9 in maize is diurnally regulated and negatively regulates the expression of the florigen ZCN8 through a CACTA-like TE insertion in ZmCCT promoter region145, resulting in reduction of photoperiod sensitivity, thus accelerating maize spread to long-day environments146. The circadian clock of cultivated tomatoes has slowed during domestication. EMPFINDLICHER IM DUNKELROTEN LICHT1 (EID1) is an F-box protein that targets phytochrome A for degradation in Arabidopsis147. The EID1 allele in cultivated tomatoes is under selection sweep and enhances plant performance under long-day photoperiods presumably resulting from moving away from the equator148. Fruit yield in hybrid tomato is related to SINGLE FLOWER TRUSS (SFT)149, a homolog of FT in Arabidopsis. Moreover, epigenetic alteration of circadian clock genes including CCA1 and LHY in plant hybrids are related to growth vigor in Arabidopsis119,120,121 and maize72,150. In cotton, GhCOL2 is an epiallele, which may be selected during domestication to increase its expression and thereby reduce photoperiod sensitivity, helping spread worldwide cotton cultivation22. These examples will help us design strategies to optimize circadian input and output signals and improve flowering time and crop yield using genome-editing tools. Likewise, discovery and utilization of new epigenes and epialleles in combination of targeted-gene editing will improve flowering time and crop yield and resilience.
References
Xu, X. et al. Circadian clock in plants: linking timing to fitness. J. Integr. Plant Biol. 64, 792–811 (2022).
Imaizumi, T. Arabidopsis circadian clock and photoperiodism: time to think about location. Curr. Opin. Plant Biol. 13, 83–89 (2010).
Searle, I. & Coupland, G. Induction of flowering by seasonal changes in photoperiod. EMBO J. 23, 1217–1222 (2004).
Hayama, R. & Coupland, G. Shedding light on the circadian clock and the photoperiodic control of flowering. Curr. Opin. Plant Biol. 6, 13–19 (2003).
Srikanth, A. & Schmid, M. Regulation of flowering time: all roads lead to Rome. Cell Mol. Life Sci. 68, 2013–2037 (2011).
Kobayashi, Y. & Weigel, D. Move on up, it’s time for change-mobile signals controlling photoperiod-dependent flowering. Genes Dev. 21, 2371–2384 (2007).
Hendricks, S. B. Rates of change of phytochrome as an essential factor determining photoperiodism in plants. Cold Spring Harb. Symp. Quant. Biol. 25, 245–248 (1960).
Song, Y. H., Shim, J. S., Kinmonth-Schultz, H. A. & Imaizumi, T. Photoperiodic flowering: time measurement mechanisms in leaves. Annu Rev. Plant Biol. 66, 441–464 (2015).
Thomas, B. & Vince-Prue, D. Photoperiodism in Plants, (Academic Press, San Diego, California, 1997).
Pittendrigh, C.S. The circadian oscillation in Drosophila pseudoobscura pupae: a model for the photoperiodic clock. Z. Pflanzenphysiol. 54, 275–307 (1966).
Bünning, E. Die endonome Tagesrhythmik als Grundlage der photoperiodischen Reaktion. Ber. dtsch. bot. Ges. 54, 590–607 (1936).
Edgar, R. S. et al. Peroxiredoxins are conserved markers of circadian rhythms. Nature 485, 459–464 (2012).
Yanovsky, M. J. & Kay, S. A. Molecular basis of seasonal time measurement in Arabidopsis. Nature 419, 308–312 (2002).
Valverde, F. et al. Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. Science 303, 1003–1006 (2004).
Gil, K. E. & Park, C. M. Thermal adaptation and plasticity of the plant circadian clock. N. Phytol. 221, 1215–1229 (2019).
Kakutani, T. Genetic characterization of late-flowering traits induced by DNA hypomethylation mutation in Arabidopsis thaliana. Plant J. 12, 1447–1451 (1997).
Soppe, W. J. et al. The late flowering phenotype of fwa mutants is caused by gain-of-function epigenetic alleles of a homeodomain gene. Mol. Cell 6, 791–802 (2000).
Finnegan, J. E. et al. The downregulation of FLOWERING LOCUS C (FLC) expression in plants with low levels of DNA methylation and by vernalization occurs by distinct mechanisms. Plant J. 44, 420–432 (2005).
Bastow, R. et al. Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427, 164–167 (2004).
Crevillen, P. et al. Epigenetic reprogramming that prevents transgenerational inheritance of the vernalized state. Nature 515, 587–590 (2014).
Sung, S. & Amasino, R. M. Vernalization and epigenetics: how plants remember winter. Curr. Opin. Plant Biol. 7, 4–10 (2004).
Song, Q., Zhang, T., Stelly, D. M. & Chen, Z. J. Epigenomic and functional analyses reveal roles of epialleles in the loss of photoperiod sensitivity during domestication of allotetraploid cottons. Genome Biol. 18, 99 (2017).
Chen, Z. J. & Mas, P. Interactive roles of chromatin regulation and circadian clock function in plants. Genome Biol. 20, 62 (2019).
Chen, Z. J. Genomic and epigenetic insights into the molecular bases of heterosis. Nat. Rev. Genet 14, 471–482 (2013).
Chen, Z. J. Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annu. Rev. Plant Biol. 58, 377–406 (2007).
Chen, Z. J. Molecular mechanisms of polyploidy and hybrid vigor. Trends Plant Sci. 15, 57–71 (2010).
Chen, Z. J. & Birchler, J. A. Polyploid and Hybrid Genomics, 363 (Wiley-Blackwell, New York, 2013).
Wang, Z. Y. & Tobin, E. M. Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression. Cell 93, 1207–1217 (1998).
Mizoguchi, T. et al. LHY and CCA1 are partially redundant genes required to maintain circadian rhythms in Arabidopsis. Dev. Cell 2, 629–641 (2002).
Huang, W. et al. Mapping the core of the Arabidopsis circadian clock defines the network structure of the oscillator. Science 336, 75–79 (2012).
Pruneda-Paz, J. L., Breton, G., Para, A. & Kay, S. A. A functional genomics approach reveals CHE as a component of the Arabidopsis circadian clock. Science 323, 1481–1485 (2009).
Nakamichi, N. et al. PSEUDO-RESPONSE REGULATORS 9, 7, and 5 are transcriptional repressors in the Arabidopsis circadian clock. Plant Cell 22, 594–605 (2010).
Nusinow, D. A. et al. The ELF4-ELF3-LUX complex links the circadian clock to diurnal control of hypocotyl growth. Nature 475, 398–402 (2011).
Kamioka, M. et al. Direct repression of evening genes by CIRCADIAN CLOCK-ASSOCIATED1 in the Arabidopsis circadian clock. Plant Cell 28, 696–711 (2016).
Lu, S. X. et al. CCA1 and ELF3 Interact in the control of hypocotyl length and flowering time in Arabidopsis. Plant Physiol. 158, 1079–1088 (2012).
Farre, E. M., Harmer, S. L., Harmon, F. G., Yanovsky, M. J. & Kay, S. A. Overlapping and distinct roles of PRR7 and PRR9 in the Arabidopsis circadian clock. Curr. Biol. 15, 47–54 (2005).
Herrero, E. & Davis, S. J. Time for a nuclear meeting: protein trafficking and chromatin dynamics intersect in the plant circadian system. Mol. Plant 5, 554–565 (2012).
Martin-Tryon, E. L., Kreps, J. A. & Harmer, S. L. GIGANTEA acts in blue light signaling and has biochemically separable roles in circadian clock and flowering time regulation. Plant Physiol. 143, 473–486 (2007).
Mizoguchi, T. et al. Distinct roles of GIGANTEA in promoting flowering and regulating circadian rhythms in Arabidopsis. Plant Cell 17, 2255–2270 (2005).
Mas, P., Alabadi, D., Yanovsky, M. J., Oyama, T. & Kay, S. A. Dual role of TOC1 in the control of circadian and photomorphogenic responses in Arabidopsis. Plant Cell 15, 223–236 (2003).
Kiba, T., Henriques, R., Sakakibara, H. & Chua, N. H. Targeted degradation of PSEUDO-RESPONSE REGULATOR5 by an SCFZTL complex regulates clock function and photomorphogenesis in Arabidopsis thaliana. Plant Cell 19, 2516–2530 (2007).
Wu, J. F., Wang, Y. & Wu, S. H. Two new clock proteins, LWD1 and LWD2, regulate Arabidopsis photoperiodic flowering. Plant Physiol. 148, 948–959 (2008).
Nohales, M. A. & Kay, S. A. Molecular mechanisms at the core of the plant circadian oscillator. Nat. Struct. Mol. Biol. 23, 1061–1069 (2016).
Wu, J. F. et al. LWD-TCP complex activates the morning gene CCA1 in Arabidopsis. Nat. Commun. 7, 13181 (2016).
Rawat, R. et al. REVEILLE8 and PSEUDO-REPONSE REGULATOR5 form a negative feedback loop within the Arabidopsis circadian clock. PLoS Genet. 7, e1001350 (2011).
Farinas, B. & Mas, P. Functional implication of the MYB transcription factor RVE8/LCL5 in the circadian control of histone acetylation. Plant J. 66, 318–329 (2011).
Xie, Q. et al. LNK1 and LNK2 are transcriptional coactivators in the Arabidopsis circadian oscillator. Plant Cell 26, 2843–2857 (2014).
Suarez-Lopez, P. et al. CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 410, 1116–1120 (2001).
Imaizumi, T., Schultz, T. F., Harmon, F. G., Ho, L. A. & Kay, S. A. FKF1 F-box protein mediates cyclic degradation of a repressor of CONSTANS in Arabidopsis. Science 309, 293–297 (2005).
Sawa, M., Nusinow, D. A., Kay, S. A. & Imaizumi, T. salaFKF1 and GIGANTEA Complex Formation is Required for Day-Length Measurement in Arabidopsis. Science 318, 261–265 (2007).
Andres, F. & Coupland, G. The genetic basis of flowering responses to seasonal cues. Nat. Rev. Genet. 13, 627–639 (2012).
Rosas, U. et al. Variation in Arabidopsis flowering time associated with cis-regulatory variation in CONSTANS. Nat. Commun. 5, 3651 (2014).
Nakamichi, N. et al. Arabidopsis clock-associated pseudo-response regulators PRR9, PRR7 and PRR5 coordinately and positively regulate flowering time through the canonical CONSTANS-dependent photoperiodic pathway. Plant Cell Physiol. 48, 822–832 (2007).
Seaton, D. D. et al. Linked circadian outputs control elongation growth and flowering in response to photoperiod and temperature. Mol. Syst. Biol. 11, 776 (2015).
Nakamichi, N. et al. Transcriptional repressor PRR5 directly regulates clock-output pathways. Proc. Natl Acad. Sci. USA 109, 17123–17128 (2012).
Niwa, R. & Slack, F. J. The evolution of animal microRNA function. Curr. Opin. Genet. Dev. 17, 145–150 (2007).
Kwon, E. et al. Structural analysis of the regulation of blue-light receptors by GIGANTEA. Cell Rep. 39, 110700 (2022).
Salazar, J. D. et al. Prediction of photoperiodic regulators from quantitative gene circuit models. Cell 139, 1170–1179 (2009).
Fornara, F. et al. Arabidopsis DOF transcription factors act redundantly to reduce CONSTANS expression and are essential for a photoperiodic flowering response. Dev. Cell 17, 75–86 (2009).
Somers, D. E., Kim, W. Y. & Geng, R. The F-box protein ZEITLUPE confers dosage-dependent control on the circadian clock, photomorphogenesis, and flowering time. Plant Cell 16, 769–782 (2004).
Takase, T. et al. LOV KELCH PROTEIN2 and ZEITLUPE repress Arabidopsis photoperiodic flowering under non-inductive conditions, dependent on FLAVIN-BINDING KELCH REPEAT F-BOX1. Plant J. 67, 608–621 (2011).
Lazaro, A., Valverde, F., Pineiro, M. & Jarillo, J. A. The Arabidopsis E3 ubiquitin ligase HOS1 negatively regulates CONSTANS abundance in the photoperiodic control of flowering. Plant Cell 24, 982–999 (2012).
Chamovitz, D. A. et al. The COP9 complex, a novel multisubunit nuclear regulator involved in light control of a plant developmental switch. Cell 86, 115–121 (1996).
Jang, S. et al. Arabidopsis COP1 shapes the temporal pattern of CO accumulation conferring a photoperiodic flowering response. EMBO J. 27, 1277–1288 (2008).
Seo, H. S. et al. LAF1 ubiquitination by COP1 controls photomorphogenesis and is stimulated by SPA1. Nature 423, 995–999 (2003).
Serrano-Bueno, G. et al. CONSTANS-FKBP12 interaction contributes to modulation of photoperiodic flowering in Arabidopsis. Plant J. 101, 1287–1302 (2020).
Lian, H. L. et al. Blue-light-dependent interaction of cryptochrome 1 with SPA1 defines a dynamic signaling mechanism. Genes Dev. 25, 1023–1028 (2011).
Cerdan, P. D. & Chory, J. Regulation of flowering time by light quality. Nature 423, 881–885 (2003).
Turck, F., Fornara, F. & Coupland, G. Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. Annu. Rev. Plant Biol. 59, 573–594 (2008).
Wang, F. et al. The rice circadian clock regulates tiller growth and panicle development through strigolactone signaling and sugar sensing. Plant Cell 32, 3124–3138 (2020).
Murakami, M., Ashikari, M., Miura, K., Yamashino, T. & Mizuno, T. The evolutionarily conserved OsPRR quintet: rice pseudo-response regulators implicated in circadian rhythm. Plant Cell Physiol. 44, 1229–1236 (2003).
Ko, D. K. et al. Temporal shift of circadian-mediated gene expression and carbon fixation contributes to biomass heterosis in maize hybrids. PLoS Genet. 12, e1006197 (2016).
Miwa, K., Serikawa, M., Suzuki, S., Kondo, T. & Oyama, T. Conserved expression profiles of circadian clock-related genes in two lemna species showing long-day and short-day photoperiodic flowering responses. Plant Cell Physiol. 47, 601–612 (2006).
Tsuji, H., Taoka, K. I. & Shimamoto, K. Regulation of flowering in rice: two florigen genes, a complex gene network, and natural variation. Curr. Opin. Plant Biol. 14, 45–52 (2010).
Tamaki, S., Matsuo, S., Wong, H. L., Yokoi, S. & Shimamoto, K. Hd3a protein is a mobile flowering signal in rice. Science 316, 1033–1036 (2007).
Komiya, R., Ikegami, A., Tamaki, S., Yokoi, S. & Shimamoto, K. Hd3a and RFT1 are essential for flowering in rice. Development 135, 767–774 (2008).
Yano, M. et al. Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell 12, 2473–2484 (2000).
Doi, K. et al. Ehd1, a B-type response regulator in rice, confers short-day promotion of flowering and controls FT-like gene expression independently of Hd1. Genes Dev. 18, 926–936 (2004).
Hayama, R., Yokoi, S., Tamaki, S., Yano, M. & Shimamoto, K. Adaptation of photoperiodic control pathways produces short-day flowering in rice. Nature 422, 719–722 (2003).
Izawa, T. et al. Os-GIGANTEA confers robust diurnal rhythms on the global transcriptome of rice in the field. Plant Cell 23, 1741–1755 (2011).
Takano, M. et al. Distinct and cooperative functions of phytochromes A, B, and C in the control of deetiolation and flowering in rice. Plant Cell 17, 3311–3325 (2005).
Ishikawa, R. et al. Phytochrome B regulates Heading date 1 (Hd1)-mediated expression of rice florigen Hd3a and critical day length in rice. Mol. Genet. Genomics 285, 461–470 (2011).
Xue, W. et al. Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat. Genet. 40, 761–767 (2008).
Itoh, H., Nonoue, Y., Yano, M. & Izawa, T. A pair of floral regulators sets critical day length for Hd3a florigen expression in rice. Nat. Genet. 42, 635–638 (2010).
Osugi, A., Itoh, H., Ikeda-Kawakatsu, K., Takano, M. & Izawa, T. Molecular dissection of the roles of phytochrome in photoperiodic flowering in rice. Plant Physiol. 157, 1128–1137 (2011).
Du, A. et al. The DTH8-Hd1 module mediates day-length-dependent regulation of rice flowering. Mol. Plant 10, 948–961 (2017).
Wei, X. et al. DTH8 suppresses flowering in rice, influencing plant height and yield potential simultaneously. Plant Physiol. 153, 1747–1758 (2010).
Zhu, S. et al. The OsHAPL1-DTH8-Hd1 complex functions as the transcription regulator to repress heading date in rice. J. Exp. Bot. 68, 553–568 (2017).
Nemoto, Y., Nonoue, Y., Yano, M. & Izawa, T. Hd1,a CONSTANS ortholog in rice, functions as an Ehd1 repressor through interaction with monocot-specific CCT-domain protein Ghd7. Plant J. 86, 221–233 (2016).
Murphy, R. L. et al. Coincident light and clock regulation of pseudoresponse regulator protein 37 (PRR37) controls photoperiodic flowering in sorghum. Proc. Natl Acad. Sci. USA 108, 16469–16474 (2011).
Gao, H. et al. Days to heading 7, a major quantitative locus determining photoperiod sensitivity and regional adaptation in rice. Proc. Natl Acad. Sci. USA 111, 16337–16342 (2014).
Goretti, D. et al. Transcriptional and post-transcriptional mechanisms limit heading date 1 (Hd1) function to adapt rice to high latitudes. PLoS Genet. 13, e1006530 (2017).
Fujino, K., Yamanouchi, U., Nonoue, Y., Obara, M. & Yano, M. Switching genetic effects of the flowering time gene Hd1 in LD conditions by Ghd7 and OsPRR37 in rice. Breed. Sci. 69, 127–132 (2019).
Wang, X. L., He, Y. Q., Wei, H. & Wang, L. A clock regulatory module is required for salt tolerance and control of heading date in rice. Plant Cell Environ. 44, 3283–3301 (2021).
Andrade, L. et al. The evening complex integrates photoperiod signals to control flowering in rice. Proc. Natl Acad. Sci. USA 119, e2122582119 (2022).
Schmutz, J. et al. Genome sequence of the palaeopolyploid soybean. Nature 463, 178–183 (2010).
Kong, F. et al. Two coordinately regulated homologs of FLOWERING LOCUS T are involved in the control of photoperiodic flowering in soybean. Plant Physiol. 154, 1220–1231 (2010).
Zhai, H. et al. GmFT4, a homolog of FLOWERING LOCUS T, is positively regulated by E1 and functions as a flowering repressor in soybean. PLoS One 9, e89030 (2014).
Liu, W. et al. Functional diversification of Flowering Locus T homologs in soybean: GmFT1a and GmFT2a/5a have opposite roles in controlling flowering and maturation. New Phytol. 217, 1335–1345 (2018).
Wu, F., Sedivy, E. J., Price, W. B., Haider, W. & Hanzawa, Y. Evolutionary trajectories of duplicated FT homologues and their roles in soybean domestication. Plant J. 90, 941–953 (2017).
Watanabe, S. et al. A map-based cloning strategy employing a residual heterozygous line reveals that the GIGANTEA gene is involved in soybean maturity and flowering. Genetics 188, 395–407 (2011).
Yang, S., Weers, B. D., Morishige, D. T. & Mullet, J. E. CONSTANS is a photoperiod regulated activator of flowering in sorghum. BMC Plant Biol. 14, 148 (2014).
Cao, D. et al. GmCOL1a and GmCOL1b function as flowering repressors in soybean under long-day conditions. Plant Cell Physiol. 56, 2409–2422 (2015).
Awal Khan, M. A. et al. CONSTANS polymorphism modulates flowering time and maturity in soybean. Front. Plant Sci. 13, 817544 (2022).
Lu, S. et al. Stepwise selection on homeologous PRR genes controlling flowering and maturity during soybean domestication. Nat. Genet 52, 428–436 (2020).
Li, C. et al. A domestication-associated gene GmPRR3b regulates the circadian clock and flowering time in soybean. Mol. Plant 13, 745–759 (2020).
Li, F. et al. Identification and molecular characterization of FKF1 and GI homologous genes in soybean. PLoS One 8, e79036 (2013).
Fang, X. et al. Modulation of evening complex activity enables north-to-south adaptation of soybean. Sci. China Life Sci. 64, 179–195 (2021).
Liu, B. et al. Genetic redundancy in soybean photoresponses associated with duplication of the phytochrome A gene. Genetics 180, 995–1007 (2008).
Watanabe, S. et al. Map-based cloning of the gene associated with the soybean maturity locus E3. Genetics 182, 1251–1262 (2009).
Zhang, Q. et al. Association of the circadian rhythmic expression of GmCRY1a with a latitudinal cline in photoperiodic flowering of soybean. Proc. Natl Acad. Sci. USA 105, 21028–21033 (2008).
Whittaker, C. & Dean, C. The FLC locus: a platform for discoveries in epigenetics and adaptation. Annu. Rev. Cell Dev. Biol. 33, 555–575 (2017).
Swiezewski, S., Liu, F., Magusin, A. & Dean, C. Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target. Nature 462, 799–802 (2009).
Heo, J. B. & Sung, S. Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331, 76–79 (2011).
Jeon, M. et al. Vernalization-triggered expression of the antisense transcript COOLAIR is mediated by CBF genes. Elife 12, e84594 (2023).
Ikeda, Y., Kobayashi, Y., Yamaguchi, A., Abe, M. & Araki, T. Molecular basis of late-flowering phenotype caused by dominant epi-alleles of the FWA locus in Arabidopsis. Plant Cell Physiol. 48, 205–220 (2007).
Ferguson-Smith, A. C. Genomic imprinting: the emergence of an epigenetic paradigm. Nat. Rev. Genet. 12, 565–575 (2011).
Reik, W., Collick, A., Norris, M. L., Barton, S. C. & Surani, M. A. Genomic imprinting determines methylation of parental alleles in transgenic mice. Nature 328, 248–251 (1987).
Miller, M., Song, Q., Shi, X., Juenger, T. E. & Chen, Z. J. Natural variation in timing of stress-responsive gene expression predicts heterosis in intraspecific hybrids of Arabidopsis. Nat. Commun. 6, 7453 (2015).
Ng, D. W. et al. A role for CHH methylation in the parent-of-origin effect on altered circadian rhythms and biomass heterosis in Arabidopsis intraspecific hybrids. Plant Cell 26, 2430–2440 (2014).
Ni, Z. et al. Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids. Nature 457, 327–331 (2009).
Fowler, S. G., Cook, D. & Thomashow, M. F. Low temperature induction of Arabidopsis CBF1, 2, and 3 is gated by the circadian clock. Plant Physiol. 137, 961–968 (2005).
Song, Q. et al. Diurnal down-regulation of ethylene biosynthesis mediates biomass heterosis. Proc. Natl Acad. Sci. USA 115, 5606–5611 (2018).
Song, Q. et al. Diurnal regulation of SDG2 and JMJ14 by circadian clock oscillators orchestrates histone modification rhythms in Arabidopsis. Genome Biol. 20, 170 (2019).
Jiao, Y. et al. Ancestral polyploidy in seed plants and angiosperms. Nature 473, 97–100 (2011).
Soltis, D. E., Visger, C. J. & Soltis, P. S. The polyploidy revolution then…and now: Stebbins revisited. Am. J. Bot. 101, 1057–1078 (2014).
Mayfield, D., Chen, Z. J. & Pires, J. C. Epigenetic regulation of flowering time in polyploids. Curr. Opin. Plant Biol. 14, 174–178 (2011).
Wang, J., Tian, L., Lee, H. S. & Chen, Z. J. Nonadditive regulation of FRI and FLC loci mediates flowering-time variation in Arabidopsis allopolyploids. Genetics 173, 965–974 (2006).
He, Y. & Amasino, R. M. Role of chromatin modification in flowering-time control. Trends Plant Sci. 10, 30–35 (2005).
Simpson, G. G. & Dean, C. Arabidopsis, the Rosetta stone of flowering time? Science 296, 285–289 (2002).
Johanson, U. et al. Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290, 344–347 (2000).
Comai, L. et al. Phenotypic instability and rapid gene silencing in newly formed Arabidopsis allotetraploids. Plant Cell 12, 1551–1568 (2000).
Wang, J. et al. Genomewide nonadditive gene regulation in Arabidopsis allotetraploids. Genetics 172, 507–517 (2006).
Wendel, J. F. & Grover, C. E. Taxonomy and Evolution of the Cotton Genus, Gossypium. in Cotton 2nd Edition, Vol. 57 (eds Fang, D. D. & Percy, R. G.) 25–44 (Madison, WI, 2015).
Splitstoser, J. C., Dillehay, T. D., Wouters, J. & Claro, A. Early pre-Hispanic use of indigo blue in Peru. Sci. Adv. 2, e1501623 (2016).
Grover, C. E. et al. Re-evaluating the phylogeny of allopolyploid Gossypium L. Mol. Phylogenet Evol. 92, 45–52 (2015).
Li, Z. & Chen, Z. J. Nonadditive gene expression and epigenetic changes in polyploid plants and crops. Adv. Agron. 176, 179–208 (2022).
Percival, A. E., Wendel, J. F. & Stewart, J. M. Taxonomy and germplasm resources. in Cotton: Origin, History, Technology, and Production (eds Smith, C. W. & Cothren, J. T.) 33–63 (John Wiley & Sons, Inc., New York, 1999).
Olsen, K. M. & Wendel, J. F. A bountiful harvest: genomic insights into crop domestication phenotypes. Annu. Rev. Plant Biol. 64, 47–70 (2013).
Chen, Z. J. et al. Toward sequencing cotton (Gossypium) genomes. Plant Physiol. 145, 1303–1310 (2007).
Putterill, J., Robson, F., Lee, K., Simon, R. & Coupland, G. The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell 80, 847–857 (1995).
Zhang, R. et al. Molecular evolution and phylogenetic analysis of eight COL superfamily genes in group I related to photoperiodic regulation of flowering time in wild and domesticated cotton (Gossypium) species. PLoS One 10, e0118669 (2015).
Haaf, T., Werner, P. & Schmid, M. 5-Azadeoxycytidine distinguishes between active and inactive X chromosome condensation. Cytogenetics Cell Genet. 63, 160–168 (1993).
Gao, X. et al. Silencing GhNDR1 and GhMKK2 compromises cotton resistance to Verticillium wilt. Plant J. 66, 293–305 (2011).
Yang, Q. et al. CACTA-like transposable element in ZmCCT attenuated photoperiod sensitivity and accelerated the postdomestication spread of maize. Proc. Natl Acad. Sci. USA 110, 16969–16974 (2013).
Huang, C. et al. ZmCCT9 enhances maize adaptation to higher latitudes. Proc. Natl Acad. Sci. USA 115, E334–E341 (2018).
Marrocco, K. et al. Functional analysis of EID1, an F-box protein involved in phytochrome A-dependent light signal transduction. Plant J. 45, 423–438 (2006).
Muller, N. A. et al. Domestication selected for deceleration of the circadian clock in cultivated tomato. Nat. Genet. 48, 89–93 (2016).
Krieger, U., Lippman, Z. B. & Zamir, D. The flowering gene SINGLE FLOWER TRUSS drives heterosis for yield in tomato. Nat. Genet. 42, 459–463 (2010).
Li, Z. et al. Temporal regulation of the metabolome and proteome in photosynthetic and photorespiratory pathways contributes to maize heterosis. Plant Cell 32, 3706–3722 (2020).
Acknowledgements
This work was supported in part by National Natural Science Foundation of China (32200264, F.W.), National Natural Science Foundation of Shandong (ZR2022QC050, F.W.), Taishan Scholar Project of Shandong Province of China (tsqn202211101, T.H.), National Institute of General Medical Sciences (GM109076, Z.J.C.), National Science Foundation (ISO1238048 and IOS1739092, Z.J.C.), a Stengl-Wyer Endowment Research Grant (2022–2024, Z.J.C.), and the Winkler Fellowship (2024–2025, Z.J.C.).
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Wang, F., Han, T. & Jeffrey Chen, Z. Circadian and photoperiodic regulation of the vegetative to reproductive transition in plants. Commun Biol 7, 579 (2024). https://doi.org/10.1038/s42003-024-06275-6
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DOI: https://doi.org/10.1038/s42003-024-06275-6
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