Journal of Experimental Botany, Vol. 76, No. 3 pp.

851–872, 2025
https://doi.org/10.1093/jxb/erae471 Advance Access Publication 22 November 2024

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REVIEW PAPER

Photoperiodic control of growth and reproduction in non-

flowering plants
Durga Prasad Biswal1,2,3, and Kishore Chandra Sekhar Panigrahi1,2,*,
1
School of Biological Sciences, National Institute of Science Education and Research (NISER), Bhubaneswar, Odisha, India
2
Homi Bhabha National Institute (HBNI), Training School Complex, Anushakti Nagar, Mumbai, 400094, India
3
Department of Botany, S.K.C.G. (Autonomous) College, Paralakhemundi, Gajapati, 761200, Odisha, India
* Correspondence: panigrahi@niser.ac.in

Received 30 April 2024; Editorial decision 15 November 2024; Accepted 21 November 2024

Editor: Sourav Datta, Indian Institute of Science Education and Research, India

Abstract
Photoperiodic responses shape plant fitness to the changing environment and are important regulators of growth,
development, and productivity. Photoperiod sensing is one of the most important cues to track seasonal variations.
It is also a major cue for reproductive success. The photoperiodic information conveyed through the combined ac-
tion of photoreceptors and the circadian clock orchestrates an output response in plants. Multiple responses such as
hypocotyl elongation, induction of dormancy, and flowering are photoperiodically regulated in seed plants (eg. angio-
sperms). Flowering plants such as Arabidopsis or rice have served as important model systems to understand the
molecular players involved in photoperiodic signalling. However, photoperiodic responses in non-angiosperm plants
have not been investigated and documented in detail. Genomic and transcriptomic studies have provided evidence
on the conserved and distinct molecular mechanisms across the plant kingdom. In this review, we have attempted to
compile and compare photoperiodic responses in the plant kingdom with a special focus on non-angiosperms.

Keywords: Algae, angiosperm, bryophyte, circadian rhythm, fern, gymnosperm, lycophyte, photoperiod.

Introduction
In their natural habitat, plants are forced to experience con- direction, and duration. Among these parameters, the dura-
stant fluctuations in the environment. Since they are immo- tion of light or day length is an important factor affecting the
bile in nature, plants have to face and respond to biotic and phenology of plants. The intensity and duration of sunlight
abiotic challenges in situ. Unlike animals, they cannot escape establishe an environmental gradient; a parameter for seasonal
unfavourable situations. Light is one of the most essential abi- variation, and thereby act as major determinants of plant com-
otic factors required for the growth and development of plants. munity in a region. Photosynthetic eukaryotes have evolved
Sunlight is the primary source of energy for photosynthesis with the ability to perceive day length through an endoge-
and drives many metabolic activities in the plants. In the nat- nous circadian clock. The circadian clock is an endogenous
ural environment, the intensity of light fluctuates to a great timekeeping mechanism, which regulates the phase, period,
extent throughout the day as well as on a seasonal basis. The and amplitude of output gene expression (Harmer, 2009; Song
availability of sunlight may vary in terms of quality, quantity, et al., 2010; Greenham and McClung, 2015; Serrano-Bueno

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852 | Biswal and Panigrahi

et al., 2017). The components of the circadian clock track to perturbations such as night-breaks. SD plants respond even
the day length or photoperiod and influence the response of to a brief pulse of light in the middle of the dark period and

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plants to the photoperiod. The ability of plants to respond to thus show LD behaviour. However, in some cases, the classical
photoperiod is known as photoperiodism. This phenomenon night-break cues may not inhibit the SD responses. This does
was first described by Garner and Allard (1920) in tobacco not imply that the SD response is non-photoperiodic.The sen-
plants. Later this was demonstrated in various other plants sitivity to night-break may vary among plants and may also be
such as Irish potato, Jerusalem artichoke, yam, Oenothera bien- governed by other factors such as temperature (Vince-Prue,
nis, Cosmos, and Sorghum (Kellerman, 1926; Redington, 1929). 1975, 1994; Terry and Moss, 1980).
The regulation of photoperiodism by the circadian clock was
observed by Bünning (1969). In subsequent years, photoperi-
odic responses have also been studied extensively in different Photoperiodic response pathway
plants (Imaizumi and Kay, 2006; Jackson, 2009; Lagercrantz,
There are three fundamental processes in photoperiodic
2009; Song et al., 2010; Engelmann, 2015). However, most of
responses: (i) perception of light; (ii) measurement of the du-
these studies are focused on flowering plants. In recent years,
ration of light; and (iii) subsequent output responses. While
attempts have been made to understand the molecular basis of
photoreceptors primarily sense the light, the circadian clock
photoperiod sensing (Linde et al., 2017; Serrano-Bueno et al.,
predominantly senses the duration of light. Finally, the light-
2017). Photoperiodic responses have also been demonstrated
regulated responses require different downstream components
in various non-flowering plants. However, these pieces of scat-
for the occurrence and regulation of a photoperiodic response.
tered information are probably not helpful to establish the role
of photoperiodism in plants from an evolutionary perspective.
This review is an attempt to understand the photoperiodic re- Photoreceptors: the light sensors
sponse and its molecular basis across the plant kingdom, with a
special focus on non-angiosperms. The spectrum of sunlight is made up of a mixture of different
wavelengths. However, plants require and sense specific com-
ponents of the spectrum such as blue light (BL), red light (RL),
far-red light (FR), and ultraviolet (UV) light for their growth
Photomorphogenic versus circadian versus
and development. While BL is perceived by photoreceptors
photoperiodic responses such as cryptochromes (CRYs), phototropins (PHOTs), and
The light-mediated responses of plants vary depending on ZEITLUPE (ZTL) proteins, RL is sensed by phytochromes
the environmental condition and developmental requirement. (PHYs). UV resistance locus 8 (UVR8) proteins sense UV-B
They can be categorized into three broad classes: (i) photo- light. These photoreceptors sense the quality, quantity, and di-
morphogenic; (ii) circadian; and (iii) photoperiodic responses. rection of light, and regulate different photomorphogenic
Plants adjust their growth and development in response responses such as flowering, circadian rhythm, shade avoidance,
to light signals (photomorphogenesis). Light-triggered de- and phototropism (Galvão and Fankhauser, 2015).
etiolation is a major physiological phenomenon that induces
the formation of a seedling from a seed. These responses are
Circadian clock components: sensors of photoperiod
dependent on the quantity, quality, or direction of light, along
with a long list of abiotic and biotic factors. While photoreceptors sense the spectral quality, the circadian
In turn, circadian responses are anticipatory mechanisms, clock senses the photoperiod and any variation in its dura-
rhythmic/recurring events of plant life, that occur in a peri- tion. The components of the circadian clock regulate the daily
odic manner when entrained in a light–dark cycle of 24 h. rhythmic responses, which are generally day length inde-
These responses are sensitive to the dark-to-light or light-to- pendent, but may affect the output of photoperiodic response.
dark transitions and generally maintain the rhythmicity in the In Arabidopsis thaliana, the circadian clock is regulated by
free-running conditions of constant light (LL) or constant dark a network of three interlocked feedback loops, namely the
(DD). The circadian clock regulates many physiological pro- morning loop, central loop, and evening loop (Pokhilko
cesses such as the cell cycle, flowering, stomatal opening, petal et al., 2012; McClung, 2014; Linde et al., 2017; Serrano-
opening, photosynthesis, leaf movement, hormonal signalling, Bueno et al., 2017; Shalit-Kaneh et al., 2018). The morning
metabolism, and stress responses (Sanchez and Kay, 2016; Inoue loop comprises two MYB-like transcription factor (TF) genes,
et al., 2018). CIRCADIAN CLOCK-ASSOCIATED 1 (CCA1) and
In contrast, photoperiodic responses are strictly day length- LATE ELONGATED HYPOCOTYL (LHY), and members
dependent processes. Plants are classified as either long-day of PSEUDO-RESPONSE REGULATOR (PRR) 5, 7, and
(LD), short-day (SD), or day-neutral species depending on the 9. CCA1 and LHY are members of the REVEILLE (RVE)
critical light period required for flowering (Garner and Allard, family of MYB TFs and show peak expression in the early
1920). In general, true photoperiodic responses are sensitive morning (Rawat et al., 2011). They repress the expression of
 Photoperiod-mediated development in non-flowering plants | 853

several day- and evening-phased genes (which includes both The coordinated and integrated signalling of photoreceptors
core clock and output genes) by binding to a specific motif and circadian clock components regulates the photoperiodic

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called the evening element (EE) in the promoters of these genes response pathways through downstream photo-responsive/
(Harmer et al., 2000; Kamioka et al., 2016). In turn, PRR pro- photo-regulated components. In angiosperms, flowering is one
teins also repress the expression of CCA1/LHY genes during of the major photoperiodic responses and it is regulated by the
the day to restrict their expression to the late night and early protein CONSTANS (CO), which is considered as a central
morning, and thus complete the feedback loop (Nakamichi regulator of photoperiodic and circadian pathways (Putterill
et al., 2010; Liu et al., 2015). et al., 1995; Robson et al., 2001; Song et al., 2015; Romero
The central feedback loop consists of CCA1/LHY and et al., 2024). CO contains two zinc finger domains in the
TIMING OF CAB2 EXPRESSION 1 (TOC1). TOC1 N-terminus (B-Box I and B-Box II) and belongs to a larger
(PRR1) is one of the members of the PRR family and shows BBX (B-box) family. In addition, it contains a CCT (CO,
peak expression at dusk. Expression of TOC1 is repressed by CO-Like, and TOC1) domain (Serrano et al., 2009; Valverde,
the binding of CCA1/LHY to the EE present in its promoter. 2011). CO and CO-like (COL) proteins form a family of
TOC1 also represses the expression of CCA1, forming the 17 proteins in Arabidopsis. COL proteins in Arabidopsis have
negative feedback loop (Alabadı́ et al., 2001; Liu et al., 2015). been grouped into group-1 containing two B-box domains,
The evening loop consists of TOC1, GI, and ZTL. group-2 containing one B-box domain, and group-3 contain-
Expression of GI and ZTL has been shown to be regulated ing one B-box and one degraded B-box. Homologues of COL
by CCA1, PRRs, and TOC1 (Liu et al., 2015; Kamioka et al., proteins have been identified across all plant lineages (Zobell
2016). It is noteworthy that ZTL is a photoreceptor sensing et al., 2005; Valverde, 2011; Fan et al., 2014). Group-1 COL
BL. GI and ZTL form a complex involved in BL and temper- proteins have been further subdivided on the basis of the pres-
ature sensing, and it induces degradation of TOC1 by the 26S ence of some additional conserved sequences (Griffiths et al.,
proteasome (Kim et al., 2007). The evening loop also includes 2003). CO regulates the activity of FLOWERING LOCUS
LUX ARRHYTHMO (LUX), EARLY FLOWERING 3 T (FT) in a photoperiod-dependent pathway (Suárez-López
(ELF3), and ELF4. Proteins encoded by these genes form a et al., 2001).
complex called the ‘Evening Complex’ (EC) which represses FT is a member of the phosphatidylethanolamine-binding
the expression of PRR9 and LUX itself (Helfer et al., 2011; protein (PEBP) gene family. This family includes another two
Nusinow et al., 2011). subfamilies of genes namely MOTHER OF FT AND TFL1
While the previously described clock components act (MFT) and TERMINAL FLOWER 1 (TFL1). The PEBP
mainly as repressors, some of the members of the RVE family gene members control flowering and plant architecture in
such as RVE4, RVE6, and RVE8 have been suggested to ex- plants (Hedman et al., 2009; Karlgren et al., 2011). The CO–
hibit peak expression in the afternoon and activate the expres- FT module controls photoperiodic flowering and growth ces-
sion of PRR5, TOC1, and other evening-phased genes (Hsu sation in plants (Böhlenius et al., 2006; Kobayashi and Weigel,
et al., 2013). One or more PRRs constitute a negative feed- 2007; Fan et al., 2014).
back loop by repressing the expression of RVE8 and possibly In Arabidopsis DNA-Binding with One Finger-type (DOF-
other RVE genes (Rawat et al., 2011; Nakamichi et al., 2012; type) transcriptional repressors namely Cycling DOF Factors
McClung, 2014). (CDFs) repress the expression of CO (Imaizumi and Kay, 2006;
Fornara et al., 2009). Arabidopsis ZTL homologue FKF1, to-
Photo-responsive/photo-regulated components: the gether with GI, mediates the degradation of CDFs and the
mediators of the photoperiodic response subsequent CO activation (Imaizumi et al., 2005; Fornara et al.,
2009; Song et al., 2010; Serrano-Bueno et al., 2017).
While the photoreceptors recognize light, and circadian clock In this section, we presented an overview of the light signal-
components track light duration, the information from light, ling and circadian clock components, which are regulators of
day length, and the circadian clock must be coordinated for photoperiodic responses in the angiosperm model Arabidopsis.
an effective response. In Arabidopsis, circadian clock com- The following sections will deal with the photoperiodic
ponents such as ELF3 and GI play a role in conveying in- responses and their signalling components in non-angiosperm
formation on the input light to the central oscillator (Park plants.
et al., 1999; Ni, 2005; Anwer et al., 2020). CONSTITUTIVE
PHOTOMORPHOGENIC 1 (COP1) protein is a major
repressor of the photomorphogenic response as it targets the Photoperiod regulates cell division-,
positive regulators of light-mediated development for degrada- reproduction-, metabolism-, and
tion (Podolec and Ulm, 2018). COP1 plays an important role dormancy-related responses in algae
in integrating the photoreceptor and circadian clock signalling
in Arabidopsis and Chlamydomonas reinhardtii (Serrano-Bueno Algae represent the primitive groups of photosynthetic eu-
et al., 2017). karyotic plants chiefly comprised of aquatic unicellular to
854 | Biswal and Panigrahi

multicellular organisms. Historically they have been consid- exceptions. Light regulates different responses such as photo-
ered as plants, though phylogenetic analysis reveals that some taxis, chloroplast movement, reproductive responses, and the

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organisms classified as algae are more closely related to the circadian clock in algae (Hegemann, 2008; Kianianmomeni and
protists than to true algae or any other plants. Therefore, some Hallmann, 2014; Biswal and Panigrahi, 2021). Photoperiod-
researchers consider algae as phototropic protists comprising dependent responses have been described in different species of
members of different eukaryotic supergroups (Burki et al., chlorophytes, diatoms, and xanthophytes (Dring, 1984; Powell,
2021; Singer et al., 2021). Thus, in modern phylogenetic clas- 1986; Suzuki and Johnson, 2001). These responses in algae can
sification, algae are considered as an artificial group due to the be categorized into three types (Powell, 1986). In the first type,
grouping of non-related taxa with true algae (Bhattacharya growth is affected, which sometimes may not necessarily be a
and Medlin, 1998; Blaby-Haas and Merchant, 2019). Despite true photoperiodic response, but rather an energy-dependent
all the debates, algae are considered as plants since they pos- process attributable to the differences in photosynthesis in LDs
sess chloroplasts.The mode of acquisition of chloroplasts varies and SDs. In the second type, a change in the growth form/
among different algal groups. Plastids originated by the engulf- morphology is observed, depending on the photoperiod. In
ment of an ancestor of modern-day cyanobacteria by a hetero- the third type, changes in photoperiod induce reproductive
trophic eukaryote and its retention as a symbiont in a primary responses (Powell, 1986). It is well known that photoperiodic
symbiosis event (Sibbald and Archibald, 2020). This primary responses are fine-tuned by the circadian clock components.
plastid was transferred to the members of the eukaryotic su- Circadian responses and putative clock components have been
pergroup Archaeplastida (green algae, land plants, red algae, and studied in chlorophytes, euglenophytes, rhodophytes, and dino-
glaucophytes) through a common algal ancestor (Rodríguez- flagellates (Noordally and Millar, 2015).The circadian clocks of
Ezpeleta et al., 2005; Kim and Maruyama, 2014; Burki et al., two chlorophytes, namely C. reinhardtii and Ostreococcus tauri,
2020; Sibbald and Archibald, 2020; Miyagishima, 2023). Later, are among the most-studied algal clocks (Corellou et al., 2009;
the primary plastids of green and red algae spread across the McClung, 2013; Linde et al., 2017; Serrano-Bueno et al., 2017).
eukaryotic lineage through eukaryote-to-eukaryote secondary Ostreococcus tauri is the smallest known free-living eukaryote
(or higher order) symbiosis. For instance, two independent sec- (Courties et al., 1994). Its circadian clock consists of two clock
ondary endosymbiosis events of green algal chloroplasts gave genes of the central loop: OtCCA1 and OtTOC1, but other
rise to the euglenoids and chlorarachinophytes (Rogers et al., clock components, such as GI and ELF, are absent.The expres-
2007; Burki et al., 2020; Sibbald and Archibald, 2020). The ac- sion patterns of OtCCA1 and OtTOC1 are similar to those of
quisition of red algae-derived plastids, on the other hand, has their orthologues present in Arabidopsis (Corellou et al., 2009;
been challenging to interpret since plastid evolution barely Linde et al., 2017; Serrano-Bueno et al., 2017). Repression of
corresponds to the phylogeny of the host lineages. (Burki et al., OtCCA1 has been shown not to affect the circadian rhythm
2020; Strassert et al., 2021; Miyagishima, 2023). Secondary under LL, but down-regulation of OtTOC1 disrupts circadian
symbiosis of red alga-derived plastids gave rise to different output under LL, indicating the central role of OtTOC1 in the
algal groups such as brown algae, diatoms, chrysophytes, and O. tauri clock (Corellou et al., 2009).The genes involved in cell
dinoflagellates (Strassert et al., 2021). All the algal members of division such as cyclin genes and CYCLIN-DEPENDENT
the eukaryotic tree except the supergroup Archaeplastida have KINASE (CDK) are under the control of both circadian
been grouped with heterotrophic flagellates, protozoans, and rhythm and photoperiod in O. tauri (Moulager et al., 2007).
fungi distributed in different supergroups (Burki et al., 2020). The clock components of O. tauri change expression pat-
For example, brown algae and diatoms are included in a group tern upon changes in photoperiod and become entrained in
called the stramenopiles along with some fungal members a manner similar to Arabidopsis (Pfeuty et al., 2012). However,
(Yoon et al., 2009). Even in Archaeplastida, it has been shown the clock architecture of O. tauri is a simple single loop con-
that red algae are close relatives of non-photosynthetic picozoa. sisting of only two genes compared with the complex clock
Their inclusion as plants is under debate (Ragan and Gutell, present in Arabidopsis. While the entrainment in the Arabidopsis
1995; Stiller et al., 2014; Gawryluk et al., 2019; Schön et al., clock to varying photoperiods might be due to multiple feed-
2021). The phylogenetic relationship between land plants and back loops, in O. tauri this is achieved by multiple light inputs
different lineages of algae is shown in Fig. 1. As algae show (Troein et al., 2011; Thommen et al., 2012; Dixon et al., 2014).
great diversity in their morphological form and occupy diverse Putative circadian clock components in Chlamydomonas
aquatic habitats, perception of light and its duration is crucial were first identified using a forward genetic approach (Matsuo
for their adaptation and survival. et al., 2008; Schulze et al., 2010). Subsequent studies identified
Algae possess diverse types of photoreceptors such as rho- the Arabidopsis clock homologues present in Chlamydomonas.
dopsins, PHOTs, CRYs, PHYs, aureochromes, and neo- The circadian clock in Chlamydomonas is similar to that of
chromes, which have evolved in different groups of algae as O. tauri, consisting of CrCCA1 and CrTOC1 (Linde et al.,
adaptive requirements. Photoreceptors such as rhodopsins, 2017; Serrano-Bueno et al., 2017). In addition, a homologue
aureochromes, or neochromes are specific to different algal of ELF4 has been identified in Chlamydomonas (Zhao et al.,
groups and are generally not present in land plants, with a few 2019). However, it lacks homologues of GI and ZTL (Linde
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Fig. 1. Cladogram showing the phylogenetic relationship among major plant groups and different lineages of algae and their photoperiodic responses.
Major photoperiodic responses are shown alongside the lineages. The cladogram is based on the eukaryotic trees described in Burki et al. (2020),
Sibbald and Archibald (2020), and Miyagishima (2023). The relationship between members of bryophytes is based on Su et al. (2021). The evolutionary
relationship among different plant lineages and the different algal groups is shown on the basis of the origin of plastids. Members of the supergroup
Archaeplastida (land plants+green algae+glaucophytes+red algae) possess plastids acquired by primary symbiosis. Euglenoids and Chlorarachinophytes
possess green algal plastids acquired by secondary symbiosis. Algal members of the supergroup TSAR, haptophytes, and cryptophytes possess plastids
of red algal origin through secondary (or higher order) symbiosis. Groups possessing plastids of green algal origin are shown in green and plastids of red
algae and groups possessing plastids of red algal origin are shown in dark red. The tree only shows the phylogenetic relationships, but not the time of
divergence of lineages.
856 | Biswal and Panigrahi

et al., 2017; Serrano-Bueno et al., 2017). Different circadian Furthermore, RNAi-mediated silencing of CrCO increased
responses such as phototaxis, chemotaxis, starch metabolism, the lipid content and its overexpression decreased the lipid

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cell division, UV light sensitivity, and adherence to glass surface content in Chlamydomonas cells. The lipid content was found
have been demonstrated in Chlamydomonas (Mittag et al., 2005; to be higher in the RNAi-mediated transgenic lines under
Schulze et al., 2010; Matsuo and Ishiura, 2011). In addition, SD conditions (Deng et al., 2015). Starch and lipids are two
the circadian clock in Chlamydomonas also regulates numerous major storage products in Chlamydomonas. Synthesis of these
photoperiod-dependent processes. Germination of zygo- metabolites is induced in stress conditions such as nutrient de-
spores in Chlamydomonas is a photoperiod-regulated process. pletion (Liu and Benning, 2013; Li-Beisson et al., 2019; Ran
Zygospores are diploid spores formed by mating of haploid et al., 2019; Deschamps et al., 2023). Both metabolites share
gametes (formed by differentiation of haploid vegetative cells) common carbon precursors and compete for these during
under non-optimal conditions.These are resistant to stress such stress conditions (Ran et al., 2019). Generally, under nutrient
as darkness, desiccation, or starvation. They germinate when depletion conditions, starch is synthesized prior to lipids in
the conditions become favourable. The germination efficiency Chlamydomonas and other microalgae (Fan et al., 2012; Ran
of zygospores is higher in LDs compared with SDs and it is also et al., 2019). Blocking starch synthesis enhances lipid synthesis
fluence dependent. Zygospores are more resistant to freezing and accumulation in Chlamydomonas (Li et al., 2010;Work et al.,
than vegetative cells. In nature, this strategy might have been 2010). CrCO inhibits the synthesis of both starch and lipids in
employed by this alga to cope with the winter SDs (Suzuki and Chlamydomonas. This inhibition of biosynthesis may be due to
Johnson, 2002). the following possible reasons: (i) since the accumulation of
Chlamydomonas possesses a homologue of CO (CrCO), the starch and lipids is correlated with stress conditions, their inhi-
master regulator of photoperiodic flowering. Heterologously bition by CrCO is possibly related to stress alleviation mecha-
expressed CrCO has been shown to rescue the late flowering nisms in algae; (ii) CrCO may be involved in regulating the
phenotype in co mutants of Arabidopsis and also to promote early metabolic balance by partitioning the carbon precursors for
flowering in wild-type plants when expressed under different starch or lipid synthesis; or (iii) CrCO may be involved in the
promoters. It also promotes the expression of the FT gene in inhibition of starch or lipid accumulation in a feedback inhi-
a manner similar to plants overexpressing CO (Serrano et al., bition mechanism along with other regulators, which are not
2009).The expression of CrCO is both circadian and photope- known yet (Fig. 2).
riod regulated. Interestingly CrCO expression is higher under Plants dissipate excess light energy as thermal energy by a
SDs, in contrast to its Arabidopsis homologue, which shows photoprotective response mechanism called qE. CrCO and nu-
higher expression in LDs. Reduction of CrCO expression by clear transcription factor Y (NF-Y) form a complex that con-
antisense RNA has been shown to reduce growth in the algal fers a photoprotective response in Chlamydomonas (Kumimoto
cells (Serrano et al., 2009). It has been mentioned earlier that et al., 2010; Tokutsu et al., 2019). NF-Y is a heterotrimeric
the germination of zygospores is regulated by photoperiod. TF complex consisting of three subunits NF-YA, NF-YB,
Since the expression of CrCO is also photoperiod dependent, and NF-YC. Different subunits of NF-Y interact with CO to
its possible involvement in regulating zygospore germination regulate photoperiodic flowering in Arabidopsis (Zhao et al.,
in Chlamydomonas cannot be ruled out (Schulze et al., 2010). 2017). Crco and Crnfyb mutants of Chlamydomonas do not show
Starch accumulation in Chlamydomonas has been shown to be a qE response. It is presumed that photoperiod signalling and
a circadian clock-regulated process. An enzyme, GRANULE- photoprotective response are interlinked in Chlamydomonas
BOUND STARCH SYNTHASE I (GBSSI), binds to starch (Tokutsu et al., 2019).
and is involved in amylopectin synthesis in Chlamydomonas Homologues of ELF4 have been identified in Chlamydomonas
(Ral et al., 2006). Starch accumulation shows a peak at the (CrELF4). Heterologous expression of these genes in the elf4
beginning of the dark period and minimal levels just before mutant of Arabidopsis has been shown to rescue the early flow-
dawn. LD-grown algae show increased starch accumulation ering phenotype, long hypocotyl, and inhibits the expression
compared with cells grown under SDs. However, overexpres- of CO and FT (Zhao et al., 2019).
sion lines of CrCO (CrCOox) accumulate a lower amount of Chlamydomonas possesses one copy of a DOF gene (CrDOF)
starch than the wild type under both LDs and SDs. The ex- (Moreno-Risueno et al., 2007; Ibáñez-Salazar et al., 2014).
pression of GBSSI was also observed to be altered. Generally, Misexpression of CrDOF was shown to result in slowing
GBSSI expression shows a peak before dawn. However, the growth of Chlamydomonas (Lucas-Reina et al., 2015).
CrCOox lines show GBSSI expression throughout the day. CrDOF induced the expression of CrCO under SD condi-
These findings show that starch metabolism is under photope- tions, and reducing the expression of CrDOF resulted in re-
riodic control in algae (Serrano et al., 2009). Photoperiod also duction of expression of CrCO. Interestingly, this contrasts
influences lipid metabolism in Chlamydomonas. Chlamydomonas with what is observed in Arabidopsis where DOF inhibits the
cells accumulated more lipids when cultured in a sulfur-free expression of the CO gene. The study also revealed that in
medium in SD conditions. In the sulfur-free medium, the LDs CrDOF inhibits the expression of cell division genes in
expression of CrCO was observed to be down-regulated. a CrCO-independent manner. Transgenic Arabidopsis plants
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Fig. 2. Schematic diagram showing the possible interactions of CrCO with starch and lipid metabolism in Chlamydomonas. CrCO suppresses the biosynthesis
of both starch and lipids. The inhibition may be through feedback inhibition. Alternatively, the inhibition may be a result of carbon precursor partitioning by CrCO
during stress response or to maintain the metabolic balance. Solid lines indicate the observed responses. Dashed lines indicate possible regulation. Lines with
blunt ends indicate inhibition of a response. Lines with arrowheads indicate the promotion of a response.

overexpressing CrDOF show reduced expression of CO and In the red alga Constantinea subulifera, new blade formation at
FT as well as delayed flowering, and thus functional conser- the tip of the stipes is initiated in SDs. The blade formation
vation of DOF (Lucas-Reina et al., 2015). Interestingly over- is inhibited by a night-break in the middle of the dark phase
expression of CrDOF has been shown to increase the lipid by BL or RL (Powell, 1986). In the red alga Dumontia contorta,
content in Chlamydomonas (Ibáñez-Salazar et al., 2014). Since both sporophytic and gametophytic microthalli persist in the
the lipid content also increases upon silencing CrCO, and vegetative state in LDs. They form erect, branched, and tu-
since CrDOF is an inducer of CrCO, it presents a curious case bular macrothalli when subjected to SD conditions. This is a
to investigate the possible crosstalk among lipid metabolism, genuine photoperiodic response since macrothalli formation
CrCO, and CrDOF. It is possible that lipid synthesis may be is inhibited by night-breaks (Rietema, 1982). Photoperiod is
mediated by both photoperiod-dependent and photoperiod- a major determinant of reproductive transition in many spe-
independent pathways in Chlamydomonas. cies of red algae (Dixon and Richardson, 1970; Guiry, 1984;
As mentioned earlier, photoperiodic responses are not only Kain, 1996). While most of the photoperiodic studies in red
limited to green algae; they have also been observed in other algae are focused on physiological aspects, no significant studies
groups of algae such as red algae, euglenoids, dinoflagellates, have been conducted at the molecular level. Lack of genome
diatoms, and brown algae (Dring, 1984; Powell, 1986). In the data or model systems may be one of the limitations in this
red alga Rhodochorton purpureum, tetrasporangium formation regard. However, in the recent past, genomic and transcrip-
occurs in SDs and this is inhibited by a night-break in the tomic studies have been initiated on different red algal spe-
middle of the dark period. Both BL and RL have been shown cies. Future studies need to focus more on molecular aspects of
to be effective as night-breaks, and the effect of RL is not re- photoperiod-regulated development in red algae (García-
versible by FR (Dring and West, 1983). In Acrosymphyton purpu- Jiménez and Robaina, 2015).
riferum, tetrasporogenesis is not inhibited by night-break during In Euglena gracilis, cell division has been shown to be an
the dark period, but it is inhibited when the SD light period is LD-dependent process.This LD-dependent cell division is also
extended beyond the critical day length (Cortel-Breeman and regulated by the light spectrum, typically of BL, RL, and FR,
Hoopen, 1978; Breeman and Hoopen, 1987; Breeman, 1993). indicating the involvement of PHYs and CRYs (Bolige and
858 | Biswal and Panigrahi

Goto, 2007). However, the putative photoreceptors have not morphogenesis is regulated by photoperiod. It has been shown
been identified in E. gracilis. Dinoflagellates also show photo- that when the dark period is interrupted by short pulse BL,

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periodic responses.The dinoflagellate Lingulodinium polyedra re- the production of macrothalli is inhibited, and remains unaf-
mains at the surface of oceans during warmer parts of the year. fected by treatment with RL or FR during the dark period in
In the autumn, these cells sink to the bottom of the sea and SD conditions. Thus this is a BL-regulated process (Dring and
form a temporary cyst. SDs and lower temperatures have been Lüning, 1975). Aureochromes, a class of photoreceptor found
shown to promote dormant cyst formation. Interruption of the in stramenopiles, possibly regulate this photoperiodic response
dark period with light prevents cyst production. Application of in S. lomentaria (Miller and Connell, 2012). Many genes in-
melatonin (found in the alga) in non-inducing photoperiods volved in biosynthesis of cell organelles such as chloroplasts
promotes cyst formation (Balzer and Hardeland, 1991). This and mitochondria are up-regulated in SD conditions, which is
finding has been supported by SD-promoted cyst formation in consistent with the increase in cellular growth in SDs (Miller
other species of dinoflagellates (Sgrosso et al., 2001). and Connell, 2012).
Circadian rhythm-related responses have been demonstrated In the brown alga Glossophora kunthii, LD conditions along
in diatoms and brown algae (algal members of stramenopiles). with high light irradiance induce the formation of primary lig-
In diatoms, resting stages such as resting cells and resting spores ulae. On the other hand, growth of secondary ligulae and their
are influenced by photoperiod. Resting stages allow the algae differentiation to tetrasporangia is induced under SD condi-
to survive under adverse conditions (Sicko-goad et al., 1989). tions. Sporangium induction is further enhanced under low
Resting stages include resting cells and resting spores. Resting irradiation. Interruption of the dark period with light inhibits
cells show morphological similarity to vegetative cells, but the formation of tetrasporangia, indicating the photoperiodic
have dense cytoplasm at the centre. In diatoms, resting cell regulation of this response (Hoffmann, 1988; Hoffmann and
formation is possibly accelerated by SDs and low temperature Malbrán, 1989).
(Sicko-goad et al., 1989). Photoperiod is one of the major trig- Photoperiod plays an important role in the induction of re-
gers of resting spore germination in diatoms (Eilertsen et al., productive responses in different lineages of algae. Since algae
1995; McQuoid and Hobson, 1995). Genomic studies have exhibit great diversity in their form and function, the regula-
indicated the presence of a novel type of oscillator, different tion of photoperiodic responses might also show mechanistic
from the green lineage, in stramenopiles. Recently, the first variations. However, limited data are available concerning the
circadian clock component has been discovered in a diatom, regulation of photoperiodic responses at the molecular level.
Nannochloropsis (Poliner et al., 2019; Farré, 2020). Photoperiod- Moreover, how the photoperiodic components interact with
related responses have been described in a number of brown other regulatory pathways in algae is yet to be investigated. It
algae, mostly demonstrating reproductive transitions. is expected that future studies would focus on these aspects
The sporophytic body of brown algae consists of a hold- using genomic and transcriptomic approaches involving algal
fast, stipe, and frond. A frond is a leaf/lamina-like structure that model systems.
performs photosynthesis. In the marine macro alga Laminaria
hyperborea, frond formation is a photoperiod-controlled pro-
cess. Laminaria hyperborea produces new fronds under SD con- Photoperiod regulates reproductive
ditions, which is inhibited by a night-break during the dark responses in bryophytes
period. In LD conditions, new frond formation and develop-
ment are inhibited. Laminaria hyperborea uses the day length Bryophytes represent one of the earliest lineages of land plants
as a cue to initiate frond formation in winter SDs in natural along with the members of the charophytic algae. They have
condition. This may be an adaptation to harvest the maximum been classified into three groups, namely liverworts, hornworts,
amount of sunlight available during the summer in photosyn- and mosses (Troitsky et al., 2007; Shaw et al., 2011; Su et al.,
thesis (Lüning, 1986). 2021). Many photomorphogenic and phototropic responses
In the brown alga Ascophyllum nodosum, receptacle initiation have been demonstrated in different bryophytes (Imaizumi
is induced under SD conditions and is inhibited under LD and et al., 2002; Possart et al., 2014; Nishihama et al., 2015; Inoue
LL conditions as well as by a white light night-break in the et al., 2019). However, the day length-dependent processes have
dark period. The day length for receptacle initiation follows not been extensively studied in bryophytes as compared with
the seasonal pattern in natural conditions (Terry and Moss, photomorphogenic responses. Photoperiodism was first dem-
1980). onstrated in the liverwort Marchantia polymorpha.The formation
Scytosiphon lomentaria is a brown alga found in colder tem- of antheridiophores and archegoniophores is enhanced in LD
perate oceans. Some of the populations of S. lomentaria in their conditions in Marchantia. LD-grown Marchantia plants are also
asexual phase show distinct heteromorphic morphologies. In larger in size (Wann, 1925; Voth and Hamner, 1940; Yamaoka
summer (LD conditions) they exist as small disc-like crustose et al., 2021). On the other hand, SD-grown Marchantia form
microthalli, which in winter (SD conditions) produce large more gemmae cups than LD-grown plants. Gemmae are prop-
erect macrothalli (Miller and Connell, 2012). This transition in agules that help in vegetative reproduction. Thus SD-to-LD
 Photoperiod-mediated development in non-flowering plants | 859

transition also induces the transition in reproductive response the evolutionary basis of development (Ishizaki et al., 2016;
in Marchantia (Voth and Hamner, 1940; Carter and Romine, Rensing et al., 2020; Naramoto et al., 2022). The components

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1969). A similar response has been observed in another liver- of light signalling and perception have been identified in these
wort Cephalozia lunulifolia (earlier known as Cephalozia media) plants (Possart et al., 2014; Li et al., 2015a; Kondou et al., 2019).
(Lockwood, 1975). In a study by Larpent-Gourgaud and Photoperiod-dependent regulation of reproductive response
Aumaitre (1980), protonema elongation in the moss Ceratodon in Marchantia has been described earlier. Physcomitrium also dis-
purpureus was shown to be enhanced under LD conditions. plays photoperiod-dependent reproductive transition. SDs and
Protonema growth was observed to be further enhanced when low temperature, which mimic the natural growth conditions
the dark period was interrupted with light. Since LD plants in autumn, induce sporophyte formation in Physcomitrium.
respond to night-breaks positively, this response was assumed Therefore, Physcomitrium is an SD plant with regard to sexual
to be an LD phenomenon (Larpent-Gourgaud and Aumaitre, reproduction (Hohe et al., 2002).
1980). However, it may be an energy-dependent phenomenon, Circadian clock components have been identified in
since lowering the light energy lengthened the optimum pho- Physcomitrium and Marchantia. Physcomitrium possesses two
toperiod requirement for this process. On the other hand, in homologues of CCA1/LHY, PpCCA1a and PpCCA1b
the same study, protonema branching was observed to be an (Okada et al., 2009a). These genes show rhythmic expression
SD phenomenon, since interruption of the dark period with similar to Arabidopsis, with peak expression at dawn under
light inhibited protonema branching (Larpent-Gourgaud light–dark cycle or DD, but become arrhythmic under LL in
and Aumaitre, 1980). In the liverwort Reboulia hemisphaerica, contrast to their angiosperm counterparts. The potential func-
archegoniophores elongated under LDs, but not under SDs. tions of PpCCA1a and PpCCA1b were analysed by gener-
This photoperiod effect may also be regulated by tempera- ating single and double disruptant knockout lines using the
ture, since the elongation was not observed at low tempera- wild-type PpCCA1b::LUC+ strain as the parental strain (Okada
ture in LDs (Koevenig, 1973). Mosses such as Polytrichum aloides et al., 2009a). The rhythmic expression of PpCCA1b showed
and Polytrichum piliferum show a day-neutral response (Hughes, dampened amplitude and shortened periodicity in the double
1962). The liverwort Riccia glauca and the hornwort Anthoceros disruptant lines. Double disruption of the PpCCA genes in
laevia produced gametangia under SD conditions (Benson- Physcomitrium also results in shortening of periodicity of cir-
Evans, 1961). In the moss Pohlia nutans, gametangial induction cadian response-related gene such as plastid sigma factor 5
was observed to a greater extent when the plants were trans- (PpSIG5) and one PpPRR gene (Ichikawa et al., 2004; Okada
ferred from LD to SD conditions, as compared with plants et al., 2009a). The CCA/LHY homologues of Physcomitrium
grown under LDs, SDs, or transferred from SD to LD condi- not only play a role in circadian rhythm, but also appear to
tions. This indicates that P. nutans responded to the change in regulate the growth in a photoperiod-dependent manner.
the day length transition rather than the day length per se (Lee The protonema of single and double disruptant mutant lines
et al., 2010).This behaviour of P. nutans is typical of long–short- as well as wild-type plants show no significant difference in
day plants such as Kalanchoe daigremontiana (formerly known growth under SDs. However, the double disruptant lines show
as Bryophyllum daigremontianum), which are SD plants, but re- increased growth as compared with the single disruptant and
quire exposure to LD in the early days of growth for flowering wild-type plants under LDs (Okada et al., 2009b). The bio-
(Zeevaart and Lang, 1962). Photoperiod-dependent responses luminescence rhythm of the promoter PCCA1b::LUC+ was
have been described in different bryophytes (Benson-Evans, also significantly affected in the double disruptant lines under
1961; Chopra and Bhatla, 1983). Among bryophytes, liverworts LDs. These facts suggest that PpCCA1a and PpCCA1b acts
are more sensitive to photoperiod than mosses, and the photo- redundantly in the development of Physcomitrium (Okada et al.,
periodic response increases with an increase in light intensity 2009a). The increased protonemal growth in the double dis-
(Chopra and Bhatla, 1983). ruptant lines suggests that these genes may be involved in pro-
In recent years, the moss Physcomitrium patens (formerly tonema to gametophore transition, and double disruption of
Physcomitrella patens) has emerged as a major non-angiosperm these genes thus results in enhancement of protonemal growth.
land plant model. It is the first plant model system to be geneti- Five COL genes have been identified in Physcomitrium, two
cally modified by homologous recombination-based protoplast of which are distantly related to CO or COL genes and in-
transformation (Schaefer, 2002). Apart from Physcomitrium, cluded in group-2 or group-3 of COL genes of Arabidopsis.
Marchantia has also been employed as another bryophyte model Three genes, namely PpCOL1, PpCOL2, and PpCOL3, show
(Bowman et al., 2016; Shimamura, 2016; Kohchi et al., 2021). more similarity to group-1 COL genes such as COL1–COL5,
Marchantia is also amenable to genetic manipulations. It can more specifically to the group-1c genes (COL3–COL5) of
also be genetically modified by homologous recombination, Arabidopsis (Griffiths et al., 2003; Zobell et al., 2005). CO is the
through Agrobacterium-mediated transformation of the sporel- only member of the COL family to play a role in flowering.
ings (Ishizaki et al., 2013). Since extant bryophytes are consid- Therefore, PpCOL genes may not have an analogous function
ered to be one of the closest relatives of ancient land plants, similar to flowering in the bryophyte lineage, but this indicates
these model plants provide an opportunity to understand that COL genes were present in the last common ancestor of
860 | Biswal and Panigrahi

land plants (Zobell et al., 2005). The functional role of PpCOL In Arabidopsis. ELF4 delays flowering, inhibits hypocotyl
genes in light- or photoperiod-related responses is not known, elongation, and delays the circadian period (Doyle et al.,

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but these proteins show peak expression during the day time, 2002). Heterologous expression of PpELF4 in the elf4 mu-
which may be due to the effect of either light or the circadian tant of Arabidopsis rescued the early flowering phenotype and
clock (Zobell et al., 2005). In an earlier report, the expression elongated hypocotyl, and inhibited the expression of CO and
of PpCOL1 was shown to be photoperiod dependent, with a FT, which are positive regulators of photoperiodic flowering.
peak in LDs and decreased expression under SDs in the game- However, the physiological significance of PpELF4 in pho-
tophores. Since the combination of SDs and low temperature toperiodism in Physcomitrium has not been elucidated (Zhao
induces sporophyte formation in Physcomitrium gametophores, et al., 2019).
PpCOL1 may have a role in the photoperiod control of sporo- Physcomitrium possesses four homologues of PRR genes,
phyte production in Physcomitrium (Hohe et al., 2002; Shimizu namely PpPRR1–PpPRR4. PpPRR genes show circadian
et al., 2004). However, temperature also influences this process, and light-dependent expression (Satbhai et al., 2011b). When
and the role of temperature in regulating the expression of PpPRR2 was heterologously expressed in Arabidopsis, it
PpCOL genes is not known. changed the mechanism of the intrinsic circadian clock and
Physcomitrium possesses a family of DOF genes having 19 the transgenic lines displayed early flowering and short hypo-
members which are similar to CDF genes (Moreno-Risueno cotyl under SDs, indicating their putative role in photoperi-
et al., 2006; Shigyo et al., 2007). Among these, PpDOF3 and odic signaling (Satbhai et al., 2011a). Physcomitrium has been
PpDOF4 show close similarity to CDF genes. These PpDOF predicted to possess other clock components such as PpELF3
genes show a diurnal expression pattern. Single disruptant (three orthologues) and PpLUX, but lacks homologues of
lines ppdof3 and ppdof4 and the double disruptant ppdof3 the TOC1, GI, and ZTL family of genes. These compo-
ppdof4 showed no significant change in the expression pat- nents constitute the three-loop circadian clock in Arabidopsis.
tern of PpCOL genes. This indicates that unlike Arabidopsis, Interestingly these genes are present in the moss Takakia lepi-
in Physcomitrium these TFs do not repress the expression of dozioides. Therefore, the absence of these genes may be due
PpCOL genes (Ishida et al., 2014). to gene loss in Physcomitrium (Linde et al., 2017). It has been
Genomic studies show that homologues of PEBP family proposed that the circadian clock in Physcomitrium comprises
(MFT, FT, and TFL1) genes are absent in Chlamydomonas and a single loop and represents an ancestral simple clock (Holm
Ostreococcus lucimarinus. On the other hand, basal land plants et al., 2010). However, this simple clock is yet to be understood
such as Physcomitrium and lycophytes possess only MFT-like in detail.
genes, but lack FT-like genes. Physcomitrium possesses four Marchantia possesses orthologues of circadian clock compo-
MFT-like genes. All members of the PEBP family of genes nents such as LHY/CCA1-LIKE (LCL), TOC1, PRR, ELF3,
are present in gymnosperms and angiosperms. These find- ELF4, LUX, and ZTL. LCL is one of the members of the
ings suggest that PEBP family genes are specific to multicel- RVE family of genes.The expression of these genes is circadian
lular plants and MFT is a possible ancestor of FT/TFL genes, regulated (Linde et al., 2017). However, how these genes are
which arose as a result of gene duplication of ancestral MFT- involved in photoperiodic responses has not been understood.
like genes (Hedman et al., 2009). Expression of PpMFT genes Marchantia possesses orthologues of GI (MpGI) and FKF1
increases with the progression of plants from protonema- to (MpFKF1). The expression of MpGI and MpFKF1 is circa-
gametangia-bearing gametophores. While protonema shows dian clock regulated. Gametangiophore formation is much
the lowest degree of expression, gametangia and sporophyte delayed in the knockout lines of MpGI (Mpgiko) and MpFKF1
tissue exhibit maximum expression. All the PpMFT genes (Mpfkf1ko) under LDs compared with wild-type plants. This
show a transient increase in expression shortly after the ini- indicates the failure of the growth phase transition in the
tiation of the light period in LD conditions, indicating pho- knockout lines (Kubota et al., 2014). Similar to Arabidopsis,
toperiodic control. PpMFT2, PpMFT3, and PpMFT4 show a MpGI and MpFKF1 form a complex (MpGI–MpFKF1) in the
circadian pattern of expression. Expression of all the PpMFT gametophyte of Marchantia, which promotes the growth phase
genes becomes arrhythmic under LL, similar to other clock- transition under LDs. Consistent with this, overexpression lines
regulated genes. The predominant expression of PpMFT MpGIOX, MpFKFOX, and MpGIOXFKFOX show gametangio-
genes in sporophytes of Physcomitrium indicates their pos- phore formation even under SD conditions or much earlier in
sible role in moss reproduction, which is also a day length- LD conditions than wild-type plants (Kubota et al., 2014). It
dependent process (Hohe et al., 2002; Hedman et al., 2009). has been suggested that overexpression of MpGI or MpFKF1
However, expression of PpMFT genes show a transient in- or possibly both increases the amount of the MpGI–MpFKF
crease in LDs, and they also show predominant expression in complex and promotes growth phase transition irrespective
sporophytes, which are induced under SDs; further investiga- of photoperiod (Kubota et al., 2014). Heterologous expres-
tion is required to understand the photoperiodic regulation sion of MpGI in the gi mutant of Arabidopsis partially comple-
of PpMFT genes. mented the late-flowering phenotype, indicating the partial
 Photoperiod-mediated development in non-flowering plants | 861

conservation of function.The presence of the MpGI–MpFKF1 142 d and they were suggested to be SD plants (Ridgway, 1967).
complex in Marchantia suggests the origin of this regulatory However, recently it has been reported that A. agrestis is an LD

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mechanism in the common ancestor of land plants (Kubota plant, as it shows antheridia induction under LL and LD condi-
et al., 2014). However, its absence in Physcomitrium suggests a tions (in 1 month) (Szövényi et al., 2015). It is noteworthy that
possible gene loss in the moss lineage. While the Mpgiko and A. agrestis plants show faster growth under LL than LDs, further
Mpfkf1ko mutants indicate that the reproductive transition in corroborating it as an LD plant (Szövényi et al., 2015).The faster
Marchantia might be a circadian clock-regulated process, a re- growth under LL conditions may be due to increased photo-
cent study involving the mutants of MpTOC1 (Mptocge) and synthesis. More studies involving photoperiodic responses, their
MpPRR (Mpprrge) contradicts this assumption. Mptocge and regulation by the circadian clock, and interaction with other
Mpprrge mutants display no significant differences in gametan- regulatory pathways are yet to be carried out in A. agrestris.
giophore formation compared with wild-type plants under Photoperiod is a major environmental factor regulating the
both LDs and SDs (Kanesaka et al., 2023). The lengthening reproductive transition in bryophytes (Fig. 1). However, re-
of the circadian clock by a chemical, namely AMI-331, also productive transition is also regulated by other factors such as
induces no significant alterations in gametangiophore for- phytohormones. For example, in Physcomitrium auxin plays an
mation in Marchantia. It further establishes the dispensability important role in gametangial organ development (Landberg
of the circadian clock in the growth phase transition in the et al., 2013).This implies that photoperiod and auxin signalling
model liverwort (Kanesaka et al., 2023). The day length meas- may crosstalk in regulating reproductive organ development
urement is not regulated by the circadian rhythm in Marchantia, in mosses. Alternatively, photoperiod may regulate the hor-
but possibly by the light–dark ratio in a circadian cycle, since mone signalling genes to control the reproductive responses
decreasing the dark period in non-24 h light/dark cycles pro- in mosses. In addition, photoperiod may also be involved in
motes gametangiophore formation (Kanesaka et al., 2023). other developmental and metabolic responses in bryophytes.
Since the MpGI–MpFKF1 module has been shown to regulate The interactions of photoperiod with other regulatory path-
photoperiod-dependent gametangiophore formation, further ways are not known in bryophytes. Future studies on this as-
studies are required to investigate the downstream components pect will reveal their crosstalk.
of the photoperiodic response pathway.
In a recent study, photoperiod has been shown to act as an
environmental determinant for the retention of chloroplast- Photoperiodism-related genes have been
encoded genes involved in chlorophyll biosynthesis in
identified in ferns and lycophytes
Marchantia (Ueda et al., 2014). Conversion of protochloro-
phyllide (Pchlide) to chlorophyllide (Chlide) by enzymatic Ferns and lycophytes are close relatives of early vascular plants.
reduction is one of the steps of chlorophyll biosynthesis. Historically they have been referred to as pteridophytes.
This reduction step is carried out by nucleus-encoded light- However, according to modern phylogenetic analysis, ferns
dependent NADPH-Pchlide oxidoreductase (LPOR) and and lycophytes are distinct lineages (Fig. 1). These plant groups
chloroplast-encoded light-independent Pchlide oxidoreduc- were included in one lineage due to a unique feature common
tase (DPOR) (Ueda et al., 2014).Vascular plants solely depend to both—the presence of nutritionally and ecologically inde-
on LPOR, since DPOR has been lost in these plants. Marchantia pendent, distinct sporophyte and gametophyte generations.
possesses both of these enzymes. chlB genes encode one of the This is not observed in other major plant lineages and has been
subunits of DPOR. chlB knockout plants of Marchantia gener- a hallmark to differentiate ferns and lycophytes from other
ated by plastid transformation show no significant differences plant groups, and thus the term ‘pteridophyte’ is still preferred
in morphology from wild-type plants under LDs. However, to describe ferns and lycophytes (Sessa, 2018). Phylogenetically
the mutant lines display pale green colour, slow growth, and ferns are closer to seed plants than lycophytes. Lycophytes
decreased chlorophyll content under SD conditions. They also bear microphylls and form a sister clade to the euphyllophytes
show accumulation of Pchlide in the dark. These results sug- (ferns and seed plants bearing megaphylls or true leaves) (Fig.
gest that the retention of DPOR and its SD-dependent regu- 1) (Spencer et al., 2021). In fact, lycophytes gained vasculature
lation may be an adaptation to LL conditions. However, further before ferns (Sessa and Der, 2016; Sessa, 2018; Spencer et al.,
studies are required to understand additional aspects of this re- 2021). Since ferns and lycophytes exhibit independent sporo-
sponse (Ueda et al., 2014). phyte and gametophyte generations, they are the key to un-
Circadian clock components have also been identified in the derstand many evolutionarily important phenomenon.Various
hornwort Anthoceros agrestis, and the expression of core clock light-regulated responses have been described in ferns and
genes has been demonstrated to be regulated in a circadian lycophytes. Photoreceptors such as PHYs, CRYs, and PHOTs
manner (Linde et al., 2017). Photoperiod acts as a limiting factor have also been identified in these groups of plants (Nozue
in reproduction of A. agrestis. In an earlier study, different species et al., 1998; Imaizumi et al., 2000; Kanegae and Kimura, 2015;
of Anthoceros showed antheridia induction in SD conditions after Li et al., 2015a, b). However, most of the reported phenomena
862 | Biswal and Panigrahi

are photoreceptor-mediated; scanty information is available on Various phototropic and photomorphogenic responses have
the day length- or photoperiod-regulated responses. been demonstrated in the fern Adiantum (Yamauchi et al.,

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Initial studies on sporangia formation in ferns suggested that 2005; Wada, 2007), but the photoperiodic responses are poorly
induction of sporangia formation is mainly regulated by car- understood in this species. Adiantum possesses one homologue
bohydrate or photosynthate supply, but not by environmental of CO (Yamauchi et al., 2005), whose functional significance
factors such as photoperiod (Steeves and Wetmore, 1953; has not been investigated. MFT-like genes have been identi-
Wardlaw and Sharma, 1963; Harvey and Caponetti, 1978). fied in Adiantum. AcMFT partially complements the late flow-
Labouriau (1958), however, described that sporangium for- ering phenotype of Arabidopsis ft-1 mutants, suggesting that
mation in ferns is regulated by photoperiod as well as temper- AcMFT functions similarly to FT. AcMFT shows photoperiod-
ature. In Claytosmunda claytoniana (earlier known as Osmunda dependent expression. The expression of AcMFT is photope-
claytoniana), sporophylls are formed under LDs and high tem- riodically regulated and similar to FT of Arabidopsis. AcMFT
perature (Labouriau, 1958). Salvinia auriculata (earlier known expression was observed to be higher in the leaf before sori
as Salvinia rotundifolia) behaved as an SD plant at temperature formation and decreased after sori production. In Arabidopsis,
above 20 °C and as an LD plant at 17 °C. Sporophyll produc- FT has also been observed to be expressed in the leaf under
tion in Regnellidium diphyllum was found to be regulated by LDs and translocated to the shoot apex to promote shoot
seasonal variations in thermo-periodicity and photoperiodism development (Hou and Yang, 2016). Different components
(Labouriau, 1958). Patterson and Freeman (1963) studied the of the circadian clock have been identified in the lycophyte
growth of different fern species under LD and SD condi- Selaginella. It lacks a homologue of the CCA/LHY gene, but
tions. They observed that Pteris vittata is day-neutral (showing possesses one homologue of the LCL gene. Lycophyte PRRs
growth and sporulation under both LDs and SDs). Adiantum are more closely related to moss PRRs (Satbhai et al., 2011b;
capillus-veneris sporulated under LD conditions. Asplenium Linde et al., 2017). In addition, single copies of ELF3, GI, LUX,
platyneuron, Woodsia obtusa, Parathelypteris noveboracensis (ear- and ZTL, and two copies of ELF4 have been identified in
lier known as Dryopteris noveboracensis), and Polystichum acros- Selaginella (Linde et al., 2017). Selaginella therefore possesses all
tichoides did not grow under SDs, but showed growth under the components of the circadian clock but with fewer copies
LDs. However, except Polystichum, these plants did not spor- compared with Arabidopsis. However, the role of these genes
ulate under LDs. Asplenium platyneuron and W. obtusa were in photoperiod-regulated development has not been demon-
later observed to sporulate upon lengthening the light pe- strated yet. Homologues of COL genes have been identified
riod (Patterson and Freeman, 1963). In Osmundastrum cinna- in Selaginella (Serrano et al., 2009; Song et al., 2015; Hu et al.,
momeum (earlier known as Osmunda cinnamomea), decreasing 2018). Four copies of MFT-like genes are present in Selaginella
the day length was found to enhance sporophyll differentia- (Hedman et al., 2009). The presence of these genes impli-
tion. It indicated that LDs are inhibitory for sporangia forma- cates their role in photoperiodic development analogous to
tion. Increasing the light intensity also negatively impacted Arabidopsis, but yet to be demonstrated.
sporophyll differentiation. Interestingly, sucrose was found to In most plants, the dominant growth form is either a game-
increase the fertility in this plant. Since longer photoperiods tophyte (algae and bryophytes) or a sporophyte (gymnosperms
or higher intensity of light are associated with a higher endog- and angiosperms). Light as a signal or seasonal factor mainly
enous sugar level, the results suggest that the observed effects affects the dominant growth form. Since ferns and lycophytes
were not sugar dependent, but photoperiod dependent, where grow independently in both forms, the light regulation of these
SDs appeared to positively regulate sporogenesis (Harvey and growth forms must have adaptive specialization compared with
Caponetti, 1978). other plant groups. Available data from different early vascular
In recent years, ferns such as A. capillus-veneris and Ceratopteris model plants support the presence of endogenous clock and
richardii and the lycophyte Selaginella moellendorffii have emerged photoperiodic control of growth and development. However,
as major non-angiosperm vascular plant models (Li et al., 2013; insufficient physiological and functional studies is a hindrance
Plackett et al., 2014; Marchant et al., 2019; Petlewski and Li, to establishing the role of photoperiod in fern and lycophyte
2019; Ferrari et al., 2020). However, fewer studies have been development. Future work in this regard may provide insight
carried out on these plants to understand the photoperiodic into the photoperiod-regulated development in these groups
basis of development. of plants.
Transcriptome analysis as well as comparative phylogenom-
ics of Ceratopteris with various vascular and non-vascular plants
reveals that genes related to photoperiodism have been gained Photoperiod regulates seasonal dormancy
in the last common ancestor (LCA) of euphyllophytes, and
induction and bud set in gymnosperms
these genes expanded in the LCA of ferns (Geng et al., 2021).
This indicates that ferns may have acquired new functions with Gymnosperms are the first group of plants bearing seed in
their separation in the euphyllophyte clade, and these functions the plant kingdom, comprising cycads, gnetophytes, conifers,
might have expanded within the ferns. and one member of the ginkgophytes (Fragnière et al., 2015).
 Photoperiod-mediated development in non-flowering plants | 863

Photoreceptors such as PHYs, CRYs, and PHOTs have been metabolism. The metabolite profile changes upon transfer
identified in gymnosperms, and light-regulated responses have to LD conditions (Lee et al., 2014). Gibberellic acid (GA) is

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been demonstrated (Mathews, 2006; Mathews et al., 2010; Li known to play a role in organ elongation-related responses in
et al., 2015b; Alakärppä et al., 2019). It has also been shown plants. GA1 and GA4 are bioactive GAs in plants. GA20 and
that light-regulated responses in gymnosperms are affected by GA9 are precursors of GA1 and GA4, respectively (Binenbaum
the latitudinal origin (Mølmann et al., 2006; Alakärppä et al., et al., 2018). In a study on P. abies, the amounts of GA9, GA4,
2019). Most of the gymnosperm photoreceptors and light- and GA1 were found to be less in SDs compared with LDs.
regulated responses have been described in conifers. Conifers Application of GA1 and GA4 increased the seedling length of P.
form the largest group of the extant gymnosperms (Fragnière abies, but a similar experiment with GA9 and G20 did not show
et al., 2015). They respond to the variations in day length by an increase in the seedling length under SDs.This suggests that
changes in growth profile. Conifers are among the major trees the conversion of GA9 and GA20 to their respective bioactive
in temperate and boreal forests. The seasonal variation in day GAs is under photoperiodic control (Moritz, 1995).
length becomes more prominent with increasing latitude in SD-induced bud formation is also regulated by light quality.
the temperate and boreal regions. Forest trees of these regions In P. abies, growth cessation and vegetative bud formation is
respond to seasonal variations in photoperiod and temperature. induced under BL and is similar to SD conditions. In RL,
The majority of the trees in these forests including conifers bud formation is delayed and reduced, indicating that RL is
show photoperiod-dependent shoot elongation where SDs a stronger signal than BL for delaying bud formation (Opseth
(or long nights) induce growth cessation accompanied by bud et al., 2016). The delayed bud set under RL is further delayed
set and dormancy (Wareing, 1949, 1954, 1956; Nitsch, 1957; with an increase in temperature.This indicates the involvement
Jensen and Gatherum, 1965; Heide, 1974; Ekberg et al., 1979; of temperature in photoperiod-mediated bud set (Chiang
Thomas and Vince-Prue, 1996; Partanen and Beuker, 1999). et al., 2021). Interestingly BL-induced bud formation is irra-
Picea abies (Norway spruce), a conifer, is one of the plants diance dependent since lower irradiance of BL is effective in
which has been widely studied to understand gymnosperm bud formation, but higher irradiance of BL enhances shoot
physiology. In conifers including P. abies, SD-induced bud set growth in P. abies (Opseth et al., 2016; Chiang et al., 2021).
is accompanied by formation of a thick-walled cell plate called On the other hand, FR and LDs are inhibitory for bud for-
the crown at the base of the developing bud.The crown helps in mation and stimulatory for shoot elongation (Opseth et al.,
impeding the entry of water into the winter bud, thereby pre- 2016). In a recent report, a low RL to FR light ratio (low
venting rehydration and increasing freezing tolerance (Owens R:FR) and GA has been shown to promote shoot elongation
and Molder, 1976; Sakai, 1979; MacDonald and Owens, 1993). in Pinus tabuliformis. The amounts of bioactive GA1 and GA4
The formation of this crown is seasonally regulated by pho- were higher in low R:FR compared with the control. The ex-
toperiod. In LDs, the cell wall of growing shoots primarily pression of a GA biosynthesis gene, ent-KAURENOIC ACID
consists of methyl-esterified homogalacturonan (HG) pectin. OXIDASE (PtKAO), was strongly stimulated by low R:FR,
During SD-induced bud formation, this component becomes but was unaffected by GA feedback regulation or the photo-
de-methyl-esterified and cross-links with Ca2+ ions, forming period (Li et al., 2020). Since in P. abies the biosynthesis of GAs
a gel-like structure known as the ‘egg-box’ (Grant et al., 1973; has been suggested to be under photoperiodic control (Moritz,
Willats et al., 2001). Pectin has been shown to prevent entry of 1995) and FR-induced shoot elongation is similar to the LD
macromolecules across the cell wall (Baron-Epel et al., 1988; response (Chiang et al., 2021), it would be interesting to deci-
Wisniewski et al., 1991). De-methyl-esterification of HG cross- pher whether any crosstalk exists among the light quality, pho-
linked with Ca2+ reduces the porosity and thus the egg-box toperiod, and hormonal signalling pathways in P. abies.
prevents entry of water into the developing bud. In addition, it Picea abies was the first gymnosperm to having its genome
was observed that the plasmodesmata were blocked with cal- sequenced completely (Nystedt et al., 2013). Analysis of the
lose tissue and the xylem connections were discontinued at the P. abies genome revealed the presence of core components of
crown region under SDs. The de-methyl-esterified HG was the circadian clock. Picea abies possesses homologues of CCA1,
again methyl-esterified upon transfer from SDs to bud break- TOC1, PRR, ELF4, LUX, GI, and ZTL (Karlgren et al., 2013;
inducing LD conditions. Plasmodesmata blockage was found Gyllenstrand et al., 2014; Linde et al., 2017). Phylogenetic anal-
to be reversed and the xylem continuity was restored under ysis revealed the conservation of key circadian clock genes in
LDs. In agreement with these findings, the expression of aqua- angiosperms and gymnosperms. However, fewer homologues
porin genes also increased under LDs (Lee et al., 2017). of these genes are present in gymnosperms (Gyllenstrand et al.,
The metabolite profile of P. abies also changes according 2014). Heterologous expression PaCCA1, PaGI, and PaZTL in
to photoperiod. While the seedlings in SDs produce a higher Arabidopsis shows that the functions of these proteins are par-
amount of abscisic acid (ABA), antioxidants, flavonoids, terpe- tially conserved (Karlgren et al., 2013). It has been suggested
noids, phenylpropanoids, sugars, amino acids, and lipids partic- that the three-loop circadian clock present in Arabidopsis was
ularly involved in stress response and hardening, they contain conserved before the divergence of gymnosperms and angio-
low levels of nucleosides and metabolites involved in energy sperms. However, the circadian expression of core clock genes
864 | Biswal and Panigrahi

is arrested in LL or DD conditions.This indicates that photope- winter SDs. Transcripts involved in drought and heat tolerance
riodic responses in gymnosperms may not require a strong and and stress responses showed peak expression in spring LDs

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persistent circadian rhythm (Karlgren et al., 2013; Gyllenstrand (Cronn et al., 2017).
et al., 2014). In Cryptomeria japonica (Japanese cedar), microarray analysis
Different components of photoperiodic flowering have of summer and winter transcriptomes showed a significant
also been identified in gymnosperms. Picea abies possesses two difference in the gene expression pattern. While the tran-
homologues of COL genes (PaCOL1 and PaCOL2). These scripts of summer showed diurnal expression, the rhythm was
genes are more closely related to group-1c of COL genes arrested in transcripts of winter (Nose and Watanabe, 2014).
rather than CO and show similarity with moss PpCOL genes. The variation in differential transcript expression may be due
These genes show peak expression at dawn and decreased ex- to day length or temperature, or both. Further study with an-
pression during the dark period. The expression of these genes nual transcriptome analysis of C. japonica revealed that though
is also photoperiodically regulated, showing higher expression growth is inhibited by both SDs and low temperature, they
in LDs compared with SDs. The SD-induced growth cessa- regulate distinct responses in this conifer. Primarily growth-
tion and terminal bud development is preceded by decreased related genes are down-regulated by SDs, but not by temper-
expression of these genes (Holefors et al., 2009). Expression ature in C. japonica. However, interactions among the SD- and
of PaCOL1, PaCOL2, and PaSOC2 decreased under BL and temperature-induced responses control the dynamics of the an-
SD conditions and to a lower extent under RL prior to bud nual transcriptome. Cryptomeria japonica possesses homologues
set and growth cessation (Opseth et al., 2016). PaMADS7 and of core clock components such as LHY (CCA1/CjLHY1a,
PaTFL1 exhibited a higher transcript level in SDs compared LHY/CjLHYb), GI, TOC1, PRR3, PRR7, COL4, COL9,
with LDs.The homologues of these genes in Arabidopsis are in- and ZTL. Out of these genes, the expression of CjTOC1,
volved in organ identity and floral transition, respectively. The CCA1/CjLHY, LHY/CjLHYb, and CjCOL9 was down-
up-regulation of PaTFL1 expression under SDs is correlated regulated under SD conditions. Expression of CjGI and
with SD-induced growth cessation and dormancy induction CjCOL4 showed no significant difference in SDs and LDs
(Asante et al., 2011). Expression of PaFT4, a homologue of (Nose et al., 2020). The expression of CjCOL9 is similar to
Arabidopsis FT, is also up-regulated under SDs and is correlated that of PaCOL genes which also show down-regulation under
with bud set in P. abies (Gyllenstrand et al., 2007). The expres- SDs (Holefors et al., 2009). Expression of CjMFT was down-
sion pattern of PaFT4 is opposite to that of the FT gene of regulated both in SDs and at low temperature. CjMFT may
Picea sitchensis (Sitka spruce), where expression of the FT gene have an important role in regulation of photoperiod- and
is down-regulated under SDs (Holliday et al., 2008). Therefore, temperature-regulated responses in C. japonica (Nose et al., 2020).
the pattern of PaFT4 expression is more similar to that of the Ginkgo biloba, the only living member of the ginkgophytes,
TFL1 gene in Arabidopsis than to known FT genes. This indi- has one copy of CO (GbCO). GbCO is grouped with CO in
cates that though orthologues of FT/TFL appeared in the group-1a of the COL gene family. Consistent with this, GbCO
ancestors of seed plants, true orthologues of FT with a prom- complemented the co mutant of Arabidopsis and restored the
inent role in flowering appeared in angiosperms. It has been early flowering phenotype, which was also associated with
observed that the transcript level of FLOWERING LOCUS an increase in FT expression. GbCO also shows an expres-
T (FT)-TERMINAL FLOWER 1 (TFL1)-LIKE (FTL2) is sion pattern similar to CO in a circadian manner. The tran-
increased under bud-inducing BL preceding bud formation. In script of GbCO accumulates more in the shoot than in other
RL, the accumulation of FT2 transcript was lower compared plant parts (Yan et al., 2017).The expression of GbCO has been
with BL, consistent with the delayed bud set. On the other observed to be higher under LD conditions compared with
hand, FTL2 expression was lower in growth-inducing FR SD conditions. Higher levels of GbCO have been associated
and LD conditions. These findings indicate the central role of with higher shoot growth under LDs. However, under SDs, the
FTL2 in photoperiodic bud set and growth cessation (Opseth shoot growth ceased after a gradual decline in GbCO mRNA
et al., 2016).Transcript analysis of P. abies revealed that genes in- and it did not increase further. The expression of GbCO is
volved in meristem differentiation, defence, and stress response diurnally regulated in LDs, with its peak in early morning.
have a major role in SD-induced growth cessation and dor- These pieces of information strongly argue for an analogous
mancy induction (Asante et al., 2011). role for GbCO in the photoperiodic response of G. biloba (Yan
Different clock genes such as CCA1, COP1, RVE1, et al., 2017). Interestingly, GbCO is the second example after
GI, TOC1, LUX, ELF4, and ZTL have been identified in CrCO which complemented the co mutant of Arabidopsis and
Pseudotsuga menziesii (Douglas fir). The seasonal transcrip- restored normal flowering. While in the evolutionary tree,
tome variation in this species has been analysed and found Chlamydomonas, being an alga is distantly related to Arabidopsis,
to be associated with the seasonal variation in photoperiod. G. biloba, a gymnosperm, is more closely related to Arabidopsis
Transcriptome analysis of conifer needles of P. menziesii re- (Fig. 1), but the CO proteins of these plants have been shown
vealed that transcripts involved in cold and freezing tolerance to have the ability to restore flowering. It is highly unlikely
and induction of dormancy were predominantly expressed in that the COL gene from any other non-flowering plant can
 Photoperiod-mediated development in non-flowering plants | 865

complement the function of the co mutant of Arabidopsis, since Flowering in Arabidopsis is also regulated in CO-independent,
COL genes from other non-flowering plants have no close but photoperiod-dependent pathways. GI regulates an

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similarity to CO. However, this raises a new question regarding miRNA called miR172, which is a repressor of floral inhibitor
the evolutionary significance of this phenomenon, which genes such as TARGET OF EAT 1 (TOE1), TOE2, TOE3,
needs further research. SCHLAFMUTZE (SMZ), and SCHNARCHZAPFEN
In addition to day length-dependent growth cessation and (SNZ). While expression of miR172 increases with plant age
bud development, photoperiod may also regulate the secondary till flowering, expression of the TOE genes decreases with
growth in conifers. In a recent study, Huang et al. (2020a, b) age. miR172 levels are higher in LDs compared with SDs.
have reported that photoperiod and temperature drive wood Expression of miR172 in the co mutant of Arabidopsis causes
formation in northern hemisphere conifers. By correlating the very early flowering. Thus, miR172 induces flowering in LDs.
day of year of wood formation with the photoperiod on the However, the expression of miR172 is not circadian regulated,
day of year of wood formation, it was concluded that photo- but its processing is regulated by GI, which shows rhythmic
period interacts with mean annual temperature to resume sec- expression (Jung et al., 2007; Jackson, 2009).
ondary growth in conifers (Huang et al., 2020b). However, this Tuber formation in potato is another photoperiod-
view has been questioned, and the role of these factors in wood mediated process. Wild species of potato form tubers in SDs
formation in conifers is still debatable (Elmendorf and Ettinger, before the onset of winter. Growth ceases and the tubers re-
2020; Huang et al., 2020a). main dormant throughout winter, and new plants appear in
spring. Some molecular components playing a role in flow-
ering may also play role in tuber formation. Overexpression
Photoperiod regulates multiple growth and of Arabidopsis CO in potato resulted in delayed tuberization
developmental responses in angiosperms (Martínez-García et al., 2002). Orthologues of MFT, TFL1,
and FT genes are represented by family of SELF-PRUNING
Angiosperms are the flower-bearing most recently evolved (SP) genes in members of the Solanaceae (e.g. potato and to-
plants, having a high degree of reproductive specialization and mato) (Carmel-Goren et al., 2003; Abelenda et al., 2014). Two
adaptation (Fig. 1). They are cosmopolitan, having adapted to members of potato FT-like family genes StSP6A and StSP3D
varied habitat and climate.They are the benchmarks in modern control tuberization in SDs and flowering, respectively. These
plant science, since many model plants such as Arabidopsis, rice, genes respond to SDs to promote tuberization and to LDs to
and tobacco have often been used in comparative and func- promote flowering (Navarro et al., 2011; Engelmann, 2015).
tional studies. Consistent with their diversity and adaptability, Homologues of CDF, GI, and FKF1 in potato (StCDF, StGI,
they possess complex molecular systems for the differential and StFKF1) also regulate tuberization by regulating the
responses. Photomorphogenic responses and their molec- CO–FT module (Kloosterman et al., 2013; Abelenda et al.,
ular basis are well characterized in angiosperms compared 2014). Photoreceptors such as PHYs also regulate photope-
with other vascular and non-vascular plants. Photoperiodic riodic tuberization. PHYB-antisense plants have been shown
responses are also well studied in angiosperms. to tuberize in SDs as well as LDs. This indicates that PHYB
It has been mentioned earlier that in Arabidopsis induction prevents the formation of tubers in non-inductive photoperi-
of flowering is photoperiod regulated (Johansson and Staiger, ods, rather than promoting it in inductive SDs (Jackson et al.,
2015). CO is the master regulator of photoperiodic flowering. 1996). PHYA also prevents tuber formation in LDs. PHYA
CO expression is circadian regulated, showing peak expression and CRY are involved in entraining the circadian clock in
towards the end of the LD (at dusk). The stability of CO is potato (Yanovsky et al., 2000).
promoted during this time in LDs. However, in SDs, the CO Succulence of stems and leaves in plants has been shown to
peak is achieved late in the day (after dusk) and it is degraded be under photoperiodic control. Kalanchoe blossfeldiana forms
in the dark. In LDs, CO activates the expression of FT, which succulent leaves under SDs and thinner, longer, and larger
is a small molecule synthesized in the leaf and transported to leaves under LDs. RL and BL have been reported to be effec-
the shoot apical meristem. FT is the positive inducer of flow- tive for photoperiodic control of succulence in K. blossfeldiana
ering in Arabidopsis. Thus, CO induces flowering by activat- (Kröner, 1955; Schwabe and Wilson, 1965; Engelmann, 2015).
ing FT in a photoperiod-dependent manner. According to Like conifers, temperate forest trees also show growth ces-
a recent report, CO also inhibits flowering in Arabidopsis in sation and bud set in SDs (Lagercrantz, 2009; Singh et al.,
SDs (Luccioni et al., 2019). Interestingly, in rice (Oryza sativa), 2017). In Populus trichocarpa, PtFT (FT orthologue) inhibits the
which is a monocot SD plant, Heading Date 1 (OsHd1) (CO SD-induced bud set and growth cessation. Plants overexpress-
orthologue) promotes the expression of OsHd3a (FT ortho- ing PtFT1 do not display growth cessation and bud set under
logue) in SDs, but inhibits its expression in LDs (Yano et al., SDs. Expression of PtFT is regulated by the level of PtCO
2000; Kojima et al., 2002; Komiya et al., 2008). Thus CO func- (orthologue of CO). Expression of these two genes shows a
tions differentially in Arabidopsis and rice to regulate photope- similar pattern to those in Arabidopsis (Olsen, 2010; Engelmann,
riodic flowering (Valverde, 2011; Fan et al., 2014). 2015; Maurya and Bhalerao, 2017).
866 | Biswal and Panigrahi

Photoperiod has been shown to affect hormone levels to Author contributions

regulate dormancy, vegetative growth, and flowering (Vince-
KCSP and DPB: conceptualization; DPB: wrote the manuscript; KCSP:

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Prue, 1985). revised and edited the manuscript. Both authors read and approved the
Photoperiodism and related responses have been demon- final version of the manuscript.
strated in numerous flowering plants. It is beyond the scope
of this review to discuss the photoperiodic responses in
angiosperms more elaborately. Some nice reviews published Conflict of interest
on this topic are available (Jackson, 2009; Lagercrantz, 2009;
Abelenda et al., 2014; Engelmann, 2015; Brambilla et al., The authors declare no conflicts of interest.
2017).
Funding
Concluding remarks KCSP acknowledges funding from the Department of Atomic Energy
(DAE), Government of India. DPB has received no financial assistance
Photoperiod plays an important role in the adaptation of plants
for this work.
to the changing environment. A summary of photoperiodic
responses across the green plant lineage has been presented in
Fig. 1. Photoperiod and the circadian clock together regulate References
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